Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin‐related modifiers
Identifieur interne : 000873 ( Pmc/Corpus ); précédent : 000872; suivant : 000874Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin‐related modifiers
Auteurs : Yao E. Wang ; Olivier Pernet ; Benhur LeeSource :
- Biology of the Cell [ 0248-4900 ] ; 2011.
Abstract
Nucleocytoplasmic trafficking of many cellular proteins is regulated by nuclear import/export signals as well as post‐translational modifications such as covalent conjugation of ubiquitin and small ubiquitin‐related modifiers (SUMOs). Ubiquitination and SUMOylation are rapid and reversible ways to modulate the intracellular localisation and function of substrate proteins. These pathways have been co‐opted by some viruses, which depend on the host cell machinery to transport their proteins in and out of the nucleus. In this review, we will summarise our current knowledge on the ubiquitin/SUMO‐regulated nuclear/subnuclear trafficking of cellular proteins and describe examples of viral exploitation of these pathways.
Url:
DOI: 10.1111/boc.201100105
PubMed: 22188262
PubMed Central: 3625690
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PMC:3625690Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin‐related modifiers</title><author><name sortKey="Wang, Yao E" sort="Wang, Yao E" uniqKey="Wang Y" first="Yao E." last="Wang">Yao E. Wang</name><affiliation><nlm:aff id="af1"></nlm:aff></affiliation></author><author><name sortKey="Pernet, Olivier" sort="Pernet, Olivier" uniqKey="Pernet O" first="Olivier" last="Pernet">Olivier Pernet</name><affiliation><nlm:aff id="af1"></nlm:aff></affiliation><affiliation><nlm:aff id="af2"></nlm:aff></affiliation></author><author><name sortKey="Lee, Benhur" sort="Lee, Benhur" uniqKey="Lee B" first="Benhur" last="Lee">Benhur Lee</name><affiliation><nlm:aff id="af1"></nlm:aff></affiliation><affiliation><nlm:aff id="af2"></nlm:aff></affiliation><affiliation><nlm:aff id="af3"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22188262</idno><idno type="pmc">3625690</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3625690</idno><idno type="RBID">PMC:3625690</idno><idno type="doi">10.1111/boc.201100105</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">000873</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000873</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin‐related modifiers</title><author><name sortKey="Wang, Yao E" sort="Wang, Yao E" uniqKey="Wang Y" first="Yao E." last="Wang">Yao E. Wang</name><affiliation><nlm:aff id="af1"></nlm:aff></affiliation></author><author><name sortKey="Pernet, Olivier" sort="Pernet, Olivier" uniqKey="Pernet O" first="Olivier" last="Pernet">Olivier Pernet</name><affiliation><nlm:aff id="af1"></nlm:aff></affiliation><affiliation><nlm:aff id="af2"></nlm:aff></affiliation></author><author><name sortKey="Lee, Benhur" sort="Lee, Benhur" uniqKey="Lee B" first="Benhur" last="Lee">Benhur Lee</name><affiliation><nlm:aff id="af1"></nlm:aff></affiliation><affiliation><nlm:aff id="af2"></nlm:aff></affiliation><affiliation><nlm:aff id="af3"></nlm:aff></affiliation></author></analytic><series><title level="j">Biology of the Cell</title><idno type="ISSN">0248-4900</idno><idno type="eISSN">1768-322X</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p>Nucleocytoplasmic trafficking of many cellular proteins is regulated by nuclear import/export signals as well as post‐translational modifications such as covalent conjugation of ubiquitin and small ubiquitin‐related modifiers (SUMOs). Ubiquitination and SUMOylation are rapid and reversible ways to modulate the intracellular localisation and function of substrate proteins. These pathways have been co‐opted by some viruses, which depend on the host cell machinery to transport their proteins in and out of the nucleus. In this review, we will summarise our current knowledge on the ubiquitin/SUMO‐regulated nuclear/subnuclear trafficking of cellular proteins and describe examples of viral exploitation of these pathways.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Knipe, D M" uniqKey="Knipe D">D.M. Knipe</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Biol Cell</journal-id><journal-id journal-id-type="iso-abbrev">Biol. Cell</journal-id><journal-id journal-id-type="doi">10.1111/(ISSN)1768-322X</journal-id><journal-id journal-id-type="publisher-id">BOC</journal-id><journal-title-group><journal-title>Biology of the Cell</journal-title></journal-title-group><issn pub-type="ppub">0248-4900</issn><issn pub-type="epub">1768-322X</issn><publisher><publisher-name>WILEY‐VCH Verlag</publisher-name><publisher-loc>Hoboken</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22188262</article-id><article-id pub-id-type="pmc">3625690</article-id><article-id pub-id-type="doi">10.1111/boc.201100105</article-id><article-id pub-id-type="publisher-id">BOC201100105</article-id><article-categories><subj-group subj-group-type="overline"><subject>Review</subject></subj-group><subj-group subj-group-type="heading"><subject>Reviews</subject></subj-group></article-categories><title-group><article-title>Regulation of the nucleocytoplasmic trafficking of viral and cellular proteins by ubiquitin and small ubiquitin‐related modifiers</article-title><alt-title alt-title-type="right-running-head">Ub/SUMO‐regulated nucleocytoplasmic trafficking</alt-title></title-group><contrib-group><contrib id="au1" contrib-type="author"><name><surname>Wang</surname><given-names>Yao E.</given-names></name><xref ref-type="aff" rid="af1"><sup>1</sup></xref></contrib><contrib id="au2" contrib-type="author"><name><surname>Pernet</surname><given-names>Olivier</given-names></name><xref ref-type="aff" rid="af1"><sup>1</sup></xref><xref ref-type="aff" rid="af2"><sup>2</sup></xref></contrib><contrib id="au3" contrib-type="author" corresp="yes"><name><surname>Lee</surname><given-names>Benhur</given-names></name><xref ref-type="aff" rid="af1"><sup>1</sup></xref><xref ref-type="aff" rid="af2"><sup>2</sup></xref><xref ref-type="aff" rid="af3"><sup>3</sup></xref><address><email>bleebhl@ucla.edu</email></address></contrib></contrib-group><aff id="af1"><label><sup>1</sup></label>Department of Microbiology, Immunology, and Molecular Genetics, UCLA, Los Angeles, CA 90095, U.S.A.</aff><aff id="af2"><label><sup>2</sup></label>Department of Pathology and Laboratory Medicine, UCLA, Los Angeles, CA 90095, U.S.A.</aff><aff id="af3"><label><sup>3</sup></label>UCLA AIDS Institute, UCLA, Los Angeles, CA 90095, U.S.A.</aff><author-notes><corresp id="correspondenceTo"><label>*</label>Department of Microbiology, Immunology, and Molecular Genetics, UCLA, Los Angeles, CA 90095, U.S.A.</corresp></author-notes><pub-date pub-type="ppub"><month>3</month><year>2012</year></pub-date><pub-date pub-type="epub"><day>28</day><month>12</month><year>2011</year></pub-date><volume>104</volume><issue>3</issue><issue-id pub-id-type="doi">10.1111/boc.v104.3</issue-id><fpage>121</fpage><lpage>138</lpage><history><date date-type="received"><day>25</day><month>8</month><year>2011</year></date><date date-type="accepted"><day>22</day><month>11</month><year>2011</year></date></history><permissions><copyright-statement content-type="article-copyright">Copyright © 2012 Soçiété Francaise des Microscopies and Société de Biologie Cellulaire de France</copyright-statement><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="file:BOC-104-121.pdf"></self-uri><abstract><title>Abstract</title><p>Nucleocytoplasmic trafficking of many cellular proteins is regulated by nuclear import/export signals as well as post‐translational modifications such as covalent conjugation of ubiquitin and small ubiquitin‐related modifiers (SUMOs). Ubiquitination and SUMOylation are rapid and reversible ways to modulate the intracellular localisation and function of substrate proteins. These pathways have been co‐opted by some viruses, which depend on the host cell machinery to transport their proteins in and out of the nucleus. In this review, we will summarise our current knowledge on the ubiquitin/SUMO‐regulated nuclear/subnuclear trafficking of cellular proteins and describe examples of viral exploitation of these pathways.</p></abstract><abstract abstract-type="graphical"><p>Viruses are obligate parasites. They exploit the cellular machinery to facilitate various steps of their life cycle including the nucleocytoplasmic trafficking of some viral proteins. The host's nuclear trafficking is regulated by post‐translational modifications in addition to specific targeting signals. In this review, we summarize our current knowledge on ubiquitin/SUMO‐regulated nucleocytoplasmic trafficking of cellular proteins and how these pathways are co‐opted by viruses.
<boxed-text position="anchor" content-type="graphic" orientation="portrait"><graphic xlink:href="BOC-104-121-g006.jpg" position="anchor" id="nlm-graphic-1" orientation="portrait"><permissions><copyright-holder>Wiley Periodicals, Inc.</copyright-holder><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions></graphic></boxed-text></p></abstract><kwd-group kwd-group-type="author-generated"><kwd id="kwd1">Post‐translational modification</kwd><kwd id="kwd2">Proteasomes/ubiquitin</kwd><kwd id="kwd3">Protein sorting/trafficking/targeting</kwd><kwd id="kwd4">Viruses</kwd></kwd-group><counts><fig-count count="4"></fig-count><table-count count="3"></table-count><ref-count count="160"></ref-count><page-count count="18"></page-count></counts><custom-meta-group><custom-meta><meta-name>source-schema-version-number</meta-name><meta-value>2.0</meta-value></custom-meta><custom-meta><meta-name>cover-date</meta-name><meta-value>March 2012</meta-value></custom-meta><custom-meta><meta-name>details-of-publishers-convertor</meta-name><meta-value>Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.0 mode:remove_FC converted:15.04.2020</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="sec1-1"><title>Introduction</title><p>The replication of many viruses (particularly DNA viruses and retroviruses) involves nuclear steps (<xref rid="bib50" ref-type="ref">Griffin et al., 2007</xref>). Even for viruses that replicate in the cytoplasm (<italic>e.g.</italic> many negative‐stranded RNA viruses), it is not uncommon for specific viral proteins to enter the nucleus during certain stages of infection to achieve specific functions such as antagonising the host's immune activation (<xref rid="bib67" ref-type="ref">Katze et al., 2002</xref>; <xref rid="bib115" ref-type="ref">Ramachandran and Horvath, 2009</xref>; <xref rid="bib47" ref-type="ref">Goodbourn and Randall, 2009</xref>) or global inhibition of host gene expression (<xref rid="bib110" ref-type="ref">Petersen et al., 2000</xref>; <xref rid="bib147" ref-type="ref">von Kobbe et al., 2000</xref>). The nuclear import and export of viral proteins depend on the host cell machinery and are subject to regulation by pathways that normally modulate the trafficking of cellular proteins, including post‐translational modifications. Conjugation of modifying groups such as phosphate, acetyl group, ubiquitin (Ub), and Ub‐like molecules is a rapid and efficient way of modulating the properties of proteins after their synthesis (<xref rid="bib146" ref-type="ref">Ulrich, 2005</xref>). Particularly, Ub and small ubiquitin‐related modifiers (SUMOs) have drawn much attention in recent years due to their roles in diverse biological functions (<xref rid="bib30" ref-type="ref">Denuc and Marfany, 2010</xref>; <xref rid="bib84" ref-type="ref">Liu and Walters, 2010</xref>). Although the regulatory functions of Ub and SUMO in the nucleocytoplasmic trafficking of cellular proteins have been extensively studied (<xref rid="bib150" ref-type="ref">Wilson and Rangasamy, 2001</xref>; <xref rid="bib112" ref-type="ref">Pichler and Melchior, 2002</xref>; <xref rid="bib132" ref-type="ref">Shcherbik and Haines, 2004</xref>), their involvement in viral protein trafficking has been only recently appreciated. In this review, we will summarise our current knowledge on Ub‐ and SUMO‐regulated nucleocytoplasmic trafficking of cellular proteins and give a few examples of how these pathways are exploited by viruses.</p></sec><sec id="sec1-2"><title>Nuclear import and export machinery</title><p>For proteins larger than 30 kDa, efficient trafficking across the nuclear membrane requires transporters and depends on the presence of specific nuclear import/export signals (<xref rid="bib53" ref-type="ref">Güttler and Görlich, 2011</xref>; <xref rid="bib64" ref-type="ref">Jamali et al., 2011</xref>). In most cases, these signals are recognised by import or export receptors of the karyopherin‐β family either directly or via an adapter (<xref rid="bib138" ref-type="ref">Sorokin et al., 2007</xref>). The best‐characterised nuclear import pathway involves importin α/β, which mediates the nuclear translocation of nuclear localisation signal (NLS)‐containing cargoes in a Ran‐dependent manner, as illustrated in Figure <xref rid="fig1" ref-type="fig">1</xref>. Similarly, the export transporter chromosome region maintenance 1 (CRM‐1; or exportin 1) mediates the nuclear export of a large number of cargoes containing nuclear export signals (NESs) [steps (5) and (6) in Figure <xref rid="fig1" ref-type="fig">1</xref>]. For a comprehensive review of the nuclear import/export machinery, readers are referred to <xref rid="bib99" ref-type="ref">Moroianu (1999)</xref>, <xref rid="bib138" ref-type="ref">Sorokin et al. (2007)</xref> and <xref rid="bib64" ref-type="ref">Jamali et al. (2011)</xref>. In addition, the nucleocytoplasmic trafficking of many proteins is also subject to regulation by post‐translational modifications such as phosphorylation, ubiquitination and SUMOylation (<xref rid="bib65" ref-type="ref">Jans and Hübner, 1996</xref>; <xref rid="bib150" ref-type="ref">Wilson and Rangasamy, 2001</xref>; <xref rid="bib132" ref-type="ref">Shcherbik and Haines, 2004</xref>).</p><fig fig-type="Figure" xml:lang="en" id="fig1" orientation="portrait" position="float"><label>Figure 1</label><caption><p><bold>Simplified illustration of Ran‐dependent nuclear import and export pathways</bold></p><p><named-content content-type="attribution">Steps (1) to (4) illustrate importin α/β‐dependent nuclear import; steps (5) and (6) illustrate CRM‐1‐dependent nuclear export. (1) Importin α binds to the NLS of the cargo protein and forms a complex with importin β. The complex is transported into the nucleus through the nuclear pore complex. (2) In the nucleus, binding of RanGTP to importin β results in its dissociation from importin α and the release of the cargo. (3) RanGTP‐bound importin β is exported to the cytoplasm. (4) Importin β is released upon hydrolysis of RanGTP to RanGDP, allowing for a new cycle of nuclear import. (5) CRM‐1 binds to the NES of the cargo protein and forms a complex with RanGTP. (6) The complex is transported into the cytoplasm, where hydrolysis of RanGTP results in the release of the cargo.</named-content></p></caption><graphic id="nlm-graphic-3" xlink:href="BOC-104-121-g004"><permissions><copyright-holder>Wiley Periodicals, Inc.</copyright-holder><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions></graphic></fig></sec><sec id="sec1-3"><title>Ub and SUMO pathways</title><p>Ubiquitin is a small 76‐amino‐acid protein modifier that is covalently attached to the substrate protein usually via an acceptor lysine residue. Ub conjugation occurs by the sequential action of three enzymes: (i) a Ub‐activating enzyme (E1), (ii) a Ub‐conjugating enzyme (E2) and (iii) a Ub ligase (E3), which determines substrate specificity and the type of conjugation (<italic>e.g.</italic> monoUb versus polyUb, K48‐ versus K63‐linked Ub). The ubiquitination machinery has been reviewed in <xref rid="bib68" ref-type="ref">Kerscher et al. (2006)</xref>. Though initially described as a regulator of protein degradation (<xref rid="bib149" ref-type="ref">Wilkinson et al., 1980</xref>), Ub is now known to play important roles in a broad spectrum of cellular activities such as intracellular protein trafficking, transcriptional regulation, DNA repair, cell‐cycle progression and apoptosis (<xref rid="bib132" ref-type="ref">Shcherbik and Haines, 2004</xref>; <xref rid="bib84" ref-type="ref">Liu and Walters, 2010</xref>).</p><p>SUMO's involvement in nuclear trafficking was initially suggested by its first known substrate, Ran GTPase‐activating protein 1 (RanGAP1), which is a part of the nuclear import/export machinery (<xref rid="bib27" ref-type="ref">Cole and Hammell, 1998</xref>; <xref rid="bib38" ref-type="ref">Fried and Kutay, 2003</xref>). Unmodified RanGAP1 is diffused in the cytoplasm, whereas SUMO conjugation targets it to the nuclear pore complex, where it regulates protein/RNA trafficking across the nuclear membrane (<xref rid="bib94" ref-type="ref">Matunis et al., 1996</xref>; <xref rid="bib88" ref-type="ref">Mahajan et al., 1997</xref>; <xref rid="bib95" ref-type="ref">Matunis et al., 1998</xref>). Since then SUMO has been associated with the nuclear/subnuclear targeting of various cellular proteins (discussed below). The vertebrate genome encodes at least four SUMO isoforms, namely SUMO1‐4. Similar to ubiquitination, SUMOylation is a three‐step process involving an E1‐activating enzyme heterodimer Aos/Uba2, an E2‐conjugating enzyme Ubc9 and substrate‐specific E3 ligases (reviewed in <xref rid="bib40" ref-type="ref">Gareau and Lima, 2010</xref>).</p><p>Given that proteins can be modified by both Ub and SUMO, sometimes on the same lysine residue, it is not surprising that these two modification systems communicate. Indeed, the interaction between Ub and SUMO pathways is complex and could be either competitive, cooperative or differential (<xref rid="bib146" ref-type="ref">Ulrich, 2005</xref>; <xref rid="bib30" ref-type="ref">Denuc and Marfany, 2010</xref>). In the following section, we will briefly summarise examples of cellular proteins whose nucleocytoplasmic trafficking is regulated by Ub and/or SUMO and discuss the crosstalk between the two pathways so as to provide a better context when we later review viral exploitation of these pathways.</p></sec><sec id="sec1-4"><title>Ub/SUMO‐regulated nucleocytoplasmic trafficking of cellular proteins</title><sec id="sec2-1"><title>Ub and nuclear import/export</title><p>Ubiquitination is usually associated with cytoplasmic localisation via promoting either nuclear export or cytoplasmic retention. The best‐characterised example is the tumour suppressor gene p53 (reviewed in <xref rid="bib132" ref-type="ref">Shcherbik and Haines, 2004</xref>; <xref rid="bib141" ref-type="ref">Stehmeier and Muller, 2009</xref>; <xref rid="bib79" ref-type="ref">Lee and Gu, 2010</xref>). P53 is ubiquitinated on its six C‐terminal lysine residues by the E3 Ub ligase Mdm2 (<xref rid="bib58" ref-type="ref">Honda et al., 1997</xref>; <xref rid="bib118" ref-type="ref">Rodriguez et al., 2000</xref>; <xref rid="bib86" ref-type="ref">Lohrum et al., 2001</xref>; <xref rid="bib102" ref-type="ref">Nakamura et al., 2002</xref>). Although polyubiquitination results in proteasomal degradation, monoubiquitination by the same E3 ligase leads to nuclear export (<xref rid="bib81" ref-type="ref">Li et al., 2003</xref>) [pathways (1) and (2) in Figure <xref rid="fig2" ref-type="fig">2</xref>]. It has been postulated that Ub modification induces a conformational change, leading to unmasking of the NES which resides in the proximity of the Ub sites (<xref rid="bib132" ref-type="ref">Shcherbik and Haines, 2004</xref>). Once in the cytoplasm, p53 can be deubiquitinated by the deubiquitinase USP10, resulting in its translocation back to the nucleus (<xref rid="bib157" ref-type="ref">Yuan et al., 2010</xref>) [pathway (3) in Figure <xref rid="fig2" ref-type="fig">2</xref>]. Polyubiquitination of transcription factors Sma‐ and MAD‐related protein 3 (Smad3) and hypoxia inducible factor alpha (HIF‐α) has also been linked to their export from the nucleus and termination of transcriptional activation (<xref rid="bib39" ref-type="ref">Fukuchi et al., 2001</xref>; <xref rid="bib51" ref-type="ref">Groulx and Lee, 2002</xref>). Alternatively, ubiquitination can favour cytoplasmic localisation by inhibiting nuclear import, which is exemplified in the case of CTP–phosphocholine cytidylyltransferase (CCT‐α). The regulatory enzyme CCT‐α can switch between an inactive form in the cytoplasm and an active form in the nucleus. It possesses an NLS located in close proximity of the putative ubiquitination site. By using CCTα–Ub hybrid constructs that vary in the intermolecular distance between Ub and the NLS, the authors showed that monoubiquitination masks the NLS, resulting in the disruption of importin‐α binding and consequently a blockage in the nuclear import (<xref rid="bib22" ref-type="ref">Chen and Mallampalli, 2009</xref>).</p><fig fig-type="Figure" xml:lang="en" id="fig2" orientation="portrait" position="float"><label>Figure 2</label><caption><p><bold>Schematic illustration of p53 nucleocytoplasmic trafficking regulated by Ub and SUMO</bold></p><p><named-content content-type="attribution">(1) p53 polyubiquitination by Mdm2 leads to protein degradation (<xref rid="bib81" ref-type="ref">Li et al., 2003</xref>). (2) p53 monoubiquitination by Mdm2 and SUMOylation by PIASy cooperatively lead to nuclear export (<xref rid="bib81" ref-type="ref">Li et al., 2003</xref>, <xref rid="bib18" ref-type="ref">Carter et al., 2007</xref>). (3) Demodified p53 translocates back to the nucleus (<xref rid="bib157" ref-type="ref">Yuan et al., 2010</xref>) (see text for details).</named-content></p></caption><p><named-content content-type="no eRights">The publisher did not receive permission from the copyright owner to include this object in this version of this product. Please refer either to the publisher's own online version of this product or the printed product where one exists.</named-content> Wiley Periodicals, Inc.</p></fig><p>There are currently few examples of Ub playing a direct role in the nuclear import of target proteins. A good example is the tumour suppressor phosphatase and tensin homolog on chromosome 10 (PTEN) (<xref rid="bib145" ref-type="ref">Trotman et al., 2007</xref>). Though no conventional NLSs have been identified in PTEN, the tumour suppressor is able to translocate into the nucleus. Ubiquitination on lysine residue K289 likely plays a role in the nuclear import of PTEN because the K289E mutant, associated with Cowden syndrome, is defective in nuclear import, monoubiquitination, as well as its tumour suppression ability. The authors further identified another monoubiquitination site K13, which is also found to be mutated in spontaneous cancer, as being important for nuclear import.</p><p>A list of cellular proteins whose nuclear import/export is regulated by ubiquitination can be found in Table <xref rid="tbl1" ref-type="table">1</xref>.</p><table-wrap id="tbl1" xml:lang="en" orientation="portrait" position="float"><label>Table 1</label><caption><p>Nucleocytoplasmic trafficking of cellular proteins regulated by Ub and/or SUMO</p></caption><table frame="hsides" rules="groups"><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><thead><tr style="border-bottom:solid 1px #000000"><th align="left" rowspan="1" colspan="1">Protein</th><th align="left" rowspan="1" colspan="1">Major functions</th><th align="left" rowspan="1" colspan="1">Ub regulation</th><th align="left" rowspan="1" colspan="1">SUMO regulation</th><th align="left" rowspan="1" colspan="1">References</th></tr></thead><tbody><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">CCTα</td><td align="left" rowspan="1" colspan="1">Enzyme involved in the synthesis of phosphatidylcholine</td><td align="left" rowspan="1" colspan="1">Ub site is in close proximity of the NLS. Ub results in masking of the NLS and disruption of importin‐α binding, leading to an inhibition of nuclear import.</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1"><xref rid="bib22" ref-type="ref">Chen and Mallampalli, 2009</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">CREB</td><td align="left" rowspan="1" colspan="1">Transcriptional regulation</td><td align="left" rowspan="1" colspan="1">Phosphorylation‐dependent ubiquitination results in proteasomal degradation in hypoxia</td><td align="left" rowspan="1" colspan="1">SUMO conjugation on a lysine residue within the NLS is important for nuclear import</td><td align="left" rowspan="1" colspan="1"><xref rid="bib143" ref-type="ref">Taylor et al., 2000</xref>; <xref rid="bib28" ref-type="ref">Comerford et al., 2003</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">CtBP</td><td align="left" rowspan="1" colspan="1">Transcription repressor</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">Mutation of the SUMOylation site shifts CtBP from the nucleus to the cytoplasm and abolishes its transcriptional repression activity</td><td align="left" rowspan="1" colspan="1"><xref rid="bib83" ref-type="ref">Lin et al., 2003b</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">DdMEK1</td><td align="left" rowspan="1" colspan="1">Kinase involved in the chemotaxis of dictyostelium</td><td align="left" rowspan="1" colspan="1">Ub contributes to nuclear targeting</td><td align="left" rowspan="1" colspan="1">Chemoattractant stimulation induces SUMOylation of MEK1, which is required for its translocation from the nucleus to the cytosol and cortex</td><td align="left" rowspan="1" colspan="1"><xref rid="bib136" ref-type="ref">Sobko et al., 2002</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">DEDD</td><td align="left" rowspan="1" colspan="1">Apoptosis reguator l</td><td align="left" rowspan="1" colspan="1">Ub induces cytoplasmic localisation and higher proapoptotic capacity</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1"><xref rid="bib78" ref-type="ref">Lee et al., 2005</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">HIF‐α</td><td align="left" rowspan="1" colspan="1">Transcription factor</td><td align="left" rowspan="1" colspan="1">Under hypoxic conditions, HIF‐α disassociates from the E3 ligase complex and accumulates in the nucleus. Upon return to normaxia, it binds to the ligase complex and polyUb leads to nuclear export and degradation.</td><td align="left" rowspan="1" colspan="1">SUMOylation increases HIF‐α's stability and its transcriptional activity</td><td align="left" rowspan="1" colspan="1"><xref rid="bib51" ref-type="ref">Groulx and Lee, 2002</xref>; <xref rid="bib7" ref-type="ref">Bae et al., 2004</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">HIPK2</td><td align="left" rowspan="1" colspan="1">Transcriptional regulation</td><td align="left" rowspan="1" colspan="1">PolyUb leads to protein degradation</td><td align="left" rowspan="1" colspan="1">SUMOylation is important for HIPK2 localisation to nuclear speckles</td><td align="left" rowspan="1" colspan="1"><xref rid="bib71" ref-type="ref">Kim et al., 1999</xref>; <xref rid="bib26" ref-type="ref">Choi et al., 2008</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">IGF‐1R</td><td align="left" rowspan="1" colspan="1">Receptor tyrosine kinase</td><td align="left" rowspan="1" colspan="1">Phosphorylation‐dependent ubiquitination is important for downstream signalling</td><td align="left" rowspan="1" colspan="1">Ligand‐dependent SUMOylation is required for nuclear translocation</td><td align="left" rowspan="1" colspan="1"><xref rid="bib127" ref-type="ref">Sehat et al., 2007</xref>; <xref rid="bib128" ref-type="ref">Sehat et al., 2010</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">IκBα</td><td align="left" rowspan="1" colspan="1">Inhibitor of NF‐κB</td><td align="left" rowspan="1" colspan="1">Ub results in proteasomal degradation, leading to NF‐κB activation</td><td align="left" rowspan="1" colspan="1">SUMOylation of IκBα results in its resistance to Ub‐mediated proteasomal degradation, resulting in the retention of NF‐κB in the cytoplasm</td><td align="left" rowspan="1" colspan="1"><xref rid="bib31" ref-type="ref">Desterro et al., 1998</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">KLF5</td><td align="left" rowspan="1" colspan="1">Transcription factor</td><td align="left" rowspan="1" colspan="1">Ub leads to rapid proteasomal degradation</td><td align="left" rowspan="1" colspan="1">SUMO site is close to the NES. SUMOylation enhances nuclear localisation by inhibiting the NES function.</td><td align="left" rowspan="1" colspan="1"><xref rid="bib24" ref-type="ref">Chen et al., 2005</xref>; <xref rid="bib33" ref-type="ref">Du et al., 2008</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">Lef1</td><td align="left" rowspan="1" colspan="1">Transcription factor</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMOylation by E3 ligase PIASy promotes Lef1 localisation to PML bodies and represses its function</td><td align="left" rowspan="1" colspan="1"><xref rid="bib123" ref-type="ref">Sachdev et al., 2001</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">NEMO</td><td align="left" rowspan="1" colspan="1">Regulatory subunit of the IKK complex</td><td align="left" colspan="2" rowspan="1">Upon genotoxic stress, sequential modification of NEMO by SUMO and Ub cooperatively leads to NF‐κB activation</td><td align="left" rowspan="1" colspan="1"><xref rid="bib59" ref-type="ref">Huang et al., 2003</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">p53</td><td align="left" rowspan="1" colspan="1">Tumor suppressor</td><td align="left" rowspan="1" colspan="1">MonoUb on C‐terminal lysine residues by Mdm2 promotes nuclear export, whereas polyUb leads to proteasomal degradation.</td><td align="left" rowspan="1" colspan="1">SUMOylation by PIASy E3 ligase promotes its dissociation from Mdm2 and nuclear export</td><td align="left" rowspan="1" colspan="1"><xref rid="bib58" ref-type="ref">Honda et al., 1997</xref>; <xref rid="bib118" ref-type="ref">Rodriguez et al., 2000</xref>; <xref rid="bib86" ref-type="ref">Lohrum et al., 2001</xref>; <xref rid="bib102" ref-type="ref">Nakamura et al., 2002</xref>; <xref rid="bib81" ref-type="ref">Li et al., 2003</xref>; <xref rid="bib18" ref-type="ref">Carter et al., 2007</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">PML</td><td align="left" rowspan="1" colspan="1">Major component of the PML nuclear bodies</td><td align="left" rowspan="1" colspan="1">SUMO‐dependent E3 Ub ligase RNF4 ubiquitinates PML and causes its proteasomal degradation</td><td align="left" rowspan="1" colspan="1">SUMO modification is important for nuclear body localisation</td><td align="left" rowspan="1" colspan="1"><xref rid="bib101" ref-type="ref">Müller et al., 1998</xref>; <xref rid="bib35" ref-type="ref">Duprez et al., 1999</xref>; <xref rid="bib142" ref-type="ref">Tatham et al., 2008</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">PTEN</td><td align="left" rowspan="1" colspan="1">Tumor suppressor</td><td align="left" rowspan="1" colspan="1">MonoUb by Nedd4 on residues K13 and K289 is required for nuclear import. Nuclear localisation is also controlled by the deubiquitinating enzyme HAUSP.</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1"><xref rid="bib145" ref-type="ref">Trotman et al., 2007</xref>; <xref rid="bib137" ref-type="ref">Song et al., 2008</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">RanGAP1</td><td align="left" rowspan="1" colspan="1">Nucleocytoplasmic transport</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMO modification is required for its interaction with RanBP2 and targeting to the nuclear pore complex</td><td align="left" rowspan="1" colspan="1"><xref rid="bib94" ref-type="ref">Matunis et al., 1996</xref>; <xref rid="bib88" ref-type="ref">Mahajan et al., 1997</xref>; <xref rid="bib95" ref-type="ref">Matunis et al., 1998</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">RARA</td><td align="left" rowspan="1" colspan="1">Transcriptional regulation</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMO2 modification is involved in the nucleocytoplasmic shuttling of RARA</td><td align="left" rowspan="1" colspan="1"><xref rid="bib160" ref-type="ref">Zhu et al., 2009</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">Smad3</td><td align="left" rowspan="1" colspan="1">Transcription factor</td><td align="left" rowspan="1" colspan="1">PolyUb by ROC1‐SCF complex leads to nuclear export and degradation, resulting in the termination of Smad3‐induced transcriptional activation</td><td align="left" rowspan="1" colspan="1">PIASy‐mediated SUMOylation stimulates nuclear export</td><td align="left" rowspan="1" colspan="1"><xref rid="bib39" ref-type="ref">Fukuchi et al., 2001</xref>; <xref rid="bib62" ref-type="ref">Imoto et al., 2008</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">Smad4</td><td align="left" rowspan="1" colspan="1">Transcriptional regulation</td><td align="left" rowspan="1" colspan="1">MonoUb of Smad4 enhances its transcriptional activity, whereas polyUb leads to proteasomal degradation</td><td align="left" rowspan="1" colspan="1">SUMOylation is mediated by PIAS family E3 ligases and occurs in the nucleus. SUMO enhances nuclear retention of Smad4 and increases its stability.</td><td align="left" rowspan="1" colspan="1"><xref rid="bib82" ref-type="ref">Lin et al., 2003a</xref>; <xref rid="bib80" ref-type="ref">Lee et al., 2003</xref>; <xref rid="bib98" ref-type="ref">Morén et al., 2003</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">Sp3</td><td align="left" rowspan="1" colspan="1">Transcription factor</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMO modification by PIAS1 is required for inactivation of Sp3 and its translocation to nuclear periphery and nuclear dots</td><td align="left" rowspan="1" colspan="1"><xref rid="bib122" ref-type="ref">Ross et al., 2002</xref>; <xref rid="bib125" ref-type="ref">Sapetschnig et al., 2002</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">TEL</td><td align="left" rowspan="1" colspan="1">Transcriptional repressor</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMOylation is important for nuclear speckle targeting. SUMO might also be important for nuclear export.</td><td align="left" rowspan="1" colspan="1"><xref rid="bib19" ref-type="ref">Chakrabarti et al., 2000</xref>; <xref rid="bib153" ref-type="ref">Wood et al., 2003</xref></td></tr><tr><td align="left" rowspan="1" colspan="1">VHL</td><td align="left" rowspan="1" colspan="1">Tumor suppressor</td><td align="left" rowspan="1" colspan="1">Ub contributes to nuclear export</td><td align="left" rowspan="1" colspan="1">SUMOylation by PIASy E3 ligase promotes nuclear localisation</td><td align="left" rowspan="1" colspan="1"><xref rid="bib16" ref-type="ref">Cai and Robertson, 2010</xref></td></tr></tbody></table><permissions><copyright-holder>Wiley Periodicals, Inc.</copyright-holder><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions></table-wrap></sec><sec id="sec2-2"><title>SUMO and nuclear import/export</title><p>In contrast to Ub, SUMO is usually associated with nuclear/subnuclear targeting. The first identified SUMO substrate RanGAP1 is targeted to the nuclear pore complex and binds to the nucleoporin RanBP2/Nup358 upon SUMOylation (<xref rid="bib94" ref-type="ref">Matunis et al., 1996</xref>; <xref rid="bib88" ref-type="ref">Mahajan et al., 1997</xref>; <xref rid="bib95" ref-type="ref">Matunis et al., 1998</xref>). Because RanBP2 is part of the nucleocytoplasmic transport machinery and itself has SUMO E3 ligase activity (<xref rid="bib93" ref-type="ref">Mattaj and Englmeier, 1998</xref>; <xref rid="bib48" ref-type="ref">Görlich and Kutay, 1999</xref>; <xref rid="bib111" ref-type="ref">Pichler et al., 2002</xref>), it has been postulated that SUMOylation might be coupled to translocation through the nuclear pore (<xref rid="bib112" ref-type="ref">Pichler and Melchior, 2002</xref>).</p><p>Examples of proteins whose intracellular distribution is affected by SUMOylation are listed in Table <xref rid="tbl1" ref-type="table">1</xref>. In the case of Krüppel‐like factor 5 (KLF5), SUMOylation on a site close to the endogenous NES inhibits the NES function and leads to nuclear retention (<xref rid="bib33" ref-type="ref">Du et al., 2008</xref>). SUMO also enhances the nuclear accumulation of insulin‐like growth factor 1 receptor (IGF‐1R) (<xref rid="bib128" ref-type="ref">Sehat et al., 2010</xref>), cAMP‐response‐element‐binding protein (CREB) (<xref rid="bib28" ref-type="ref">Comerford et al., 2003</xref>) and C‐terminal binding protein of adenovirus E1A (CtBP) (<xref rid="bib83" ref-type="ref">Lin et al., 2003b</xref>). SUMO site mutation favours cytoplasmic localisation in all three cases; however, whether this is mediated through promoting nuclear import or inhibiting nuclear export is not clear. On the other hand, nuclear targeting of promyelocytic leukaemia protein (PML) <italic>per se</italic> does not seem to require SUMOylation, as mutating the SUMO site does not prevent its nuclear accumulation. However, SUMOylation of PML is important for its localisation in nuclear bodies (<xref rid="bib158" ref-type="ref">Zhong et al., 2000</xref>; <xref rid="bib76" ref-type="ref">Lallemand‐Breitenbach et al., 2001</xref>).</p><p>The involvement of SUMO in regulating nuclear export has been suggested by studies of the retinoic acid receptor alpha (RARA) (<xref rid="bib160" ref-type="ref">Zhu et al., 2009</xref>) and the E‐twenty‐six family transcriptional repressor TEL (<xref rid="bib153" ref-type="ref">Wood et al., 2003</xref>). In both cases, the putative SUMO site mutants are restricted to the nucleus. However, one caveat is that ubiquitination was not examined in these studies and the observed effect, therefore, could potentially be due to the lack of ubiquitination.</p></sec><sec id="sec2-3"><title>Crosstalk between Ub and SUMO systems</title><p>Because proteins can be modified by both Ub and SUMO, the interaction between the two systems determines the eventual outcome of the modification.</p><p>When the same lysine residue serves as both Ub and SUMO sites, as seen in the examples of the inhibitor of NF‐κB alpha (IκBα) (<xref rid="bib31" ref-type="ref">Desterro et al., 1998</xref>) and von Hippel–Lindau protein (VHL) (<xref rid="bib16" ref-type="ref">Cai and Robertson, 2010</xref>), modifications by Ub and SUMO usually have opposing effects on the localisation and functions of the target protein, although there may be exceptions (discussed below). For example, although ubiquitination of IκBα leads to its degradation and consequently the nuclear translocation of NF‐κB subunits, SUMOylation leads to its resistance to Ub‐mediated proteasomal degradation, resulting in retention of NF‐κB in the cytoplasm (<xref rid="bib31" ref-type="ref">Desterro et al., 1998</xref>). VHL is SUMOylated by the PIASy E3 ligase, which promotes its nuclear localisation, whereas ubiquitination on the same lysine residue contributes to nuclear export (<xref rid="bib16" ref-type="ref">Cai and Robertson, 2010</xref>).</p><p>However, ubiquitination and SUMOylation occurring on the same lysine residue do not necessarily lead to antagonistic effects on the function of the target protein, as exemplified by the sequential modifications of the NF‐κB essential modulator (NEMO) during genotoxic stress (<xref rid="bib59" ref-type="ref">Huang et al., 2003</xref>). After treatment with DNA‐damaging reagents, IκB kinase (IKK) complex activation requires the passage of the regulatory subunit NEMO through the nucleus. Although SUMOylation seems to target NEMO to the nucleus, ubiquitination, which occurs at a later time point, results in the shuttling of the protein back to the cytoplasm. In this case, the sequential modifications by SUMO and Ub cooperatively lead to the activation of IKK.</p><p>Ubiquitin and SUMO also appear to cooperate in regulating the nuclear export of p53. As discussed in the section ‘Ub and nuclear import/export,’ p53 nuclear export depends on monoubiquitination on C‐terminal lysine residues (<xref rid="bib86" ref-type="ref">Lohrum et al., 2001</xref>; <xref rid="bib81" ref-type="ref">Li et al., 2003</xref>). <xref rid="bib18" ref-type="ref">Carter et al. (2007)</xref> have shown that SUMOylation also plays a role in this process. According to the model proposed by these authors, the attachment of a single Ub serves as an initiation event, allowing for access to the NES and recognition of p53 by SUMO E3 ligases such as PIASy, which leads to further modification of p53 to release Mdm2 and allow nuclear export [pathway (2) in Figure <xref rid="fig2" ref-type="fig">2</xref>].</p><p>Recent identification and characterisation of SUMO‐targeted ubiquitin ligases (STUbLs) in yeast (reviewed in <xref rid="bib45" ref-type="ref">Geoffroy and Hay, 2009</xref>), fly (<xref rid="bib10" ref-type="ref">Barry et al., 2011</xref>; <xref rid="bib1" ref-type="ref">Abed et al., 2011a</xref>) and mammalian cells (<xref rid="bib75" ref-type="ref">Lallemand‐Breitenbach et al., 2008</xref>; <xref rid="bib142" ref-type="ref">Tatham et al., 2008</xref>; <xref rid="bib100" ref-type="ref">Mukhopadhyay et al., 2010</xref>) have added yet another layer of complexity to the Ub/SUMO network. STUbLs selectively ubiquitinate SUMOylated proteins and proteins that contain SUMO‐like domains, resulting in their deSUMOylation and/or degradation (<xref rid="bib113" ref-type="ref">Prudden et al., 2007</xref>). The presence of STUbLs helps to maintain the delicate balance between SUMOylation and ubiquitination (<xref rid="bib2" ref-type="ref">Abed et al., 2011b</xref>).</p></sec><sec id="sec2-4"><title>Viral exploitation of the Ub/SUMO pathways</title><p>Viruses are obligate parasites. Because of the extremely limited protein encoding ability of the viral genome, viruses have evolved ways to utilise the host cell machinery, including the Ub/SUMO pathways. One example of viruses exploiting the Ub pathway is the involvement of cellular endosomal sorting complex required for transport (ESCRT) in the budding of viruses from the multivesicular bodies, which was initially shown for retroviruses (<xref rid="bib91" ref-type="ref">Martin‐Serrano et al., 2001</xref>; <xref rid="bib41" ref-type="ref">Garrus et al., 2001</xref>) and then extended to other viral families (<xref rid="bib126" ref-type="ref">Schmitt et al., 2002</xref>; <xref rid="bib154" ref-type="ref">Yasuda et al., 2003</xref>; <xref rid="bib152" ref-type="ref">Wirblich et al., 2008</xref>). The interaction between viral proteins and the ESCRT complexes has been extensively studied, and there are a few excellent reviews on this subject (<xref rid="bib13" ref-type="ref">Bieniasz, 2006</xref>; <xref rid="bib90" ref-type="ref">Martin‐Serrano, 2007</xref>; <xref rid="bib23" ref-type="ref">Chen and Lamb, 2008</xref>; <xref rid="bib96" ref-type="ref">McDonald and Martin‐Serrano, 2009</xref>; <xref rid="bib52" ref-type="ref">Gustin et al., 2011</xref>). Here, we will focus on a much lesser known aspect of viral interaction with the Ub/SUMO system: the regulation of nucleocytoplasmic trafficking of viral proteins by Ub and SUMO.</p></sec><sec id="sec2-5"><title>Retrovirus</title><p>To date, the best‐characterised example of a viral protein whose nucleocytoplasmic trafficking is regulated by the Ub/SUMO pathways is the Tax protein of the human T‐cell leukaemia virus type 1 (HTLV‐1). HTLV‐1 is the etiological agent of adult T‐cell leukaemia/ lymphoma, and tropical spastic paraparesis/HTLV‐associated myelopathy (<xref rid="bib66" ref-type="ref">Jeang, 2010</xref>; <xref rid="bib133" ref-type="ref">Shembade and Harhaj, 2010</xref>). Tax, a 40 kDa phosphoprotein encoded by the pX region of the virus, is a multifunctional protein that plays key roles in viral replication as well as T‐cell transformation (<xref rid="bib92" ref-type="ref">Matsuoka and Jeang, 2011</xref>). It promotes cell survival by constitutively activating the NF‐κB family transcription factors via interactions with the components of the pathway at both cytoplasmic and nuclear steps (<xref rid="bib103" ref-type="ref">Nasr et al., 2006</xref>).</p><p>Tax shuttles between the nuclear and cytoplasmic compartments (<xref rid="bib15" ref-type="ref">Burton et al., 2000</xref>; <xref rid="bib70" ref-type="ref">Kfoury et al., 2011</xref>). In the nucleus, Tax is predominantly localised to heterogeneous nuclear foci known as Tax speckled structures (TSS), which contain a variety of cellular proteins including transcription factors, splicing cofactors, and DNA damage recognition and cell cycle regulatory factors (<xref rid="bib129" ref-type="ref">Semmes et al., 1996</xref>; <xref rid="bib11" ref-type="ref">Bex et al., 1997</xref>; <xref rid="bib55" ref-type="ref">Haoudi et al., 2003</xref>). In the cytoplasm, a major fraction of Tax localises to perinuclear structures colocalising with the centrosome or microtubule‐organising center in close association with the <italic>cis</italic>‐Golgi compartment (<xref rid="bib104" ref-type="ref">Nejmeddine et al., 2005</xref>; <xref rid="bib69" ref-type="ref">Kfoury et al., 2008</xref>; <xref rid="bib70" ref-type="ref">Kfoury et al., 2011</xref>). Using a photoconvertible fluorophore (Dendra‐2) coupled with live cell confocal microscopy, <xref rid="bib70" ref-type="ref">Kfoury et al. (2011)</xref> recently showed that the same Tax molecule can shuttle amongst Tax nuclear bodies as well as between Tax nuclear bodies and the centrosome. This dynamic shuttling is important for its function in interaction with NEMO and activation of NF‐κB (<xref rid="bib70" ref-type="ref">Kfoury et al., 2011</xref>). Cellular stress such as UV irradiation induces the translocation of Tax from TSS to the cytoplasm (<xref rid="bib43" ref-type="ref">Gatza and Marriott, 2006</xref>; <xref rid="bib42" ref-type="ref">Gatza et al., 2007</xref>). The nucleocytoplasmic shuttling of Tax is mediated by a non‐canonical NLS at the N‐terminal (<xref rid="bib134" ref-type="ref">Smith and Greene, 1990</xref>; <xref rid="bib135" ref-type="ref">Smith and Greene, 1992</xref>; <xref rid="bib97" ref-type="ref">Meertens et al., 2004</xref>) and a leucine‐rich NES (<xref rid="bib15" ref-type="ref">Burton et al., 2000</xref>; <xref rid="bib6" ref-type="ref">Alefantis et al., 2003</xref>). However, Tax also undergoes different forms of post‐translational modification, including phosphorylation (<xref rid="bib12" ref-type="ref">Bex et al., 1999</xref>), acetylation (<xref rid="bib85" ref-type="ref">Lodewick et al., 2009</xref>), ubiquitination (<xref rid="bib103" ref-type="ref">Nasr et al., 2006</xref>; <xref rid="bib69" ref-type="ref">Kfoury et al., 2008</xref>) and SUMOylation (<xref rid="bib103" ref-type="ref">Nasr et al., 2006</xref>; <xref rid="bib70" ref-type="ref">Kfoury et al., 2011</xref>), all of which are implicated in its functions. Particularly, ubiquitination and SUMOylation have been shown to be involved in its nucleocytoplasmic trafficking (Figure <xref rid="fig3" ref-type="fig">3</xref>).</p><fig fig-type="Figure" xml:lang="en" id="fig3" orientation="portrait" position="float"><label>Figure 3</label><caption><p><bold>Schematic illustration of HTLV‐1 Tax nucleocytoplasmic trafficking regulated by Ub and SUMO</bold></p><p><named-content content-type="attribution">(1) UV induces monoubiquitination of Tax, its dissociation from nuclear body proteins and nuclear export (<xref rid="bib42" ref-type="ref">Gatza et al., 2007</xref>). (2) SUMOylation targets Tax to the nuclear bodies (<xref rid="bib77" ref-type="ref">Lamsoul et al., 2005</xref>). (3) K63‐linked polyubiquitination targets Tax to microtubule organising center as well as nuclear bodies (<xref rid="bib70" ref-type="ref">Kfoury et al., 2011</xref>). Polyubiquitination is also important for targeting the IKK signalosome to the centrosome and nuclear translocation of RelA (<xref rid="bib69" ref-type="ref">Kfoury et al., 2008</xref>, <xref rid="bib103" ref-type="ref">Nasr et al., 2006</xref>) (see text for details).</named-content></p></caption><p><named-content content-type="no eRights">The publisher did not receive permission from the copyright owner to include this object in this version of this product. Please refer either to the publisher's own online version of this product or the printed product where one exists.</named-content> Wiley Periodicals, Inc.</p></fig><p>Tax is modified by monoUb as well as K48‐ and K63‐linked Ub chains (<xref rid="bib25" ref-type="ref">Chiari et al., 2004</xref>; <xref rid="bib109" ref-type="ref">Peloponese et al., 2004</xref>; <xref rid="bib69" ref-type="ref">Kfoury et al., 2008</xref>). Although K48 Ub chains lead to Tax degradation, K63 Ub chains mediate binding to NEMO, recruitment of the IKK signalosome to the centrosome and activation of NF‐κB (<xref rid="bib109" ref-type="ref">Peloponese et al., 2004</xref>; <xref rid="bib69" ref-type="ref">Kfoury et al., 2008</xref>). The ubiquitination sites have been mapped to the C‐terminal lysine residues (K263, K280 and K284). Mutating these three K residue results in a dramatic reduction of polyUb and monoUb of Tax, whereas the three N‐terminal K residues have minimal effect on Tax Ub (<xref rid="bib25" ref-type="ref">Chiari et al., 2004</xref>). Several groups have shown that ubiquitination of Tax is associated with its cytoplasmic localisation, although whether this is effectuated through promoting nuclear export or cytoplasmic retention is still controversial (discussed below).</p><p><xref rid="bib42" ref-type="ref">Gatza et al. (2007)</xref> showed that monoUb promotes the nuclear export of Tax in response to DNA damage [pathway (1) in Figure <xref rid="fig3" ref-type="fig">3</xref>]. Following UV irradiation, a rapid translocation of Tax from the nucleus to the cytoplasm was observed. The UV‐induced translocation correlates with an increase in monoUb of Tax at K280 and K284 residues. The K280/284R double mutant is not ubiquitinated and does not translocate to the cytoplasm after UV treatment. Moreover, fusing a copy of Ub to either the N‐terminal or C‐terminal of Tax to mimic monoubiquitination induces nuclear export. Interestingly, the nuclear export of the Tax–Ub fusion protein is blocked by leptomycin B (LMB), an inhibitor of CRM‐1‐dependent pathway, indicating that the Ub‐induced nuclear export of Tax is still dependent on a functional NES. The authors proposed that monoUb facilitates the dissociation of Tax from TSS in the nucleus, promoting its nuclear export (<xref rid="bib42" ref-type="ref">Gatza et al., 2007</xref>). <xref rid="bib77" ref-type="ref">Lamsoul et al. (2005)</xref> also reported that Ub favours cytoplasmic localisation of Tax. Overexpression of Ub results in increased cytoplasmic localisation of Tax, which is phenocopied by fusing one copy of Ub to the C‐terminal of the protein. Because co‐localisation between Tax and exogenously expressed Ub is observed only in the cytoplasm, the authors concluded that ubiquitination is involved in the cytoplasmic retention of Tax. However, the absence of detectable co‐localisation between Tax and Ub in the nucleus does not preclude the possibility that the ubiquitinated species are rapidly exported out of the nucleus.</p><p>Tax is also SUMOylated on lysine residues that overlap the Ub conjugation sites (<xref rid="bib77" ref-type="ref">Lamsoul et al., 2005</xref>; <xref rid="bib103" ref-type="ref">Nasr et al., 2006</xref>). Ub and SUMO seem to have opposing effects on Tax subcellular distribution. Although Ub favours cytoplasmic localisation, as discussed above, SUMO overexpression leads to predominantly nuclear body localisation. SUMOylation seems to be required for targeting Tax to nuclear bodies [pathway (2) in Figure <xref rid="fig3" ref-type="fig">3</xref>] because Ub/SUMO site mutants fail to localise to nuclear speckles, and nuclear body formation can be restored by C‐terminal fusion of SUMO but not Ub (<xref rid="bib77" ref-type="ref">Lamsoul et al., 2005</xref>). <xref rid="bib70" ref-type="ref">Kfoury et al. (2011)</xref> showed later that Ub fusion to the same K mutants can restore nuclear body localisation as well, suggesting that Ub can also target Tax to nuclear bodies [pathway (3) in Figure <xref rid="fig3" ref-type="fig">3</xref>]. The discrepancy between the two studies possibly stems from the different cell types used (293T cells in the Lamsoul paper versus HeLa cells in the Kfoury paper) because the localisation of Tax is known to be cell type dependent (<xref rid="bib6" ref-type="ref">Alefantis et al., 2003</xref>). The nuclear retention induced by SUMOylation is possibly via NES masking, in agreement with an earlier report suggesting that the Tax NES likely exists as a conditionally masked signal (<xref rid="bib6" ref-type="ref">Alefantis et al., 2003</xref>).</p><p>Despite their opposing effect on Tax localisation, Ub and SUMO are both required for NF‐κB activation. They control critical cytoplasmic and nuclear steps of NF‐κB activation, respectively. Ubiquitinated Tax binds to the IKK complex and induces its activation, leading to the degradation of IκB and nuclear translocation of Rel A, whereas SUMOylated Tax recruits Rel A to Tax nuclear bodies, promoting its complete transcriptional activation (<xref rid="bib103" ref-type="ref">Nasr et al., 2006</xref>).</p><p>Besides HTLV‐1 Tax, the nucleocytoplasmic trafficking of a few other viral proteins has also been linked to Ub and/or SUMO. Examples are listed in Table <xref rid="tbl2" ref-type="table">2</xref> and will be briefly discussed below.</p><table-wrap id="tbl2" xml:lang="en" orientation="portrait" position="float"><label>Table 2</label><caption><p>Nucleocytoplasmic trafficking of viral proteins regulated by Ub and/or SUMO</p></caption><table frame="hsides" rules="groups"><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><col style="border-right:solid 1px #000000; border-bottom:solid 1px #000000" span="1"></col><thead><tr style="border-bottom:solid 1px #000000"><th align="left" rowspan="1" colspan="1">Protein</th><th align="left" rowspan="1" colspan="1">Major functions</th><th align="left" rowspan="1" colspan="1">Ub regulation</th><th align="left" rowspan="1" colspan="1">SUMO regulation</th><th align="left" rowspan="1" colspan="1">References</th></tr></thead><tbody><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">Ad5 E1B‐55K</td><td align="left" rowspan="1" colspan="1">Viral replication, viral mRNA export, inactivation of p53</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMO is involved in targeting E1B‐55K to subnuclear structures. SUMOylation also negatively regulates nuclear export by promoting nuclear retention.</td><td align="left" rowspan="1" colspan="1"><xref rid="bib36" ref-type="ref">Endter et al., 2001</xref>; <xref rid="bib72" ref-type="ref">Kindsmüller et al., 2007</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">BPV E1</td><td align="left" rowspan="1" colspan="1">Viral replication</td><td align="left" rowspan="1" colspan="1">Free E1 is readily degraded via Ub‐mediated proteasomal degradation. It is stabilised when bound to cyclin E/Cdk2.</td><td align="left" rowspan="1" colspan="1">SUMOylation is potentially involved in nuclear import/export</td><td align="left" rowspan="1" colspan="1"><xref rid="bib117" ref-type="ref">Rangasamy et al., 2000</xref>; <xref rid="bib89" ref-type="ref">Malcles et al., 2002</xref>; <xref rid="bib120" ref-type="ref">Rosas‐Acosta and Wilson, 2008</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">EBV EBNA3C</td><td align="left" rowspan="1" colspan="1">Viral latent antigen</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1">SUMO‐3 modification might be involved in localisation to nuclear dots</td><td align="left" rowspan="1" colspan="1"><xref rid="bib121" ref-type="ref">Rosendorff et al., 2004</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">HTLV‐1 Tax</td><td align="left" rowspan="1" colspan="1">Viral replication, T‐cell transformation</td><td align="left" rowspan="1" colspan="1">In response to DNA damage, Tax is monoubiquitinated on K280 and K284, inducing nuclear export. Ub may also favour cytoplasmic localisation by promoting cytoplasmic retention.</td><td align="left" rowspan="1" colspan="1">SUMO is important for targeting Tax to nuclear bodies, and it promotes its nuclear retention</td><td align="left" rowspan="1" colspan="1"><xref rid="bib77" ref-type="ref">Lamsoul et al., 2005</xref>; <xref rid="bib42" ref-type="ref">Gatza et al., 2007</xref>; <xref rid="bib70" ref-type="ref">Kfoury et al., 2011</xref></td></tr><tr style="border-bottom:solid 1px #000000"><td align="left" rowspan="1" colspan="1">NiV Matrix</td><td align="left" rowspan="1" colspan="1">Viral assembly and budding, possible nuclear functions</td><td align="left" rowspan="1" colspan="1">Ubiquitination on a lysine residue within the NLS is important for nuclear export. Ub might also be involved in membrane targeting and budding of NiV matrix.</td><td align="left" rowspan="1" colspan="1">Not examined</td><td align="left" rowspan="1" colspan="1"><xref rid="bib148" ref-type="ref">Wang et al., 2010</xref></td></tr></tbody></table><permissions><copyright-holder>Wiley Periodicals, Inc.</copyright-holder><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions></table-wrap></sec><sec id="sec2-6"><title>DNA viruses</title><sec id="sec3-1"><title>Adenovirus type 5 E1B‐55K protein</title><p>The 55 kDa phosphoprotein encoded in early region 1B (E1B‐55K) from adenovirus type 5 (Ad5) is required for efficient viral DNA replication, selective viral late mRNA nuclear export and inactivation of the tumour suppressor protein p53 (<xref rid="bib9" ref-type="ref">Berk, 2005</xref>). E1B‐55K shuttles between the nuclear and cytoplasmic compartments. It possesses a C‐terminal NLS and an N‐terminal leucine‐rich NES (<xref rid="bib73" ref-type="ref">Krätzer et al., 2000</xref>). In addition, nucleocytoplasmic trafficking may also involve covalent conjugation of SUMO1, which appears to facilitate efficient nuclear import and/or subnuclear targeting. Overexpression of SUMO1 in transformed rat cells expressing E1B‐55K causes the accumulation of E1B‐55K at defined subnuclear structures, whereas arginine substitution of the major SUMOylation site, K104, results in a defect in nuclear import and accumulation in cytoplasmic inclusions (<xref rid="bib36" ref-type="ref">Endter et al., 2001</xref>).</p><p>SUMOylation also seems to be involved in regulating the nuclear export of E1B‐55K. The nuclear export of E1B‐55K is mediated by CRM‐1‐dependent and ‐independent pathways. Inactivation of CRM‐1‐dependent pathway by mutating the NES or LMB treatment causes redistribution of the viral protein from the cytoplasm to the nucleus and its accumulation at the viral replication centers, suggesting that CRM‐1 is a major export receptor. However, this nuclear restriction is relieved by concurrent mutation of the SUMOylation site, suggesting that deconjugation of SUMO1 allows nuclear export via CRM‐1‐independent pathways (<xref rid="bib72" ref-type="ref">Kindsmüller et al., 2007</xref>). The authors proposed that SUMO facilitates nuclear retention of E1B‐55K, thus negatively regulating nuclear export.</p></sec><sec id="sec3-2"><title>Bovine papillomavirus E1 protein</title><p>The E1 protein of papillomaviruses (PV) is the major initiator protein for viral DNA replication and plays important roles in the establishment of stable episomal viral genomes in the host cell nucleus (<xref rid="bib151" ref-type="ref">Wilson et al., 2002</xref>). Similar to E1B‐55K, the E1 protein of bovine papillomavirus (BPV) has been shown to be SUMOylated by host cell machinery, although the role of SUMOylation in the intracellular distribution of BPV E1 is controversial (see below). SUMOylation of BPV E1 is possibly mediated through the host SUMO conjugating enzyme Ubc9 and PIAS family E3 SUMO ligases (<xref rid="bib116" ref-type="ref">Rangasamy and Wilson, 2000</xref>; <xref rid="bib119" ref-type="ref">Rosas‐Acosta et al., 2005</xref>). SUMOylation on lysine residue 514 seems to be important for nuclear targeting. In transfected COS‐1 cells, although wild‐type E1 accumulates in intranuclear foci in addition to diffused nucleoplasmic distribution with little or no cytoplasmic staining, the SUMO site mutant K514R as well as the Ubc9‐binding defective mutants are unable to localise to the nucleus (<xref rid="bib116" ref-type="ref">Rangasamy and Wilson, 2000</xref>; <xref rid="bib117" ref-type="ref">Rangasamy et al., 2000</xref>). However, <xref rid="bib37" ref-type="ref">Fradet‐Turcotte et al. (2009)</xref> found that in C33A cells, the nuclear localisation of the E1 proteins of human papillomavirus (HPV) 11, HPV16 and BPV is independent of SUMOylation. These authors showed that HPV11 E1 binds to Ubc9 similar to BPV E1, as reported previously, but the nuclear accumulation of HPV11 E1 is not affected by mutations that weaken Ubc9 binding and by inhibition of the SUMO pathway using a SUMO‐activating enzyme inhibitor Gam1, a dominant negative version of Ubc9 or shRNA depletion of Ubc9 (<xref rid="bib37" ref-type="ref">Fradet‐Turcotte et al., 2009</xref>). Quite surprisingly, the authors also found that contrary to the previous report by <xref rid="bib117" ref-type="ref">Rangasamy et al. (2000)</xref>, the SUMOylation site mutants of BPV E1 are not defective in the nuclear localisation in C33A cells (<xref rid="bib37" ref-type="ref">Fradet‐Turcotte et al., 2009</xref>). Interestingly, another report by <xref rid="bib119" ref-type="ref">Rosas‐Acosta et al. (2005)</xref> suggested that SUMOylation might mediate nuclear export of BPV E1 by enhancing its interaction with CRM‐1 (<xref rid="bib120" ref-type="ref">Rosas‐Acosta and Wilson, 2008</xref>). According to this report, the non‐SUMOylatable mutant is almost exclusively nuclear and is more enriched in close proximity to the nuclear envelope as compared with the wild‐type form, supporting a role for SUMO in the intracellular distribution of BPV E1 albeit different from the one previously suggested (<xref rid="bib117" ref-type="ref">Rangasamy et al., 2000</xref>).</p></sec><sec id="sec3-3"><title>Epstein–Barr virus proteins</title><p>Epstein–Barr virus (EBV) is a human gammaherpesvirus that has been associated with a variety of cancers (<xref rid="bib29" ref-type="ref">de Oliveira et al., 2010</xref>). Multiple proteins encoded by EBV have been shown to be modified by Ub or SUMO, including Rta, Zta and Epstein–Barr virus nuclear antigen (EBNA) 3C, but a role for Ub/SUMO in regulating the cellular localisation of these proteins has not been established in most cases (see below).</p><p>Rta and Zta are two immediate early proteins that mediate the switch between the latent and lytic forms of EBV infection (<xref rid="bib139" ref-type="ref">Speck et al., 1997</xref>). SUMO‐1 modification of Rta by the E3 ligases PIAS1 and RanBPM enhances its transactivation activity, although the effect of SUMO‐1 on the subcellular localisation of Rta was not examined in these studies (<xref rid="bib20" ref-type="ref">Chang et al., 2004</xref>, <xref rid="bib21" ref-type="ref">2008</xref>). Rta can also be modified by SUMO2/3 in the presence of viral protein LF2. LF2 binding induces the translocation of Rta from the nucleus to the cytoplasm and represses its activity, but this redistribution of Rta seems to be independent of its SUMOylation (<xref rid="bib17" ref-type="ref">Calderwood et al., 2008</xref>; <xref rid="bib56" ref-type="ref">Heilmann et al., 2010</xref>). Similarly, Zta can be modified by SUMO‐1, 2 and 3, but in contrast to Rta, SUMO‐1 modification of Zta seems to repress its transactivation activity (<xref rid="bib4" ref-type="ref">Adamson and Kenney, 2001</xref>; <xref rid="bib3" ref-type="ref">Adamson, 2005</xref>; <xref rid="bib54" ref-type="ref">Hagemeier et al., 2010</xref>). SUMOylation does not seem to play a role in the subcellular localisation of Zta because its localisation pattern remains unaltered when SUMO‐1 is overexpressed or when its SUMO‐1 conjugation site is mutated (<xref rid="bib3" ref-type="ref">Adamson, 2005</xref>; <xref rid="bib54" ref-type="ref">Hagemeier et al., 2010</xref>).</p><p>EBNA3C is a viral latent antigen involved in primary B cell transformation by EBV (<xref rid="bib124" ref-type="ref">Saha et al., 2009</xref>). <xref rid="bib121" ref-type="ref">Rosendorff et al. (2004)</xref> found that EBNA3C is modified by SUMO2/3. SUMO‐3 modification might be involved in the subnuclear localisation of EBNA3C because the wild‐type protein localises to nuclear dots, whereas truncation mutants defective in SUMO‐3 conjugation exhibit diffused localisation patterns in the nucleus. However, the SUMOylation site in EBNA3C has not been pinpointed and a definitive role for SUMO‐3 in the subnuclear targeting of ENBA3C is yet to be confirmed.</p><p>LMP2A, a transmembrane protein expressed during EBV latency, was found to be ubiquitinated by Nedd4 family ubiquitin E3 ligases on amino terminal non‐lysine residues (<xref rid="bib61" ref-type="ref">Ikeda et al., 2002</xref>). This modification affects protein stability (<xref rid="bib60" ref-type="ref">Ikeda et al., 2001</xref>), but its functional relevance is not clear.</p></sec><sec id="sec3-4"><title>Immediate early proteins of other herpesviruses</title><p>Besides EBV, the immediate early proteins of a few other human herpesviruses (HHVs) have been shown to be modified by SUMO, including the K‐bZIP protein of Kaposi's sarcoma‐associated herpesvirus (KSHV) (<xref rid="bib63" ref-type="ref">Izumiya et al., 2005</xref>), the IE1 and IE2 proteins of human cytomegalovirus (HCMV) (<xref rid="bib57" ref-type="ref">Hofmann et al., 2000</xref>; <xref rid="bib5" ref-type="ref">Ahn et al., 2001</xref>, <xref rid="bib140" ref-type="ref">Spengler et al., 2002</xref>; <xref rid="bib105" ref-type="ref">Nevels et al., 2004</xref>) and the IE1 protein of human herpesvirus 6 (HHV‐6) (<xref rid="bib49" ref-type="ref">Gravel et al., 2004</xref>). SUMOylation modulates the substrate protein's transcriptional activation or repression function in some cases (<italic>e.g.</italic> KSHV K‐bZIP and HCMV IE2); however, in all cases examined, SUMO does not seem to affect the subcellular localisation of the substrate protein (<xref rid="bib57" ref-type="ref">Hofmann et al., 2000</xref>; <xref rid="bib5" ref-type="ref">Ahn et al., 2001</xref>; <xref rid="bib140" ref-type="ref">Spengler et al., 2002</xref>; <xref rid="bib105" ref-type="ref">Nevels et al., 2004</xref>; <xref rid="bib49" ref-type="ref">Gravel et al., 2004</xref>; <xref rid="bib63" ref-type="ref">Izumiya et al., 2005</xref>).</p></sec><sec id="sec3-5"><title>Negative‐stranded RNA virus</title><p>Most negative‐stranded RNA viruses replicate in the cytoplasm, and there is no nuclear stage required to complete the viral life cycle (<xref rid="bib50" ref-type="ref">Griffin et al., 2007</xref>). However, both non‐structural and structural proteins of these cytoplasmic viruses have been shown to translocate to the nuclear compartment. Examples include the matrix protein of the vesicular stomatitis virus (<xref rid="bib110" ref-type="ref">Petersen et al., 2000</xref>), the W proteins of paramyxoviruses (<xref rid="bib131" ref-type="ref">Shaw et al., 2004</xref>) and the matrix proteins of several paramyxoviruses (<xref rid="bib155" ref-type="ref">Yoshida et al., 1976</xref>; <xref rid="bib108" ref-type="ref">Peeples et al., 1992</xref>; <xref rid="bib46" ref-type="ref">Ghildyal et al., 2003</xref>). The nuclear translocation is usually associated with host antagonistic activities of these viral proteins to facilitate viral replication (<xref rid="bib110" ref-type="ref">Petersen et al., 2000</xref>; <xref rid="bib46" ref-type="ref">Ghildyal et al., 2003</xref>; <xref rid="bib130" ref-type="ref">Shaw et al., 2005</xref>).</p><p>We recently demonstrated that the matrix protein of Nipah virus (NiV), a lethal member of the family <italic>Paramyxoviridae</italic>, shuttles between the nuclear and cytoplasmic compartments (<xref rid="bib148" ref-type="ref">Wang et al., 2010</xref>). During live NiV infection, the matrix protein is first found in the nucleus of infected cells before it localises to cytoplasmic and plasma membrane locations at later time points. The nucleocytoplasmic trafficking of NiV matrix is regulated by ubiquitination in addition to its bi‐partite NLS and leucine‐rich NES (Figure <xref rid="fig4" ref-type="fig">4</xref>). Ub depletion by proteasome inhibitors including MG132 and bortezomib restricts matrix to the nucleus, which is phenocopied by mutating the putative ubiquitination site (K258) from lysine to arginine. Moreover, fusing a copy of Ub to mimic monoubiquitination restores nuclear export to the K258R mutant, supporting the hypothesis that monoubiquitination of matrix promotes its nuclear export. However, our current data are also compatible with an alternative model in which ubiquitination inhibits nuclear import of the protein, favouring cytoplasmic retention. Further investigation is needed to distinguish between these two possibilities. We also showed that nuclear translocation of NiV matrix is functionally correlated with matrix‐mediated viral budding. The ubiquitination site mutants are defective in plasma membrane targeting and viral budding, implying a potential role of ubiquitination in these processes.</p><fig fig-type="Figure" xml:lang="en" id="fig4" orientation="portrait" position="float"><label>Figure 4</label><caption><p><bold>Proposed model for NiV matrix protein (NiV M) nucleocytoplasmic trafficking</bold></p><p><named-content content-type="attribution">(1) NiV M translocates to the nucleus in an NLS‐dependent manner. (2) NiV M is ubiquitinated via an unknown mechanism. (3) Ubiquitination of M promotes its nuclear export via an NES‐dependent mechanism. Ubiquitination of M may also be important for its membrane targeting and budding, although the mechanism is currently unclear (<xref rid="bib148" ref-type="ref">Wang et al., 2010</xref>).</named-content></p></caption><p><named-content content-type="no eRights">The publisher did not receive permission from the copyright owner to include this object in this version of this product. Please refer either to the publisher's own online version of this product or the printed product where one exists.</named-content> Wiley Periodicals, Inc.</p></fig><p>Very interestingly, sequence alignment of matrix proteins from viruses across <italic>Paramyxoviridae</italic> reveals that the putative Ub site in NiV (K258) is absolutely conserved in all viruses examined (Table <xref rid="tbl3" ref-type="table">3</xref>). Previous studies as well as our own research have shown that NiV matrix is by no means the only paramyxoviral matrix protein to translocate to the nucleus. The matrix proteins of Sendai virus (<xref rid="bib155" ref-type="ref">Yoshida et al., 1976</xref>), Newcastle disease virus (<xref rid="bib107" ref-type="ref">Peeples, 1988</xref>; <xref rid="bib108" ref-type="ref">Peeples et al., 1992</xref>), human respiratory syncytial virus (<xref rid="bib46" ref-type="ref">Ghildyal et al., 2003</xref>), mumps virus, Hendra virus and tupaia paramyovirus (last three are our unpublished data) all exhibit nuclear localisation under viral infection or cell transfection conditions. It would be interesting to test whether the nucleocytoplasmic trafficking of other paramyxoviral matrix proteins might also be regulated by ubiquitination similar to NiV matrix.</p><table-wrap id="tbl3" xml:lang="en" orientation="portrait" position="float"><label>Table 3</label><caption><p>Sequence alignment of matrix proteins of different paramyxoviruses</p></caption><graphic id="nlm-graphic-11" xlink:href="BOC-104-121-g001"><permissions><copyright-holder>Wiley Periodicals, Inc.</copyright-holder><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions></graphic><table-wrap-foot><fn id="note-p-77"><p>The matrix protein sequences of 12 viruses from different genera within the family <italic>Paramyxoviridae</italic> were aligned using CLUSTAL W (version 1.83). Positively charged amino acid residues that conform to the consensus for bipartite NLSs are coloured green. The red arrow points to the lysine residue conserved amongst all 12 viruses (<xref rid="bib148" ref-type="ref">Wang et al., 2010</xref>).</p></fn></table-wrap-foot><permissions><copyright-holder>Wiley Periodicals, Inc.</copyright-holder><license><license-p>This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.</license-p></license></permissions></table-wrap></sec></sec></sec><sec id="sec1-5"><title>Conclusions and perspectives</title><p>The nucleocytoplasmic trafficking of many cellular proteins is regulated by post‐translational modifications including ubiquitination and SUMOylation in addition to their endogenous NLSs and NESs, as discussed above. However, although the role of Ub/SUMO in regulating the intracellular localisation and functions of cellular proteins has been well established, to our knowledge, their involvement in viral protein trafficking remains largely unknown, with the exception of only a few examples (<italic>e.g.</italic> HTLV‐1 Tax, Ad5 E1B‐55K, BPV E1 and NiV matrix). Nevertheless, these past few years have witnessed a fast‐growing list of viruses that utilise the host's Ub/SUMO system to facilitate various steps of their life cycle [for a complete review of viral takeover of the Ub/SUMO system, readers are referred to references <xref rid="bib14" ref-type="ref">Boggio and Chiocca (2006)</xref>; <xref rid="bib52" ref-type="ref">Gustin et al. (2011)</xref>). Therefore, targeting the Ub/SUMO system (via either global inhibition of the pathways or modulating the functions of individual components such as Ub/SUMO ligases and deubiquitinating/deSUMOylating enzymes) can potentially be a way to develop broad‐spectrum antivirals. Indeed, the US Food and Drug Administration‐approved proteasome inhibitor, bortezomib, has been shown to inhibit different families of viruses including Hepatitis B virus (<italic>Hepadnaviridae</italic>) (<xref rid="bib8" ref-type="ref">Bandi et al., 2010</xref>), HIV (<italic>Retroviridae</italic>) (<xref rid="bib156" ref-type="ref">Yu et al., 2009</xref>), vesicular stomatitis virus (<italic>Rhabdoviridae</italic>) (<xref rid="bib106" ref-type="ref">Neznanov et al., 2008</xref>; <xref rid="bib34" ref-type="ref">Dudek et al., 2010</xref>), influenza A virus (<italic>Orthomyxoviridae</italic>) (<xref rid="bib34" ref-type="ref">Dudek et al., 2010</xref>), NiV (<italic>Paramyxoviridae</italic>) (<xref rid="bib148" ref-type="ref">Wang et al., 2010</xref>), coronaviruses (<italic>Coronaviridae</italic>) (<xref rid="bib114" ref-type="ref">Raaben et al., 2010</xref>; <xref rid="bib87" ref-type="ref">Ma et al., 2010</xref>) and orthopoxviruses (<italic>Poxviridae</italic>) (<xref rid="bib144" ref-type="ref">Teale et al., 2009</xref>). However, most of these studies have been done in <italic>in vitro</italic> models, and it is important to evaluate the <italic>in vivo</italic> efficacy of bortezomib and its oral equivalents such as MLN9708 and PR‐047 (<xref rid="bib159" ref-type="ref">Zhou et al., 2009</xref>; <xref rid="bib74" ref-type="ref">Kupperman et al., 2010</xref>; <xref rid="bib32" ref-type="ref">Dick and Fleming, 2010</xref>) as potential broad‐spectrum antivirals.</p></sec><sec sec-type="COI-statement" id="sec1-6"><title>Conflict of interest statement</title><p>The authors have declared no conflict of interest.</p></sec><sec><def-list list-content="abbreviations" id="def1"><title>Abbreviations used:</title><def-item><term>Ad5</term><def><p>adenovirus type 5</p></def></def-item><def-item><term>BPV</term><def><p>bovine papillomavirus</p></def></def-item><def-item><term>CCT‐a</term><def><p>CTP–phosphocholine cytidylyltransferase</p></def></def-item><def-item><term>CREB</term><def><p>cAMP response element‐binding protein</p></def></def-item><def-item><term>CRM‐1</term><def><p>chromosome region maintenance 1</p></def></def-item><def-item><term>CtBP</term><def><p>C‐terminal binding protein of adenovirus E1A</p></def></def-item><def-item><term>EBNA</term><def><p>Epstein–Barr virus nuclear antigen</p></def></def-item><def-item><term>EBV</term><def><p>Epstein–Barr virus</p></def></def-item><def-item><term>ESCRT</term><def><p>endosomal sorting complex required for transport</p></def></def-item><def-item><term>HCMV</term><def><p>human cytomegalovirus</p></def></def-item><def-item><term>HHV‐6</term><def><p>human herpesvirus 6</p></def></def-item><def-item><term>HIF‐a</term><def><p>hypoxia inducible factor alpha</p></def></def-item><def-item><term>HPV</term><def><p>human papillomavirus</p></def></def-item><def-item><term>HTLV‐1</term><def><p>human T‐cell leukaemia virus type 1</p></def></def-item><def-item><term>IGF‐1R</term><def><p>insulin‐like growth factor 1 receptor</p></def></def-item><def-item><term>IKK</term><def><p>IkB kinase</p></def></def-item><def-item><term>IkBa</term><def><p>inhibitor of NF‐kB alpha</p></def></def-item><def-item><term>KLF5</term><def><p>Krüppel‐like factor 5</p></def></def-item><def-item><term>KSHV</term><def><p>Kaposi's sarcoma‐associated herpesvirus</p></def></def-item><def-item><term>LMB</term><def><p>leptomycin B</p></def></def-item><def-item><term>NEMO</term><def><p>NF‐kB essential modulator</p></def></def-item><def-item><term>NES</term><def><p>nuclear export signal</p></def></def-item><def-item><term>NiV</term><def><p>Nipah virus</p></def></def-item><def-item><term>NLS</term><def><p>nuclear localisation signal</p></def></def-item><def-item><term>PIAS</term><def><p>protein inhibitor of activated STAT</p></def></def-item><def-item><term>PML</term><def><p>promyelocytic leukaemia protein</p></def></def-item><def-item><term>PTEN</term><def><p>phosphatase and tensin homolog on chromosome 10</p></def></def-item><def-item><term>RanGAP1</term><def><p>Ran GTPase‐activating protein 1</p></def></def-item><def-item><term>RARA</term><def><p>retinoic acid receptor alpha</p></def></def-item><def-item><term>Smad3</term><def><p>Sma‐ and MAD‐related protein 3</p></def></def-item><def-item><term>STUbL</term><def><p>SUMO‐targeted ubiquitin ligase</p></def></def-item><def-item><term>SUMO</term><def><p>small ubiquitin‐related modifier</p></def></def-item><def-item><term>TSS</term><def><p>Tax speckled structure</p></def></def-item><def-item><term>Ub</term><def><p>ubiquitin</p></def></def-item><def-item><term>VHL</term><def><p>von Hippel–Lindau protein</p></def></def-item></def-list></sec></body><back><ack id="sec1-ack-1"><title>Acknowledgements</title><p>This work was supported by the Pacific Southwest Regional Center of Excellence for Biodefense and Emerging Infectious Diseases [U54 AI065359] and National Institutes of Health grant to B.L. 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