A Golgi-associated redox switch regulates catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I
Identifieur interne : 000798 ( Pmc/Curation ); précédent : 000797; suivant : 000799A Golgi-associated redox switch regulates catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I
Auteurs : Antti Hassinen [Finlande] ; Fawzi Khoder-Agha [Finlande] ; Elham Khosrowabadi [Finlande] ; Daniela Mennerich [Finlande] ; Deborah Harrus [Finlande] ; Maxence Noel [France] ; Elitsa Y. Dimova [Finlande] ; Tuomo Glumoff [Finlande] ; Anne Harduin-Lepers [France] ; Thomas Kietzmann [Finlande] ; Sakari Kellokumpu [Finlande]Source :
- Redox Biology [ 2213-2317 ] ; 2019.
Abstract
Glycosylation, a common modification of cellular proteins and lipids, is often altered in diseases and pathophysiological states such as hypoxia, yet the underlying molecular causes remain poorly understood. By utilizing lectin microarray glycan profiling, Golgi pH and redox screens, we show here that hypoxia inhibits terminal sialylation of N- and O-linked glycans in a HIF- independent manner by lowering Golgi oxidative potential. This redox state change was accompanied by loss of two surface-exposed disulfide bonds in the catalytic domain of the α-2,6-sialyltransferase (ST6Gal-I) and its ability to functionally interact with B4GalT-I, an enzyme adding the preceding galactose to complex N-glycans. Mutagenesis of selected cysteine residues in ST6Gal-I mimicked these effects, and also rendered the enzyme inactive. Cells expressing the inactive mutant, but not those expressing the wild type ST6Gal-I, were able to proliferate and migrate normally, supporting the view that inactivation of the ST6Gal-I help cells to adapt to hypoxic environment. Structure comparisons revealed similar disulfide bonds also in ST3Gal-I, suggesting that this O-glycan and glycolipid modifying sialyltransferase is also sensitive to hypoxia and thereby contribute to attenuated sialylation of O-linked glycans in hypoxic cells. Collectively, these findings unveil a previously unknown redox switch in the Golgi apparatus that is responsible for the catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I.
Url:
DOI: 10.1016/j.redox.2019.101182
PubMed: 30959459
PubMed Central: 6454061
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<front><div type="abstract" xml:lang="en"><p>Glycosylation, a common modification of cellular proteins and lipids, is often altered in diseases and pathophysiological states such as hypoxia, yet the underlying molecular causes remain poorly understood. By utilizing lectin microarray glycan profiling, Golgi pH and redox screens, we show here that hypoxia inhibits terminal sialylation of N- and O-linked glycans in a HIF- independent manner by lowering Golgi oxidative potential. This redox state change was accompanied by loss of two surface-exposed disulfide bonds in the catalytic domain of the α-2,6-sialyltransferase (ST6Gal-I) and its ability to functionally interact with B4GalT-I, an enzyme adding the preceding galactose to complex N-glycans. Mutagenesis of selected cysteine residues in ST6Gal-I mimicked these effects, and also rendered the enzyme inactive. Cells expressing the inactive mutant, but not those expressing the wild type ST6Gal-I, were able to proliferate and migrate normally, supporting the view that inactivation of the ST6Gal-I help cells to adapt to hypoxic environment. Structure comparisons revealed similar disulfide bonds also in ST3Gal-I, suggesting that this O-glycan and glycolipid modifying sialyltransferase is also sensitive to hypoxia and thereby contribute to attenuated sialylation of O-linked glycans in hypoxic cells. Collectively, these findings unveil a previously unknown redox switch in the Golgi apparatus that is responsible for the catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Redox Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">Redox Biol</journal-id>
<journal-title-group><journal-title>Redox Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">2213-2317</issn>
<publisher><publisher-name>Elsevier</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">30959459</article-id>
<article-id pub-id-type="pmc">6454061</article-id>
<article-id pub-id-type="publisher-id">S2213-2317(19)30198-3</article-id>
<article-id pub-id-type="doi">10.1016/j.redox.2019.101182</article-id>
<article-id pub-id-type="publisher-id">101182</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Paper</subject>
</subj-group>
</article-categories>
<title-group><article-title>A Golgi-associated redox switch regulates catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Hassinen</surname>
<given-names>Antti</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="fn1" ref-type="fn">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Khoder-Agha</surname>
<given-names>Fawzi</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Khosrowabadi</surname>
<given-names>Elham</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mennerich</surname>
<given-names>Daniela</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harrus</surname>
<given-names>Deborah</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Noel</surname>
<given-names>Maxence</given-names>
</name>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dimova</surname>
<given-names>Elitsa Y.</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Glumoff</surname>
<given-names>Tuomo</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harduin-Lepers</surname>
<given-names>Anne</given-names>
</name>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kietzmann</surname>
<given-names>Thomas</given-names>
</name>
<xref rid="aff1" ref-type="aff">a</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kellokumpu</surname>
<given-names>Sakari</given-names>
</name>
<email>sakari.kellokumpu@oulu.fi</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>a</label>
University of Oulu, Faculty of Biochemistry and Molecular Medicine, Oulu, Finland</aff>
<aff id="aff2"><label>b</label>
Université de Lille, CNRS, UMR 8576, UGSF - Unité de Glycobiologie Structurale et Fonctionnelle, F-59000 Lille, France</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Corresponding author. University of Oulu, Faculty of Biochemistry and Molecular Medicine, PO Box 5400, FI-90014, Oulun Yliopisto, Oulu, Finland. <email>sakari.kellokumpu@oulu.fi</email>
</corresp>
<fn id="fn1"><label>1</label>
<p id="ntpara0010">Current address: Institute of Molecular Medicine, Helsinki, Finland.</p>
</fn>
</author-notes>
<pub-date pub-type="pmc-release"><day>04</day>
<month>4</month>
<year>2019</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="collection"><month>6</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="epub"><day>04</day>
<month>4</month>
<year>2019</year>
</pub-date>
<volume>24</volume>
<elocation-id>101182</elocation-id>
<history><date date-type="received"><day>11</day>
<month>2</month>
<year>2019</year>
</date>
<date date-type="rev-recd"><day>22</day>
<month>3</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>28</day>
<month>3</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 The Authors</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="CC BY" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).</license-p>
</license>
</permissions>
<abstract id="abs0010"><p>Glycosylation, a common modification of cellular proteins and lipids, is often altered in diseases and pathophysiological states such as hypoxia, yet the underlying molecular causes remain poorly understood. By utilizing lectin microarray glycan profiling, Golgi pH and redox screens, we show here that hypoxia inhibits terminal sialylation of N- and O-linked glycans in a HIF- independent manner by lowering Golgi oxidative potential. This redox state change was accompanied by loss of two surface-exposed disulfide bonds in the catalytic domain of the α-2,6-sialyltransferase (ST6Gal-I) and its ability to functionally interact with B4GalT-I, an enzyme adding the preceding galactose to complex N-glycans. Mutagenesis of selected cysteine residues in ST6Gal-I mimicked these effects, and also rendered the enzyme inactive. Cells expressing the inactive mutant, but not those expressing the wild type ST6Gal-I, were able to proliferate and migrate normally, supporting the view that inactivation of the ST6Gal-I help cells to adapt to hypoxic environment. Structure comparisons revealed similar disulfide bonds also in ST3Gal-I, suggesting that this O-glycan and glycolipid modifying sialyltransferase is also sensitive to hypoxia and thereby contribute to attenuated sialylation of O-linked glycans in hypoxic cells. Collectively, these findings unveil a previously unknown redox switch in the Golgi apparatus that is responsible for the catalytic activation and cooperative functioning of ST6Gal-I with B4GalT-I.</p>
</abstract>
<abstract abstract-type="graphical" id="abs0015"><title>Graphical abstract</title>
<p><fig id="undfig1" position="anchor"><alt-text id="alttext0010">Image 1</alt-text>
<graphic xlink:href="fx1"></graphic>
</fig>
</p>
</abstract>
<kwd-group id="kwrds0010"><title>Keywords</title>
<kwd>Hypoxia</kwd>
<kwd>Glycosylation</kwd>
<kwd>Golgi homeostasis</kwd>
<kwd>Redox state</kwd>
<kwd>Sialyltransferase</kwd>
</kwd-group>
</article-meta>
</front>
</pmc>
</record>
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