Novel replisome-associated proteins at cellular replication forks in EBV-transformed B lymphocytes
Identifieur interne : 000580 ( Main/Exploration ); précédent : 000579; suivant : 000581Novel replisome-associated proteins at cellular replication forks in EBV-transformed B lymphocytes
Auteurs : Huanzhou Xu [États-Unis] ; Ramon D. Perez ; Tiffany R. Frey [États-Unis] ; Eric M. Burton [États-Unis] ; Sudha Mannemuddhu [États-Unis] ; John D. Haley [États-Unis] ; Michael T. Mcintosh [États-Unis] ; Sumita Bhaduri-Mcintosh [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2019.
Abstract
Epstein-Barr virus (EBV) is an oncogenic herpesvirus and WHO class 1 carcinogen that resides in B lymphocytes of nearly all humans. While silent in most, EBV can cause endemic Burkitt lymphoma in children and post-transplant lymphoproliferative disorders/lymphomas in immunocompromised hosts. The pathogenesis of such lymphomas is multifactorial but to a large extent depends on EBV’s ability to aggressively drive cellular DNA replication and B cell proliferation despite cell-intrinsic barriers to replication. One such barrier is oncogenic replication stress which hinders the progression of DNA replication forks. To understand how EBV successfully overcomes replication stress, we examined cellular replication forks in EBV-transformed B cells using iPOND (isolation of Proteins on Nascent DNA)-mass spectrometry and identified several cellular proteins that had not previously been linked to DNA replication. Of eight candidate replisome-associated proteins that we validated at forks in EBV-transformed cells and Burkitt lymphoma-derived cells, three zinc finger proteins (ZFPs) were upregulated early in B cells newly-infected with EBV in culture as well as expressed at high levels in EBV-infected B blasts in the blood of immunocompromised transplant recipients. Expressed highly in S- and G2-phase cells, knockdown of each ZFP resulted in stalling of proliferating cells in the S-phase, cleavage of caspase 3, and cell death. These proteins, newly-identified at replication forks of EBV-transformed and Burkitt lymphoma cells therefore contribute to cell survival and cell cycle progression, and represent novel targets for intervention of EBV-lymphomas while simultaneously offering a window into how the replication machinery may be similarly modified in other cancers.
Url:
DOI: 10.1371/journal.ppat.1008228
PubMed: 31841561
PubMed Central: 6936862
Affiliations:
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Mcintosh</name><affiliation wicri:level="2"><nlm:aff id="aff005"><addr-line>Child Health Research Institute, Department of Pediatrics and of Molecular Genetics and Microbiology, University of Florida, Gainesville, Florida, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Child Health Research Institute, Department of Pediatrics and of Molecular Genetics and Microbiology, University of Florida, Gainesville, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Bhaduri Mcintosh, Sumita" sort="Bhaduri Mcintosh, Sumita" uniqKey="Bhaduri Mcintosh S" first="Sumita" last="Bhaduri-Mcintosh">Sumita Bhaduri-Mcintosh</name><affiliation wicri:level="2"><nlm:aff id="aff006"><addr-line>Division of Infectious Disease, Departments of Pediatrics and of Molecular Genetics and Microbiology, University of Florida, Gainesville, Florida, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Infectious Disease, Departments of Pediatrics and of Molecular Genetics and Microbiology, University of Florida, Gainesville, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Epstein-Barr virus (EBV) is an oncogenic herpesvirus and WHO class 1 carcinogen that resides in B lymphocytes of nearly all humans. While silent in most, EBV can cause endemic Burkitt lymphoma in children and post-transplant lymphoproliferative disorders/lymphomas in immunocompromised hosts. The pathogenesis of such lymphomas is multifactorial but to a large extent depends on EBV’s ability to aggressively drive cellular DNA replication and B cell proliferation despite cell-intrinsic barriers to replication. One such barrier is oncogenic replication stress which hinders the progression of DNA replication forks. To understand how EBV successfully overcomes replication stress, we examined cellular replication forks in EBV-transformed B cells using iPOND (isolation of Proteins on Nascent DNA)-mass spectrometry and identified several cellular proteins that had not previously been linked to DNA replication. Of eight candidate replisome-associated proteins that we validated at forks in EBV-transformed cells and Burkitt lymphoma-derived cells, three zinc finger proteins (ZFPs) were upregulated early in B cells newly-infected with EBV in culture as well as expressed at high levels in EBV-infected B blasts in the blood of immunocompromised transplant recipients. Expressed highly in S- and G2-phase cells, knockdown of each ZFP resulted in stalling of proliferating cells in the S-phase, cleavage of caspase 3, and cell death. These proteins, newly-identified at replication forks of EBV-transformed and Burkitt lymphoma cells therefore contribute to cell survival and cell cycle progression, and represent novel targets for intervention of EBV-lymphomas while simultaneously offering a window into how the replication machinery may be similarly modified in other cancers.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Gottschalk, S" uniqKey="Gottschalk S">S Gottschalk</name></author><author><name sortKey="Rooney, Cm" uniqKey="Rooney C">CM Rooney</name></author><author><name sortKey="Heslop, He" uniqKey="Heslop H">HE Heslop</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Allen, Ud" uniqKey="Allen U">UD Allen</name></author><author><name sortKey="Preiksaitis, Jk" uniqKey="Preiksaitis J">JK Preiksaitis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Crombie, Jl" uniqKey="Crombie J">JL 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Perez</name></noCountry><country name="États-Unis"><region name="Floride"><name sortKey="Xu, Huanzhou" sort="Xu, Huanzhou" uniqKey="Xu H" first="Huanzhou" last="Xu">Huanzhou Xu</name></region><name sortKey="Bhaduri Mcintosh, Sumita" sort="Bhaduri Mcintosh, Sumita" uniqKey="Bhaduri Mcintosh S" first="Sumita" last="Bhaduri-Mcintosh">Sumita Bhaduri-Mcintosh</name><name sortKey="Burton, Eric M" sort="Burton, Eric M" uniqKey="Burton E" first="Eric M." last="Burton">Eric M. Burton</name><name sortKey="Frey, Tiffany R" sort="Frey, Tiffany R" uniqKey="Frey T" first="Tiffany R." last="Frey">Tiffany R. Frey</name><name sortKey="Haley, John D" sort="Haley, John D" uniqKey="Haley J" first="John D." last="Haley">John D. Haley</name><name sortKey="Mannemuddhu, Sudha" sort="Mannemuddhu, Sudha" uniqKey="Mannemuddhu S" first="Sudha" last="Mannemuddhu">Sudha Mannemuddhu</name><name sortKey="Mcintosh, Michael T" sort="Mcintosh, Michael T" uniqKey="Mcintosh M" first="Michael T." last="Mcintosh">Michael T. Mcintosh</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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