HIV-1 Nef蛋白最新功能及其增强病毒感染性分子机理的研究进展
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摘要
Nef蛋白是人类免疫缺陷病毒Ⅰ型(HIV-1)及其他灵长类动物慢病毒编码的一种附属蛋白,在获得性免疫缺陷综合症(AIDS)疾病进程和病毒的复制过程中起着重要作用。抑制附属蛋白活性的策略可以改善传统抗逆转录病毒方案的疗效,因此深入理解这一附属蛋白的功能和其分子作用机制具有重要意义。Nef蛋白通过三个主要活性调节宿主细胞环境,增强病毒复制。下调细胞表面分子如CD4,MHC-Ⅰ,MHC-Ⅱ等的表达,使病毒逃逸宿主的免疫应答;通过调节T细胞的信号通路降低T细胞的活化,从而营造有利于病毒复制的环境;直接增强新生子代病毒粒子的感染性。这一功能的分子机制直到最近宿主限制性因子丝氨酸转运蛋白(SERINC5)的发现才得以明晰。本文总结了Nef的功能及其增强病毒感染性的最新研究进展,同时也归纳了SERINC5蛋白与Nef蛋白的相互作用的研究报道,为深入了解病毒复制机理,改善HIV-1防治方案提供新的理论线索。
Nef is an auxiliary protein of lentiviruses.It is encoded by nef within the genomes of the primate lentiviruses human immunodeficiency virus(HIV)-1,HIV-2 and Simian immunodeficiency virus(SIV).This protein is required for the maintenance of high viral load and disease progression,such as acquired immune deficiency syndrome(AIDS).Updated knowledge of the mechanism(s)of Nef could lead to novel anti-retroviral strategies to prevent/delay HIV pathogenesis.Nef is a multifunctional protein that regulates the environment of host cells and enhances the replication of virions through various mechanisms:Nef downmodulates the surface levels of important molecules,such as cluster of differentiation-4,major histocompatibility complex(MHC)-Ⅰ and MHC-Ⅱ,to escape the host′s immune response;Nef can alter T-cell activation,and favor preliminary virus replication before massive stimulation following exposure to mitogens;Nef enhances the intrinsic infectivity of progeny virions through a mechanism involving the novel host restriction factor SERINC3/5.Here,we review the current knowledge surrounding Nef activities and discuss how Nef enhances the infectivity of HIV-1 virions.
Nef is an auxiliary protein of lentiviruses.It is encoded by nef within the genomes of the primate lentiviruses human immunodeficiency virus(HIV)-1,HIV-2 and Simian immunodeficiency virus(SIV).This protein is required for the maintenance of high viral load and disease progression,such as acquired immune deficiency syndrome(AIDS).Updated knowledge of the mechanism(s)of Nef could lead to novel anti-retroviral strategies to prevent/delay HIV pathogenesis.Nef is a multifunctional protein that regulates the environment of host cells and enhances the replication of virions through various mechanisms:Nef downmodulates the surface levels of important molecules,such as cluster of differentiation-4,major histocompatibility complex(MHC)-Ⅰ and MHC-Ⅱ,to escape the host′s immune response;Nef can alter T-cell activation,and favor preliminary virus replication before massive stimulation following exposure to mitogens;Nef enhances the intrinsic infectivity of progeny virions through a mechanism involving the novel host restriction factor SERINC3/5.Here,we review the current knowledge surrounding Nef activities and discuss how Nef enhances the infectivity of HIV-1 virions.
引文
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[5]Arold S,Franken P,Benarous R.The crystal structure of HIV-1Nef protein bound to the Fyn kinase SH3domain suggests a role for this complex in altered T cell receptor signaling[J].Structure,1997,5:1361-1372.
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[11]Shen Q T,Ren X,Zhang R,Lee IH,Hurley J H.HIV-1Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons[J].Science,2015,350(6259):paac5137.
[12]daSilva L L,Sougrat R,Burgos P V,Janvier K,Mattera R,Bonifacino J S.Human immunodeficiency virus type 1 Nef protein targets CD4to the multivesicular body pathway[J].J Virol,2009,83:6578-6590.
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[14]Stolp B,Reichman-Fried M,Abraham L,Pan X,Giese S I,Hannemann S,Goulimari P,Raz E,Grosse R,Fackler O T.HIV-1 Nef interferes with host cell motility by deregulation of Cofilin[J].Cell Host Microbe,2009,6(2):174-186.
[15]Pereira,E A,daSilva L L.HIV-1Nef:Taking control of protein trafficking[J].Traffic,2016,17(9):976-996.
[16]Amorim N A,daSilva E M,de Castro R O,daSilvaJanuário M E,Mendon9a L M,Bonifacino J S,daCosta L J,daSilva L L.Interaction of HIV-1Nef protein with the host protein Alix promotes lysosomal targeting of CD4receptor[J].J Biol Chem,2014,289(40):27744-27756.
[17]Schaefer M R,Wonderlich E R,Roeth J F,Leonard J A,Collins K L.HIV-1 Nef targets MHC-I and CD4for degradation via a final common beta-COP-dependent pathway in T cells[J/OL].PLoS Pathog,2008,4(8):e1000131.
[18]Dirk B S,Pawlak E N,Johnson A L,Van Nynatten L R,Jacob R A,Heit B,Dikeakos J D.HIV-1Nef sequesters MHC-I intracellularly by targeting early stages of endocytosis and recycling[J].Sci Rep,2016,6:37021.
[19]Schindler M,Wildum S,Casartelli N,Doria M,Kirchhoff F.Nef alleles from children with non-progressive HIV-1infection modulate MHC-II expression more efficiently than those from rapid progressors[J].AIDS,2007,21(9):1103-1107.
[20]Geyer M,Fackler O T,Peterlin B M.Structure--function relationships in HIV-1Nef[J].EMBO Rep,2001,2(7):580-585.
[21]Ren X,Park S Y,Bonifacino J S,Hurley J H.How HIV-1Nef hijacks the AP-2clathrin adaptor to downregulate CD4[J/OL].Elife,2014,3:e01754.
[22]Foster J L,Denial S J,Temple B R,Garcia J V.Mechanisms of HIV-1 Nef function and intracellular signaling[J].J Neuroimmune Pharmacol,2011,6:230-246.
[23]Abraham L,Fackler O T.HIV-1Nef:a multifaceted modulator of T cell receptor signaling[J].Cell Commun Signal 2012,10(1):39.
[24]Saxena S K,Shrivastava G,Tiwari S,Swamy M A,Nair M P.Modulation of HIV pathogenesis and T-cell signaling by HIV-1Nef[J].Future Virol,2012,7(6):609-620.
[25]Markle T J,Philip M,Brockman M A.HIV-1Nef and T-cell activation:a history of contradictions[J].Future Virol,2013,8(4):10.2217
[26]Li C1,Wang H B,Kuang W D,Ren X X,Song S T,Zhu H Z,Li Q,Xu L R,Guo H J,Wu L,Wang J H.Naf1regulates HIV-1latency by suppressing viral promoter-driven gene expression in primary CD4+T cells[J].J Virol,2017,91(1):e01830-16.
[27]Chowers M Y,Spina C A,Kwoh T J,Fitch N J,Richman D D,Guatelli J C.Optimal infectivity in vitro of human immunodeficiency virus type 1requires an intact nef gene[J].J Virol,1994,68:2906-2914.
[28]Tokunaga K,Kojima A,Kurata T,Ikuta K,Akari H,Koyama A H,Kawamura M,Inubushi R,Shimano R,Adachi A.Enhancement of human immunodeficiency virus type 1infectivity by Nef is producer cell-dependent[J].J Gen Virol,1998,79(Pt 10):2447-2453.
[29]Schiavoni I,Trapp S,Santarcangelo A C,Piacentini V,Pugliese K,Baur A,Federico M.HIV-1 Nef enhances both membrane expression and virion incorporation of Env products.A model for the Nef-dependent increase of HIV-1infectivity[J].J Biol Chem,2004,279:22996-23006.
[30]Qi M,Aiken C.Nef enhances HIV-1infectivity via association with the virus assembly complex[J].Virology,2008,373:287-297.
[31]Zheng Y H,Plemenitas A,Linnemann T,Fackler O T,Peterlin B M.Nef increases infectivity of HIV via lipid rafts[J].Curr Biol,2001,11:875-879.
[32]Zheng Y H,Plemenitas A,Fielding C J,Peterlin B M.Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1progeny virions[J].Proc Natl Acad Sci USA,2003,100:8460-8465.
[33]Brügger B,Krautkramer E,Tibroni N,Munte C E,Rauch S,Leibrecht I,Glass B,Breuer S,Geyer M,Krausslich H G,Kalbitzer H R,Wieland F T,Fackler O T.Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains[J].Retrovirology,2007,4:70.
[34]Pizzato M,Helander A,Popova E,Calistri A,Zamborlini A,PalùG,G9ttlinger H G.Dynamin 2is required for the enhancement of HIV-1infectivity by Nef[J].Proc Natl Acad Sci USA,2007,104:6812-6817.
[35]Usami Y,Wu Y,Gottlinger H G.SERINC3 and SERINC5restrict HIV-1infectivity and are counteracted by Nef[J].Nature,2015,526:218-223.
[36]Rosa A,Chande A,Ziglio S,De Sanctis V,Bertorelli R,Goh S L,McCauley S M,Nowosielska A,Antonarakis S E,Luban J,Santoni F A,Pizzato M.HIV-1Nef promotes infection by excluding SERINC5from virion incorporation[J].Nature,2015,526:212-217.
[37]Inuzuka M,Hayakawa M,Ingi T.Serinc,an activityregulated protein family,incorporates serine into membrane lipid synthesis[J].J Biol Chem,2005,280:35776-35783.
[38]Chu E P,Elso C M,Pollock A H,Alsayb M A,Mackin L,Thomas H E,Kay T W,Silveira PA,Mansell A S,Gaus K,Brodnicki T C.Disruption of Serinc1,which facilitates serine-derived lipid synthesis,fails to alter macrophage function,lymphocyte proliferation or autoimmune disease susceptibility[J].Mol Immunol,2017,82:19-33.
[39]Fackler O T.Spotlight on HIV-1 Nef:SERINC3and SERINC5identified as restriction factors antagonized by the pathogenesis factor[J].Viruses,2015,7:6730-6738.
[40]Ahi YS,Zhang S,Thappeta Y,Denman A,Feizpour A,Gummuluru S,Reinhard B,Muriaux D,Fivash MJ,Rein A.Functional interplay between Murine Leukemia Virus glycogag,Serinc5,and surface glycoprotein governs virus entry,with opposite effects on Gamma retroviral and Ebolavirus glycoproteins[J/OL].mBio,2016,7(6).pii:e01985-16.
[41]Sood C,Marin M,Chande A,Pizzato M,Melikyan G B.SERINC5protein inhibits HIV-1fusion pore formation by promoting functional inactivation of envelope glycoproteins[J].J Biol Chem,2017,292(14):6014-6026.
[42]Usami Y,Popov S,Gottlinger H G.The Nef-like effect of murine leukemia virus glycosylated gag on HIV-1infectivity is mediated by its cytoplasmic domain and depends on the AP-2adaptor complex[J].J Virol,2014,88:3443-3454.
[43]Chande A,Cuccurullo E C,Rosa A,Ziglio S,Carpenter S,Pizzato M.S2from equine infectious anemia virus is an infectivity factor which counteracts the retroviral inhibitors SERINC5and SERINC3[J].Proc Natl Acad Sci USA,2016,113:13197-13202.
[44]Beitari S,Ding S,Pan Q,Finzi A,Liang C.The effect of HIV-1Env on SERINC5antagonism[J/OL].J Virol,2016,91(4):e02214-2216.
[2]Luciw P A,Cheng-Mayer C,Levy J A.Mutational analysis of the human immunodeficiency virus:the orf-B region down-regulates virus replication[J].Proc Natl Acad Sci USA,1987,84(5):1434-1438.
[3]Kestler H W,Ringler D J,Mori K,Panicali D L,Sehgal P K,Daniel M D,Desrosiers R C.Importance of the nef gene for maintenance of high virus loads and for development of AIDS[J].Cell,1991,65(4):651-662.
[4]Basmaciogullari S,Pizzato M.The activity of Nef on HIV-1infectivity[J].Front Microbiol,2014,5:232.
[5]Arold S,Franken P,Benarous R.The crystal structure of HIV-1Nef protein bound to the Fyn kinase SH3domain suggests a role for this complex in altered T cell receptor signaling[J].Structure,1997,5:1361-1372.
[6]Jager S,Cimermancic P,Gulbahce N,Johnson J R,McGovern K E,Clarke S C,Shales M,Mercenne G,Pache L,Li K,Hernandez H,Jang G M,Roth S L,Akiva E,Marlett J,Stephens M,D′Orso I,Fernandes J,Fahey M,Mahon C,O′Donoghue A J,Todorovic A,Morris J H,Maltby D A,Alber T,Cagney G,Bushman F D,Young J A,Chanda S K,Sundquist W I,Kortemme T,Hernandez R D,Craik C S,Burlingame A,Sali A,Frankel A D,Krogan N J.Global landscape of HIV-human protein complexes[J].Nature,2011,481(7381):365-370.
[7]Bentham M,Mazaleyrat S,Harris M.Role of myristoylation and N-terminal basic residues in membrane association of the human immunodeficiency virus type 1 Nef protein[J].J Gen Virol,2006,87:563-571.
[8]Arold S,Hoh F,Domergue S,Birck C,Delsuc M A,Jullien M,Dumas C.Characterization and molecular basis of the oligomeric structure of HIV-1nef protein[J].Protein Sci,2000,9:1137-1148.
[9]Van den Broeke C,Radu M,Chernoff J,Favoreel H W.An emerging role for p21-activated kinases(Paks)in viral infections[J].Trends Cell Biol,2010,20(3):160-169.
[10]Wonderlich E R,Leonard J A,Collins K L.HIV immune evasion disruption of antigen presentation by the HIV Nef protein[J].Adv Virus Res,2011,80:103-127.
[11]Shen Q T,Ren X,Zhang R,Lee IH,Hurley J H.HIV-1Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons[J].Science,2015,350(6259):paac5137.
[12]daSilva L L,Sougrat R,Burgos P V,Janvier K,Mattera R,Bonifacino J S.Human immunodeficiency virus type 1 Nef protein targets CD4to the multivesicular body pathway[J].J Virol,2009,83:6578-6590.
[13]Trautz B,Pierini V,Wombacher R,Stolp B,Chase A J,Pizzato M,Fackler O T.The antagonism of HIV-1Nef to SERINC5particle infectivity restriction involves the counteraction of virion-associated pools of the restriction factor[J].J Virol,2016,90(23):10915-10927.
[14]Stolp B,Reichman-Fried M,Abraham L,Pan X,Giese S I,Hannemann S,Goulimari P,Raz E,Grosse R,Fackler O T.HIV-1 Nef interferes with host cell motility by deregulation of Cofilin[J].Cell Host Microbe,2009,6(2):174-186.
[15]Pereira,E A,daSilva L L.HIV-1Nef:Taking control of protein trafficking[J].Traffic,2016,17(9):976-996.
[16]Amorim N A,daSilva E M,de Castro R O,daSilvaJanuário M E,Mendon9a L M,Bonifacino J S,daCosta L J,daSilva L L.Interaction of HIV-1Nef protein with the host protein Alix promotes lysosomal targeting of CD4receptor[J].J Biol Chem,2014,289(40):27744-27756.
[17]Schaefer M R,Wonderlich E R,Roeth J F,Leonard J A,Collins K L.HIV-1 Nef targets MHC-I and CD4for degradation via a final common beta-COP-dependent pathway in T cells[J/OL].PLoS Pathog,2008,4(8):e1000131.
[18]Dirk B S,Pawlak E N,Johnson A L,Van Nynatten L R,Jacob R A,Heit B,Dikeakos J D.HIV-1Nef sequesters MHC-I intracellularly by targeting early stages of endocytosis and recycling[J].Sci Rep,2016,6:37021.
[19]Schindler M,Wildum S,Casartelli N,Doria M,Kirchhoff F.Nef alleles from children with non-progressive HIV-1infection modulate MHC-II expression more efficiently than those from rapid progressors[J].AIDS,2007,21(9):1103-1107.
[20]Geyer M,Fackler O T,Peterlin B M.Structure--function relationships in HIV-1Nef[J].EMBO Rep,2001,2(7):580-585.
[21]Ren X,Park S Y,Bonifacino J S,Hurley J H.How HIV-1Nef hijacks the AP-2clathrin adaptor to downregulate CD4[J/OL].Elife,2014,3:e01754.
[22]Foster J L,Denial S J,Temple B R,Garcia J V.Mechanisms of HIV-1 Nef function and intracellular signaling[J].J Neuroimmune Pharmacol,2011,6:230-246.
[23]Abraham L,Fackler O T.HIV-1Nef:a multifaceted modulator of T cell receptor signaling[J].Cell Commun Signal 2012,10(1):39.
[24]Saxena S K,Shrivastava G,Tiwari S,Swamy M A,Nair M P.Modulation of HIV pathogenesis and T-cell signaling by HIV-1Nef[J].Future Virol,2012,7(6):609-620.
[25]Markle T J,Philip M,Brockman M A.HIV-1Nef and T-cell activation:a history of contradictions[J].Future Virol,2013,8(4):10.2217
[26]Li C1,Wang H B,Kuang W D,Ren X X,Song S T,Zhu H Z,Li Q,Xu L R,Guo H J,Wu L,Wang J H.Naf1regulates HIV-1latency by suppressing viral promoter-driven gene expression in primary CD4+T cells[J].J Virol,2017,91(1):e01830-16.
[27]Chowers M Y,Spina C A,Kwoh T J,Fitch N J,Richman D D,Guatelli J C.Optimal infectivity in vitro of human immunodeficiency virus type 1requires an intact nef gene[J].J Virol,1994,68:2906-2914.
[28]Tokunaga K,Kojima A,Kurata T,Ikuta K,Akari H,Koyama A H,Kawamura M,Inubushi R,Shimano R,Adachi A.Enhancement of human immunodeficiency virus type 1infectivity by Nef is producer cell-dependent[J].J Gen Virol,1998,79(Pt 10):2447-2453.
[29]Schiavoni I,Trapp S,Santarcangelo A C,Piacentini V,Pugliese K,Baur A,Federico M.HIV-1 Nef enhances both membrane expression and virion incorporation of Env products.A model for the Nef-dependent increase of HIV-1infectivity[J].J Biol Chem,2004,279:22996-23006.
[30]Qi M,Aiken C.Nef enhances HIV-1infectivity via association with the virus assembly complex[J].Virology,2008,373:287-297.
[31]Zheng Y H,Plemenitas A,Linnemann T,Fackler O T,Peterlin B M.Nef increases infectivity of HIV via lipid rafts[J].Curr Biol,2001,11:875-879.
[32]Zheng Y H,Plemenitas A,Fielding C J,Peterlin B M.Nef increases the synthesis of and transports cholesterol to lipid rafts and HIV-1progeny virions[J].Proc Natl Acad Sci USA,2003,100:8460-8465.
[33]Brügger B,Krautkramer E,Tibroni N,Munte C E,Rauch S,Leibrecht I,Glass B,Breuer S,Geyer M,Krausslich H G,Kalbitzer H R,Wieland F T,Fackler O T.Human immunodeficiency virus type 1 Nef protein modulates the lipid composition of virions and host cell membrane microdomains[J].Retrovirology,2007,4:70.
[34]Pizzato M,Helander A,Popova E,Calistri A,Zamborlini A,PalùG,G9ttlinger H G.Dynamin 2is required for the enhancement of HIV-1infectivity by Nef[J].Proc Natl Acad Sci USA,2007,104:6812-6817.
[35]Usami Y,Wu Y,Gottlinger H G.SERINC3 and SERINC5restrict HIV-1infectivity and are counteracted by Nef[J].Nature,2015,526:218-223.
[36]Rosa A,Chande A,Ziglio S,De Sanctis V,Bertorelli R,Goh S L,McCauley S M,Nowosielska A,Antonarakis S E,Luban J,Santoni F A,Pizzato M.HIV-1Nef promotes infection by excluding SERINC5from virion incorporation[J].Nature,2015,526:212-217.
[37]Inuzuka M,Hayakawa M,Ingi T.Serinc,an activityregulated protein family,incorporates serine into membrane lipid synthesis[J].J Biol Chem,2005,280:35776-35783.
[38]Chu E P,Elso C M,Pollock A H,Alsayb M A,Mackin L,Thomas H E,Kay T W,Silveira PA,Mansell A S,Gaus K,Brodnicki T C.Disruption of Serinc1,which facilitates serine-derived lipid synthesis,fails to alter macrophage function,lymphocyte proliferation or autoimmune disease susceptibility[J].Mol Immunol,2017,82:19-33.
[39]Fackler O T.Spotlight on HIV-1 Nef:SERINC3and SERINC5identified as restriction factors antagonized by the pathogenesis factor[J].Viruses,2015,7:6730-6738.
[40]Ahi YS,Zhang S,Thappeta Y,Denman A,Feizpour A,Gummuluru S,Reinhard B,Muriaux D,Fivash MJ,Rein A.Functional interplay between Murine Leukemia Virus glycogag,Serinc5,and surface glycoprotein governs virus entry,with opposite effects on Gamma retroviral and Ebolavirus glycoproteins[J/OL].mBio,2016,7(6).pii:e01985-16.
[41]Sood C,Marin M,Chande A,Pizzato M,Melikyan G B.SERINC5protein inhibits HIV-1fusion pore formation by promoting functional inactivation of envelope glycoproteins[J].J Biol Chem,2017,292(14):6014-6026.
[42]Usami Y,Popov S,Gottlinger H G.The Nef-like effect of murine leukemia virus glycosylated gag on HIV-1infectivity is mediated by its cytoplasmic domain and depends on the AP-2adaptor complex[J].J Virol,2014,88:3443-3454.
[43]Chande A,Cuccurullo E C,Rosa A,Ziglio S,Carpenter S,Pizzato M.S2from equine infectious anemia virus is an infectivity factor which counteracts the retroviral inhibitors SERINC5and SERINC3[J].Proc Natl Acad Sci USA,2016,113:13197-13202.
[44]Beitari S,Ding S,Pan Q,Finzi A,Liang C.The effect of HIV-1Env on SERINC5antagonism[J/OL].J Virol,2016,91(4):e02214-2216.