Viral protein R upregulates expression of ULBP2 on uninfected bystander cells during HIV-1 infection of primary CD4+ T lymphocytes

Virology

Volumn 443, Issue 2, 2013, Pages 248-256

  Richard, Jonathan ^a   Pham, Tram N Q ^a   Ishizaka, Yukihito ^b   Cohen, Éric A ^a,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

CD4+ T cell depletion; DNA damage response; HIV 1 Vpr; Natural killer cell; NKG2D ligand; ULBP2

Indexed keywords

VPR PROTEIN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL CYCLE ARREST; CELL KILLING; CELL LOSS; CONTROLLED STUDY; DNA DAMAGE; GENE; GENE EXPRESSION REGULATION; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; UL16 BINDING PROTEIN 2 GENE; UPREGULATION; VIRION; VIRUS PARTICLE;

CD4+ T CELL DEPLETION; DNA DAMAGE RESPONSE; HIV-1 VPR; NATURAL KILLER CELL; NKG2D LIGAND; ULBP2;

CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; DNA DAMAGE; GPI-LINKED PROTEINS; HEK293 CELLS; HELA CELLS; HIV-1; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KILLER CELLS, NATURAL; UP-REGULATION; VIRION; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84880509486     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.04.037     Document Type: Article

References (50)

1. Alter G., Teigen N., Ahern R., Streeck H., Meier A., Rosenberg E.S., Altfeld M. Evolution of innate and adaptive effector cell functions during acute HIV-1 infection. J. Infect. Dis. 2007, 195:1452-1460.
2. Bachand F., Yao X.J., Hrimech M., Rougeau N., Cohen E.A. Incorporation of Vpr into human immunodeficiency virus type 1 requires a direct interaction with the p6 domain of the p55 gag precursor. J. Biol. Chem. 1999, 274:9083-9091.
3. Belzile J.P., Duisit G., Rougeau N., Mercier J., Finzi A., Cohen E.A. HIV-1 Vpr-mediated G2 arrest involves the DDB1-CUL4AVPRBP E3 ubiquitin ligase. Plos Pathog. 2007, 3:e85.
4. Belzile J.P., Abrahamyan L.G., Gerard F.C., Rougeau N., Cohen E.A. Formation of mobile chromatin-associated nuclear foci containing HIV-1 Vpr and VPRBP is critical for the induction of G2 cell cycle arrest. Plos Pathog. 2010, 6:e1001080.
5. Belzile J.P., Richard J., Rougeau N., Xiao Y., Cohen E.A. HIV-1 Vpr induces the K48-linked polyubiquitination and proteasomal degradation of target cellular proteins to activate ATR and promote G2 arrest. J. Virol. 2010, 84:3320-3330.
6. Bourinbaiar A.S. The ratio of defective HIV-1 particles to replication-competent infectious virions. Acta Virol. 1994, 38:59-61.
7. Brenchley J.M., Schacker T.W., Ruff L.E., Price D.A., Taylor J.H., Beilman G.J., Nguyen P.L., Khoruts A., Larson M., Haase A.T., Douek D.C. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 2004, 200:749-759.
8. Cerboni C., Neri F., Casartelli N., Zingoni A., Cosman D., Rossi P., Santoni A., Doria M. Human immunodeficiency virus 1 Nef protein downmodulates the ligands of the activating receptor NKG2D and inhibits natural killer cell-mediated cytotoxicity. J. Gen. Virol. 2007, 88:242-250.
9. Dimitrov D.S., Willey R.L., Sato H., Chang L.J., Blumenthal R., Martin M.A. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 1993, 67:2182-2190.
10. Doitsh G., Cavrois M., Lassen K.G., Zepeda O., Yang Z., Santiago M.L., Hebbeler A.M., Greene W.C. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell 2010, 143:789-801.
11. Esser M.T., Bess J.W., Suryanarayana K., Chertova E., Marti D., Carrington M., Arthur L.O., Lifson J.D. Partial activation and induction of apoptosis in CD4(+) and CD8(+) T lymphocytes by conformationally authentic noninfectious human immunodeficiency virus type 1. J. Virol. 2001, 75:1152-1164.
12. Fausther-Bovendo H., Sol-Foulon N., Candotti D., Agut H., Schwartz O., Debre P., Vieillard V. HIV escape from natural killer cytotoxicity: nef inhibits NKp44L expression on CD4+ T cells. AIDS 2009, 23:1077-1087.
13. Finkel T.H., Tudor-Williams G., Banda N.K., Cotton M.F., Curiel T., Monks C., Baba T.W., Ruprecht R.M., Kupfer A. Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat. Med. 1995, 1:129-134.
14. Fogli M., Mavilio D., Brunetta E., Varchetta S., Ata K., Roby G., Kovacs C., Follmann D., Pende D., Ward J., Barker E., Marcenaro E., Moretta A., Fauci A.S. Lysis of endogenously infected CD4+ T cell blasts by rIL-2 activated autologous natural killer cells from HIV-infected viremic individuals. Plos Pathog. 2008, 4:e1000101.
15. He J., Choe S., Walker R., Di Marzio P., Morgan D.O., Landau N.R. Human immunodeficiency virus type 1 viral protein R (Vpr) arrests cells in the G2 phase of the cell cycle by inhibiting p34cdc2 activity. J. Virol. 1995, 69:6705-6711.
16. Herbeuval J.P., Grivel J.C., Boasso A., Hardy A.W., Chougnet C., Dolan M.J., Yagita H., Lifson J.D., Shearer G.M. CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 2005, 106:3524-3531.
17. Hoshino S., Sun B., Konishi M., Shimura M., Segawa T., Hagiwara Y., Koyanagi Y., Iwamoto A., Mimaya J., Terunuma H., Kano S., Ishizaka Y. Vpr in plasma of HIV type 1-positive patients is correlated with the HIV type 1 RNA titers. AIDS Res. Hum. Retroviruses 2007, 23:391-397.
18. Hrimech M., Yao X.J., Bachand F., Rougeau N., Cohen E.A. Human immunodeficiency virus type 1 (HIV-1) Vpr functions as an immediate-early protein during HIV-1 infection. J. Virol. 1999, 73:4101-4109.
19. Jekle A., Keppler O.T., De Clercq E., Schols D., Weinstein M., Goldsmith M.A. In vivo evolution of human immunodeficiency virus type 1 toward increased pathogenicity through CXCR4-mediated killing of uninfected CD4 T cells. J. Virol. 2003, 77:5846-5854.
20. Jowett J.B., Planelles V., Poon B., Shah N.P., Chen M.L., Chen I.S. The human immunodeficiency virus type 1 vpr gene arrests infected T cells in the G2+M phase of the cell cycle. J. Virol. 1995, 69:6304-6313.
21. Laakso M.M., Lee F.H., Haggarty B., Agrawal C., Nolan K.M., Biscone M., Romano J., Jordan A.P., Leslie G.J., Meissner E.G., Su L., Hoxie J.A., Doms R.W. V3 loop truncations in HIV-1 envelope impart resistance to coreceptor inhibitors and enhanced sensitivity to neutralizing antibodies. Plos Pathog. 2007, 3:e117.
22. Lahm H.W., Stein S. Characterization of recombinant human interleukin-2 with micromethods. J. Chromatogr. 1985, 326:357-361.
23. Lai M., Zimmerman E.S., Planelles V., Chen J. Activation of the ATR pathway by human immunodeficiency virus type 1 Vpr involves its direct binding to chromatin in vivo. J. Virol. 2005, 79:15443-15451.
24. Lavallee C., Yao X.J., Ladha A., Gottlinger H., Haseltine W.A., Cohen E.A. Requirement of the Pr55gag precursor for incorporation of the Vpr product into human immunodeficiency virus type 1 viral particles. J. Virol. 1994, 68:1926-1934.
25. Levesque K., Zhao Y.S., Cohen E.A. Vpu exerts a positive effect on HIV-1 infectivity by down-modulating CD4 receptor molecules at the surface of HIV-1-producing cells. J. Biol. Chem. 2003, 278:28346-28353.
26. Levy D.N., Refaeli Y., MacGregor R.R., Weiner D.B. Serum Vpr regulates productive infection and latency of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 1994, 91:10873-10877.
27. Lu Y.L., Bennett R.P., Wills J.W., Gorelick R., Ratner L. A leucine triplet repeat sequence (LXX)4 in p6gag is important for Vpr incorporation into human immunodeficiency virus type 1 particles. J. Virol. 1995, 69:6873-6879.
28. Majumder B., Venkatachari N.J., Srinivasan A., Ayyavoo V. HIV-1 mediated immune pathogenesis: spotlight on the role of viral protein R (Vpr). Curr. HIV Res. 2009, 7:169-177.
29. Mattapallil J.J., Douek D.C., Hill B., Nishimura Y., Martin M., Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-1097.
30. Norman J.M., Mashiba M., McNamara L.A., Onafuwa-Nuga A., Chiari-Fort E., Shen W., Collins K.L. The antiviral factor APOBEC3G enhances the recognition of HIV-infected primary T cells by natural killer cells. Nat. Immunol. 2011, 12:975-983.
31. Pantaleo G., Graziosi C., Butini L., Pizzo P.A., Schnittman S.M., Kotler D.P., Fauci A.S. Lymphoid organs function as major reservoirs for human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 1991, 88:9838-9842.
32. Pham T.N., Richard J., Gerard F.C., Power C., Cohen E.A. Modulation of NKG2D-mediated cytotoxic functions of natural killer cells by viral protein R from HIV-1 primary isolates. J. Virol. 2011, 85:12254-12261.
33. Piatak M., Saag M.S., Yang L.C., Clark S.J., Kappes J.C., Luk K.C., Hahn B.H., Shaw G.M., Lifson J.D. High levels of HIV-1 in plasma during all stages of infection determined by competitive PCR. Science 1993, 259:1749-1754.
34. Poon B., Grovit-Ferbas K., Stewart S.A., Chen I.S. Cell cycle arrest by Vpr in HIV-1 virions and insensitivity to antiretroviral agents. Science 1998, 281:266-269.
35. Re F., Braaten D., Franke E.K., Luban J. Human immunodeficiency virus type 1 Vpr arrests the cell cycle in G2 by inhibiting the activation of p34cdc2-cyclin B. J. Virol. 1995, 69:6859-6864.
36. Richard J., Sindhu S., Pham T.N., Belzile J.P., Cohen E.A. HIV-1 Vpr up-regulates expression of ligands for the activating NKG2D receptor and promotes NK cell-mediated killing. Blood 2010, 115:1354-1363.
37. Romani B., Cohen E.A. Lentivirus Vpr and Vpx accessory proteins usurp the cullin4-DDB1 (DCAF1) E3 ubiquitin ligase. Curr. Opin. Virol. 2012, 2:749-757.
38. Sarkaria J.N., Busby E.C., Tibbetts R.S., Roos P., Taya Y., Karnitz L.M., Abraham R.T. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 1999, 59:4375-4382.
39. Shah A.H., Sowrirajan B., Davis Z.B., Ward J.P., Campbell E.M., Planelles V., Barker E. Degranulation of natural killer cells following interaction with HIV-1-infected cells is hindered by downmodulation of NTB-A by Vpu. Cell Host Microbe 2010, 8:397-409.
40. Sherman M.P., de Noronha C.M., Heusch M.I., Greene S., Greene W.C. Nucleocytoplasmic shuttling by human immunodeficiency virus type 1 Vpr. J. Virol. 2001, 75:1522-1532.
41. Sherman M.P., Schubert U., Williams S.A., de Noronha C.M., Kreisberg J.F., Henklein P., Greene W.C. HIV-1 Vpr displays natural protein-transducing properties: implications for viral pathogenesis. Virology 2002, 302:95-105.
42. Sorgel S., Fraedrich K., Votteler J., Thomas M., Stamminger T., Schubert U. Perinuclear localization of the HIV-1 regulatory protein Vpr is important for induction of G2-arrest. Virology 2012, 432:444-451.
43. Varbanov M., Espert L., Biard-Piechaczyk M. Mechanisms of CD4 T-cell depletion triggered by HIV-1 viral proteins. AIDS Rev. 2006, 8:221-236.
44. Vieillard V., Strominger J.L., Debre P. NK cytotoxicity against CD4+ T cells during HIV-1 infection: a gp41 peptide induces the expression of an NKp44 ligand. Proc. Natl. Acad. Sci. USA 2005, 102:10981-10986.
45. Ward J., Bonaparte M., Sacks J., Guterman J., Fogli M., Mavilio D., Barker E. HIV modulates the expression of ligands important in triggering natural killer cell cytotoxic responses on infected primary T-cell blasts. Blood 2007, 110:1207-1214.
46. Ward J., Davis Z., DeHart J., Zimmerman E., Bosque A., Brunetta E., Mavilio D., Planelles V., Barker E. HIV-1 Vpr triggers natural killer cell-mediated lysis of infected cells through activation of the ATR-mediated DNA damage response. Plos Pathog. 2009, 5:e1000613.
47. Xiao Y., Chen G., Richard J., Rougeau N., Li H., Seidah N.G., Cohen E.A. Cell-surface processing of extracellular human immunodeficiency virus type 1 Vpr by proprotein convertases. Virology 2008, 372:384-397.
48. Yao X.J., Mouland A.J., Subbramanian R.A., Forget J., Rougeau N., Bergeron D., Cohen E.A. Vpr stimulates viral expression and induces cell killing in human immunodeficiency virus type 1-infected dividing Jurkat T cells. J. Virol. 1998, 72:4686-4693.
49. Yao X.J., Subbramanian R.A., Rougeau N., Boisvert F., Bergeron D., Cohen E.A. Mutagenic analysis of human immunodeficiency virus type 1 Vpr: role of a predicted N-terminal alpha-helical structure in Vpr nuclear localization and virion incorporation. J. Virol. 1995, 69:7032-7044.
50. Zimmerman E.S., Chen J., Andersen J.L., Ardon O., Dehart J.L., Blackett J., Choudhary S.K., Camerini D., Nghiem P., Planelles V. Human immunodeficiency virus type 1 Vpr-mediated G2 arrest requires Rad17 and Hus1 and induces nuclear BRCA1 and gamma-H2AX focus formation. Mol. Cell. Biol. 2004, 24:9286-9294.