Lentiviral Nef proteins manipulate T cells in a subset-specific manner

Journal of Virology

Volumn 89, Issue 4, 2015, Pages 1986-2001

  Yu, Hangxing ^a   Khalid, Mohammad ^a   Heigele, Anke ^a   Schmökel, Jan ^a   Usmani, Shariq M ^a   van der Merwe, Johannes ^a   Münch, Jan ^a   Silvestri, Guido ^b   Kirchhoff, Frank ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD45RA ANTIGEN; CD45RO ANTIGEN; LYMPHOCYTE MEMBRANE RECEPTOR; NEF PROTEIN; T LYMPHOCYTE RECEPTOR; CD45 ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; NEF PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; PTPRC PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD45RA+ CD45RO+ CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL SPECIFICITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LENTIVIRINAE; LYMPHOCYTE PROLIFERATION; LYMPHOID CELL; MEMORY T LYMPHOCYTE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE SUBPOPULATION; VIRION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS INFECTIVITY; VIRUS REPLICATION; VPU GENE; ANIMAL; CELL SURVIVAL; IMMUNOLOGY; METABOLISM; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; PRIMATES; SIMIAE; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; ANTIGENS, CD3; ANTIGENS, CD45; APOPTOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; HIV-1; HUMANS; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS;

EID: 84921628192     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03104-14     Document Type: Article

References (39)

1. Ariën K, Verhasselt B. 2008. HIV Nef: role in pathogenesis and viral fitness. Curr HIV Res 6:200-208. http://dx.doi.org/10.2174/157016208784325001.
2. Kirchhoff F, Schindler M, Specht A, Arhel N, Münch J. 2008. Role of Nef in primate lentiviral immunopathogenesis. Cell Mol Life Sci 65:2621-2636. http://dx.doi.org/10.1007/s00018-008-8094-2.
3. Kestler HW, Ringler DJ, Mori K, Panicali DL, Sehgal PK, Daniel MD, Desrosiers RC. 1991. Importance of the nef gene for maintenance of high virus loads and for development of AIDS. Cell 65:651-662. http://dx.doi.org/10.1016/0092-8674(91)90097-I.
4. Kirchhoff F, Greenough TC, Brettler DB, Sullivan JL, Desrosiers RC. 1995. Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. NEngl J Med 332:228-232. http://dx.doi.org/10.1056/NEJM199501263320405.
5. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, Hooker DJ, McPhee DA, Greenway AL, Ellett A, Chatfield C, Lawson VA, Crowe S, Maerz A, Sonza S, Learmont J, Sullivan JS, Cunningham A, Dwyer D, Dowton D, Mills J. 1995. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science 270:988-991. http://dx.doi.org/10.1126/science.270.5238.988.
6. Fackler OT, Alcover A, Schwartz O. 2007. Modulation of the immunological synapse: a key to HIV-1 pathogenesis? Nat Rev Immunol 7:310-317. http://dx.doi.org/10.1038/nri2041.
7. Wonderlich ER, Leonard JA, Collins KL. 2011. HIV immune evasion disruption of antigen presentation by the HIV Nef protein. Adv Virus Res 80:103-127. http://dx.doi.org/10.1016/B978-0-12-385987-7.00005-1.
8. Fenard D, Yonemoto W, Noronha C de, Cavrois M, Williams SA, Greene WC. 2005. Nefisphysicallyrecruitedintotheimmunologicalsynapseandpotentiates T cell activation early after TC Rengagement. JImmunol 175:6050-6057. http://dx.doi.org/10.4049/jimmunol.175.9.6050.
9. Fortin J, Barat C, Beausejour Y, Barbeau B, Tremblay MJ. 2004. Hyper-responsiveness to stimulation of human immunodeficiency virusinfected CD4+ T cells requires Nef and Tat virus gene products and results from higher NFAT, NF-B, and AP-1 induction. J Biol Chem 279: 39520-39531. http://dx.doi.org/10.1074/jbc.M407477200.
10. Glushakova S, Grivel JC, Suryanarayana K, Meylan P, Lifson JD, Desrosiers R, Margolis L. 1999. Nef enhances human immunodeficiency virus replication and responsiveness to interleukin-2 in human lymphoid tissue ex vivo. J Virol 73:3968-3974.
11. Schindler M, Münch J, Kutsch O, Li H, Santiago ML, Bibollet-Ruche F, Müller-Trutwin MC, Novembre FJ, Peeters M, Courgnaud V, Bailes E, Roques P, Sodora DL, Silvestri G, Sharp PM, Hahn BH, Kirchhoff F. 2006. Nef-mediated suppression of T cell activation was lost in a lentiviral lineage that gave rise to HIV-1. Cell 125:1055-1067. http://dx.doi.org/10.1016/j.cell.2006.04.033.
12. Peter F. 1998. HIV nef: the mother of all evil? Immunity 9:433-437. http://dx.doi.org/10.1016/S1074-7613(00)80626-3.
13. Saksela K. 2011. Interactions of the HIV/SIV pathogenicity factor Nef with SH3 domain-containing host cell proteins. Curr HIV Res 9:531-542. http://dx.doi.org/10.2174/157016211798842107.
14. Sodora DL, Allan JS, Apetrei C, Brenchley JM, Douek DC, Else JG, Estes JD, Hahn BH, Hirsch VM, Kaur A, Kirchhoff F, Muller-Trutwin M, Pandrea I, Schmitz JE, Silvestri G. 2009. Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat Med 15:861-865. http://dx.doi.org/10.1038/nm.2013.
15. Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G. 2012. Natural SIV hosts: showing AIDS the door. Science 335:1188-1193. http://dx.doi.org/10.1126/science.1217550.
16. Kirchhoff F. 2009. Is the high virulence of HIV-1 an unfortunate coincidence of primate lentiviral evolution? Nat Rev Microbiol 7:467-476. http://dx.doi.org/10.1038/nrmicro2111.
17. Iafrate AJ, Bronson S, Skowronski J. 1997. Separable functions of Nef disrupt two aspects of T cell receptor machinery: CD4 expression and CD3 signaling. EMBOJ 16:673-684. http://dx.doi.org/10.1093/emboj/16.4.673.
18. Schaefer TM, Bell I, Pfeifer ME, Ghosh M, Trible RP, Fuller CL, Ashman C, Reinhart TA. 2002. The conserved process of TCR/CD3 complex down-modulation by SIV Nef is mediated by the central core, not endocytic motifs. Virology 302:106-122. http://dx.doi.org/10.1006/viro.2002.1628.
19. Schmökel J, Sauter D, Schindler M, Leendertz FH, Bailes E, Dazza M, Saragosti S, Bibollet-Ruche F, Peeters M, Hahn BH, Kirchhoff F. 2011. The presence of a vpu gene and the lack of Nef-mediated downmodulation of T cell receptor-CD3 are not always linked in primate lentiviruses. J Virol 85:742-752. http://dx.doi.org/10.1128/JVI.02087-10.
20. Schindler M, Schmökel J, Specht A, Li H, Münch J, Khalid M, Sodora DL, Hahn BH, Silvestri G, Kirchhoff F. 2008. Inefficient Nef-mediated downmodulation of CD3 and MHC-I correlates with loss of CD4+T cells in natural SIV infection. PLoS Pathog 4:e1000107. http://dx.doi.org/10.1371/journal.ppat.1000107.
21. Khalid M, Yu H, Sauter D, Usmani SM, Schmokel J, Feldman J, Gruters RA, van der Ende ME, Geyer M, Rowland-Jones S, Osterhaus AD, Kirchhoff F. 2012. Efficient Nef-mediated downmodulation of TCR-CD3 and CD28 is associated with high CD4+ T cell counts in viremic HIV-2 infection. J Virol 86:4906-4920. http://dx.doi.org/10.1128/JVI.06856-11.
22. Bell I, Schaefer TM, Trible RP, Amedee A, Reinhart TA. 2001. Downmodulation of the costimulatory molecule, CD28, is a conserved activity of multiple SIV Nefs and is dependent on histidine 196 of Nef. Virology 283:148-158. http://dx.doi.org/10.1006/viro.2001.0872.
23. Swigut T, Shohdy N, Skowronski J. 2001. Mechanism for downregulation of CD28 by Nef. EMBO J 20:1593-1604. http://dx.doi.org/10.1093/emboj/20.7.1593.
24. Brenchley JM, Vinton C, Tabb B, Hao XP, Connick E, Paiardini M, Lifson JD, Silvestri G, Estes JD. 2012. Differential infection patterns of CD4+ T cells and lymphoid tissue viral burden distinguish progressive and nonprogressive lentiviral infections. Blood 120:4172-4181. http://dx.doi.org/10.1182/blood-2012-06-437608.
25. Paiardini M, Cervasi B, Reyes-Aviles E, Micci L, Ortiz AM, Chahroudi A, Vinton C, Gordon SN, Bosinger SE, Francella N, Hallberg PL, Cramer E, Schlub T, Chan ML, Riddick NE, Collman RG, Apetrei C, Pandrea I, Else J, Munch J, Kirchhoff F, Davenport MP, Brenchley JM, Silvestri G. 2011. Low levels of SIV infection in sooty mangabey central memory CD4+ T cells are associated with limited CCR5 expression. Nat Med 17:830-836. http://dx.doi.org/10.1038/nm.2395.
26. Brenchley JM, Silvestri G, Douek DC. 2010. Nonprogressive and progressive primate immunodeficiency lentivirus infections. Immunity 32: 737-742. http://dx.doi.org/10.1016/j.immuni.2010.06.004.
27. Schindler M, Münch JJ, Kirchhoff F. 2005. Human immunodeficiency virus type 1 inhibits DNA damage-triggered apoptosis by a Nef-independent mechanism. J Virol 79:5489-5498. http://dx.doi.org/10.1128/JVI.79.9.5489-5498.2005.
28. Eckstein DA, Penn ML, Korin YD, Scripture-Adams DD, Zack JA, Kreisberg JF, Roederer M, Sherman MP, Chin PS, Goldsmith MA. 2001. HIV-1 actively replicates in naive CD4+ T cells residing within human lymphoid tissues. Immunity 15:671-682. http://dx.doi.org/10.1016/S1074-7613(01)00217-5.
29. Papkalla A, Münch J, Otto C, Kirchhoff F. 2002. Nef enhances human immunodeficiency virus type 1 infectivity and replication independently of viral coreceptor tropism. J Virol 76:8455-8459. http://dx.doi.org/10.1128/JVI.76.16.8455-8459.2002.
30. Schmökel J, Li H, Shabir A, Yu H, Geyer M, Silvestri G, Sodora DL, Hahn BH, Kirchhoff F. 2013. Link between primate lentiviral coreceptor usage and Nef function. Cell Rep 5:997-1009. http://dx.doi.org/10.1016/j.celrep.2013.10.028.
31. Grivel JC, Margolis LB. 1999. CCR5-and CXCR4-tropic HIV-1 are equally cytopathic for their T-cell targets in human lymphoid tissue. Nat Med 5:344-346. http://dx.doi.org/10.1038/6565.
32. Lenassi M, Cagney G, Liao M, Vaupotic T, Bartholomeeusen K, Cheng Y, Krogan NJ, Plemenitas A, Peterlin BM. 2010. HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic 11: 110-122. http://dx.doi.org/10.1111/j.1600-0854.2009.01006.x.
33. Gordon SN, Dunham RM, Engram JC, Estes J, Wang Z, Klatt NR, Paiardini M, Pandrea IV, Apetrei C, Sodora DL, Lee HY, Haase AT, Miller MD, Kaur A, Staprans SI, Perelson AS, Feinberg MB, Silvestri G. 2008. Short-lived infected cells support virus replication in sooty mangabeys naturally infected with simian immunodeficiency virus: implications for AIDS pathogenesis. J Virol 82:3725-3735. http://dx.doi.org/10.1128/JVI.02408-07.
34. Pandrea I, Ribeiro RM, Gautam R, Gaufin T, Pattison M, Barnes M, Monjure C, Stoulig C, Dufour J, Cyprian W, Silvestri G, Miller MD, Perelson AS, Apetrei C. 2008. Simian immunodeficiency virus SIVagm dynamics in African green monkeys. J Virol 82:3713-3724. http://dx.doi.org/10.1128/JVI.02402-07.
35. Perelson AS, Neumann AU, Markowitz M, Leonard JM, Ho DD. 1996. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, and viral generation time. Science 271:1582-1586. http://dx.doi.org/10.1126/science.271.5255.1582.
36. Arhel N, Lehmann M, Clauß K, Nienhaus GU, Piguet V, Kirchhoff F. 2009. The inability to disrupt the immunological synapse between infected human T cells and APCs distinguishes HIV-1 from most other primate lentiviruses. J Clin Invest 119:2965-2975.
37. Beaumier CM, Harris LD, Goldstein S, Klatt NR, Whitted S, McGinty J, Apetrei C, Pandrea I, Hirsch VM, Brenchley JM. 2009. CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat Med 15:879-885. http://dx.doi.org/10.1038/nm.1970.
38. Feldmann J, Leligdowicz A, Jaye A, Dong T, Whittle H, Rowland-Jones SL. 2009. Downregulation of the T-cell receptor by human immunodeficiency virus type 2 Nef does not protect against disease progression. J Virol 83:12968-12972. http://dx.doi.org/10.1128/JVI.01252-09.
39. Sauter D, Hotter D, Van Driessche B, Stürzel CM, Kluge SF, Wildum S, Yu H, Baumann B, Wirth T, Hahn BH, Van Lint C, Kirchhoff F. Differential regulation of NF-κB-mediated proviral and antiviral host gene expression by primate lentiviral Nef and Vpu proteins. Cell Rep, in press.