Mechanisms of HIV-1 escape from immune responses and antiretroviral drugs

Current Opinion in Immunology

Volumn 16, Issue 4, 2004, Pages 470-476

  Bailey, Justin ^a   Blankson, Joel N ^a   Wind Rotolo, Megan ^a   Siliciano, Robert F ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

acquired immunodeficiency syndrome; AIDS; CTL; cytotoxic T lymphocyte; env; HAART; highly active antiretroviral therapy; HIV; HIV 1 envelope; human immunodeficiency virus; I B; inhibitor of B; major histocompatibility complex; MHC; nAb

Indexed keywords

ANTIRETROVIRUS AGENT; CD4 ANTIGEN; EPITOPE;

B LYMPHOCYTE; CYTOTOXIC T LYMPHOCYTE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; LATENT VIRUS INFECTION; MEMORY CELL; NONHUMAN; PERSISTENT VIRUS INFECTION; REVIEW; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS INACTIVATION; VIRUS INDUCTION; VIRUS INFECTIVITY; VIRUS LATENCY; VIRUS NEUTRALIZATION; VIRUS REPLICATION;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANTI-HIV AGENTS; CD4-POSITIVE T-LYMPHOCYTES; DRUG RESISTANCE, VIRAL; EPITOPES, B-LYMPHOCYTE; EPITOPES, T-LYMPHOCYTE; HIV ANTIBODIES; HIV-1; HUMANS; MUTATION; T-LYMPHOCYTES, CYTOTOXIC; VIRUS LATENCY; VIRUS REPLICATION;

EID: 3042818396     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2004.05.005     Document Type: Review

References (63)

1. Little S.J., Mclean A.R., Spina C.A., Richman D.D., Havlir D.V. Viral dynamics of acute HIV-1 infection. J Exp Med. 190:1999;841-850
2. Koup R.A., Safrit J.A., Cao Y., Andrews C.A., McLeod G., Borkowsky W., Farthing C., Ho D.D. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol. 68:1994;4650-4655
3. Schmitz J.E., Kuroda M.J., Santra S., Sasseville V.G., Simon M.A., Lifton M.A., Racz P., Tenner-Racz K., Dalesandro M., Scallon B.J., et al. Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science. 283:1999;857-860
4. Rosenberg E.S., Billingsley J.M., Caliendo A.M., Boswell S.L., Sax P.E., Kalams S.A., Walker B.D. Vigorous HIV-1-specific CD4+ T cell responses associated with the control of viremia. Science. 278:1997;1447-1450
5. Johnson W.E., Desrosiers R.C. Viral persistance: HIV's strategies of immune system evasion. Annu Rev Med. 53:2002;499-518
6. Gandhi R.T., Walker B.D. Immunologic control of HIV-1. Annu Rev Med. 53:2002;149-172
7. Sheehy A.M., Gaddis N.C., Choi J.D., Malim M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature. 418:2002;646-650
8. Ho D.D., Neumann A.U., Perelson A.S., Chen W., Leonard J.M., Markowitz M. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature. 373:1995;123-126
9. Wei X., Ghosh S.K., Taylor M.E., Johnson V.A., Emini E.A., Deutsch P., Lifson J.D., Bonhoeffer S., Nowak M.A., Hahn B.H., Shaw G.M. Viral dynamics in human immunodeficiency virus type 1 infection. Nature. 373:1995;117-122
10. Perelson A.S., Neumann A.U., Markowitz M., Leonard J.M., Ho D.D. HIV-1 dynamics in vivo: virion clearance rate, infected cell life-span, viral generation time. Science. 271:1996;1582-1586
11. Perelson A.S., Essunger P., Cao Y., Vesanen M., Hurley A., Saksela K., Markowitz M., Ho D.D. Decay characteristics of HIV-1-infected compartments during combination therapy. Nature. 387:1997;188-191
12. Nowak M.A., Bangham C.R. Population dynamics of immune responses to persistent viruses. Science. 272:1996;74-79
13. Markowitz M., Louie M., Hurley A., Sun E., Di Mascio M., Perelson A.S., Ho D.D. A novel antiviral intervention results in more accurate assessment of human immunodeficiency virus type 1 replication dynamics and T-cell decay in vivo. J Virol. 77:2003;5037-5038
14. Mansky L.M., Temin H.M. Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol. 69:1995;5087-5094
15. Burton D.R. Antibodies, viruses and vaccines. Nat Rev Immunol. 2:2002;706-713
16. Lu M., Blacklow S.C., Kim P.S. A trimeric structural domain of the HIV-1 transmembrane glycoprotein. Nat Struct Biol. 2:1995;1075-1082
17. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature. 393:1998;648-659
18. Wyatt R., Kwong P.D., Desjardins E., Sweet R.W., Robinson J., Hendrickson W.A., Sodroski J.G. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature. 393:1998;705-711
19. Leonard C.K., Spellman M.W., Riddle L., Harris R.J., Thomas J.N., Gregory T.J. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J Biol Chem. 265:1990;10373-10382
20. Reitter J.N., Means R.E., Desrosiers R.C. A role for carbohydrates in immune evasion in AIDS. Nat Med. 4:1998;679-684
21. Koch M., Pancera M., Kwong P.D., Kolchinsky P., Grundner C., Wang L., Hendrickson W.A., Sodroski J., Wyatt R. Structure-based, targeted deglycosylation of HIV-1 gp120 and effects on neutralization sensitivity and antibody recognition. Virology. 313:2003;387-400
22. Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S., et al. Antibody neutralization and escape by HIV-1. Nature. 422:2003;307-312 This study shows a repetitive pattern of neutralizing antibody development and rapid viral escape that could generally be attributed to evolving patterns of N-linked glycosylation. Site-directed mutagenesis studies confirmed that specific patterns of N-linked glycosylation conveyed sensitivity or resistance to neutralization by autologous plasma.
23. Cole K.S., Steckbeck J.D., Rowles J.L., Desrosiers R.C., Montelaro R.C. Removal of N-linked glycosylation sites in the V1 region of simian immunodeficiency virus gp120 results in redirection of B-cell responses to V3. J Virol. 78:2004;1525-1539
24. Burton D.R., Desrosiers R.C., Doms R.W., Koff W.C., Kwong P.D., Moore J.P., Nabel G.J., Sodroski J., Wilson I.A., Wyatt R.T. HIV vaccine design and the neutralizing antibody problem. Nat Immunol. 5:2004;233-236
25. Labrijn A.F., Poignard P., Raja A., Zwick M.B., Delgado K., Franti M., Binley J., Vivona V., Grundner C., Huang C.C., et al. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1. J Virol. 77:2003;10557-10565
26. Kwong P.D., Doyle M.L., Casper D.J., Cicala C., Leavitt S.A., Majeed S., Steenbeke T.D., Venturi M., Chaiken I., Fung M., et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature. 420:2002;678-682
27. Poignard P., Sabbe R., Picchio G.R., Wang M., Gulizia R.J., Katinger H., Parren P.W., Mosier D.E., Burton D.R. Neutralizing antibodies have limited effects on the control of established HIV-1 infection in vivo. Immunity. 10:1999;431-438
28. Richman D.D., Wrin T., Little S.J., Petropoulos C.J. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc Natl Acad Sci USA. 100:2003;4144-4149 This study showed patterns of antibody-mediated neutralization and escape using virus and plasma isolated every three months for two years. The work emphasizes the powerful selective pressure exerted by neutralizing antibody, as well as the relative ease of viral escape from that response.
29. Draenert R., Verrill C.L., Tang Y., Allen T.M., Wurcel A.G., Boczanowski M., Lechner A., Kim A.Y., Suscovich T., Brown N.V., et al. Persistent recognition of autologous virus by high-avidity CD8 T cells in chronic, progressive human immunodeficiency virus type 1 infection. J Virol. 78:2004;630-641
30. Jin X., Bauer D.E., Tuttleton S.E., Lewin S., Gettie A., Blanchard J., Irwin C.E., Safrit J.T., Mittler J., Weinberger L., et al. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med. 189:1999;991-998
31. Collins K.L., Chen B.K., Kalams S.A., Walker B.D., Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature. 391:1998;397-401
32. Migueles S.A., Laborico A.C., Shupert W.L., Sabbaghian M.S., Rabin R., Hallahan C.W., Van Baarle D., Kostense S., Miedema F., McLaughlin M., et al. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat Immunol. 3:2002;1061-1068
33. Allen T.M., O'Connor D.H., Jing P., Dzuris J.L., Mothe B.R., Vogel T.U., Dunphy E., Liebl M.E., Emerson C., Wilson N., et al. Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature. 407:2000;386-390
34. Goulder P.J., Phillips R.E., Colbert R.A., McAdam S., Ogg G., Nowak M.A., Giangrande P., Luzzi G., Morgan B., Edwards A., et al. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med. 3:1997;212-217
35. Borrow P., Lewicki H., Wei X., Horwitz M.S., Peffer N., Meyers H., Nelson J.A., Gairin J.E., Hahn B.H., Oldstone M.B., Shaw G.M. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med. 3:1997;205-211
36. Barouch D.H., Kunstman J., Kuroda M.J., Schmitz J.E., Santra S., Peyerl F.W., Krivulka G.R., Beaudry K., Lifton M.A., Gorgone D.A., et al. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature. 415:2002;335-339
37. Altfeld M., Addo M.M., Shankarappa R., Lee P.K., Allen T.M., Yu X.G., Rathod A., Harlow J., O'Sullivan K., Johnston M.N., et al. Enhanced detection of human immunodeficiency virus type 1-specific T-cell responses to highly variable regions by using peptides based on autologous virus sequences. J Virol. 77:2003;7330-7340
38. Addo M.M., Yu X.G., Rathod A., Cohen D., Eldridge R.L., Strick D., Johnston M.N., Corcoran C., Wurcel A.G., Fitzpatrick C.A., et al. Comprehensive epitope analysis of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses directed against the entire expressed HIV-1 genome demonstrate broadly directed responses, but no correlation to viral load. J Virol. 77:2003;2081-2092 This paper provides a good illustration of the power of comprehensive approaches to the analysis of HIV-1-specific immunity.
39. Leslie A.J., Pfafferott K.J., Chetty P., Draenert R., Addo M.M., Feeney M., Tang Y., Holmes E.C., Allen T., Prado J.G., et al. HIV evolution: CTL escape mutation and reversion after transmission. Nat Med. 10:2004;282-289 One of two recent studies showing the reversion to wild-type sequence after the transmission of CTL escape mutants into hosts not expressing the relevant MHC molecules.
40. ••].
41. Finzi D., Blankson J., Siliciano J.D., Margolick J.B., Chadwick K., Pierson T., Smith K., Lisziewicz J., Lori F., Flexner C., et al. Latent infection of CD4+ T cells provides a mechanism for lifelong persistence of HIV-1, even in patients on effective combination therapy. Nat Med. 5:1999;512-517
42. 1/2 of the latent reservoir as 44 months, using long-term follow-up of patients receiving HAART with no detectable viremia for up to seven years.
43. + T cells from viremic versus aviremic patients were also defined.
44. Finzi D., Hermankova M., Pierson T., Carruth L.M., Buck C., Chaisson R.E., Quinn T.C., Chadwick K., Margolick J., Brookmeyer R., et al. Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science. 278:1997;1295-1300
45. Wong J.K., Hezareh M., Gunthard H.F., Havlir D.V., Ignacio C.C., Spina C.A., Richman D.D. Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science. 278:1997;1291-1295
46. Chun T.W., Stuyver L., Mizell S.B., Ehler L.A., Mican J.M., Baseler M., Lloyd A.L., Nowak M.A., Fauci A.S. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci USA. 94:1997;13193-13197
47. Ruff C.T., Ray S.C., Kwon P., Zinn R., Pendleton A., Hutton N., Ashworth R., Gange S., Quinn T.C., Siliciano R.F., Persaud D. Persistence of wild-type virus and lack of temporal structure in the latent reservoir for human immunodeficiency virus type 1 in pediatric patients with extensive antiretroviral exposure. J Virol. 76:2002;9481-9492
48. Strain M.C., Gunthard H.F., Havlir D.V., Ignacio C.C., Smith D.M., Leigh-Brown A.J., Macaranas T.R., Lam R.Y., Daly O.A., Fischer M., et al. Heterogeneous clearance rates of long-lived lymphocytes infected with HIV: intrinsic stability predicts lifelong persistence. Proc Natl Acad Sci USA. 100:2003;4819-4824
49. Nabel G., Baltimore D. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature. 326:1987;711-713
50. Tong-Starksen S.E., Luciw P.A., Peterlin B.M. Human immunodeficiency virus long terminal repeat responds to T- cell activation signals. Proc Natl Acad Sci USA. 84:1987;6845-6849
51. Bohnlein E., Lowenthal J.W., Siekevitz M., Ballard D.W., Franza B.R., Greene W.C. The same inducible nuclear proteins regulates mitogen activation of both the interleukin-2 receptor-alpha gene and type 1 HIV. Cell. 53:1988;827-836
52. Duh E.J., Maury W.J., Folks T.M., Fauci A.S., Rabson A.B. Tumor necrosis factor alpha activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-kappa B sites in the long terminal repeat. Proc Natl Acad Sci USA. 86:1989;5974-5978
53. + T cells.
54. Kao S.Y., Calman A.F., Luciw P.A., Peterlin B.M. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature. 330:1987;489-493
55. Adams M., Sharmeen L., Kimpton J., Romeo J.M., Garcia J.V., Peterlin B.M., Groudine M., Emerman M. Cellular latency in human immunodeficiency virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc Natl Acad Sci USA. 91:1994;3862-3866
56. Jones K.A., Peterlin B.M. Control of RNA initiation and elongation at the HIV-1 promoter. Annu Rev Biochem. 63:1994;717-743
57. Herrmann C.H., Rice A.P. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxyl-terminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J Virol. 69:1995;1612-1620
58. Jordan A., Bisgrove D., Verdin E. HIV reproducibly establishes a latent infection after acute infection of T cells in vitro. EMBO J. 22:2003;1868-1877
59. Han Y, Lassen K, Monie D, Sedaghat AR, Shimoji S, Liu X, Pierson TC, Margolick JB, Siliciano RF, Siliciano JD: Resting CD4+ T cells from HIV-1-infected individuals carry integrated HIV-1 genomes within actively transcribed host genes. J Virol 2004, in press.
60. Perng G.C., Jones C., Ciacci-Zanella J., Stone M., Henderson G., Yukht A., Slanina S.M., Hofman F.M., Ghiasi H., Nesburn A.B., Wechsler S.L. Virus-induced neuronal apoptosis blocked by the herpes simplex virus latency-associated transcript. Science. 287:2000;1500-1503
61. Silvestri G., Sodora D.L., Koup R.A., Paiardini M., O'Neil S.P., McClure H.M., Staprans S.I., Feinberg M.B. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity. 18:2003;441-452 This is an important study of differences between non-pathogenic and pathogenic SIV infection.
62. + T cells to become susceptible to viral infection.
63. Persaud D., Zhou Y., Siliciano J.M., Siliciano R.F. Latency in human immunodeficiency virus type 1 infection: no easy answers. J Virol. 77:2003;1660-1661