GagCM9-specific CD8 + T cells expressing limited public TCR clonotypes do not suppress SIV replication in vivo

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Vojnov, Lara ^a   Martins, Mauricio A ^a   Almeida, Jorge R ^b   Ende, Zachary ^b   Rakasz, Eva G ^a,c   Reynolds, Matthew R ^a   Leon, Enrique J ^c   Weisgrau, Kim L ^c   Burwitz, Benjamin J ^a   Folkvord, Joy M ^d   de Santana, Marlon G Veloso ^e   Neves, Patrícia C Costa ^e   Connick, Elizabeth ^d   Skinner, Pamela J ^f   Gostick, Emma ^h   O'Connor, David H ^a   Wilson, Nancy A ^a   Bonaldo, Myrna C ^e   Galler, Ricardo ^g   Price, David A ^h   Douek, Danny C ^b   Watkins, David I ^a,c   more..

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF WISCONSIN   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e INSTITUTO OSWALDO CRUZ   (Brazil)

^f UNIVERSITY OF MINNESOTA   (United States)

^g Instituto de Technologia em Imunobiologicos   (Brazil)

^h CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GAG PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN CM9; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS VACCINE; HLA ANTIGEN CLASS 1; LYMPHOCYTE ANTIGEN RECEPTOR; MAMU A 01 ANTIGEN; MAMU-A 01 ANTIGEN;

AMPLICON; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; GENE FREQUENCY; GENE SEQUENCE; LYMPHOCYTE SUBPOPULATION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; SIMIAN IMMUNODEFICIENCY VIRUS; TRANSGENE; VACCINATION; VIRUS INFECTION; VIRUS LOAD; VIRUS REPLICATION; YELLOW FEVER; AMINO ACID SEQUENCE; ANIMAL; CELL CLONE; CHEMISTRY; GENETICS; IMMUNOLOGY; INTESTINE MUCOSA; LYMPH NODE; MACACA MULATTA; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; SEQUENCE ANALYSIS; VIROLOGY;

ANIMALIA; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

AMINO ACID SEQUENCE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CLONE CELLS; GENE PRODUCTS, GAG; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNODOMINANT EPITOPES; INTESTINAL MUCOSA; LYMPH NODES; MACACA MULATTA; MOLECULAR SEQUENCE DATA; MUTATION; RECEPTORS, ANTIGEN, T-CELL; SEQUENCE ANALYSIS, PROTEIN; SIMIAN IMMUNODEFICIENCY VIRUS; VACCINATION; VIRAL LOAD; VIRUS REPLICATION;

EID: 80052065199     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023515     Document Type: Article

References (60)

1. Borrow P, Lewicki H, Hahn BH, Shaw GM, Oldstone MB, (1994) Virus-specific CD8+ cytotoxic T-lymphocyte activity associated with control of viremia in primary human immunodeficiency virus type 1 infection. J Virol 68: 6103-6110.
2. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, et al. (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J Virol 68: 4650-4655.
3. Kuroda MJ, Schmitz JE, Charini WA, Nickerson CE, Lifton MA, et al. (1999) Emergence of CTL coincides with clearance of virus during primary simian immunodeficiency virus infection in rhesus monkeys. J Immunol 162: 5127-5133.
4. Reimann KA, Tenner-Racz K, Racz P, Montefiori DC, Yasutomi Y, et al. (1994) Immunopathogenic events in acute infection of rhesus monkeys with simian immunodeficiency virus of macaques. J Virol 68: 2362-2370.
5. Friedrich TC, Valentine LE, Yant LJ, Rakasz EG, Piaskowski SM, et al. (2007) Subdominant CD8+ T-cell responses are involved in durable control of AIDS virus replication. J Virol 81: 3465-3476.
6. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, et al. (1999) Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J Exp Med 189: 991-998.
7. Matano T, Shibata R, Siemon C, Connors M, Lane HC, et al. (1998) Administration of an anti-CD8 monoclonal antibody interferes with the clearance of chimeric simian/human immunodeficiency virus during primary infections of rhesus macaques. J Virol 72: 164-169.
8. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, et al. (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283: 857-860.
9. Allen TM, O'Connor DH, Jing P, Dzuris JL, Mothé BR, et al. (2000) Tat-specific cytotoxic T lymphocytes select for SIV escape variants during resolution of primary viraemia. Nature 407: 386-390.
10. Barouch DH, Kunstman J, Kuroda MJ, Schmitz JE, Santra S, et al. (2002) Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature 415: 335-339.
11. Borrow P, Lewicki H, Wei X, Horwitz MS, Peffer N, et al. (1997) 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: 205-211.
12. Goulder PJ, Brander C, Tang Y, Tremblay C, Colbert RA, et al. (2001) Evolution and transmission of stable CTL escape mutations in HIV infection. Nature 412: 334-338.
13. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, et al. (1997) Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat Med 3: 212-217.
14. Koenig S, Conley AJ, Brewah YA, Jones GM, Leath S, et al. (1995) Transfer of HIV-1-specific cytotoxic T lymphocytes to an AIDS patient leads to selection for mutant HIV variants and subsequent disease progression. Nat Med 1: 330-336.
15. O'Connor DH, Allen TM, Vogel TU, Jing P, DeSouza IP, et al. (2002) Acute phase cytotoxic T lymphocyte escape is a hallmark of simian immunodeficiency virus infection. Nat Med 8: 493-499.
16. Phillips RE, Rowland-Jones S, Nixon DF, Gotch FM, Edwards JP, et al. (1991) Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition. Nature 354: 453-459.
17. Wolinsky SM, Korber BT, Neumann AU, Daniels M, Kunstman KJ, et al. (1996) Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 272: 537-542.
18. Kaslow RA, Carrington M, Apple R, Park L, Muñoz A, et al. (1996) Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat Med 2: 405-411.
19. Kiepiela P, Leslie AJ, Honeyborne I, Ramduth D, Thobakgale C, et al. (2004) Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432: 769-775.
20. Loffredo JT, Maxwell J, Qi Y, Glidden CE, Borchardt GJ, et al. (2007) Mamu-B*08-positive macaques control simian immunodeficiency virus replication. J Virol 81: 8827-8832.
21. Migueles SA, Sabbaghian MS, Shupert WL, Bettinotti MP, Marincola FM, et al. (2000) HLA B*5701 is highly associated with restriction of virus replication in a subgroup of HIV-infected long term nonprogressors. Proc Natl Acad Sci USA 97: 2709-2714.
22. Yant LJ, Friedrich TC, Johnson RC, May GE, Maness NJ, et al. (2006) The high-frequency major histocompatibility complex class I allele Mamu-B*17 is associated with control of simian immunodeficiency virus SIVmac239 replication. J Virol 80: 5074-5077.
23. Allen TM, Jing P, Calore B, Horton H, O'Connor DH, et al. (2002) Effects of cytotoxic T lymphocytes (CTL) directed against a single simian immunodeficiency virus (SIV) Gag CTL epitope on the course of SIVmac239 infection. J Virol 76: 10507-10511.
24. Brodie SJ, Lewinsohn DA, Patterson BK, Jiyamapa D, Krieger J, et al. (1999) In vivo migration and function of transferred HIV-1-specific cytotoxic T cells. Nat Med 5: 34-41.
25. Kawada M, Tsukamoto T, Yamamoto H, Iwamoto N, Kurihara K, et al. (2008) Gag-Specific Cytotoxic T-Lymphocyte-Based Control of Primary Simian Immunodeficiency Virus Replication in a Vaccine Trial. J Virol 82: 10199-10206.
26. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, et al. (2007) CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat Med 13: 46-53.
27. Liang X, Casimiro DR, Schleif WA, Wang F, Davies ME, et al. (2005) Vectored Gag and Env but not Tat show efficacy against simian-human immunodeficiency virus 89.6P challenge in Mamu-A*01-negative rhesus monkeys. J Virol 79: 12321-12331.
28. Liu J, O'Brien KL, Lynch DM, Simmons NL, La Porte A, et al. (2009) Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457: 87-91.
29. Sacha JB, Chung C, Rakasz EG, Spencer SP, Jonas AK, et al. (2007) Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J Immunol 178: 2746-2754.
30. Wilson NA, Reed J, Napoe GS, Piaskowski S, Szymanski A, et al. (2006) Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J Virol 80: 5875-5885.
31. Sacha JB, Chung C, Reed J, Jonas AK, Bean AT, et al. (2007) Pol-specific CD8+ T cells recognize simian immunodeficiency virus-infected cells prior to Nef-mediated major histocompatibility complex class I downregulation. J Virol 81: 11703-11712.
32. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, et al. (2006) HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
33. Horton H, Frank I, Baydo R, Jalbert E, Penn J, et al. (2006) Preservation of T cell proliferation restricted by protective HLA alleles is critical for immune control of HIV-1 infection. J Immunol 177: 7406-7415.
34. Lichterfeld M, Kaufmann DE, Yu XG, Mui SK, Addo MM, et al. (2004) Loss of HIV-1-specific CD8+ T cell proliferation after acute HIV-1 infection and restoration by vaccine-induced HIV-1-specific CD4+ T cells. J Exp Med 200: 701-712.
35. Migueles S, Osborne C, Royce C, Compton A, Joshi R, et al. (2008) Lytic Granule Loading of CD8+ T Cells Is Required for HIV-Infected Cell Elimination Associated with Immune Control. Immunity 29: 1009-1021.
36. Price D, Asher T, Wilson N, Nason M, Brenchley J, et al. (2009) Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. Journal of Experimental Medicine 206: 923-936.
37. Bonaldo MC, Martins MA, Rudersdorf R, Mudd PA, Sacha JB, et al. (2010) Recombinant yellow fever vaccine virus 17D expressing simian immunodeficiency virus SIVmac239 gag induces SIV-specific CD8+ T-cell responses in rhesus macaques. J Virol 84: 3699-3706.
38. Kaizu M, Borchardt GJ, Glidden CE, Fisk DL, Loffredo JT, et al. (2007) Molecular typing of major histocompatibility complex class I alleles in the Indian rhesus macaque which restrict SIV CD8+ T cell epitopes. Immunogenetics 59: 693-703.
39. Friedrich TC, Dodds EJ, Yant LJ, Vojnov L, Rudersdorf R, et al. (2004) Reversion of CTL escape-variant immunodeficiency viruses in vivo. Nat Med 10: 275-281.
40. Friedrich TC, McDermott AB, Reynolds MR, Piaskowski S, Fuenger S, et al. (2004) Consequences of cytotoxic T-lymphocyte escape: common escape mutations in simian immunodeficiency virus are poorly recognized in naive hosts. J Virol 78: 10064-10073.
41. Bimber BN, Burwitz BJ, O'Connor S, Detmer A, Gostick E, et al. (2009) Ultradeep pyrosequencing detects complex patterns of CD8+ T-lymphocyte escape in simian immunodeficiency virus-infected macaques. J Virol 83: 8247-8253.
42. Cline AN, Bess JW, Piatak M, Lifson JD, (2005) Highly sensitive SIV plasma viral load assay: practical considerations, realistic performance expectations, and application to reverse engineering of vaccines for AIDS. J Med Primatol 34: 303-312.
43. Vogel TU, Reynolds MR, Fuller DH, Vielhuber K, Shipley T, et al. (2003) Multispecific vaccine-induced mucosal cytotoxic T lymphocytes reduce acute-phase viral replication but fail in long-term control of simian immunodeficiency virus SIVmac239. J Virol 77: 13348-13360.
44. Skinner PJ, Daniels MA, Schmidt CS, Jameson SC, Haase AT, (2000) Cutting edge: In situ tetramer staining of antigen-specific T cells in tissues. J Immunol 165: 613-617.
45. Folkvord JM, Anderson DM, Arya J, Mawhinney S, Connick E, (2003) Microanatomic relationships between CD8+ cells and HIV-1-producing cells in human lymphoid tissue in vivo. J Acquir Immune Defic Syndr 32: 469-476.
46. Allen TM, Mothé BR, Sidney J, Jing P, Dzuris JL, et al. (2001) CD8(+) lymphocytes from simian immunodeficiency virus-infected rhesus macaques recognize 14 different epitopes bound by the major histocompatibility complex class I molecule mamu-A*01: implications for vaccine design and testing. J Virol 75: 738-749.
47. Seder RA, Darrah PA, Roederer M, (2008) T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8: 247-258.
48. Roederer M, Nozzi JL, Nason MC, (2011) SPICE: Exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79A: 167-174.
49. Reynolds MR, Weiler AM, Weisgrau KL, Piaskowski SM, Furlott JR, et al. (2008) Macaques vaccinated with live-attenuated SIV control replication of heterologous virus. J Exp Med 205: 2537-2550.
50. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, et al. (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200: 749-759.
51. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, et al. (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280: 427-431.
52. Vanderford T, Bleckwehl C, Engram JC, Dunham RM, Klatt N, et al. (2011) Viral CTL Escape Mutants Are Generated in Lymph Nodes and Subsequently Become Fixed in Plasma and Rectal Mucosa during Acute SIV Infection of Macaques. PLoS Pathog 7: e1002048.
53. Folkvord JM, Armon C, Connick E, (2005) Lymphoid follicles are sites of heightened human immunodeficiency virus type 1 (HIV-1) replication and reduced antiretroviral effector mechanisms. AIDS Res Hum Retroviruses 21: 363-370.
54. Barouch DH, Kunstman J, Glowczwskie J, Kunstman KJ, Egan MA, et al. (2003) Viral escape from dominant simian immunodeficiency virus epitope-specific cytotoxic T lymphocytes in DNA-vaccinated rhesus monkeys. J Virol 77: 7367-7375.
55. Friedrich TC, Frye CA, Yant LJ, O'Connor DH, Kriewaldt NA, et al. (2004) Extraepitopic compensatory substitutions partially restore fitness to simian immunodeficiency virus variants that escape from an immunodominant cytotoxic-T-lymphocyte response. J Virol 78: 2581-2585.
56. Reynolds MR, Rakasz E, Skinner PJ, White C, Abel K, et al. (2005) CD8+ T-lymphocyte response to major immunodominant epitopes after vaginal exposure to simian immunodeficiency virus: too late and too little. J Virol 79: 9228-9235.
57. Venturi V, Chin HY, Price DA, Douek DC, Davenport MP, (2008) The role of production frequency in the sharing of simian immunodeficiency virus-specific CD8+ TCRs between macaques. J Immunol 181: 2597-2609.
58. Venturi V, Price DA, Douek DC, Davenport MP, (2008) The molecular basis for public T-cell responses? Nat Rev Immunol 8: 231-238.
59. Loffredo JT, Bean AT, Beal DR, León EJ, May GE, et al. (2008) Patterns of CD8+ immunodominance may influence the ability of Mamu-B*08-positive macaques to naturally control simian immunodeficiency virus SIVmac239 replication. J Virol 82: 1723-1738.
60. Martins MA, Wilson NA, Reed JS, Ahn CD, Klimentidis YC, et al. (2010) T-cell correlates of vaccine efficacy after a heterologous simian immunodeficiency virus challenge. J Virol 84: 4352-4365.