TCR Affinity Associated with Functional Differences between Dominant and Subdominant SIV Epitope-Specific CD8+ T Cells in Mamu-A*01+ Rhesus Monkeys

PLoS Pathogens

Volumn 10, Issue 4, 2014, Pages

  Osuna, Christa E ^a,b   Gonzalez, Ana Maria ^a   Chang, Hsun Hsien ^c   Hung, Amy Shi ^a   Ehlinger, Elizabeth ^a   Anasti, Kara ^d   Alam, S Munir ^d   Letvin, Norman L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CHEMOKINE; CYTOKINE; EPITOPE; INTERLEUKIN 2; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTEIN P68; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; VIRUS PROTEIN; HLA ANTIGEN CLASS 1; LYMPHOCYTE ANTIGEN RECEPTOR; MAMU-A 01 ANTIGEN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL MATURATION; CELL PROLIFERATION; CYTOTOXICITY; FLOW CYTOMETRY; GENE EXPRESSION; LYMPHOCYTE SUBPOPULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROARRAY ANALYSIS; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR AFFINITY; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; SURFACE PLASMON RESONANCE; VIRUS REPLICATION; ANIMAL; CHRONIC DISEASE; IMMUNOLOGY; PATHOLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; EPITOPES, T-LYMPHOCYTE; HISTOCOMPATIBILITY ANTIGENS CLASS I; MACACA MULATTA; RECEPTORS, ANTIGEN, T-CELL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84901380623     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004069     Document Type: Article

References (89)

1. Walker CM, Moody DJ, Stites DP, Levy JA, (1986) CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science 234: 1563-1566.
2. 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.
3. Loffredo JT, Bean AT, Beal DR, Leon 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.
4. Yu XG, Addo MM, Rosenberg ES, Rodriguez WR, Lee PK, et al. (2002) Consistent patterns in the development and immunodominance of human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T-cell responses following acute HIV-1 infection. J Virol 76: 8690-8701.
5. Yewdell JW, Bennink JR, (1999) Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 17: 51-88.
6. Akram A, Inman RD, (2012) Immunodominance: a pivotal principle in host response to viral infections. Clin Immunol 143: 99-115.
7. Chen W, McCluskey J, (2006) Immunodominance and immunodomination: critical factors in developing effective CD8+ T-cell-based cancer vaccines. Adv Cancer Res 95: 203-247.
8. Cao W, Myers-Powell BA, Braciale TJ, (1996) The weak CD8+ CTL response to an influenza hemagglutinin epitope reflects limited T cell availability. J Immunol 157: 505-511.
9. Haeryfar SM, Hickman HD, Irvine KR, Tscharke DC, Bennink JR, et al. (2008) Terminal deoxynucleotidyl transferase establishes and broadens antiviral CD8+ T cell immunodominance hierarchies. J Immunol 181: 649-659.
10. Messaoudi I, Guevara Patino JA, Dyall R, LeMaoult J, Nikolich-Zugich J, (2002) Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 298: 1797-1800.
11. Belz GT, Stevenson PG, Doherty PC, (2000) Contemporary analysis of MHC-related immunodominance hierarchies in the CD8+ T cell response to influenza A viruses. J Immunol 165: 2404-2409.
12. Deng Y, Yewdell JW, Eisenlohr LC, Bennink JR, (1997) MHC affinity, peptide liberation, T cell repertoire, and immunodominance all contribute to the paucity of MHC class I-restricted peptides recognized by antiviral CTL. J Immunol 158: 1507-1515.
13. Harari A, Dutoit V, Cellerai C, Bart PA, Du Pasquier RA, et al. (2006) Functional signatures of protective antiviral T-cell immunity in human virus infections. Immunol Rev 211: 236-254.
14. 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.
15. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, et al. (2007) Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J Exp Med 204: 2473-2485.
16. Critchfield JW, Lemongello D, Walker DH, Garcia JC, Asmuth DM, et al. (2007) Multifunctional human immunodeficiency virus (HIV) gag-specific CD8+ T-cell responses in rectal mucosa and peripheral blood mononuclear cells during chronic HIV type 1 infection. J Virol 81: 5460-5471.
17. Ferre AL, Hunt PW, Critchfield JW, Young DH, Morris MM, et al. (2009) Mucosal immune responses to HIV-1 in elite controllers: a potential correlate of immune control. Blood 113: 3978-3989.
18. Perreau M, Levy Y, Pantaleo G, (2013) Immune response to HIV. Curr Opin HIV AIDS 8: 333-340.
19. Rodriguez F, Slifka MK, Harkins S, Whitton JL, (2001) Two overlapping subdominant epitopes identified by DNA immunization induce protective CD8(+) T-cell populations with differing cytolytic activities. J Virol 75: 7399-7409.
20. Baron C, Meunier MC, Caron E, Cote C, Cameron MJ, et al. (2006) Asynchronous differentiation of CD8 T cells that recognize dominant and cryptic antigens. J Immunol 177: 8466-8475.
21. Payne RP, Kloverpris H, Sacha JB, Brumme Z, Brumme C, et al. (2010) Efficacious early antiviral activity of HIV Gag- and Pol-specific HLA-B 2705-restricted CD8+ T cells. J Virol 84: 10543-10557.
22. Allen TM, Mothe 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.
23. Newberg MH, McEvers KJ, Gorgone DA, Lifton MA, Baumeister SH, et al. (2006) Immunodomination in the evolution of dominant epitope-specific CD8+ T lymphocyte responses in simian immunodeficiency virus-infected rhesus monkeys. J Immunol 176: 319-328.
24. Seth A, Ourmanov I, Schmitz JE, Kuroda MJ, Lifton MA, et al. (2000) Immunization with a modified vaccinia virus expressing simian immunodeficiency virus (SIV) Gag-Pol primes for an anamnestic Gag-specific cytotoxic T-lymphocyte response and is associated with reduction of viremia after SIV challenge. J Virol 74: 2502-2509.
25. Price DA, Asher TE, Wilson NA, Nason MC, Brenchley JM, et al. (2009) Public clonotype usage identifies protective Gag-specific CD8+ T cell responses in SIV infection. J Exp Med 206: 923-936.
26. Yamamoto T, Johnson MJ, Price DA, Wolinsky DI, Almeida JR, et al. (2012) Virus inhibition activity of effector memory CD8(+) T cells determines simian immunodeficiency virus load in vaccinated monkeys after vaccine breakthrough infection. J Virol 86: 5877-5884.
27. Wrzesien-Kus A, Smolewski P, Sobczak-Pluta A, Wierzbowska A, Robak T, (2004) The inhibitor of apoptosis protein family and its antagonists in acute leukemias. Apoptosis 9: 705-715.
28. Kumar S, (2009) Caspase 2 in apoptosis, the DNA damage response and tumour suppression: enigma no more? Nat Rev Cancer 9: 897-903.
29. Nguyen HG, Chinnappan D, Urano T, Ravid K, (2005) Mechanism of Aurora-B degradation and its dependency on intact KEN and A-boxes: identification of an aneuploidy-promoting property. Mol Cell Biol 25: 4977-4992.
30. Stewart S, Fang G, (2005) Destruction box-dependent degradation of aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Res 65: 8730-8735.
31. Satyanarayana A, Kaldis P, (2009) Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28: 2925-2939.
32. Olson MF, Ashworth A, Hall A, (1995) An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269: 1270-1272.
33. Iyer J, Moghe S, Furukawa M, Tsai MY, (2011) What's Nu(SAP) in mitosis and cancer? Cell Signal 23: 991-998.
34. Fang Z, Xing F, Bronner C, Teng Z, Guo Z, (2009) ICBP90 mediates the ERK1/2 signaling to regulate the proliferation of Jurkat T cells. Cell Immunol 257: 80-87.
35. Tien AL, Senbanerjee S, Kulkarni A, Mudbhary R, Goudreau B, et al. (2011) UHRF1 depletion causes a G2/M arrest, activation of DNA damage response and apoptosis. Biochem J 435: 175-185.
36. Kastan MB, Zhan Q, el-Deiry WS, Carrier F, Jacks T, et al. (1992) A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71: 587-597.
37. Letvin NL, Rao SS, Montefiori DC, Seaman MS, Sun Y, et al. (2011) Immune and Genetic Correlates of Vaccine Protection Against Mucosal Infection by SIV in Monkeys. Sci Transl Med 3: 81ra36.
38. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, et al. (2002) Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168: 29-43.
39. Takata H, Takiguchi M, (2006) Three memory subsets of human CD8+ T cells differently expressing three cytolytic effector molecules. J Immunol 177: 4330-4340.
40. Tomiyama H, Matsuda T, Takiguchi M, (2002) Differentiation of human CD8(+) T cells from a memory to memory/effector phenotype. J Immunol 168: 5538-5550.
41. Champagne P, Ogg GS, King AS, Knabenhans C, Ellefsen K, et al. (2001) Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410: 106-111.
42. Slifka MK, Rodriguez F, Whitton JL, (1999) Rapid on/off cycling of cytokine production by virus-specific CD8+ T cells. Nature 401: 76-79.
43. Valitutti S, Muller S, Dessing M, Lanzavecchia A, (1996) Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J Exp Med 183: 1917-1921.
44. Kersh GJ, Kersh EN, Fremont DH, Allen PM, (1998) High- and low-potency ligands with similar affinities for the TCR: the importance of kinetics in TCR signaling. Immunity 9: 817-826.
45. Holler PD, Kranz DM, (2003) Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18: 255-264.
46. Matsui K, Boniface JJ, Steffner P, Reay PA, Davis MM, (1994) Kinetics of T-cell receptor binding to peptide/I-Ek complexes: correlation of the dissociation rate with T-cell responsiveness. Proc Natl Acad Sci U S A 91: 12862-12866.
47. Tian S, Maile R, Collins EJ, Frelinger JA, (2007) CD8+ T cell activation is governed by TCR-peptide/MHC affinity, not dissociation rate. J Immunol 179: 2952-2960.
48. Lyons DS, Lieberman SA, Hampl J, Boniface JJ, Chien Y, et al. (1996) A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity 5: 53-61.
49. Ueno T, Tomiyama H, Fujiwara M, Oka S, Takiguchi M, (2004) Functionally impaired HIV-specific CD8 T cells show high affinity TCR-ligand interactions. J Immunol 173: 5451-5457.
50. Cale EM, Bazick HS, Rianprakaisang TA, Alam SM, Letvin NL, (2011) Mutations in a dominant Nef epitope of simian immunodeficiency virus diminish TCR:epitope peptide affinity but not epitope peptide:MHC class I binding. J Immunol 187: 3300-3313.
51. Triebel F, Jitsukawa S, Baixeras E, Roman-Roman S, Genevee C, et al. (1990) LAG-3, a novel lymphocyte activation gene closely related to CD4. J Exp Med 171: 1393-1405.
52. Linsley PS, Greene JL, Tan P, Bradshaw J, Ledbetter JA, et al. (1992) Coexpression and functional cooperation of CTLA-4 and CD28 on activated T lymphocytes. J Exp Med 176: 1595-1604.
53. Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, et al. (2007) Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
54. Takamura S, Tsuji-Kawahara S, Yagita H, Akiba H, Sakamoto M, et al. (2010) Premature terminal exhaustion of Friend virus-specific effector CD8+ T cells by rapid induction of multiple inhibitory receptors. J Immunol 184: 4696-4707.
55. Price P, Keane N, Gray L, Lee S, Gorry PR, et al. (2006) CXCR4 or CCR5 tropism of human immunodeficiency virus type 1 isolates does not determine the immunological milieu in patients responding to antiretroviral therapy. Viral Immunol 19: 734-740.
56. Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, et al. (2009) Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 10: 29-37.
57. Lim AY, Price P, Beilharz MW, French MA, (2006) Cell surface markers of regulatory T cells are not associated with increased forkhead box p3 expression in blood CD4+ T cells from HIV-infected patients responding to antiretroviral therapy. Immunol Cell Biol 84: 530-536.
58. Pena J, Jones NG, Bousheri S, Bangsberg DR, Cao H, (2013) Lymphocyte Activation Gene-3 Expression Defines a Discrete Subset of HIV-Specific CD8 T Cells That Is Associated with Lower Viral Load. AIDS Res Hum Retroviruses [epub ahead of print].
59. Yee C, Savage PA, Lee PP, Davis MM, Greenberg PD, (1999) Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J Immunol 162: 2227-2234.
60. Iglesias MC, Almeida JR, Fastenackels S, van Bockel DJ, Hashimoto M, et al. (2011) Escape from highly effective public CD8+ T-cell clonotypes by HIV. Blood 118: 2138-2149.
61. Bennett MS, Joseph A, Ng HL, Goldstein H, Yang OO, (2010) Fine-tuning of T-cell receptor avidity to increase HIV epitope variant recognition by cytotoxic T lymphocytes. AIDS 24: 2619-2628.
62. Harari A, Cellerai C, Enders FB, Kostler J, Codarri L, et al. (2007) Skewed association of polyfunctional antigen-specific CD8 T cell populations with HLA-B genotype. Proc Natl Acad Sci U S A 104: 16233-16238.
63. Vigano S, Enders FB, Miconnet I, Cellerai C, Savoye AL, et al. (2013) Rapid perturbation in viremia levels drives increases in functional avidity of HIV-specific CD8 T cells. PLoS Pathog 9: e1003423.
64. Conrad JA, Ramalingam RK, Smith RM, Barnett L, Lorey SL, et al. (2011) Dominant clonotypes within HIV-specific T cell responses are programmed death-1high and CD127low and display reduced variant cross-reactivity. J Immunol 186: 6871-6885.
65. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, et al. (2004) HIV evolution: CTL escape mutation and reversion after transmission. Nat Med 10: 282-289.
66. 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.
67. Vogel TU, Friedrich TC, O'Connor DH, Rehrauer W, Dodds EJ, et al. (2002) Escape in one of two cytotoxic T-lymphocyte epitopes bound by a high-frequency major histocompatibility complex class I molecule, Mamu-A*02: a paradigm for virus evolution and persistence? J Virol 76: 11623-11636.
68. Molldrem JJ, Lee PP, Kant S, Wieder E, Jiang W, et al. (2003) Chronic myelogenous leukemia shapes host immunity by selective deletion of high-avidity leukemia-specific T cells. J Clin Invest 111: 639-647.
69. Van Parijs L, Abbas AK, (1998) Homeostasis and self-tolerance in the immune system: turning lymphocytes off. Science 280: 243-248.
70. 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.
71. 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.
72. Berger CT, Frahm N, Price DA, Mothe B, Ghebremichael M, et al. (2011) High-functional-avidity cytotoxic T lymphocyte responses to HLA-B-restricted Gag-derived epitopes associated with relative HIV control. J Virol 85: 9334-9345.
73. Mothe B, Llano A, Ibarrondo J, Zamarreno J, Schiaulini M, et al. (2012) CTL responses of high functional avidity and broad variant cross-reactivity are associated with HIV control. PLoS One 7: e29717.
74. Turnbull EL, Lopes AR, Jones NA, Cornforth D, Newton P, et al. (2006) HIV-1 epitope-specific CD8+ T cell responses strongly associated with delayed disease progression cross-recognize epitope variants efficiently. J Immunol 176: 6130-6146.
75. St Leger AJ, Peters B, Sidney J, Sette A, Hendricks RL, (2011) Defining the herpes simplex virus-specific CD8+ T cell repertoire in C57BL/6 mice. J Immunol 186: 3927-3933.
76. La Gruta NL, Doherty PC, Turner SJ, (2006) A correlation between function and selected measures of T cell avidity in influenza virus-specific CD8+ T cell responses. Eur J Immunol 36: 2951-2959.
77. Fahmy TM, Bieler JG, Edidin M, Schneck JP, (2001) Increased TCR avidity after T cell activation: a mechanism for sensing low-density antigen. Immunity 14: 135-143.
78. Xiao Z, Mescher MF, Jameson SC, (2007) Detuning CD8 T cells: down-regulation of CD8 expression, tetramer binding, and response during CTL activation. J Exp Med 204: 2667-2677.
79. Wang XL, Altman JD, (2003) Caveats in the design of MHC class I tetramer/antigen-specific T lymphocytes dissociation assays. J Immunol Methods 280: 25-35.
80. Boniface JJ, Reich Z, Lyons DS, Davis MM, (1999) Thermodynamics of T cell receptor binding to peptide-MHC: evidence for a general mechanism of molecular scanning. Proc Natl Acad Sci U S A 96: 11446-11451.
81. Willcox BE, Gao GF, Wyer JR, Ladbury JE, Bell JI, et al. (1999) TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 10: 357-365.
82. Garcia KC, Radu CG, Ho J, Ober RJ, Ward ES, (2001) Kinetics and thermodynamics of T cell receptor- autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 98: 6818-6823.
83. Varela-Rohena A, Molloy PE, Dunn SM, Li Y, Suhoski MM, et al. (2008) Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 14: 1390-1395.
84. Knapp LA, Lehmann E, Piekarczyk MS, Urvater JA, Watkins DI, (1997) A high frequency of Mamu-A*01 in the rhesus macaque detected by polymerase chain reaction with sequence-specific primers and direct sequencing. Tissue Antigens 50: 657-661.
85. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, et al. (1996) Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
86. Kuroda MJ, Schmitz JE, Barouch DH, Craiu A, Allen TM, et al. (1998) Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virus-infected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J Exp Med 187: 1373-1381.
87. Makedonas G, Banerjee PP, Pandey R, Hersperger AR, Sanborn KB, et al. (2009) Rapid up-regulation and granule-independent transport of perforin to the immunological synapse define a novel mechanism of antigen-specific CD8+ T cell cytotoxic activity. J Immunol 182: 5560-5569.
88. Alam SM, Davies GM, Lin CM, Zal T, Nasholds W, et al. (1999) Qualitative and quantitative differences in T cell receptor binding of agonist and antagonist ligands. Immunity 10: 227-237.
89. Alam SM, Travers PJ, Wung JL, Nasholds W, Redpath S, et al. (1996) T-cell-receptor affinity and thymocyte positive selection. Nature 381: 616-620.