Early skewed distribution of total and HIV-specific CD8+ T-cell memory phenotypes during primary HIV infection is related to reduced antiviral activity and faster disease progression

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Ghiglione, Yanina ^a   Falivene, Juliana ^a   Ruiz, María Julia ^a   Laufer, Natalia ^a,c   Socías, María Eugenia ^b,c   Cahn, Pedro ^b,c   Giavedoni, Luis ^d   Sued, Omar ^b,c   Gherardi, María Magdalena ^a   Salomón, Horacio ^a   Turk, Gabriela ^a  

^a Universidad de Buenos Aires   (Argentina)

^b FUNDACIÓN HUÉSPED   (Argentina)

^c HOSPITAL JUAN A FERNÁNDEZ   (Argentina)

^d SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROGRAMMED DEATH 1 RECEPTOR; CYTOKINE; EPITOPE; PDCD1 PROTEIN, HUMAN; PEPTIDE; T LYMPHOCYTE RECEPTOR;

ANTIVIRAL ACTIVITY; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE STATUS; IMMUNOPHENOTYPING; LYMPHOCYTE DIFFERENTIATION; MAJOR CLINICAL STUDY; MEMORY T LYMPHOCYTE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; T LYMPHOCYTE SUBPOPULATION; VIRUS LOAD; VIRUS REPLICATION; BLOOD; CASE CONTROL STUDY; CELL DIFFERENTIATION; CYTOLOGY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV INFECTIONS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; VIREMIA; VIROLOGY;

ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CASE-CONTROL STUDIES; CD4 LYMPHOCYTE COUNT; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CYTOKINES; DISEASE PROGRESSION; EPITOPES, T-LYMPHOCYTE; HIV; HIV INFECTIONS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; PEPTIDES; PHENOTYPE; PROGRAMMED CELL DEATH 1 RECEPTOR; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTE SUBSETS; VIRAL LOAD; VIREMIA;

EID: 84905666192     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104235     Document Type: Article

References (62)

1. Simon V, Ho DD, Abdool Karim Q (2006) HIV/AIDS epidemiology, pathogenesis, prevention, and treatment. Lancet 368: 489-504. (Pubitemid 44142771)
2. McMichael AJ, Borrow P, Tomaras GD, Goonetilleke N, Haynes BF (2010) The immune response during acute HIV-1 infection: clues for vaccine development. Nature reviews 10: 11-23.
3. Streeck H, Nixon DF (2010) T cell immunity in acute HIV-1 infection. The Journal of infectious diseases 202 Suppl 2: S302-308.
4. Freel SA, Saunders KO, Tomaras GD (2011) CD8(+)T-cell-mediated control of HIV-1 and SIV infection. Immunol Res 49: 135-146.
5. McDermott AB, Koup RA (2012) CD8(+) T cells in preventing HIV infection and disease. Aids 26: 1281-1292.
6. Addo MM, Draenert R, Rathod A, Verrill CL, Davis BT, et al. (2007) Fully differentiated HIV-1 specific CD8+ T effector cells are more frequently detectable in controlled than in progressive HIV-1 infection. PloS one 2: e321.
7. Masemola A, Mashishi T, Khoury G, Mohube P, Mokgotho P, et al. (2004) Hierarchical targeting of subtype C human immunodeficiency virus type 1 proteins by CD8+ T cells: correlation with viral load. Journal of virology 78: 3233-3243. (Pubitemid 38568263)
8. Riou C, Burgers WA, Mlisana K, Koup RA, Roederer M, et al. (2014) Differential impact of magnitude, polyfunctional capacity, and specificity of HIV-specific CD8+ T cell responses on HIV set point. Journal of virology 88: 1819-1824.
9. Saez-Cirion A, Sinet M, Shin SY, Urrutia A, Versmisse P, et al. (2009) Heterogeneity in HIV suppression by CD8 T cells from HIV controllers: association with Gag-specific CD8 T cell responses. J Immunol 182: 7828-7837.
10. Zimmerli SC, Harari A, Cellerai C, Vallelian F, Bart PA, et al. (2005) HIV-1-specific IFN-gamma/IL-2-secreting CD8 T cells support CD4-independent proliferation of HIV-1-specific CD8 T cells. Proceedings of the National Academy of Sciences of the United States of America 102: 7239-7244. (Pubitemid 40696363)
11. Saez-Cirion A, Lacabaratz C, Lambotte O, Versmisse P, Urrutia A, et al. (2007) HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype. Proceedings of the National Academy of Sciences of the United States of America 104: 6776-6781. (Pubitemid 47175577)
12. Day CL, Kiepiela P, Leslie AJ, van der Stok M, Nair K, et al. (2007) Proliferative capacity of epitope-specific CD8 T-cell responses is inversely related to viral load in chronic human immunodeficiency virus type 1 infection. Journal of virology 81: 434-438. (Pubitemid 44975185)
13. 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. (Pubitemid 43882629)
14. 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. The Journal of experimental medicine 204: 2473-2485. (Pubitemid 47529331)
15. Freel SA, Lamoreaux L, Chattopadhyay PK, Saunders K, Zarkowsky D, et al. (2010) Phenotypic and functional profile of HIV-inhibitory CD8 T cells elicited by natural infection and heterologous prime/boost vaccination. Journal of virology 84: 4998-5006.
16. Burgers WA, Riou C, Mlotshwa M, Maenetje P, de Assis Rosa D, et al. (2009) Association of HIV-specific and total CD8+ T memory phenotypes in subtype C HIV-1 infection with viral set point. J Immunol 182: 4751-4761.
17. Cao W, Jamieson BD, Hultin LE, Hultin PM, Effros RB, et al. (2009) Premature aging of T cells is associated with faster HIV-1 disease progression. Journal of acquired immune deficiency syndromes (1999) 50: 137-147.
18. Streeck H, Brumme ZL, Anastario M, Cohen KW, Jolin JS, et al. (2008) Antigen load and viral sequence diversification determine the functional profile of HIV-1-specific CD8+ T cells. PLoS medicine 5: e100.
19. Ganesan A, Chattopadhyay PK, Brodie TM, Qin J, Gu W, et al. (2010) Immunologic and virologic events in early HIV infection predict subsequent rate of progression. The Journal of infectious diseases 201: 272-284.
20. Turk G, Ghiglione Y, Falivene J, Socias ME, Laufer N, et al. (2013) Early Gag immunodominance of the HIV-specific T-cell response during acute/early infection is associated with higher CD8+ T-cell antiviral activity and correlates with preservation of the CD4+ T-cell compartment. Journal of virology 87: 7445-7462.
21. Turk G, Gherardi MM, Laufer N, Saracco M, Luzzi R, et al. (2008) Magnitude, breadth, and functional profile of T-cell responses during human immunodeficiency virus primary infection with B and BF viral variants. Journal of virology 82: 2853-2866. (Pubitemid 351329176)
22. Socias ME, Sued O, Laufer N, Lazaro ME, Mingrone H, et al. (2011) Acute retroviral syndrome and high baseline viral load are predictors of rapid HIV progression among untreated Argentinean seroconverters. Journal of the International AIDS Society 14: 40.
23. Bull M, Lee D, Stucky J, Chiu YL, Rubin A, et al. (2007) Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. Journal of immunological methods 322: 57-69. (Pubitemid 46560582)
24. Maecker HT, Rinfret A, D'Souza P, Darden J, Roig E, et al. (2005) Standardization of cytokine flow cytometry assays. BMC immunology 6: 13.
25. Janetzki S, Cox JH, Oden N, Ferrari G (2005) Standardization and validation issues of the ELISPOT assay. Methods in molecular biology (Clifton, NJ 302: 51-86.
26. Currier JR, Kuta EG, Turk E, Earhart LB, Loomis-Price L, et al. (2002) A panel of MHC class I restricted viral peptides for use as a quality control for vaccine trial ELISPOT assays. Journal of immunological methods 260: 157-172. (Pubitemid 34132882)
27. Malhotra U, Li F, Nolin J, Allison M, Zhao H, et al. (2007) Enhanced detection of human immunodeficiency virus type 1 (HIV-1) Nef-specific T cells recognizing multiple variants in early HIV-1 infection. Journal of virology 81: 5225-5237. (Pubitemid 46744432)
28. Giavedoni LD (2005) Simultaneous detection of multiple cytokines and chemokines from nonhuman primates using luminex technology. Journal of immunological methods 301: 89-101.
29. Fiebig EW, Wright DJ, Rawal BD, Garrett PE, Schumacher RT, et al. (2003) Dynamics of HIV viremia and antibody seroconversion in plasma donors: implications for diagnosis and staging of primary HIV infection. Aids 17: 1871-1879.
30. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, et al. (2004) Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104: 942-947. (Pubitemid 39038012)
31. Mahnke YD, Brodie TM, Sallusto F, Roederer M, Lugli E (2013) The who's who of T-cell differentiation: human memory T-cell subsets. European journal of immunology 43: 2797-2809.
32. Patrick C, Graham SO, Abigail SK, Christian K, Kim E, et al. (2001) Skewed maturation of memory HIV-specific CD8 T lymphocytes. Nature 410.
33. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, et al. (2006) PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443: 350-354. (Pubitemid 44435155)
34. Trautmann L, Mbitikon-Kobo FM, Goulet JP, Peretz Y, Shi Y, et al. (2012) Profound metabolic, functional, and cytolytic differences characterize HIV-specific CD8 T cells in primary and chronic HIV infection. Blood 120: 3466-3477.
35. de Silva TI, Peng Y, Leligdowicz A, Zaidi I, Li L, et al. (2013) Correlates of T-cell-mediated viral control and phenotype of CD8 (+) T cells in HIV-2, a naturally contained human retroviral infection. Blood 121: 4330-4339.
36. Sauce D, Almeida JR, Larsen M, Haro L, Autran B, et al. (2007) PD-1 expression on human CD8 T cells depends on both state of differentiation and activation status. Aids 21: 2005-2013. (Pubitemid 47462149)
37. Demers KR, Reuter MA, Betts MR (2013) CD8(+) T-cell effector function and transcriptional regulation during HIV pathogenesis. Immunol Rev 254: 190-206.
38. 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. (Pubitemid 32225845)
39. Meyer-Olson D, Simons BC, Conrad JA, Smith RM, Barnett L, et al. (2010) Clonal expansion and TCR-independent differentiation shape the HIV-specific CD8+ effector-memory T-cell repertoire in vivo. Blood 116: 396-405.
40. Northfield JW, Loo CP, Barbour JD, Spotts G, Hecht FM, et al. (2007) Human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T(EMRA) cells in early infection are linked to control of HIV-1 viremia and predict the subsequent viral load set point. Journal of virology 81: 5759-5765. (Pubitemid 46847014)
41. Riou C, Treurnicht F, Abrahams MR, Mlisana K, Liu MK, et al. (2012) Increased memory differentiation is associated with decreased polyfunctionality for HIV but not for cytomegalovirus-specific CD8+ T cells. J Immunol 189: 3838-3847.
42. Mahnke YD, Song K, Sauer MM, Nason MC, Giret MT, et al. (2013) Early immunologic and virologic predictors of clinical HIV-1 disease progression. AIDS (London, England) 27: 697-706.
43. Breton G, Chomont N, Takata H, Fromentin R, Ahlers J, et al. (2013) Programmed death-1 is a marker for abnormal distribution of naive/memory T cell subsets in HIV-1 infection. J Immunol 191: 2194-2204.
44. Barbour JD, Ndhlovu LC, Xuan Tan Q, Ho T, Epling L, et al. (2009) High CD8+ T cell activation marks a less differentiated HIV-1 specific CD8+ T cell response that is not altered by suppression of viral replication. PLoS One 4: e4408.
45. Emu B, Moretto WJ, Hoh R, Krone M, Martin JN, et al. (2014) Composition and Function of T Cell Subpopulations Are Slow to Change Despite Effective Antiretroviral Treatment of HIV Disease. PLoS One 9: e85613.
46. Passaes CP, Saez-Cirion A (2014) HIV cure research: advances and prospects. Virology 454-455: 340-352.
47. Pires A, Hardy G, Gazzard B, Gotch F, Imami N (2004) Initiation of antiretroviral therapy during recent HIV-1 infection results in lower residual viral reservoirs. Journal of acquired immune deficiency syndromes (1999) 36: 783-790.
48. Julg B, Williams KL, Reddy S, Bishop K, Qi Y, et al. (2010) Enhanced anti-HIV functional activity associated with Gag-specific CD8 T-cell responses. Journal of virology 84: 5540-5549.
49. Chun TW, Justement JS, Sanford C, Hallahan CW, Planta MA, et al. (2004) Relationship between the frequency of HIV-specific CD8 + T cells and the level of CD38+ CD8+ T cells in untreated HIV-infected individuals. Proceedings of the National Academy of Sciences of the United States of America 101: 2464-2469. (Pubitemid 38269334)
50. Ferrando-Martinez S, Casazza JP, Leal M, Machmach K, Munoz-Fernandez MA, et al. (2012) Differential Gag-specific polyfunctional T cell maturation patterns in HIV-1 elite controllers. Journal of virology 86: 3667-3674.
51. Westrop SJ, Qazi NA, Pido-Lopez J, Nelson MR, Gazzard B, et al. (2009) Transient nature of long-term nonprogression and broad virus-specific proliferative T-cell responses with sustained thymic output in HIV-1 controllers. PloS one 4: e5474.
52. Trautmann L, Janbazian L, Chomont N, Said EA, Gimmig S, et al. (2006) Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med 12: 1198-1202. (Pubitemid 44527357)
53. Zhang JY, Zhang Z, Wang X, Fu JL, Yao J, et al. (2007) PD-1 up-regulation is correlated with HIV-specific memory CD8+ T-cell exhaustion in typical progressors but not in long-term nonprogressors. Blood 109: 4671-4678. (Pubitemid 46827757)
54. Yamamoto T, Price DA, Casazza JP, Ferrari G, Nason M, et al. (2011) Surface expression patterns of negative regulatory molecules identify determinants of virus-specific CD8+ T-cell exhaustion in HIV infection. Blood 117: 4805-4815.
55. Peretz Y, He Z, Shi Y, Yassine-Diab B, Goulet JP, et al. (2012) CD160 and PD-1 co-expression on HIV-specific CD8 T cells defines a subset with advanced dysfunction. PLoS Pathog 8: e1002840.
56. Hong JJ, Amancha PK, Rogers K, Ansari AA and Villinger F (2013) Reevaluation of PD-1 expression by T cells as a marker for immune exhaustion during SIV infection. PloS one 8: e60186.
57. Petrovas C, Chaon B, Ambrozak DR, Price DA, Melenhorst JJ, et al. (2009) Differential association of programmed death-1 and CD57 with ex vivo survival of CD8+ T cells in HIV infection. J Immunol 183: 1120-1132.
58. Zelinskyy G, Myers L, Dietze KK, Gibbert K, Roggendorf M, et al. (2011) Virus-specific CD8+ T cells upregulate programmed death-1 expression during acute friend retrovirus infection but are highly cytotoxic and control virus replication. J Immunol 187: 3730-3737.
59. Wei F, Zhong S, Ma Z, Kong H, Medvec A, et al. (2013) Strength of PD-1 signaling differentially affects T-cell effector functions. Proceedings of the National Academy of Sciences of the United States of America 110: E2480-2489.
60. Killian MS, Johnson C, Teque F, Fujimura S, Levy JA (2011) Natural suppression of human immunodeficiency virus type 1 replication is mediated by transitional memory CD8+ T cells. Journal of virology 85: 1696-1705.
61. 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. Journal of virology 86: 5877-5884.
62. Buckheit RW, 3rd, Salgado M, Silciano RF, Blankson JN (2012) Inhibitory potential of subpopulations of CD8+ T cells in HIV-1-infected elite suppressors. Journal of virology 86: 13679-13688.