Restoration of CD4+ responses to copathogens in HIV-infected individuals on antiretroviral therapy is dependent on T cell memory phenotype

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2273-2281

  Riou, Catherine ^a   Tanko, Ramla F ^a   Soares, Andreia P ^a   Masson, Lindi ^a,b   Werner, Lise ^b   Garrett, Nigel J ^b   Samsunder, Natasha ^b   Abdool Karim, Quarraisha ^b   Abdool Karim, Salim S ^b   Burgers, Wendy A ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; GAMMA INTERFERON; INTERLEUKIN 2; TUMOR NECROSIS FACTOR ALPHA; CD27 ANTIGEN; CD45 ANTIGEN;

ANTIGEN SPECIFICITY; ARTICLE; CD4 CD8 RATIO; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CELL MATURATION; CELL SPECIFICITY; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOMEGALOVIRUS; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOREACTIVITY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MEMORY T LYMPHOCYTE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIRUS REPLICATION; CELL CULTURE; CYTOMEGALOVIRUS INFECTION; DRUG EFFECTS; FLOW CYTOMETRY; HIV INFECTIONS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TREATMENT OUTCOME; TUBERCULOSIS; VIROLOGY; VIRUS LOAD;

ANTI-RETROVIRAL AGENTS; ANTIGENS, CD27; ANTIGENS, CD45; CD4 LYMPHOCYTE COUNT; CD4-CD8 RATIO; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FLOW CYTOMETRY; HIV INFECTIONS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; MYCOBACTERIUM TUBERCULOSIS; TREATMENT OUTCOME; TUBERCULOSIS; VIRAL LOAD;

EID: 84940116811     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500803     Document Type: Article

References (66)

1. Moir, S., T. W. Chun, and A. S. Fauci. 2011. Pathogenic mechanisms of HIV disease. Annu. Rev. Pathol. 6: 223-248.
2. Okoye, A. A., and L. J. Picker. 2013. CD4(+) T-cell depletion in HIV infection: mechanisms of immunological failure. Immunol. Rev. 254: 54-64.
3. Doitsh, G., N. L. Galloway, X. Geng, Z. Yang, K.M. Monroe, O. Zepeda, P.W. Hunt, H. Hatano, S. Sowinski, I. Muñoz-Arias, and W. C. Greene. 2014. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature 505: 509-514.
4. Shearer, G. M., and M. Clerici. 1991. Early T-helper cell defects in HIV infection. AIDS 5: 245-253.
5. Luciano, A. A., M. M. Lederman, A. Valentin-Torres, D. A. Bazdar, and S. F. Sieg. 2007. Impaired induction of CD27 and CD28 predicts naive CD4 T cell proliferation defects in HIV disease. J. Immunol. 179: 3543-3549.
6. Morou, A., B. E. Palmer, and D. E. Kaufmann. 2014. Distinctive features of CD4+ T cell dysfunction in chronic viral infections. Curr. Opin. HIV AIDS 9: 446-451.
7. Boswell, K. L., R. Paris, E. Boritz, D. Ambrozak, T. Yamamoto, S. Darko, K. Wloka, A. Wheatley, S. Narpala, A. McDermott, et al. 2014. Loss of circulating CD4 T cells with B cell helper function during chronic HIV infection. PLoS Pathog. 10: e1003853.
8. Saharia, K. K., and R. A. Koup. 2013. T cell susceptibility to HIV influences outcome of opportunistic infections. Cell 155: 505-514.
9. Sonnenberg, P., J. R. Glynn, K. Fielding, J. Murray, P. Godfrey-Faussett, and S. Shearer. 2005. How soon after infection with HIV does the risk of tuberculosis start to increase? A retrospective cohort study in South African gold miners. J. Infect. Dis. 191: 150-158.
10. Geldmacher, C., A. Zumla, and M. Hoelscher. 2012. Interaction between HIV and Mycobacterium tuberculosis: HIV-1-induced CD4 T-cell depletion and the development of active tuberculosis. Curr. Opin. HIV AIDS 7: 268-275.
11. Williams, B. G., V. Lima, and E. Gouws. 2011. Modelling the impact of antiretroviral therapy on the epidemic of HIV. Curr. HIV Res. 9: 367-382.
12. Guihot, A., A. Bourgarit, G. Carcelain, and B. Autran. 2011. Immune reconstitution after a decade of combined antiretroviral therapies for human immunodeficiency virus. Trends Immunol. 32: 131-137.
13. Corbeau, P., and J. Reynes. 2011. Immune reconstitution under antiretroviral therapy: the new challenge in HIV-1 infection. Blood 117: 5582-5590.
14. Schluger, N. W., D. Perez, and Y. M. Liu. 2002. Reconstitution of immune responses to tuberculosis in patients with HIV infection who receive antiretroviral therapy. Chest 122: 597-602.
15. Keane, N. M., P. Price, S. Lee, C. A. Almeida, S. F. Stone, I. James, and M. A. French. 2004. Restoration of CD4 T-cell responses to cytomegalovirus is short-lived in severely immunodeficient HIV-infected patients responding to highly active antiretroviral therapy. HIV Med. 5: 407-414.
16. Burgess, K., P. Price, I. R. James, S. F. Stone, N. M. Keane, A. Y. Lim, J. R. Warmington, and M. A. French. 2006. Interferon-gamma responses to Candida recover slowly or remain low in immunodeficient HIV patients responding to ART. J. Clin. Immunol. 26: 160-167.
17. Wilkinson, K. A., R. Seldon, G. Meintjes, M. X. Rangaka, W. A. Hanekom, G. Maartens, and R. J. Wilkinson. 2009. Dissection of regenerating T-Cell responses against tuberculosis in HIV-infected adults sensitized by Mycobacterium tuberculosis. Am. J. Respir. Crit. Care Med. 180: 674-683.
18. Sutherland, J. S., J. M. Young, K. L. Peterson, B. Sanneh, H. C. Whittle, S. L. Rowland-Jones, R. A. Adegbola, A. Jaye, and M. O. Ota. 2010. Polyfunctional CD4(+) and CD8(+) T cell responses to tuberculosis antigens in HIV- 1-infected patients before and after anti-retroviral treatment. J. Immunol. 184: 6537-6544.
19. Hsu, D. C., S. J. Kerr, T. Iampornsin, S. L. Pett, A. Avihingsanon, P. Thongpaeng, J. J. Zaunders, S. Ubolyam, J. Ananworanich, A. D. Kelleher, and D. A. Cooper. 2013. Restoration of CMV-specific-CD4 T cells with ART occurs early and is greater in those with more advanced immunodeficiency. PLoS One 8: e77479.
20. Jambo, K. C., D. H. Banda, L. Afran, A. M. Kankwatira, R. D. Malamba, T. J. Allain, S. B. Gordon, R. S. Heyderman, D. G. Russell, and H. C. Mwandumba. 2014. Asymptomatic HIV-infected individuals on antiretroviral therapy exhibit impaired lung CD4(+) T-cell responses to mycobacteria. Am. J. Respir. Crit. Care Med. 190: 938-947.
21. Kaufmann, G. R., H. Furrer, B. Ledergerber, L. Perrin, M. Opravil, P. Vernazza, M. Cavassini, E. Bernasconi, M. Rickenbach, B. Hirschel, and M. Battegay, Swiss HIV Cohort Study. 2005. Characteristics, determinants, and clinical relevance of CD4 T cell recovery to ,500 cells/microL in HIV type 1-infected individuals receiving potent antiretroviral therapy. Clin. Infect. Dis. 41: 361-372.
22. Aiuti, F., and I. Mezzaroma. 2006. Failure to reconstitute CD4+ T-cells despite suppression of HIV replication under HAART. AIDS Rev. 8: 88-97.
23. Le, T., E. J. Wright, D. M. Smith, W. He, G. Catano, J. F. Okulicz, J. A. Young, R. A. Clark, D. D. Richman, S. J. Little, and S. K. Ahuja. 2013. Enhanced CD4+ T-cell recovery with earlier HIV-1 antiretroviral therapy. N. Engl. J. Med. 368: 218-230.
24. Mlisana, K., L. Werner, N. J. Garrett, L. R. McKinnon, F. van Loggerenberg, J. A. Passmore, C. M. Gray, L. Morris, C. Williamson, and S. S. Abdool Karim, Centre for the AIDS Programme of Research in South Africa (CAPRISA) 002 Study Team. 2014. Rapid disease progression in HIV-1 subtype C-infected South African women. Clin. Infect. Dis. 59: 1322-1331.
25. van Loggerenberg, F., K. Mlisana, C. Williamson, S. C. Auld, L. Morris, C. M. Gray, Q. Abdool Karim, A. Grobler, N. Barnabas, I. Iriogbe, S. S. Abdool Karim, and C. A. I. S. Team. 2008. Establishing a cohort at high risk of HIV infection in South Africa: challenges and experiences of the CAPRISA 002 acute infection study. PLoS One 3: e1954.
26. Abdool Karim, Q., S. S. Abdool Karim, J. A. Frohlich, A. C. Grobler, C. Baxter, L. E. Mansoor, A. B. Kharsany, S. Sibeko, K. P. Mlisana, Z. Omar, et al; CAPRISA 004 Trial Group. 2010. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science 329: 1168-1174.
27. Roederer,M., J. L. Nozzi, andM. C. Nason. 2011. SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79: 167-174.
28. Mahnke, Y. D., J. H. Greenwald, R. DerSimonian, G. Roby, L. R. Antonelli, A. Sher, M. Roederer, and I. Sereti. 2012. Selective expansion of polyfunctional pathogen-specific CD4(+) T cells in HIV-1-infected patients with immune reconstitution inflammatory syndrome. Blood 119: 3105-3112.
29. Rehr, M., J. Cahenzli, A. Haas, D. A. Price, E. Gostick, M. Huber, U. Karrer, and A. Oxenius. 2008. Emergence of polyfunctional CD8+ T cells after prolonged suppression of human immunodeficiency virus replication by antiretroviral therapy. J. Virol. 82: 3391-3404.
30. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
31. Sallusto, F., D. Lenig, R. Fö rster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
32. Riou, C., F. Treurnicht, M. R. Abrahams, K. Mlisana, M. K. Liu, N. Goonetilleke, R. Koup, M. Roederer, S. Abdool Karim, G. de Bruyn, et al; CAPRISA 002 Study Team. 2012. Increased memory differentiation is associated with decreased polyfunctionality for HIV but not for cytomegalovirusspecific CD8+ T cells. J. Immunol. 189: 3838-3847.
33. Casazza, J. P., M. R. Betts, D. A. Price, M. L. Precopio, L. E. Ruff, J. M. Brenchley, B. J. Hill, M. Roederer, D. C. Douek, and R. A. Koup. 2006. Acquisition of direct antiviral effector functions by CMV-specific CD4+ T lymphocytes with cellular maturation. J. Exp. Med. 203: 2865-2877.
34. Wilson, E. M., and I. Sereti. 2013. Immune restoration after antiretroviral therapy: the pitfalls of hasty or incomplete repairs. Immunol. Rev. 254: 343-354.
35. Bucy, R. P., R. D. Hockett, C. A. Derdeyn, M. S. Saag, K. Squires, M. Sillers, R. T. Mitsuyasu, and J. M. Kilby. 1999. Initial increase in blood CD4(+) lymphocytes after HIV antiretroviral therapy reflects redistribution from lymphoid tissues. J. Clin. Invest. 103: 1391-1398.
36. Pakker, N. G., D. W. Notermans, R. J. de Boer, M. T. Roos, F. de Wolf, A. Hill, J. M. Leonard, S. A. Danner, F. Miedema, and P. T. Schellekens. 1998. Biphasic kinetics of peripheral blood T cells after triple combination therapy in HIV-1 infection: a composite of redistribution and proliferation. Nat. Med. 4: 208-214.
37. Marchetti, G., A. Gori, A. Casabianca, M. Magnani, F. Franzetti, M. Clerici, C. F. Perno, Ad. Monforte, M. Galli, and L. Meroni. 2006. Comparative analysis of T-cell turnover and homeostatic parameters in HIV-infected patients with discordant immune-virological responses to HAART. AIDS 20: 1727-1736.
38. Piconi, S., D. Trabattoni, A. Gori, S. Parisotto, C. Magni, P. Meraviglia, A. Bandera, A. Capetti, G. Rizzardini, and M. Clerici. 2010. Immune activation, apoptosis, and Treg activity are associated with persistently reduced CD4+ T-cell counts during antiretroviral therapy. AIDS 24: 1991-2000.
39. Delgado, J., M. Leal, E. Ruiz-Mateos, M. Martínez-Moya, A. Rubio, E. Merchante, R. de la Rosa, A. Sánchez-Quijano, and E. Lissen. 2002. Evidence of thymic function in heavily antiretroviral-treated human immunodeficiency virus type 1-infected adults with long-term virologic treatment failure. J. Infect. Dis. 186: 410-414.
40. Dion, M. L., R. Bordi, J. Zeidan, R. Asaad, M. R. Boulassel, J. P. Routy, M. M. Lederman, R. P. Sekaly, and R. Cheynier. 2007. Slow disease progression and robust therapy-mediated CD4+ T-cell recovery are associated with efficient thymopoiesis during HIV-1 infection. Blood 109: 2912-2920.
41. Goicoechea, M., D. M. Smith, L. Liu, S. May, A. R. Tenorio, C. C. Ignacio, A. Landay, and R. Haubrich. 2006. Determinants of CD4+ T cell recovery during suppressive antiretroviral therapy: association of immune activation, T cell maturation markers, and cellular HIV-1 DNA. J. Infect. Dis. 194: 29-37.
42. Kaufmann, G. R., M. Bloch, R. Finlayson, J. Zaunders, D. Smith, and D. A. Cooper. 2002. The extent of HIV-1-related immunodeficiency and age predict the long-term CD4 T lymphocyte response to potent antiretroviral therapy. AIDS 16: 359-367.
43. Allers, K., D. Bö sel, H. J. Epple, H. Karcher, W. Schmidt, D. Kunkel, A. Geelhaar-Karsch, K. Schinnerling, V. Moos, and T. Schneider. 2014. Effect of age on the CD4+ T-cell impairment in HIV-infected persons without and with cART. J. Acquir. Immune Defic. Syndr. 66: 7-15.
44. Almeida, M., M. Cordero, J. Almeida, and A. Orfao. 2007. Abnormal cytokine production by circulating monocytes and dendritic cells of myeloid origin in ART-treated HIV-1+ patients relates to CD4+ T-cell recovery and HCV co-infection. Curr. HIV Res. 5: 325-336.
45. Kaufmann, G. R., L. Elzi, R. Weber, H. Furrer, S. Giulieri, P. Vernazza, E. Bernasconi, B. Hirschel, and M. Battegay, Swiss HIV Cohort Study. 2011. Interruptions of cART limits CD4 T-cell recovery and increases the risk for opportunistic complications and death. AIDS 25: 441-451.
46. Ahlers, J. D., and I. M. Belyakov. 2010. Molecular pathways regulating CD4(+) T cell differentiation, anergy and memory with implications for vaccines. Trends Mol. Med. 16: 478-491.
47. Hodge, J. N., S. Srinivasula, Z. Hu, S. W. Read, B. O. Porter, I. Kim, J. M. Mican, C. Paik, P. Degrange, M. Di Mascio, and I. Sereti. 2011. Decreases in IL-7 levels during antiretroviral treatment of HIV infection suggest a primary mechanism of receptor-mediated clearance. Blood 118: 3244-3253.
48. Prezzemolo, T., G. Guggino, M. P. La Manna, D. Di Liberto, F. Dieli, and N. Caccamo. 2014. Functional signatures of human CD4 and CD8 T cell responses to Mycobacterium tuberculosis. Front. Immunol. 5: 180. Available at: http://journal.frontiersin.org/article/10.3389/fimmu.2014.00180/abstract.
49. Schuetz, A., J. Dirks, U. Sester, A. Haule, N. Elias, C. Geldmacher, E. Sanga, L. Maboko, K. Reither, M. Hoelscher, et al. 2012. Pathogen prevalence may determine maintenance of antigen-specific T-cell responses in HIV-infected individuals. AIDS 26: 695-700.
50. Adekambi, T., C. C. Ibegbu, A. S. Kalokhe, T. Yu, S. M. Ray, and J. Rengarajan. 2012. Distinct effector memory CD4+ T cell signatures in latent Mycobacterium tuberculosis infection, BCG vaccination and clinically resolved tuberculosis. PLoS One 7: e36046.
51. Marín, N. D., S. C. Parí's, M. Rojas, and L. F. García. 2012. Reduced frequency of memory T cells and increased Th17 responses in patients with active tuberculosis. Clin. Vaccine Immunol. 19: 1667-1676.
52. Tapaninen, P., A. Korhonen, L. Pusa, I. Seppälä, and T. Tuuminen. 2010. Effector memory T-cells dominate immune responses in tuberculosis treatment: antigen or bacteria persistence? Int. J. Tuberc. Lung Dis. 14: 347-355.
53. Mitchell, J. E., S. Chetty, P. Govender, M. Pillay, M. Jaggernath, A. Kasmar, T. Ndung'u, P. Klenerman, B. D. Walker, and V. O. Kasprowicz. 2012. Prospective monitoring reveals dynamic levels of T cell immunity to Mycobacterium tuberculosis in HIV infected individuals. PLoS One 7: e37920.
54. Caccamo, N., S. Meraviglia, C. La Mendola, G. Guggino, F. Dieli, and A. Salerno. 2006. Phenotypical and functional analysis of memory and effector human CD8 T cells specific for mycobacterial antigens. J. Immunol. 177: 1780-1785.
55. Chatterjee, S., C. E. Clark, E. Lugli, M. Roederer, and T. B. Nutman. 2015. Filarial infection modulates the immune response to Mycobacterium tuberculosis through expansion of CD4+ IL-4 memory T cells. J. Immunol. 194: 2706-2714.
56. Gattinoni, L., E. Lugli, Y. Ji, Z. Pos, C. M. Paulos, M. F. Quigley, J. R. Almeida, E. Gostick, Z. Yu, C. Carpenito, et al. 2011. A human memory T cell subset with stem cell-like properties. Nat. Med. 17: 1290-1297.
57. Lugli, E., M. H. Dominguez, L. Gattinoni, P. K. Chattopadhyay, D. L. Bolton, K. Song, N. R. Klatt, J. M. Brenchley, M. Vaccari, E. Gostick, et al. 2013. Superior T memory stem cell persistence supports long-lived T cell memory. J. Clin. Invest. 123: 594-599.
58. Betts, M. R., M. C. Nason, S. M. West, S. C. De Rosa, S. A. Migueles, J. Abraham, M. M. Lederman, J. M. Benito, P. A. Goepfert, M. Connors, et al. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107: 4781-4789.
59. Darrah, P. A., D. T. Patel, P. M. De Luca, R.W. Lindsay, D. F. Davey, B. J. Flynn, S. T. Hoff, P. Andersen, S. G. Reed, S. L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13: 843-850.
60. Day, C. L., N. Mkhwanazi, S. Reddy, Z. Mncube, M. van der Stok, P. Klenerman, and B. D. Walker. 2008. Detection of polyfunctional Mycobacterium tuberculosis- specific T cells and association with viral load in HIV-1-infected persons. J. Infect. Dis. 197: 990-999.
61. McBride, A., J. Konowich, and P. Salgame. 2013. Host defense and recruitment of Foxp3+ T regulatory cells to the lungs in chronic Mycobacterium tuberculosis infection requires toll-like receptor 2. PLoS Pathog. 9: e1003397.
62. Scriba, T. J., B. Kalsdorf, D. A. Abrahams, F. Isaacs, J. Hofmeister, G. Black, H. Y. Hassan, R. J. Wilkinson, G. Walzl, S. J. Gelderbloem, et al. 2008. Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J. Immunol. 180: 1962-1970.
63. Slight, S. R., J. Rangel-Moreno, R. Gopal, Y. Lin, B. A. Fallert Junecko, S. Mehra, M. Selman, E. Becerril-Villanueva, J. Baquera-Heredia, L. Pavon, et al. 2013. CXCR5 T helper cells mediate protective immunity against tuberculosis. J. Clin. Invest. 123: 712-726.
64. Wozniak, T. M., B. M. Saunders, A. A. Ryan, and W. J. Britton. 2010. Mycobacterium bovis BCG-specific Th17 cells confer partial protection against Mycobacterium tuberculosis infection in the absence of gamma interferon. Infect. Immun. 78: 4187-4194.
65. Girardi, E., C. A. Sabin, A. d'Arminio Monforte, B. Hogg, A. N. Phillips, M. J. Gill, F. Dabis, P. Reiss, O. Kirk, E. Bernasconi, et al; Antiretroviral Therapy Cohort Collaboration. 2005. Incidence of Tuberculosis among HIVinfected patients receiving highly active antiretroviral therapy in Europe and North America. Clin. Infect. Dis. 41: 1772-1782.
66. Danel, C., D. Gabillard, J. Le Carrou, X. Anglaret, R. Moh, S. Eholie, H. Ménan, A. Badje, G. Kouame, and J. B. Ntakpe. Early ART and IPT in HV-infected African adults with high CD4 count (Temprano trial) [Abstract 115LB]. Presented at the Conference on Retroviruses and Opportunistic Infections (CROI), February 23-26, 2015, Seattle, WA.