CD4+ T cells with an activated and exhausted phenotype distinguish immunodeficiency during aviremic HIV-2 infection

AIDS

Volumn 30, Issue 16, 2016, Pages 2415-2426

  Buggert, Marcus ^a,b   Frederiksen, Juliet ^c   Lund, Ole ^c   Betts, Michael R ^b   Biague, Antonio ^d   Nielsen, Morten ^c,e   Tauriainen, Johanna ^a   Norrgren, Hans ^f   Medstrand, Patrik ^g   Karlsson, Annika C ^a   Jansson, Marianne ^a,g  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d National Public Health Laboratory   (Guinea-Bissau)

^e UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

^f LUND UNIVERSITY   (Sweden)

^g LUND UNIVERSITY   (Sweden)

Author keywords

Activation; CD4+ T cells; Exhaustion; HIV 1; HIV 2; Immunodeficiency; Viremia

Indexed keywords

CD27 ANTIGEN; CD38 ANTIGEN; CD45RO ANTIGEN; HLA DR ANTIGEN; PROGRAMMED DEATH 1 LIGAND 1;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FLOW CYTOMETRY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS 2 INFECTION; LYMPHOCYTE DIFFERENTIATION; PATHOGEN LOAD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; CHEMISTRY; COHORT ANALYSIS; GUINEA-BISSAU; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; IMMUNOPHENOTYPING; ISOLATION AND PURIFICATION; VIROLOGY;

CD4-POSITIVE T-LYMPHOCYTES; COHORT STUDIES; FLOW CYTOMETRY; GUINEA-BISSAU; HIV INFECTIONS; HIV-2; HUMANS; IMMUNOPHENOTYPING; PHENOTYPE; T-LYMPHOCYTE SUBSETS;

EID: 84981736213     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000001223     Document Type: Article

References (47)

1. Nyamweya S, Hegedus A, Jaye A, Rowland-Jones S, Flanagan KL, Macallan DC. Comparing HIV-1 and HIV-2 infection: lessons for viral immunopathogenesis. Rev Med Virol 2013; 23:221-240.
2. Berry N, Ariyoshi K, Jaffar S, Sabally S, Corrah T, Tedder R, et al. Low peripheral blood viral HIV-2 RNA in individuals with high CD4 percentage differentiates HIV-2 from HIV-1 infection. J Hum Virol 1998; 1:457-468.
3. Andersson S, Norrgren H, da Silva Z, Biague A, Bamba S, Kwok S, et al. Plasma viral load in HIV-1 and HIV-2 singly and dually infected individuals in Guinea-Bissau, West Africa: significantly lower plasma virus set point in HIV-2 infection than in HIV-1 infection. Arch Intern Med 2000; 160:3286-3293.
4. Ariyoshi K, Jaffar S, Alabi AS, Berry N, Schim van der Loeff M, Sabally S, et al. Plasma RNA viral load predicts the rate of CD4 T cell decline and death in HIV-2-infected patients in West Africa. AIDS 2000; 14:339-344.
5. Hansmann A, Schim van der Loeff MF, Kaye S, Awasana AA, Sarge-Njie R, O'Donovan D, et al. Baseline plasma viral load and CD4 cell percentage predict survival in HIV-1-and HIV-2-infected women in a community-based cohort in The Gambia. J Acquir Immune Defic Syndr 2005; 38:335-341.
6. de Silva TI, Peng Y, Leligdowicz A, Zaidi I, Li L, Griffin H, et al. Correlates of T-cell-mediated viral control and phenotype of CD8(R) T cells in HIV-2, a naturally contained human retroviral infection. Blood 2013; 121:4330-4339.
7. Leligdowicz A, Yindom LM, Onyango C, Sarge-Njie R, Alabi A, Cotten M, et al. Robust Gag-specific T cell responses characterize viremia control in HIV-2 infection. J Clin Invest 2007; 117:3067-3074.
8. Duvall MG, Jaye A, Dong T, Brenchley JM, Alabi AS, Jeffries DJ, et al. Maintenance of HIV-specific CD4R T cell help distinguishes HIV-2 from HIV-1 infection. J Immunol 2006; 176: 6973-6981.
9. Foxall RB, Cortesao CS, Albuquerque AS, Soares RS, Victorino RM, Sousa AE. Gag-specific CD4RT-cell frequency is inversely correlated with proviral load and directly correlated with immune activation in infection with human immunodeficiency virus type 2 (HIV-2) but not HIV-1. J Virol 2008; 82:9795-9799.
10. Esbjornsson J, Mansson F, Kvist A, Isberg PE, Nowroozalizadeh S, Biague AJ, et al. Inhibition of HIV-1 disease progression by contemporaneous HIV-2 infection. N Engl J Med 2012; 367:224-232.
11. Esbjornsson J, Mansson F, Kvist A, Isberg PE, Biague AJ, da Silva ZJ, et al. Increased survival among HIV-1 and HIV-2 dualinfected individuals compared to HIV-1 single-infected individuals. AIDS 2014; 28:949-957.
12. Leligdowicz A, Feldmann J, Jaye A, Cotten M, Dong T, McMichael A, et al. Direct relationship between virus load and systemic immune activation in HIV-2 infection. J Infect Dis 2010; 201:114-122.
13. Michel P, Balde AT, Roussilhon C, Aribot G, Sarthou JL, Gougeon ML. Reduced immune activation and T cell apoptosis in human immunodeficiency virus type 2 compared with type 1: correlation of T cell apoptosis with beta2 microglobulin concentration and disease evolution. J Infect Dis 2000; 181:64-75.
14. Sousa AE, Carneiro J, Meier-Schellersheim M, Grossman Z, Victorino RM. CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J Immunol 2002; 169:3400-3406.
15. Tendeiro R, Foxall RB, Baptista AP, Pinto F, Soares RS, Cavaleiro R, et al. PD-1 and its ligand PD-L1 are progressively upregulated on CD4 and CD8 T-cells in HIV-2 infection irrespective of the presence of viremia. AIDS 2012; 26: 1065-1071.
16. Cavaleiro R, Tendeiro R, Foxall RB, Soares RS, Baptista AP, Gomes P, et al. Monocyte and myeloid dendritic cell activation occurs throughout HIV type 2 infection, an attenuated form of HIV disease. J Infect Dis 2013; 207: 1730-1742.
17. Bachle SM, Malone DFG, Buggert M, Karlsson AC, Isberg PE, Biague AJ, et al. Elevated levels of invariant natural killer T cell and natural killer cell activation correlate with disease progression in HIV-1 and HIV-2 infections. AIDS 2016; 30:1713-1722.
18. Nowroozalizadeh S, Mansson F, da Silva Z, Repits J, Dabo B, Pereira C, et al. Microbial translocation correlates with the severity of both HIV-1 and HIV-2 infections. J Infect Dis 2010; 201:1150-1154.
19. Fernandes SM, Pires AR, Ferreira C, Tendeiro R, Correia L, Paulo SE, et al. Gut disruption in HIV-2 infection despite reduced viremia. AIDS 2014; 28:290-292.
20. Hegedus A, Nyamweya S, Zhang Y, Govind S, Aspinall R, Mashanova A, et al. Protection versus pathology in aviremic and high viral load HIV-2 infection-the pivotal role of immune activation and T-cell kinetics. J Infect Dis 2014; 210:752-761.
21. Hunt PW, Brenchley J, Sinclair E, McCune JM, Roland M, Page-Shafer K, et al. Relationship between T cell activation and CD4R T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 2008; 197:126-133.
22. Lopez M, Soriano V, Peris-Pertusa A, Rallon N, Restrepo C, Benito JM. Elite controllers display higher activation on central memory CD8 T cells than HIV patients successfully on HAART. AIDS Res Hum Retroviruses 2011; 27:157-165.
23. Hatano H, Yukl SA, Ferre AL, Graf EH, Somsouk M, Sinclair E, et al. Prospective antiretroviral treatment of asymptomatic, HIV-1 infected controllers. PLoS Pathog 2013; 9:e1003691.
24. Pereyra F, Lo J, Triant VA, Wei J, Buzon MJ, Fitch KV, et al. Increased coronary atherosclerosis and immune activation in HIV-1 elite controllers. AIDS 2012; 26:2409-2412.
25. Norrgren H, Andersson S, Naucler A, Dias F, Johansson I, Biberfeld G. HIV-1, HIV-2, HTLV-I/II and Treponema pallidum infections: incidence, prevalence, and HIV-2-associated mortality in an occupational cohort in Guinea-Bissau. J Acquir Immune Defic Syndr Hum Retrovirol 1995; 9:422-428.
26. Mansson F, Biague A, da Silva ZJ, Dias F, Nilsson LA, Andersson S, et al. Prevalence and incidence of HIV-1 and HIV-2 before, during and after a civil war in an occupational cohort in Guinea-Bissau, West Africa. AIDS 2009; 23:1575-1582.
27. Ozkaya Sahin G, Holmgren B, Sheik-Khalil E, da Silva Z, Nielsen J, Nowroozalizadeh S, et al. Effect of complement on HIV-2 plasma antiviral activity is intratype specific and potent. J Virol 2013; 87:273-281.
28. Anglaret X, Diagbouga S, Mortier E, Meda N, Verge-Valette V, Sylla-Koko F, et al. CD4R T-lymphocyte counts in HIV infection: are European standards applicable to African patients? J Acquir Immune Defic Syndr Hum Retrovirol 1997; 14:361-367.
29. Norrgren H, da Silva Z, Biague A, Andersson S, Biberfeld G. Clinical progression in early and late stages of disease in a cohort of individuals infected with human immunodeficiency virus-2 in Guinea-Bissau. Scand J Infect Dis 2003; 35:265-272.
30. Ozkaya Sahin G, Mansson F, Palm AA, Vincic E, da Silva Z, Medstrand P, et al. Frequent intratype neutralization by plasma immunoglobulin a identified in HIV type 2 infection. AIDS Res Hum Retroviruses 2013; 29:470-478.
31. Ng AA, Lee BT, Teo TS, Poidinger M, Connolly JE. Optimal cellular preservation for high dimensional flow cytometric analysis of multicentre trials. J Immunol Methods 2012; 385: 79-89.
32. Buggert M, Tauriainen J, Yamamoto T, Frederiksen J, Ivarsson MA, Michaelsson J, et al. T-bet and Eomes are differentially linked to the exhausted phenotype of CD8R T cells in HIV infection. PLoS Pathog 2014; 10:e1004251.
33. Buggert M, Norstrom MM, Salemi M, Hecht FM, Karlsson AC. Functional avidity and IL-2/perforin production is linked to the emergence of mutations within HLA-BM5701-restricted epitopes and HIV-1 disease progression. J Immunol 2014; 192: 4685-4696.
34. Buggert M, Frederiksen J, Noyan K, Svard J, Barqasho B, Sonnerborg A, et al. Multiparametric bioinformatics distinguish the CD4/CD8 ratio as a suitable laboratory predictor of combined T cell pathogenesis in HIV infection. J Immunol 2014; 192:2099-2108.
35. Frederiksen J, Buggert M, Noyan K, Nowak P, Sonnerborg A, Lund O, et al. Multidimensional clusters of CD4R T cell dysfunction are primarily associated with the CD4/CD8 ratio in chronic HIV infection. PLoS One 2015; 10:e0137635.
36. Hahne F, Khodabakhshi AH, Bashashati A, Wong CJ, Gascoyne RD, Weng AP, et al. Per-channel basis normalization methods for flow cytometry data. Cytometry A 2010; 77: 121-131.
37. Roederer M, Nozzi JL, Nason MC. SPICE: exploration and analysis of postcytometric complex multivariate datasets. Cytometry A 2011; 79:167-174.
38. Team RDC. R: A Language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2011.
39. Johnson S, Eller M, Teigler JE, Maloveste SM, Schultz BT, Soghoian DZ, et al. Cooperativity of HIV-specific cytolytic CD4 T cells and CD8 T cells in control of HIV viremia. J Virol 2015; 89:7494-7505.
40. Qian Y, Wei C, Eun-Hyung Lee F, Campbell J, Halliley J, Lee JA, et al. Elucidation of seventeen human peripheral blood B-cell subsets and quantification of the tetanus response using a density-based method for the automated identification of cell populations in multidimensional flow cytometry data. Cytometry B Clin Cytom 2010; 78 (Suppl 1):S69-S82.
41. Cockerham LR, Jain V, Sinclair E, Glidden DV, Hartogenesis W, Hatano H, et al. Programmed death-1 expression on CD4(R) and CD8(R) T cells in treated and untreated HIV disease. AIDS 2014; 28:1749-1758.
42. Hatano H, Delwart EL, Norris PJ, Lee TH, Dunn-Williams J, Hunt PW, et al. Evidence for persistent low-level viremia in individuals who control human immunodeficiency virus in the absence of antiretroviral therapy. J Virol 2009; 83:329-335.
43. Pereyra F, Palmer S, Miura T, Block BL, Wiegand A, Rothchild AC, et al. Persistent low-level viremia in HIV-1 elite controllers and relationship to immunologic parameters. J Infect Dis 2009; 200:984-990.
44. Ruelle J, Yfantis V, Duquenne A, Goubau P. Validation of an ultrasensitive digital droplet PCR assay for HIV-2 plasma RNA quantification. J Int AIDS Soc 2014; 17:19675.
45. Popper SJ, Sarr AD, Gueye-Ndiaye A, Mboup S, Essex ME, Kanki PJ. Low plasma human immunodeficiency virus type 2 viral load is independent of proviral load: low virus production in vivo. J Virol 2000; 74:1554-1557.
46. Soares RS, Tendeiro R, Foxall RB, Baptista AP, Cavaleiro R, Gomes P, et al. Cell-associated viral burden provides evidence of ongoing viral replication in aviremic HIV-2-infected patients. J Virol 2011; 85:2429-2438.
47. Weinmann AS. Roles for helper T cell lineage-specifying transcription factors in cellular specialization. Adv Immunol 2014; 124:171-206.