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

Volumn 30, Issue 11, 2016, Pages 1713-1722

  Bächle, Susanna M ^a   Malone, David F G ^a   Buggert, Marcus ^b,c   Karlsson, Annika C ^b   Isberg, Per Erik ^d   Biague, Antonio J ^e   Norrgren, Hans ^f   Medstrand, Patrik ^d   Moll, Markus ^a   Sandberg, Johan K ^a   Jansson, Marianne ^b,g  

^a Center for Molecular Medicine   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d LUND UNIVERSITY   (Sweden)

^e National Public Health Laboratory   (Guinea-Bissau)

^f LUND UNIVERSITY   (Sweden)

^g LUND UNIVERSITY   (Sweden)

Author keywords

CD38; HIV 1; HIV 2; immune activation; invariant natural killer T cells; natural killer cells; viremia

Indexed keywords

CD38 ANTIGEN; CD56 ANTIGEN; PROMYELOCYTIC LEUKEMIA PROTEIN; TRANSCRIPTION FACTOR T BET;

ADULT; ARTICLE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FLOW CYTOMETRY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS 2 INFECTION; HUMAN IMMUNODEFICIENCY VIRUS TYPE 1 SUBTYPE D; MAJOR CLINICAL STUDY; NATURAL KILLER T CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS LOAD; CD4 LYMPHOCYTE COUNT; COHORT ANALYSIS; DISEASE EXACERBATION; FEMALE; GUINEA-BISSAU; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; IMMUNOPHENOTYPING; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NATURAL KILLER CELL;

ADULT; CD4 LYMPHOCYTE COUNT; COHORT STUDIES; DISEASE PROGRESSION; FEMALE; FLOW CYTOMETRY; GUINEA-BISSAU; HIV INFECTIONS; HIV-1; HIV-2; HUMANS; IMMUNOPHENOTYPING; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NATURAL KILLER T-CELLS; VIRAL LOAD;

EID: 84966397100     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000001147     Document Type: Article

References (69)

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. van der Loeff MF, Larke N, Kaye S, Berry N, Ariyoshi K, Alabi A, et al. Undetectable plasma viral load predicts normal survival in HIV-2-infected people in a West African village. Retrovirology 2010; 7:46.
7. de Silva TI, Aasa-Chapman M, Cotten M, Hue S, Robinson J, Bibollet-Ruche F, et al. Potent autologous and heterologous neutralizing antibody responses occur in HIV-2 infection across a broad range of infection outcomes. J Virol 2012; 86:930-946.
8. Duvall MG, Precopio ML, Ambrozak DA, Jaye A, McMichael AJ, Whittle HC, et al. Polyfunctional T cell responses are a hallmark of HIV-2 infection. Eur J Immunol 2008; 38:350-363.
9. Kong R, Li H, Bibollet-Ruche F, Decker JM, Zheng NN, Gottlieb GS, et al. Broad and potent neutralizing antibody responses elicited in natural HIV-2 infection. J Virol 2012; 86:947-960.
10. 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.
11. Ozkaya Sahin G, Holmgren B, da Silva Z, Nielsen J, Nowroozalizadeh S, Esbjornsson J, et al. Potent intratype neutralizing activity distinguishes human immunodeficiency virus type 2 (HIV-2) from HIV-1. J Virol 2012; 86:961-971.
12. Esbjornsso 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.
13. 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.
14. Hanson A, Sarr AD, Shea A, Jones N, Mboup S, Kanki P, et al. Distinct profile of T cell activation in HIV type 2 compared to HIV type 1 infection: differential mechanism for immunoprotection. AIDS Res Hum Retroviruses 2005; 21:791-798.
15. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narvaez AB, et al. Immune activation set point during early HIV infection predicts subsequent CD4R T-cell changes independent of viral load. Blood 2004; 104:942-947.
16. 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.
17. 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.
18. Giorgi JV, Detels R. T-cell subset alterations in HIV-infected homosexual men: NIAID Multicenter AIDS cohort study. Clin Immunol Immunopathol 1989; 52:10-18.
19. Douek DC, Roederer M, Koup RA. Emerging concepts in the immunopathogenesis of AIDS. Annu Rev Med 2009; 60:471-484.
20. Klatt NR, Chomont N, Douek DC, Deeks SG. Immune activation and HIV persistence: implications for curative approaches to HIV infection. Immunol Rev 2013; 254:326-342.
21. Lambin P, Desjobert H, Debbia M, Fine JM, Muller JY. Serum neopterin and beta 2-microglobulin in anti-HIV positive blood donors. Lancet 1986; 2:1216.
22. Pepin J, Morgan G, Dunn D, Gevao S, Mendy M, Gaye I, et al. HIV-2-induced immunosuppression among asymptomatic West African prostitutes: evidence that HIV-2 is pathogenic, but less so than HIV-1. AIDS 1991; 5:1165-1172.
23. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12:1365-1371.
24. 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.
25. Lichtfuss GF, Cheng WJ, Farsakoglu Y, Paukovics G, Rajasuriar R, Velayudham P, et al. Virologically suppressed HIV patients show activation of NK cells and persistent innate immune activation. J Immunol 2012; 189:1491-1499.
26. Bisio F, Bozzano F, Marras F, Di Biagio A, Moretta L, De Maria A. Successfully treated HIV-infected patients have differential expression of NK cell receptors (NKp46 and NKp30) according toAIDS status at presentation. Immunol Lett 2013; 152:16-24.
27. Kuri-Cervantes L, de Oca GS, Avila-Rios S, Hernandez-Juan R, Reyes-Teran G. Activation of NK cells is associated with HIV-1 disease progression. J Leukoc Biol 2014; 96:7-16.
28. Naluyima P, Eller MA, Laeyendecker O, Quinn TC, Serwadda D, Sewankambo NK, et al. Impaired natural killer cell responses are associated with loss of the highly activated NKG2A(R)CD57(R)CD56(dim) subset in HIV-1 subtype D infection in Uganda. AIDS 2014; 28:1273-1278.
29. Jost S, Altfeld M. Control of human viral infections by natural killer cells. Annu Rev Immunol 2013; 31:163-194.
30. Juno JA, Keynan Y, Fowke KR. Invariant NKT cells: regulation and function during viral infection. PLoS Pathog 2012; 8:e1002838.
31. Bjorkstrom NK, Ljunggren HG, Sandberg JK. CD56 negative NK cells: origin, function, and role in chronic viral disease. Trends Immunol 2010; 31:401-406.
32. Nuvor SV, van der Sande M, Rowland-Jones S, Whittle H, Jaye A. Natural killer cell function is well preserved in asymptomatic human immunodeficiency virus type 2 (HIV-2) infection but similar to that of HIV-1 infection when CD4 T-cell counts fall. J Virol 2006; 80:2529-2538.
33. Sandberg JK, Bhardwaj N, Nixon DF. Dominant effector memory characteristics, capacity for dynamic adaptive expansion, and sex bias in the innate Valpha24 NKT cell compartment. Eur J Immunol 2003; 33:588-596.
34. Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 2013; 13:101-117.
35. Bendelac A, Killeen N, Littman DR, Schwartz RH. A subset of CD4R thymocytes selected by MHC class I molecules. Science 1994; 263:1774-1778.
36. Motsinger A, Haas DW, Stanic AK, Van Kaer L, Joyce S, Unutmaz D. CD1d-restricted human natural killer T cells are highly susceptible to human immunodeficiency virus 1 infection. J Exp Med 2002; 195:869-879.
37. Sandberg JK, Fast NM, Palacios EH, Fennelly G, Dobroszycki J, Palumbo P, et al. Selective loss of innate CD4(R) V alpha 24 natural killer T cells in human immunodeficiency virus infection. J Virol 2002; 76:7528-7534.
38. Moll M, Kuylenstierna C, Gonzalez VD, Andersson SK, Bosnjak L, Sonnerborg A, et al. Severe functional impairment and elevated PD-1 expression in CD1d-restricted NKT cells retained during chronic HIV-1 infection. Eur J Immunol 2009; 39:902-911.
39. van der Vliet HJ, von Blomberg BM, Hazenberg MD, Nishi N, Otto SA, van Benthem BH, et al. Selective decrease in circulating V alpha 24RV beta 11RNKT cells during HIV type 1 infection. J Immunol 2002; 168:1490-1495.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. Hu PF, Hultin LE, Hultin P, Hausner MA, Hirji K, Jewett A, et al. Natural killer cell immunodeficiency in HIV disease is manifest by profoundly decreased numbers of CD16RCD56R cells and expansion of a population of CD16dimCD56-cells with low lytic activity. J Acquir Immune Defic Syndr Hum Retrovirol 1995; 10:331-340.
48. Ullum H, Gotzsche PC, Victor J, Dickmeiss E, Skinhoj P, Pedersen BK. Defective natural immunity: an early manifestation of human immunodeficiency virus infection. J Exp Med 1995; 182:789-799.
49. 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.
50. Crawford A, Angelosanto JM, Kao C, Doering TA, Odorizzi PM, Barnett BE, et al. Molecular and transcriptional basis of CD4(R) T cell dysfunction during chronic infection. Immunity 2014; 40:289-302.
51. Constantinides MG, Bendelac A. Transcriptional regulation of the NKT cell lineage. Curr Opin Immunol 2013; 25:161-167.
52. Daussy C, Faure F, Mayol K, Viel S, Gasteiger G, Charrier E, et al. T-bet and Eomes instruct the development of two distinct natural killer cell lineages in the liver and in the bone marrow. J Exp Med 2014; 211:563-577.
53. Eidson M, Wahlstrom J, Beaulieu AM, Zaidi B, Carsons SE, Crow PK, et al. Altered development of NKT cells, gammadelta T cells, CD8 T cells and NK cells in a PLZF deficient patient. PLoS One 2011; 6:e24441.
54. Gleimer M, von Boehmer H, Kreslavsky T. PLZF controls the expression of a limited number of genes essential for NKT cell function. Front Immunol 2012; 3:374.
55. Lazarevic V, Glimcher LH, Lord GM. T-bet: a bridge between innate and adaptive immunity. Nat Rev Immunol 2013; 13:777-789.
56. 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.
57. Naranbhai V, Altfeld M, Karim SS, Ndung'u T, Karim QA, Carr WH. Changes in natural killer cell activation and function during primary HIV-1 infection. PLoS One 2013; 8:e53251.
58. Paiardini M, Muller-Trutwin M. HIV-associated chronic immune activation. Immunol Rev 2013; 254:78-101.
59. Nowroozalizadeh S, Mansson F, da Silva Z, Repits J, Dabo B, Pereira C, et al. Studies on toll-like receptor stimuli responsiveness in HIV-1 and HIV-2 infections. Cytokine 2009; 46:325-331.
60. Fleuridor R, Wilson B, Hou R, Landay A, Kessler H, Al-Harthi L. CD1d-restricted natural killer T cells are potent targets for human immunodeficiency virus infection. Immunology 2003; 108:3-9.
61. Alter G, Rihn S, Streeck H, Teigen N, Piechocka-Trocha A, Moss K, et al. Ligand-independent exhaustion of killer immunoglobulin-like receptor-positive CD8R T cells in human immunodeficiency virus type 1 infection. J Virol 2008; 82:9668-9677.
62. Lunemann S, Malone DF, Grabowski J, Port K, Beziat V, Bremer B, et al. Effects ofHDVinfection and pegylated interferon alpha treatment on the natural killer cell compartment in chronically infected individuals. Gut 2015; 64:469-482.
63. 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.
64. Hasley RB, Hong C, Li W, Friesen T, Nakamura Y, Kim GY, et al. HIV immune activation drives increased Eomes expression in memory CD8 T cells in association with transcriptional downregulation of CD127. AIDS 2013; 27:1867-1877.
65. Alonzo ES, Sant'Angelo DB. Development of PLZF-expressing innate T cells. Curr Opin Immunol 2011; 23:220-227.
66. Savage AK, Constantinides MG, Han J, Picard D, Martin E, Li B, et al. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 2008; 29:391-403.
67. Gordon SM, Chaix J, Rupp LJ, Wu J, Madera S, Sun JC, et al. The transcription factors T-bet and Eomes control key checkpoints of natural killer cell maturation. Immunity 2012; 36:55-67.
68. Matsuda JL, Zhang Q, Ndonye R, Richardson SK, Howell AR, Gapin L. T-bet concomitantly controls migration, survival, and effector functions during the development of Valpha14i NKT cells. Blood 2006; 107:2797-2805.
69. Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, et al. T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 2004; 20:477-494.