IL-15 promotes activation and expansion of CD8+ T cells in HIV-1 infection

Journal of Clinical Investigation

Volumn 126, Issue 7, 2016, Pages 2745-2756

  Younes, Souheil Antoine ^a   Freeman, Michael L ^a   Mudd, Joseph C ^b   Shive, Carey L ^a   Reynaldi, Arnold ^c   Panigrahi, Soumya ^a   Estes, Jacob D ^d   Deleage, Claire ^d   Lucero, Carissa ^d   Anderson, Jodi ^e   Schacker, Timothy W ^e   Davenport, Miles P ^c   McCune, Joseph M ^f   Hunt, Peter W ^f   Lee, Sulggi A ^f   Serrano Villar, Sergio ^g   Debernardo, Robert L ^h   Jacobson, Jeffrey M ⁱ   Canaday, David H ^a   Sekaly, Raafick Pierre ^a   Rodriguez, Benigno ^a   Sieg, Scott F ^a   Lederman, Michael M ^a   more..

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g HOSPITAL RAMÓN Y CAJAL   (Spain)

^h CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

ⁱ TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45RO ANTIGEN; CHEMOKINE RECEPTOR CCR7; GRANZYME B; HLA A ANTIGEN; INTERLEUKIN 15; KI 67 ANTIGEN; T LYMPHOCYTE RECEPTOR; ANTIRETROVIRUS AGENT; CCR7 PROTEIN, MOUSE; CD45 ANTIGEN; GRANZYME; IL15 PROTEIN, HUMAN; PTPRC PROTEIN, MOUSE;

ADULT; AGED; ANTIGEN SPECIFICITY; ARTICLE; CD4 LYMPHOCYTE COUNT; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL EXPANSION; CELL PROLIFERATION; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPH NODE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; MEMORY T LYMPHOCYTE; MORBIDITY; MORTALITY; PERIPHERAL BLOOD MONONUCLEAR CELL; POPULATION; PRIORITY JOURNAL; PROTEIN BINDING; SEQUENCE ANALYSIS; ANIMAL; BIOPSY; BLOOD; CASE CONTROL STUDY; CYTOLOGY; HAPLOTYPE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; MOUSE; PATHOLOGY; PHENOTYPE;

ADULT; AGED; ANIMALS; ANTI-RETROVIRAL AGENTS; ANTIGENS, CD45; BIOPSY; CASE-CONTROL STUDIES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; GRANZYMES; HAPLOTYPES; HIV INFECTIONS; HIV-1; HUMANS; INTERLEUKIN-15; KI-67 ANTIGEN; LEUKOCYTES, MONONUCLEAR; LYMPH NODES; LYMPHOCYTE ACTIVATION; MALE; MICE; MIDDLE AGED; PHENOTYPE; RECEPTORS, CCR7;

EID: 84978374839     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85996     Document Type: Article

References (53)

1. Hellerstein MK, McCune JM. T cell turnover in HIV-1 disease. Immunity. 1997; 7 (5):583-589.
2. Kovacs JA, et al. Identification of dynamically distinct subpopulations of T lymphocytes that are differentially affected by HIV. J Exp Med. 2001; 194 (12):1731-1741.
3. Hazenberg MD, et al. T-cell division in human immunodeficiency virus (HIV)-1 infection is mainly due to immune activation: a longitudinal analysis in patients before and during highly active antiretroviral therapy (HAART). Blood. 2000; 95 (1):249-255.
4. + T cells in HIV-1-infected patients. AIDS. 1996; 10 (8):827-834.
5. + T-cell changes independent of viral load. Blood. 2004; 104 (4):942-947.
6. Hazenberg MD, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS. 2003; 17 (13):1881-1888.
7. + adolescent population. AIDS Res Hum Retroviruses. 2004; 20 (3):263-269.
8. Betts MR, et al. Analysis of total human immuno deficiency virus (HIV)-specific CD4 (+) and CD8 (+) T-cell responses: relationship to viral load in untreated HIV infection. J Virol. 2001; 75 (24):11983-11991.
9. + T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat Immunol. 2002; 3 (11):1061-1068.
10. + T cells in HIVinfected progressors and long-term nonprogressors. J Immunol. 2000; 165 (2):1082-1092.
11. Biancotto A, et al. Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood. 2007; 109 (10):4272-4279.
12. Chen G, et al. CD8 T cells specific for human immunodeficiency virus, Epstein-Barr virus, and cytomegalovirus lack molecules for homing to lymphoid sites of infection. Blood. 2001; 98 (1):156-164.
13. + T cell activation, and increased risk of non-AIDS morbidity and mortality. PLoS Pathog. 2014; 10 (5):e1004078.
14. Migueles SA, et al. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity. 2008; 29 (6):1009-1021.
15. + T cells in HIV disease have a diverse TCR repertoire a phenotype consistent with bystander activation. J Virol. 2014; 88 (10):5369-5380.
16. + T cells. Clin Immunol Immunopathol. 1996; 81 (2):200-209.
17. Giacoia-Gripp CB, Neves I Jr, Galhardo MC, Morgado MG. Flow cytometry evaluation of the T-cell receptor Vbeta repertoire among HIV-1 infected individuals before and after antiretroviral therapy. J Clin Immunol. 2005; 25 (2):116-126.
18. Grant M, Pardoe I, Whaley M, Montaner JS, Harrigan PR. The T cell receptor Vβ repertoire shows little change during treatment interruptionrelated viral rebound in chronic HIV infection. AIDS. 2002; 16 (2):287-290.
19. Tenorio AR, et al. Soluble markers of inflammation and coagulation but not T-cell activation predict non-AIDS-defining morbid events during suppressive antiretroviral treatment. J Infect Dis. 2014; 210 (8):1248-1259.
20. + T-cell cycling and impaired responsiveness to interleukin 7: implications for immune failure in HIV disease. J Infect Dis. 2014; 210 (4):619-629.
21. + T cell CD57 expression is distinct from that of CMV and aging. PLoS One. 2014; 9 (2):e89444.
22. + T cells expressing CD57 can be reversed by early ART initiation and predict mortality in treated HIV infection. J Infect Dis. 2014; 210 (3):374-382.
23. Giorgi JV, et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis. 1999; 179 (4):859-870.
24. 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 (6):3400-3406.
25. + T cells specific for EBV, cytomegalovirus, and influenza virus are acti-vated during primary HIV infection. J Immunol. 2004; 173 (4):2410-2418.
26. +T cells with a predominant Vβ usage during the primary immune response to HIV. Nature. 1994; 370 (6489):463-467.
27. +T cell clones during primary HIV infection. Proc Natl Acad Sci U S A. 1997; 94 (18):9848-9853.
28. Alves NL, Hooibrink B, Arosa FA, van Lier RA IL-15 induces antigen-independent expansion and differentiation of human naive CD8+ T cells in vitro. Blood. 2003; 102 (7):2541-2546.
29. + memory T cells. Proc Natl Acad Sci U S A. 2002; 99 (9):6192-6197.
30. Weng NP, Liu K, Catalfamo M, Li Y, Henkart PA. IL-15 is a growth factor and an activator of CD8 memory T cells. Ann NY Acad Sci. 2002; 975:46-56.
31. Tamang DL, Redelman D, Alves BN, Vollger L, Bethley C, Hudig D. Induction of granzyme B and T cell cytotoxic capacity by IL-2 or IL-15 without antigens: multiclonal responses that are extremely lytic if triggered and short-lived after cytokine withdrawal. Cytokine. 2006; 36 (3-4):148-159.
32. + T cells to acquire functional NK receptors capable of modulating cytotoxicity and cytokine secretion. Immunobiology. 2011; 216 (5):604-612.
33. Sandau MM, Kohlmeier JE, Woodland DL, Jameson SC. IL-15 regulates both quantitative and qualitative features of the memory CD8 T cell pool. J Immunol. 2010; 184 (1):35-44.
34. Agostini C, et al. Interleukin-15 triggers activation and growth of the CD8 T-cell pool in extravascular tissues of patients with acquired immunodeficiency syndrome. Blood. 1997; 90 (3):1115-1123.
35. + T cells are activated in an antigen-independent manner in HIV-infected individuals. J Immunol. 2014; 192 (4):1732-1744.
36. Waldmann TA, Tagaya Y. The multifaceted regulation of interleukin-15 expression and the role of this cytokine in NK cell differentiation and host response to intracellular pathogens. Annu Rev Immunol. 1999; 17:19-49.
37. Zeng M, et al. Cumulative mechanisms of lymphoid tissue fibrosis and T cell depletion in HIV-1 and SIV infections. J Clin Invest. 2011; 121 (3):998-1008.
38. Shive CL, et al. Inflammation perturbs the IL-7 axis, promoting senescence and exhaustion that broadly characterize immune failure in treated HIV infection. J Acquir Immune Defic Syndr. 2016; 71 (5):483-492.
39. Nguyen TP, et al. Interferon-α inhibits CD4 T cell responses to interleukin-7 and interleukin-2 and selectively interferes with Akt signaling. J Leukoc Biol. 2015; 97 (6):1139-1146.
40. Cui G, et al. Characterization of the IL-15 niche in primary and secondary lymphoid organs in vivo. Proc Natl Acad Sci U S A. 2014; 111 (5):1915-1920.
41. Jabri B, Abadie V. IL-15 functions as a danger signal to regulate tissue-resident T cells and tissue destruction. Nat Rev Immunol. 2015; 15 (12):771-783.
42. + T cells and limiting reconstitution in HIV-1 and SIV infections through damage to the secondary lymphoid organ niche. Semin Immunol. 2008; 20 (3):181-186.
43. Sprent J, Surh CD. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat Immunol. 2011; 12 (6):478-484.
44. Younes SA, Punkosdy G, Caucheteux S, Chen T, Grossman Z, Paul WE. Memory phenotype CD4 T cells undergoing rapid, nonburst-like, cytokine-driven proliferation can be distinguished from antigen-experienced memory cells. PLoS Biol. 2011; 9 (10):e1001171.
45. + T cells produces antigen-inexperienced T cells in the periphery with memory phenotype and function. J Immunol. 2013; 190 (5):1936-1947.
46. Freeman ML, et al. CD8 T cell expansion inflammation linked to CMV co-infection in ART-treated HIV infection. Clin Infect Dis. 2015; 62 (3):392-396.
47. Barrett L, Stapleton SN, Fudge NJ, Grant MD. Immune resilience in HIV-infected individuals seronegative for cytomegalovirus. AIDS. 2014; 28 (14):2045-2049.
48. Naeger DM, et al. Cytomegalovirus-specific T cells persist at very high levels during long-term antiretroviral treatment of HIV disease. PLoS One. 2010; 5 (1):e8886.
49. Dominguez-Villar M, Gautron AS, de Marcken M, Keller MJ, Hafler DA. TLR7 induces anergy in human CD4 (+) T cells. Nat Immunol. 2015; 16 (1):118-128.
50. Brenchley JM, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006; 12 (12):1365-1371.
51. Jiang W, et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis. 2009; 199 (8):1177-1185.
52. Estes JD, et al. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 2010; 6 (8):e1001052.
53. + T cells endowed with proliferative capacity. J Exp Med. 2003; 198 (12):1909-1922.