Cytomegalovirus-specific responses of CD38+ memory T cells are skewed towards IFN-γ and dissociated from CD154 in HIV-1 infection

AIDS

Volumn 28, Issue 3, 2014, Pages 311-316

  Olvera García, Gustavo ^a   Espinosa, Enrique ^a   Sieg, Scott F ^b   Lederman, Michael M ^b  

^a National Institute for Respiratory Diseases (INER)   (Mexico)

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

Author keywords

AIDS; CD38 antigen; HIV; Immune activation; Immunologic memory; T cell

Indexed keywords

ANTIGENS, CD38; CD40 LIGAND; CELLS, CULTURED; CYTOMEGALOVIRUS; ENTEROTOXINS; FEMALE; FLOW CYTOMETRY; HIV INFECTIONS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-2; LEUKOCYTES, MONONUCLEAR; MALE; MEMBRANE GLYCOPROTEINS; T-LYMPHOCYTES;

EID: 84894103687     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000162     Document Type: Article

References (52)

1. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, 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; 179:859-870.
2. Kitchen CMR, Yeghiazarian L, Hoh R, McCune JM, Sinclair E, Martin JN, et al. Immune activation, CD4R T cell counts, and viremia exhibit oscillatory patterns over time in patients with highly resistant HIV infection. PloS One 2011; 6:e21190.
3. Hazenberg MD, Otto SA, van Benthem BHB, Roos MTL, Coutinho RA, Lange JMA, et al. Persistent immune activation in HIV-1 infection is associated with progression to AIDS. AIDS Lond Engl 2003; 17:1881-1888.
4. Lederman MM, Calabrese L, Funderburg NT, Clagett B, Medvik K, Bonilla H, et al. Immunologic failure despite suppressive antiretroviral therapy is related to activation and turnover of memory CD4 cells. J Infect Dis 2011; 204:1217-1226.
5. Benito JM, Lo'pez M, Lozano S, Ballesteros C, Martinez P, González-Lahoz J, et al. Differential upregulation of CD38 on different T-cell subsets may influence the ability to reconstitute CD4R T cells under successful highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2005; 38:373-381.
6. Giorgi JV, Lyles RH, Matud JL, Yamashita TE, Mellors JW, Hultin LE, et al. Predictive value of immunologic and virologic markers after long or short duration of HIV-1 infection. J Acquir Immune Defic Syndr 2002; 29:346-355.
7. Deeks SG, Kitchen CMR, Liu L, Guo H, Gascon R, Narváez 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.
8. Card CM, Keynan Y, Lajoie J, Bell CP, Dawood M, Becker M, et al. HIV controllers are distinguished by chemokine expression profile and HIV-specific T-cell proliferative potential. J Acquir Immune Defic Syndr 2012; 59:427-437.
9. Sieg SF, Bazdar DA, Lederman MM. S-phase entry leads to cell death in circulating T cells from HIV-infected persons. J Leukoc Biol 2008; 83:1382-1387.
10. Sieg SF, Rodriguez B, Asaad R, Jiang W, Bazdar DA, Lederman MM. Peripheral S-phase T cells in HIV disease have a central memory phenotype and rarely have evidence of recent T cell receptor engagement. J Infect Dis 2005; 192:62-70.
11. Hsue PY, Hunt PW, Schnell A, Kalapus SC, Hoh R, Ganz P, et al. Role of viral replication, antiretroviral therapy, and immunodeficiency in HIV-associated atherosclerosis. AIDS Lond Engl 2009; 23:1059-1067.
12. Longenecker C, Funderburg N, Jiang Y, Debanne S, Storer N, Labbato D, et al. Markers of inflammation and CD8 T-cell activation, but not monocyte activation, are associated with subclinical carotid artery disease in HIV-infected individuals. HIV Med 2013; 14:385-390.
13. Erlandson KM, Allshouse AA, Jankowski CM, Lee EJ, Rufner KM, Palmer BE, et al. Association of functional impairment with inflammation and immune activation in HIV type 1-infected adults receiving effective antiretroviral therapy. J Infect Dis 2013; 208:249-259.
14. Chun T-W, Justement JS, Sanford C, Hallahan CW, Planta MA, Loutfy M, et al. Relationship between the frequency of HIVspecific CD8R T cells and the level of CD38RCD8R T cells in untreated HIV-infected individuals. Proc Natl Acad Sci U S A 2004; 101:2464-2469.
15. Espinosa E, Ormsby CE, Reyes-Terán G, Asaad R, Sieg SF, Lederman MM. Dissociation of CD154 and cytokine expression patterns in CD38R CD4R memory T cells in chronic HIV-1 infection. J Acquir Immune Defic Syndr 2010; 55:439-445.
16. Li H, Llera A, Malchiodi EL, Mariuzza RA. The structural basis of T cell activation by superantigens. Annu Rev Immunol 1999; 17:435-466.
17. Frentsch M, Arbach O, Kirchhoff D, Moewes B, Worm M, Rothe M, et al. Direct access to CD4R T cells specific for defined antigens according to CD154 expression. Nat Med 2005; 11:1118-1124.
18. Schwendemann J, Choi C, Schirrmacher V, Beckhove P. Dynamic differentiation of activated human peripheral blood CD8R and CD4R effector memory T cells. J Immunol Baltim 2005; 175:1433-1439.
19. Riou C, Yassine-Diab B, Van Grevenynghe J, Somogyi R, Greller LD, Gagnon D, et al. Convergence of TCR and cytokine signaling leads to FOXO3a phosphorylation and drives the survival of CD4R central memory T cells. J Exp Med 2007; 204:79-91.
20. Lozza L, Rivino L, Guarda G, Jarrossay D, Rinaldi A, Bertoni F, et al. The strength of T cell stimulation determines IL-7 responsiveness, secondary expansion, and lineage commitment of primed human CD4RIL-7Rhi T cells. Eur J Immunol 2008; 38:30-39.
21. Watson ARO, Mittler JN, Lee WT. Staphylococcal enterotoxin B induces anergy to conventional peptide in memory T cells. Cell Immunol 2003; 222:144-155.
22. Sallusto F, Lenig D, Fö rster R, Lipp M, Lanzavecchia A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 1999; 401:708-712.
23. AppayV, van LierRAW, Sallusto F, Roederer M. Phenotype and function of human T lymphocyte subsets: consensus and issues. Cytom Part J Int Soc Anal Cytol 2008; 73:975- 983.
24. Wang A, Chandran S, Shah SA, Chiu Y, Paria BC, Aghamolla T, et al. The stoichiometric production of IL-2 and IFN- (mRNA defines memory T cells that can self-renew after adoptive transfer in humans. Sci Transl Med 2012; 4:149ra120.
25. Kano Y, Shiohara T. Current understanding of cytomegalovirus infection in immunocompetent individuals. J Dermatol Sci 2000; 22:196-204.
26. Zhu J, Shearer GM, Marincola FM, Norman JE, Rott D, Zou JP, et al. Discordant cellular and humoral immune responses to cytomegalovirus infection in healthy blood donors: existence of a Th1-type dominant response. Int Immunol 2001; 13:785- 790.
27. Deeks SG, Verdin E, McCune JM. Immunosenescence and HIV. Curr Opin Immunol 2012; 24:501-506.
28. Barry SM, Johnson MA, Janossy G. Cytopathology or immunopathology? The puzzle of cytomegalovirus pneumonitis revisited. Bone Marrow Transplant 2000; 26:591-597.
29. Barrett L, Fowke KR, Grant MD. Cytomegalovirus, aging, and HIV: a perfect storm. AIDS Rev 2012; 14:159- 167.
30. Stubbe M, Vanderheyde N, Pircher H, Goldman M, Marchant A. Characterization of a subset of antigen-specific human central memory CD4R T lymphocytes producing effector cytokines. Eur J Immunol 2008; 38:273-282.
31. MacGregor RR, Pakola SJ, Graziani AL, Montzka DP, Hodinka RL, Nichols CW, et al. Evidence of active cytomegalovirus infection in clinically stable HIV-infected individuals with CD4R lymphocyte counts below 100/microliters of blood: features and relation to risk of subsequent CMV retinitis. J Acquir Immune Defic Syndr Hum Retrovirol 1995; 10:324- 330.
32. Lazzarotto T, Campisi B, Re MC, Albertini F, Furlini G, Dala Casa B, et al. An in vivo study on active cytomegalovirus infection in relation to active HIV replication in HIV-I infected drug addicts. J Infect 1994; 28:287-291.
33. Deayton JR, Prof Sabin CA, Johnson MA, Emery VC, Wilson P, Griffiths PD. Importance of cytomegalovirus viraemia in risk of disease progression and death in HIV-infected patients receiving highly active antiretroviral therapy. Lancet 2004; 363:2116-2121.
34. 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.
35. Funderburg N, Luciano AA, Jiang W, Rodriguez B, Sieg SF, Lederman MM. Toll-like receptor ligands induce human T cell activation and death, a model for HIV pathogenesis. PloS One 2008; 3:e1915.
36. Sandler NG, Douek DC. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat Rev Microbiol 2012; 10:655-666.
37. Rivino L, Messi M, Jarrossay D, Lanzavecchia A, Sallusto F, Geginat J. Chemokine receptor expression identifies Pre-T helper (Th)1, Pre-Th2, and nonpolarized cells among human CD4R central memory T cells. J Exp Med 2004; 200:725- 735.
38. Picker LJ, Hagen SI, Lum R, Reed-Inderbitzin EF, Daly LM, Sylwester AW, et al. Insufficient production and tissue delivery of CD4R memory T cells in rapidly progressive simian immunodeficiency virus infection. J Exp Med 2004; 200:1299-1314.
39. Okoye A, Meier-Schellersheim M, Brenchley JM, Hagen SI, Walker JM, Rohankhedkar M, et al. Progressive CD4R central memory T cell decline results in CD4R effector memory insufficiency and overt disease in chronic SIV infection. J Exp Med 2007; 204:2171-2185.
40. Sousa AE, Chaves AF, Loureiro A, Victorino RM. Comparison of the frequency of interleukin (IL)-2-, interferon-gamma-, and IL- 4-producing T cells in 2 diseases, human immunodeficiency virus types 1 and 2, with distinct clinical outcomes. J Infect Dis 2001; 184:552-559.
41. Clatza A, Bonifaz LC, Vignali DAA, Moreno J. CD40-induced aggregation of MHC class II and CD80 on the cell surface leads to an early enhancement in antigen presentation. J Immunol Baltim Md 2003; 1950:2003; 171:6478-6487.
42. Subauste CS, Subauste A, Wessendarp M. Role of CD40-dependent down-regulation of CD154 in impaired induction of CD154 in CD4(R) T cells from HIV-1-infected patients. J Immunol Baltim Md 2007; 1950:2007; 178:1645-1653.
43. Van Maurik A, Fazekas de St Groth B, Wood KJ, Jones ND. Dependency of direct pathway CD4R T cells on CD40-CD154 costimulation is determined by nature and microenvironment of primary contact with alloantigen. J Immunol Baltim Md 2004; 1950:2004; 172:2163-2170.
44. FujitaN, KagamuH, YoshizawaH, ItohK, KuriyamaH, Matsumoto N, et al.CD40 ligand promotes priming of fully potent antitumor CD4(R) T cells in draining lymph nodes in the presence of apoptotic tumor cells. J Immunol Baltim 2001; 167:5678-5688.
45. Van Kooten C, Banchereau J. CD40-CD40 ligand. J Leukoc Biol 2000; 67:2-17.
46. Grewal IS, Flavell RA. CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol 1998; 16:111-135.
47. Thomsen AR, Nansen A, Christensen JP, Andreasen SO, Marker O. CD40 ligand is pivotal to efficient control of virus replication in mice infected with lymphocytic choriomeningitis virus. J Immunol Baltim 1998; 161:4583-4590.
48. Ostrowski MA, Justement SJ, Ehler L, Mizell SB, Lui S, Mican J, et al. The role of CD4R T cell help and CD40 ligand in the in vitro expansion of HIV-1-specific memory cytotoxic CD8R T cell responses. J Immunol Baltim 2000; 165:6133-6141.
49. LevyJ, Espanol-BorenT, ThomasC, FischerA, TovoP, Bordigoni P, et al. Clinical spectrumof X-linked hyper-IgMsyndrome.JPediatr 1997; 131:47-54.
50. Kämmerer R, Iten A, Frei PC, Bürgisser P. Expansion of T cells negative for CD28 expression in HIV infection. Relation to activation markers and cell adhesion molecules, and correlation with prognostic markers. Med Microbiol Immunol (Berl) 1996; 185:19-25.
51. Borthwick NJ, Bofill M, Gombert WM, Akbar AN, Medina E, Sagawa K, et al. Lymphocyte activation in HIV-1 infection. II. Functional defects of CD28- T cells. AIDS Lond Engl 1994; 8:431-441.
52. Iyasere C, Tilton JC, Johnson AJ, Younes S, Yassine-Diab B, Sekaly R-P, et al. Diminished proliferation of human immunodeficiency virus-specific CD4R T cells is associated with diminished interleukin-2 (IL-2) production and is recovered by exogenous IL-2. J Virol 2003; 77:10900-10909.