Levels of CD56+TIM-3- Effector CD8 T cells distinguish HIV natural virus suppressors from patients receiving antiretroviral therapy

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Poonia, Bhawna ^a   Pauza, C David ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 METHOXYAMPHETAMINE; CELL SURFACE MARKER; EOMES; INTERLEUKIN 15; IONOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PERFORIN; T BET; TIM 3; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CD56+ CD8 T LYMPHOCYTE; CD56- CD8 T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL LOSS; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOTOXICITY; DEGRANULATION; DISEASE CARRIER; FEMALE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; INTRACELLULAR SIGNALING; MALE; PHENOTYPE; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; T CELL DEPLETION; UPREGULATION; VIREMIA; VIRUS REPLICATION;

ADULT; ANTIGENS, CD56; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CASE-CONTROL STUDIES; CD8-POSITIVE T-LYMPHOCYTES; DEMOGRAPHY; FEMALE; GRANZYMES; HIV INFECTIONS; HIV-1; HUMANS; INTERLEUKIN-15; MALE; MAP KINASE SIGNALING SYSTEM; MEMBRANE PROTEINS; MIDDLE AGED; PERFORIN; T-BOX DOMAIN PROTEINS; UP-REGULATION;

EID: 84895533088     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088884     Document Type: Article

References (50)

1. Hay CM, Ruhl DJ, Basgoz NO, Wilson CC, Billingsley JM, et al. (1999) Lack of viral escape and defective in vivo activation of human immunodeficiency virus type 1-specific cytotoxic T lymphocytes in rapidly progressive infection. J Virol 73: 5509-5519. (Pubitemid 29274834)
2. Trimble LA, Shankar P, Patterson M, Daily JP, Lieberman J (2000) Human immunodeficiency virus-specific circulating CD8 T lymphocytes have down-modulated CD3zeta and CD28, key signaling molecules for T-cell activation. J Virol 74: 7320-7330. (Pubitemid 30613077)
3. Trabattoni D, Piconi S, Biasin M, Rizzardini G, Migliorino M, et al. (2004) Granule-dependent mechanisms of lysis are defective in CD8 T cells of HIV-infected, antiretroviral therapy-treated individuals. AIDS 18: 859-869. (Pubitemid 38553706)
4. O'Connell KA, Hegarty RW, Siliciano RF, Blankson JN (2011) Viral suppression of multiple escape mutants by de novo CD8(+) T cell responses in a human immunodeficiency virus-1 infected elite suppressor. Retrovirology 8: 63.
5. Yan J, Sabbaj S, Bansal A, Amatya N, Shacka JJ, et al. (2013) HIV-Specific CD8+ T Cells from Elite Controllers Are Primed for Survival. J Virol 87: 5170-5181.
6. Alexander AA, Maniar A, Cummings JS, Hebbeler AM, Schulze DH, et al. (2008) Isopentenyl pyrophosphate-activated CD56 + {gamma}{delta} T lymphocytes display potent antitumor activity toward human squamous cell carcinoma. Clin Cancer Res 14: 4232-4240.
7. Fauci AS, Mavilio D, Kottilil S (2005) NK cells in HIV infection: paradigm for protection or targets for ambush. Nat Rev Immunol 5: 835-843. (Pubitemid 41581665)
8. Pittet MJ, Speiser DE, Valmori D, Cerottini JC, Romero P (2000) Cutting edge: cytolytic effector function in human circulating CD8+ T cells closely correlates with CD56 surface expression. J Immunol 164: 1148-1152. (Pubitemid 30067223)
9. Correia MP, Costa AV, Uhrberg M, Cardoso EM, Arosa FA (2011) IL-15 induces CD8+ T cells to acquire functional NK receptors capable of modulating cytotoxicity and cytokine secretion. Immunobiology 216: 604-612.
10. Santin AD, Hermonat PL, Ravaggi A, Bellone S, Roman JJ, et al. (2001) Expression of CD56 by human papillomavirus E7-specific CD8+ cytotoxic T lymphocytes correlates with increased intracellular perforin expression and enhanced cytotoxicity against HLA-A2-matched cervical tumor cells. Clin Cancer Res 7: 804s-810s. (Pubitemid 33600930)
11. Tarazona R, Casado JG, Delarosa O, Torre-Cisneros J, Villanueva JL, et al. (2002) Selective depletion of CD56(dim) NK cell subsets and maintenance of CD56(bright) NK cells in treatment-naive HIV-1-seropositive individuals. J Clin Immunol 22: 176-183. (Pubitemid 34596941)
12. Riedel DJ, Sajadi MM, Armstrong CL, Cummings JS, Cairo C, et al. (2009) Natural viral suppressors of HIV-1 have a unique capacity to maintain gammadelta T cells. AIDS 23: 1955-1964.
13. Brunetta E, Fogli M, Varchetta S, Bozzo L, Hudspeth KL, et al. (2009) The decreased expression of Siglec-7 represents an early marker of dysfunctional natural killer-cell subsets associated with high levels of HIV-1 viremia. Blood 114: 3822-3830.
14. De Maria A, Fogli M, Costa P, Murdaca G, Puppo F, et al. (2003) The impaired NK cell cytolytic function in viremic HIV-1 infection is associated with a reduced surface expression of natural cytotoxicity receptors (NKp46, NKp30 and NKp44). Eur J Immunol 33: 2410-2418. (Pubitemid 37138973)
15. Sondergaard SR, Ullum H, Skinhoj P, Pedersen BK (1999) Epinephrine-induced mobilization of natural killer (NK) cells and NK-like T cells in HIV-infected patients. Cell Immunol 197: 91-98. (Pubitemid 30000729)
16. Mavilio D, Lombardo G, Benjamin J, Kim D, Follman D, et al. (2005) Characterization of CD56-/CD16+ natural killer (NK) cells: a highly dysfunctional NK subset expanded in HIV-infected viremic individuals. Proc Natl Acad Sci U S A 102: 2886-2891. (Pubitemid 40299886)
17. Mavilio D, Benjamin J, Daucher M, Lombardo G, Kottilil S, et al. (2003) Natural killer cells in HIV-1 infection: dichotomous effects of viremia on inhibitory and activating receptors and their functional correlates. Proc Natl Acad Sci U S A 100: 15011-15016. (Pubitemid 37518008)
18. Chaudhry S, Cairo C, Venturi V, Pauza CD (2013) The gammadelta T cell receptor repertoire is reconstituted in HIV patients after prolonged antiretroviral therapy. AIDS.
19. Tarazona R, DelaRosa O, Casado JG, Torre-Cisneros J, Villanueva JL, et al. (2002) NK-associated receptors on CD8 T cells from treatment-naive HIV-infected individuals: defective expression of CD56. AIDS 16: 197-200. (Pubitemid 34118566)
20. Cummings JS, Cairo C, Armstrong C, Davis CE, Pauza CD (2008) Impacts of HIV infection on Vgamma2Vdelta2 T cell phenotype and function: a mechanism for reduced tumor immunity in AIDS. J Leukoc Biol 84: 371-379.
21. Boudova S, Li H, Sajadi MM, Redfield RR, Pauza CD (2012) Impact of persistent HIV replication on CD4 negative Vgamma2Vdelta2 T cells. J Infect Dis 205: 1448-1455.
22. Hersperger AR, Pereyra F, Nason M, Demers K, Sheth P, et al. (2010) Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog 6: e1000917.
23. Ribeiro-dos-Santos P, Turnbull EL, Monteiro M, Legrand A, Conrod K, et al. (2012) Chronic HIV infection affects the expression of the 2 transcription factors required for CD8 T-cell differentiation into cytolytic effectors. Blood 119: 4928-4938.
24. Intlekofer AM, Banerjee A, Takemoto N, Gordon SM, Dejong CS, et al. (2008) Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 321: 408-411. (Pubitemid 352029977)
25. Hersperger AR, Martin JN, Shin LY, Sheth PM, Kovacs CM, et al. (2011) Increased HIV-specific CD8+ T-cell cytotoxic potential in HIV elite controllers is associated with T-bet expression. Blood 117: 3799-3808.
26. Crawford TQ, Ndhlovu LC, Tan A, Carvidi A, Hecht FM, et al. (2011) HIV-1 infection abrogates CD8+ T cell mitogen-activated protein kinase signaling responses. J Virol 85: 12343-12350.
27. Crawford TQ, Hecht FM, Pilcher CD, Ndhlovu LC, Barbour JD (2013) Activation Associated ERK1/2 Signaling Impairments in CD8(+) T Cells Co-Localize with Blunted Polyclonal and HIV-1 Specific Effector Functions in Early Untreated HIV-1 Infection. PLoS One 8: e77412.
28. Jones RB, Ndhlovu LC, Barbour JD, Sheth PM, Jha AR, et al. (2008) Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 205: 2763-2779.
29. Rangachari M, Zhu C, Sakuishi K, Xiao S, Karman J, et al. (2012) Bat3 promotes T cell responses and autoimmunity by repressing Tim-3-mediated cell death and exhaustion. Nat Med 18: 1394-1400.
30. Xu H, Wang X, Pahar B, Alvarez X, Rasmussen KK, et al. (2012) Rapid down-regulation of gammac on T cells in early SIV infection correlates with impairment of T-cell function. FASEB J 26: 2294-2305.
31. Hirsch HH, Kaufmann G, Sendi P, Battegay M (2004) Immune reconstitution in HIV-infected patients. Clin Infect Dis 38: 1159-1166. (Pubitemid 38951265)
32. Lopez M, Rallon N, Soriano V, Rodriguez I, Valencia E, et al. (2008) HIV rebound after discontinuation of antiretroviral therapy increases and expands HIV-specific CD8+ responses but has no impact on its functionality. AIDS Res Hum Retroviruses 24: 1197-1201.
33. Lopez M, Soriano V, Rallon N, Cascajero A, Gonzalez-Lahoz J, et al. (2008) Suppression of viral replication with highly active antiretroviral therapy has no impact on the functional profile of HIV-specific CD8(+) T cells. Eur J Immunol 38: 1548-1558.
34. Trabattoni D, Fossati S, Biasin M, Boasso A, Rizzardini G, et al. (2002) Functional analysis of HIV-specific cytotoxic T lymphocytes in antiviral-treated-and-naive patients: a preliminary report. J Biol Regul Homeost Agents 16: 25-29. (Pubitemid 34495584)
35. Appay V, Nixon DF, Donahoe SM, Gillespie GM, Dong T, et al. (2000) HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J Exp Med 192: 63-75. (Pubitemid 30470807)
36. Kadmon G, Kowitz A, Altevogt P, Schachner M (1990) The neural cell adhesion molecule N-CAM enhances L1-dependent cell-cell interactions. J Cell Biol 110: 193-208.
37. Takasaki S, Hayashida K, Morita C, Ishibashi H, Niho Y (2000) CD56 directly interacts in the process of NCAM-positive target cell-killing by NK cells. Cell Biol Int 24: 101-108.
38. Killian MS, Johnson C, Teque F, Fujimura S, Levy JA (2011) Natural suppression of human immunodeficiency virus type 1 replication is mediated by transitional memory CD8+ T cells. J Virol 85: 1696-1705.
39. Scott-Algara D, Buseyne F, Porrot F, Corre B, Bellal N, et al. (2005) Not all tetramer binding CD8+ T cells can produce cytokines and chemokines involved in the effector functions of virus-specific CD8+ T lymphocytes in HIV-1 infected children. J Clin Immunol 25: 57-67. (Pubitemid 40386179)
40. Migueles SA, Osborne CM, Royce C, Compton AA, Joshi RP, et al. (2008) Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29: 1009-1021.
41. Hou W, Ye L, Ho WZ (2012) CD56+ T cells inhibit HIV-1 infection of macrophages. J Leukoc Biol 92: 343-351.
42. Bartsch U, Kirchhoff F, Schachner M (1990) Highly sialylated N-CAM is expressed in adult mouse optic nerve and retina. J Neurocytol 19: 550-565. (Pubitemid 20263995)
43. Rosenberg ES, LaRosa L, Flynn T, Robbins G, Walker BD (1999) Characterization of HIV-1-specific T-helper cells in acute and chronic infection. Immunol Lett 66: 89-93. (Pubitemid 29136823)
44. Hong JJ, Amancha PK, Rogers K, Ansari AA, Villinger F (2013) Re-evaluation of PD-1 expression by T cells as a marker for immune exhaustion during SIV infection. PLoS One 8: e60186.
45. Finney CA, Ayi K, Wasmuth JD, Sheth PM, Kaul R, et al. (2013) HIV Infection Deregulates Tim-3 Expression on Innate Cells; Combination Antiretroviral Therapy Results in Partial Restoration. J Acquir Immune Defic Syndr.
46. Mueller YM, Bojczuk PM, Halstead ES, Kim AH, Witek J, et al. (2003) IL-15 enhances survival and function of HIV-specific CD8+ T cells. Blood 101: 1024-1029. (Pubitemid 36139375)
47. Spits H, Lanier LL, Phillips JH (1995) Development of human T and natural killer cells. Blood 85: 2654-2670.
48. De Smedt M, Taghon T, Van de Walle I, De Smet G, Leclercq G, et al. (2007) Notch signaling induces cytoplasmic CD3 epsilon expression in human differentiating NK cells. Blood 110: 2696-2703. (Pubitemid 47523197)
49. Quiros-Roldan E, Serana F, Chiarini M, Zanotti C, Sottini A, et al. (2012) Effects of combined antiretroviral therapy on B- and T-cell release from production sites in long-term treated HIV-1+ patients. J Transl Med 10: 94.
50. Hardy G, Worrell S, Hayes P, Barnett CM, Glass D, et al. (2004) Evidence of thymic reconstitution after highly active antiretroviral therapy in HIV-1 infection. HIV Med 5: 67-73. (Pubitemid 38404658)