IL-7 and the HIV Tat protein act synergistically to down-regulate CD127 expression on CD8 T cells

International Immunology

Volumn 21, Issue 3, 2009, Pages 203-216

  Faller, Elliott ^a,b   Kakal, Juzer ^b   Kumar, Ritesh ^a   MacPherson, Paul ^a,b,c  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

CTL; IL 7 receptor; JAK

Indexed keywords

CD8 ANTIGEN; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; JANUS KINASE; KI 67 ANTIGEN; PROTEIN BCL 2; STAT5 PROTEIN; TRANSACTIVATOR PROTEIN;

APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DOWN-REGULATION; GENES, BCL-2; HIV INFECTIONS; HIV-1; HUMANS; IMMUNOMAGNETIC SEPARATION; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-7; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; JANUS KINASES; KI-67 ANTIGEN; LYMPHOCYTE ACTIVATION; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 61349105459     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxn140     Document Type: Article

References (74)

1. Giliani, S., Mori, L., de Saint Basile, G. et al. 2005. Interleukin-7 receptor alpha (IL-7Ralpha) deficiency: Cellular and molecular bases. Analysis of clinical, immunological, and molecular features in 16 novel patients. Immunol. Rev. 203:110.
2. Puel, A., Ziegler, S. F., Buckley, R. H. and Leonard, W. J. 1998. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency. Nat. Genet. 20:394.
3. Roifman, C. M., Zhang, J., Chitayat, D. and Sharfe, N. 2000. A partial deficiency of interleukin-7R alpha is sufficient to abrogate T cell development and cause severe combined immunodeficiency. Blood 96:2803.
4. Tan, J. T., Dudl, E., LeRoy, E. et al. 2001. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc. Natl Acad. Sci. USA 98:8732.
5. Fry, T. J., Connick, E., Falloon, J. et al. 2001. A potential role for interleukin-7 in T cell homeostasis. Blood 97:2983.
6. Fry, T. J. and Mackall, C. L. 2001. Interleukin-7: Master regulator of peripheral T cell homeostasis? Trends Immunol. 22:564.
7. Fry, T. J. and Mackall, C. L. 2002. Interleukin-7 and immunorestoration in HIV: Beyond the thymus. J. Hematother. Stem Cell Res. 11:803.
8. Fry, T. J., Moniuszko, M., Creekmore, S. et al. 2003. IL-7 therapy dramatically alters peripheral T cell homeostasis in normal and SIV-infected nonhuman primates. Blood 101:2294.
9. Schluns, K. S. and Lefrancois, L. 2003. Cytokine control of memory T cell development and survival. Nat. Rev. Immunol. 3:269.
10. Huster, K. M., Busch, V., Schiemann, M. et al. 2004. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. Proc. Natl Acad. Sci. USA 101:5610.
11. Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D. and Ahmed, R. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4:1191.
12. Soares, M. V., Borthwick, N. J., Maini, M. K., Janossy, G., Salmon, M. and Akbar, A. N. 1998. IL-7-dependent extrathymic expansion of CD45RA+ T cells enables preservation of a naive repertoire. J. Immunol. 161:5909.
13. Welch, P. A., Namen, A. E., Goodwin, R. G., Armitage, R. and Cooper, M. D. 1989. Human IL-7: A novel T cell growth factor. J. Immunol. 143:3562.
14. Armitage, R. J., Namen, A. E., Sassenfeld, H. M. and Grabstein, K. H. 1990. Regulation of human T cell proliferation by IL-7. J. Immunol. 144:938.
15. Westermann, J., Aicher, A., Qin, Z. et al. 1998. Retroviral interleukin-7 gene transfer into human dendritic cells enhances T cell activation. Gene Ther. 5:264.
16. Alderson, M. R., Sassenfeld, H. M. and Widmer, M. B. 1990. Interleukin 7 enhances cytolytic T lymphocyte generation and induces lymphokine-activated killer cells from human peripheral blood. J. Exp. Med. 172:577.
17. Carini, C. and Essex, M. 1994. Interleukin 2-independent interleukin 7 activity enhances cytotoxic immune response of HIV-1-infected individuals. AIDS Res. Hum. Retroviruses 10:121.
18. Jicha, D. L., Mule, J. J. and Rosenberg, S. A. 1991. Interleukin 7 generates antitumor cytotoxic T lymphocytes against murine sarcomas with efficacy in cellular adoptive immunotherapy. J. Exp. Med. 174:1511.
19. Finke, S., Trojaneck, B., Lefterova, P. et al. 1998. Increase of proliferation rate and enhancement of antitumor cytotoxicity of expanded human CD3+ CD56+ immunologic effector cells by receptor-mediated transfection with the interleukin-7 gene. Gene Ther. 5:31.
20. Lotze, M. T., Grimm, E. A., Mazumder, A., Strausser, J. L. and Rosenberg, S. A. 1981. Lysis of fresh and cultured autologous tumor by human lymphocytes cultured in T cell growth factor. Cancer Res. 41:4420.
21. Rowshani, A. T., Uss, A., Yong, S. L., van Lier, R. A. and ten Berge, I. J. 2004. Effects of CD25 monoclonal antibody on proliferative and effector functions of alloactivated human T cells in vitro. Eur. J. Immunol. 34:882.
22. Kos, F. J. and Mullbacher, A. 1992. Induction of primary anti-viral cytotoxic T cells by in vitro stimulation with short synthetic peptide and interleukin-7. Eur. J. Immunol. 22:3183.
23. Smyth, M. J., Norihisa, Y., Gerard, J. R., Young, H. A. and Ortaldo, J. R. 1991. IL-7 regulation of cytotoxic lymphocytes: Pore-forming protein gene expression, interferon-gamma production, and cytotoxicity of human peripheral blood lymphocytes subsets. Cell Immunol. 138:390.
24. Goodwin, R. G., Friend, D., Ziegler, S. F. et al. 1990. Cloning of the human and murine interleukin-7 receptors: Demonstration of a soluble form and homology to a new receptor superfamily. Cell. 60:941.
25. Noguchi, M., Nakamura, Y., Russell, S. M. et al. 1993. Interleukin-2 receptor gamma chain: A functional component of the interleukin-7 receptor. Science 262:1877.
26. Fry, T. J. and Mackall, C. L. 2002. Interleukin-7: From bench to clinic. Blood 99:3892.
27. MacPherson, P. A., Fex, C., Sanchez-Dardon, J., Hawley-Foss, N. and Angel, J. B. 2001. Interleukin-7 receptor expression on CD8(+) T cells is reduced in HIV infection and partially restored with effective antiretroviral therapy. J. Acquir. Immune Defic. Syndr. 28:454.
28. Boutboul, F., Puthier, D., Appay, V. et al. 2005. Modulation of interleukin-7 receptor expression characterizes differentiation of CD8 T cells specific for HIV, EBV and CMV. AIDS 19:1981.
29. Koesters, S. A., Alimonti, J. B., Wachihi, C. et al. 2006. IL-7Ralpha expression on CD4(+) T lymphocytes decreases with HIV disease progression and inversely correlates with immune activation. Eur. J. Immunol. 36:336.
30. Colle, J. H., Moreau, J. L., Fontanet, A. et al. 2006. CD127 expression and regulation are altered in the memory CD8 T cells of HIV-infected patients - reversal by highly active anti-retroviral therapy (HAART). Clin. Exp. Immunol. 143:398.
31. Paiardini, M., Cervasi, B., Albrecht, H. et al. 2005. Loss of CD127 expression defines an expansion of effector CD8+ T cells in HIV-infected individuals. J. Immunol. 174:2900.
32. Rethi, B., Fluur, C., Atlas, A. et al. 2005. Loss of IL-7Ralpha is associated with CD4 T cell depletion, high interleukin-7 levels and CD28 down-regulation in HIV infected patients. AIDS 19:2077.
33. Sasson, S. C., Zaunders, J. J., Zanetti, G. et al. 2006. Increased plasma interleukin-7 level correlates with decreased CD127 and increased CD132 extracellular expression on T cell subsets in patients with HIV-1 infection. J. Infect. Dis. 193:505.
34. Vingerhoets, J., Bisalinkumi, E., Penne, G. et al. 1998. Altered receptor expression and decreased sensitivity of T cells to the stimulatory cytokines IL-2, IL-7 and IL-12 in HIV infection. Immunol. Lett. 61:53.
35. Ferrari, G., King, K., Rathbun, K. et al. 1995. IL-7 enhancement of antigen-driven activation/expansion of HIV-1-specific cytotoxic T lymphocyte precursors (CTLp). Clin. Exp. Immunol. 101:239.
36. Park, J. H., Yu, Q., Erman, B. et al. 2004. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: A novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 21:289.
37. Napolitano, L. A., Grant, R. M., Deeks, S. G. et al. 2001. Increased production of IL-7 accompanies HIV-1-mediated T cell depletion: Implications for T cell homeostasis. Nat. Med. 7:73.
38. Boulassel, M. R., Smith, G. H., Gilmore, N. et al. 2003. Interleukin-7 levels may predict virological response in advanced HIV-1-infected patients receiving lopinavir/ritonavir-based therapy. HIV Med. 4:315.
39. Chiappini, E., Galli, L., Azzari, C. and de Martino, M. 2003. Interleukin-7 and immunologic failure despite treatment with highly active antiretroviral therapy in children perinatally infected with HIV-1. J. Acquir. Immune Defic. Syndr. 33:601.
40. Mussini, C., Pinti, M., Borghi, V. et al. 2002. Features of 'CD4-exploders', HIV-positive patients with an optimal immune reconstitution after potent antiretroviral therapy. AIDS 16:1609.
41. Marcello, A., Zoppe, M. and Giacca, M. 2001. Multiple modes of transcriptional regulation by the HIV-1 Tat transactivator. IUBMB Life 51:175.
42. Huigen, M. C., Kamp, W. and Nottet, H. S. 2004. Multiple effects of HIV-1 trans-activator protein on the pathogenesis of HIV-1 infection. Eur. J. Clin. Invest. 34:57.
43. Frankel, A. D. and Pabo, C. O. 1988. Cellular uptake of the tat protein from human immunodeficiency virus. Cell 55:1189.
44. Ensoli, B., Buonaguro, L., Barillari, G. et al. 1993. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J. Virol. 67:277.
45. Poggi, A., Carosio, R., Fenoglio, D. et al. 2004. Migration of V delta 1 and V delta 2 T cells in response to CXCR3 and CXCR4 ligands in healthy donors and HIV-1-infected patients: Competition by HIV-1 Tat. Blood 103:2205.
46. Helland, D. E., Welles, J. L., Caputo, A. and Haseltine, W. A. 1991. Transcellular transactivation by the human immunodeficiency virus type 1 tat protein. J. Virol. 65:4547.
47. Fittipaldi, A. and Giacca, M. 2005. Transcellular protein transduction using the Tat protein of HIV-1. Adv. Drug Deliv. Rev. 57:597.
48. Rusnati, M., Coltrini, D., Oreste, P. et al. 1997. Interaction of HIV-1 Tat protein with heparin. Role of the backbone structure, sulfation, and size. J. Biol. Chem. 272:11313.
49. Tyagi, M., Rusnati, M., Presta, M. and Giacca, M. 2001. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. Biol. Chem. 276:3254.
50. Vendeville, A., Rayne, F., Bonhoure, A., Bettache, N., Montcourrier, P. and Beaumelle, B. 2004. HIV-1 Tat enters T cells using coated pits before translocating from acidified endosomes and eliciting biological responses. Mol. Biol. Cell 15:2347.
51. Faller, E. M., McVey, M. J., Kakal, J. A. and MacPherson, P. A. 2006. Interleukin-7 receptor expression on CD8 T cells is down-regulated by the HIV Tat protein. J. Acquir. Immune Defic. Syndr. 43:257.
52. Col, E., Caron, C., Seigneurin-Berny, D., Gracia, J., Favier, A. and Khochbin, S. 2001. The histone acetyltransferase, hGCN5, interacts with and acetylates the HIV transactivator, Tat. J. Biol. Chem. 276:28179.
53. Kiernan, R. E., Vanhulle, C., Schiltz, L. et al. 1999. HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J 18:6106.
54. Ott, M., Schnolzer, M., Garnica, J. et al. 1999. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 9:1489.
55. Jiang, Q., Li, W. Q., Aiello, F. B. et al. 2005. Cell biology of IL-7, a key lymphotrophin. Cytokine Growth Factor Rev. 16:513.
56. Kang, J. and Der, S. D. 2004. Cytokine functions in the formative stages of a lymphocyte's life. Curr. Opin. Immunol. 16:180.
57. Schluns, K. S., Kieper, W. C., Jameson, S. C. and Lefrancois, L. 2000. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 1:426.
58. Maraskovsky, E., Teepe, M., Morrissey, P. J. et al. 1996. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J. Immunol. 157:5315.
59. Morelon, E. and Dautry-Varsat, A. 1998. Endocytosis of the common cytokine receptor gammac chain. Identification of sequences involved in internalization and degradation. J. Biol. Chem. 273:22044.
60. Mummery, R. S. and Rider, C. C. 2000. Characterization of the heparin-binding properties of IL-6. J. Immunol. 165:5671.
61. Clarke, D., Katoh, O., Gibbs, R. V., Griffiths, S. D. and Gordon, M. Y. 1995. Interaction of interleukin 7 (IL-7) with glycosaminoglycans and its biological relevance. Cytokine 7:325.
62. Borghesi, L. A., Yamashita, Y. and Kincade, P. W. 1999. Heparan sulfate proteoglycans mediate interleukin-7-dependent B lymphopoiesis. Blood 93:140.
63. Huang, J., Durum, S. K. and Muegge, K. 2001. Cutting edge: Histone acetylation and recombination at the TCR gamma locus follows IL-7 induction. J. Immunol. 167:6073.
64. Ye, S. K., Agata, Y., Lee, H. C. et al. 2001. The IL-7 receptor controls the accessibility of the TCRgamma locus by Stat5 and histone acetylation. Immunity 15:813.
65. Creaven, M., Hans, F., Mutskov, V. et al. 1999. Control of the histone-acetyltransferase activity of Tip60 by the HIV-1 transactivator protein, Tat. Biochemistry 38:8826.
66. Col, E., Caron, C., Chable-Bessia, C. et al. 2005. HIV-1 Tat targets Tip60 to impair the apoptotic cell response to genotoxic stresses. EMBO J 24:2634.
67. Col, E., Gilquin, B., Caron, C. and Khochbin, S. 2002. Tat-controlled protein acetylation. J. Biol. Chem. 277:37955.
68. Vendel, A. C. and Lumb, K. J. 2004. NMR mapping of the HIV-1 Tat interaction surface of the KIX domain of the human coactivator CBP. Biochemistry 43:904.
69. Weissman, J. D., Brown, J. A., Howcroft, T. K. et al. 1998. HIV-1 tat binds TAFII250 and represses TAFII250-dependent transcription of major histocompatibility class I genes. Proc. Natl Acad. Sci. USA 95:11601.
70. Milani, D., Mazzoni, M., Borgatti, P., Zauli, G., Cantley, L. and Capitani, S. 1996. Extracellular human immunodeficiency virus type-1 Tat protein activates phosphatidylinositol 3-kinase in PC12 neuronal cells. J. Biol. Chem. 271:22961.
71. Borgatti, P., Zauli, G., Colamussi, M. L. et al. 1997. Extracellular HIV-1 Tat protein activates phosphatidylinositol 3- and Akt/PKB kinases in CD4+ T lymphoblastoid Jurkat cells. Eur. J. Immunol. 27:2805.
72. Li, W. Q., Jiang, Q., Khaled, A. R., Keller, J. R. and Durum, S. K. 2004. Interleukin-7 inactivates the pro-apoptotic protein Bad promoting T cell survival. J. Biol. Chem. 279:29160.
73. Gibellini, D., Re, M. C., Ponti, C. et al. 2001. Extracellular Tat activates c-fos promoter in low serum-starved CD4+ T cells. Br. J. Haematol. 112:663.
74. Rajnavolgyi, E., Benbernou, N., Rethi, B. et al. 2002. IL-7 withdrawal induces a stress pathway activating p38 and Jun N-terminal kinases. Cell. Signal. 14:761.