IL-7 downregulates IL-7Rα expression in human CD8 T cells by two independent mechanisms

Immunology and Cell Biology

Volumn 91, Issue 2, 2013, Pages 149-158

  Ghazawi, Feras M ^a,b   Faller, Elliott M ^a,b   Sugden, Scott M ^a,b   Kakal, Juzer A ^a,b   MacPherson, Paul A ^a,b,c  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

CD127; cytotoxic T lymphocytes; interleukin 7; interleukin 7 receptor

Indexed keywords

INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR ALPHA; JANUS KINASE; MEMBRANE PROTEIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; STAT5 PROTEIN;

ARTICLE; CD8+ T LYMPHOCYTE; CELL SURFACE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; RECEPTOR DOWN REGULATION;

CD8-POSITIVE T-LYMPHOCYTES; CELL MEMBRANE; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; DOWN-REGULATION; HUMANS; INTERLEUKIN-7; JANUS KINASES; JURKAT CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; RECEPTORS, INTERLEUKIN-7; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84873711707     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2012.69     Document Type: Article

References (55)

1. Jiang Q, Li WQ, Aiello FB, Mazzucchelli R, Asefa B, Khaled AR et al. Cell biology of IL-7, a key lymphotrophin. Cytokine Growth Factor Rev 2005; 16: 513-533.
2. Fry TJ, Mackall CL. Interleukin-7: from bench to clinic. Blood 2002; 99: 3892-3904.
3. Khaled AR, Durum SK. Lymphocide: cytokines and the control of lymphoid homeostasis. Nat Rev Immunol 2002; 2: 817-830.
4. Becker TC, Wherry EJ, Boone D, Murali-Krishna K, Antia R, Ma A et al. Interleukin 15 is required for proliferative renewal of virus-specific memory CD8 T cells. J Exp Med 2002; 195: 1541-1548.
5. Goldrath AW, Sivakumar PV, Glaccum M, Kennedy MK, Bevan MJ, Benoist C et al. Cytokine requirements for acute and Basal homeostatic proliferation of naive and memory CD8\+ T cells. J Exp Med 2002; 195: 1515-1522.
6. Kieper WC, Tan JT, Bondi-Boyd B, Gapin L, Sprent J, Ceredig R et al. Overexpression of interleukin (IL)-7 leads to IL-15-independent generation of memory phenotype CD8\+ T cells. J Exp Med 2002; 195: 1533-1539.
7. Tan JT, Ernst B, Kieper WC, LeRoy E, Sprent J, Surh CD. Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8\+ cells but are not required for memory phenotype CD4\+ cells. J Exp Med 2002; 195: 1523-1532.
8. Maraskovsky E, Teepe M, Morrissey PJ, Braddy S, Miller RE, Lynch DH et al. Impaired survival and proliferation in IL-7 receptor-deficient peripheral T cells. J Immunol 1996; 157: 5315-5323.
9. Jicha DL, Mule JJ, Rosenberg SA. Interleukin 7 generates antitumor cytotoxic T lymphocytes against murine sarcomas with efficacy in cellular adoptive immunotherapy. J Exp Med 1991; 174: 1511-1515.
10. Sun JC, Lehar SM, Bevan MJ. Augmented IL-7 signaling during viral infection drives greater expansion of effector T cells but does not enhance memory. J Immunol 2006; 177: 4458-4463.
11. Saini M, Pearson C, Seddon B. Regulation of T cell-dendritic cell interactions by IL-7 governs T-cell activation and homeostasis. Blood 2009; 113: 5793-5800.
12. Sin JI, Kim J, Pachuk C, Weiner DB. Interleukin 7 can enhance antigen-specific cytotoxic-T-lymphocyte and/or Th2-type immune responses in vivo. Clin Diagn Lab Immunol 2000; 7: 751-758.
13. Kos FJ, Mullbacher A. Induction of primary anti-viral cytotoxic T cells by in vitro stimulation with short synthetic peptide and interleukin-7. Eur J Immunol 1992; 22: 3183-3185.
14. Carini C, Essex M. Interleukin 2-independent interleukin 7 activity enhances cytotoxic immune response of HIV-1-infected individuals. AIDS Res Hum Retroviruses 1994; 10: 121-130.
15. Faller EM, McVey MJ, Kakal JA, MacPherson PA. Interleukin-7 receptor expression on CD8 T-cells is downregulated by the HIV Tat protein. J Acquir Immune Defic Syndr 2006; 43: 257-269.
16. Catalfamo M, Henkart PA. Perforin and the granule exocytosis cytotoxicity pathway. Curr Opin Immunol 2003; 15: 522-527.
17. Goodwin RG, Friend D, Ziegler SF, Jerzy R, Falk BA, Gimpel S et al. Cloning of the human and murine interleukin-7 receptors: demonstration of a soluble form and homology to a new receptor superfamily. Cell 1990; 60: 941-951.
18. Kang J, Der SD. Cytokine functions in the formative stages of a lymphocyte's life. Curr Opin Immunol 2004; 16: 180-190.
19. Park JH, Yu Q, Erman B, Appelbaum JS, Montoya-Durango D, Grimes HL et al. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 2004; 21: 289-302.
20. Swainson L, Verhoeyen E, Cosset FL, Taylor N. IL-7R alpha gene expression is inversely correlated with cell cycle progression in IL-7-stimulated T lymphocytes. J Immunol 2006; 176: 6702-6708.
21. Vranjkovic A, Crawley AM, Gee K, Kumar A, Angel JB. IL-7 decreases IL-7 receptor alpha (CD127) expression and induces the shedding of CD127 by human CD8\+ T cells. Int Immunol 2007; 19: 1329-1339.
22. Alves NL, van Leeuwen EM, Derks IA, van Lier RA. Differential regulation of human IL-7 receptor alpha expression by IL-7 and TCR signaling. J Immunol 2008; 180: 5201-5210.
23. Faller E, Kakal J, Kumar R, Macpherson P. IL-7 and the HIV Tat protein act synergistically to down-regulate CD127 expression on CD8 T cells. Int Immunol 2009; 21: 203-216.
24. Henriques CM, Rino J, Nibbs RJ, Graham GJ, Barata JT. IL-7 induces rapid clathrinmediated internalization and JAK3-dependent degradation of IL-7Ralpha in T cells. Blood 2010; 115: 3269-3277.
25. Sasson SC, Zaunders JJ, Zanetti G, King EM, Merlin KM, Smith DE et al. 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 2006; 193: 505-514.
26. Faller EM, Sugden SM, McVey MJ, Kakal JA, MacPherson PA. Soluble HIV Tat protein removes the IL-7 receptor alpha-chain from the surface of resting CD8 T cells and targets it for degradation. J Immunol 2010; 185: 2854-2866.
27. Lee HC, Shibata H, Ogawa S, Maki K, Ikuta K. Transcriptional regulation of the mouse IL-7 receptor alpha promoter by glucocorticoid receptor. J Immunol 2005; 174: 7800-7806.
28. Mittelstadt PR, Ashwell JD. Disruption of glucocorticoid receptor exon 2 yields a ligand-responsive C-terminal fragment that regulates gene expression. Mol Endocrinol 2003; 17: 1534-1542.
29. Crawley AM, Vranjkovic A, Young C, Angel JB. Interleukin-4 downregulates CD127 expression and activity on human thymocytes and mature CD8\+ T cells. Eur J Immunol 2010; 40: 1396-1407.
30. Johnston JA, Bacon CM, Finbloom DS, Rees RC, Kaplan D, Shibuya K et al. Tyrosine phosphorylation and activation of STAT5, STAT3, and Janus kinases by interleukins 2 and 15. Proc Natl Acad Sci USA 1995; 92: 8705-8709.
31. Demoulin JB, Van Snick J, Renauld JC. Interleukin-9 (IL-9) induces cell growth arrest associated with sustained signal transducer and activator of transcription activation in lymphoma cells overexpressing the IL-9 receptor. Cell Growth Differ 2001; 12: 169-174.
32. Goodman WA, Young AB, McCormick TS, Cooper KD, Levine AD. Stat3 phosphorylation mediates resistance of primary human T cells to regulatory T cell suppression. J Immunol 2011; 186: 3336-3345.
33. Murray PJ. The JAK-STAT signaling pathway: input and output integration. J Immunol 2007; 178: 2623-2629.
34. Zhang B, Zhang Y, Niu L, Vella AT, Mittler RS. Dendritic cells and Stat3 are essential for CD137-induced CD8 T cell activation-induced cell death. J Immunol 2010; 184: 4770-4778.
35. Hirata N, Yanagawa Y, Iwabuchi K, Onoe K. Selective regulation of interleukin-10 production via Janus kinase pathway in murine conventional dendritic cells. Cell Immunol 2009; 258: 9-17.
36. Kim HR, Hwang KA, Kim KC, Kang I. Down-regulation of IL-7Ralpha expression in human T cells via DNA methylation. J Immunol 2007; 178: 5473-5479.
37. Kim K, Khaled AR, Reynolds D, Young HA, Lee CK, Durum SK. Characterization of an interleukin-7-dependent thymic cell line derived from a p53(-/-) mouse. J Immunol Methods 2003; 274: 177-184.
38. Wofford JA, Wieman HL, Jacobs SR, Zhao Y, Rathmell JC. IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T-cell survival. Blood 2008; 111: 2101-2111.
39. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 2003; 4: 1191-1198.
40. Prlic M, Lefrancois L, Jameson SC. Multiple choices: regulation of memory CD8 T cell generation and homeostasis by interleukin (IL)-7 and IL-15. J Exp Med 2002; 195: F49-F52.
41. Gregory SG, Schmidt S, Seth P, Oksenberg JR, Hart J, Prokop A et al. Interleukin 7 receptor alpha chain (IL7R) shows allelic and functional association with multiple sclerosis. Nat Genet 2007; 39: 1083-1091.
42. Kreft KL, Verbraak E, Wierenga-Wolf AF, van Meurs M, Oostra BA, Laman JD et al. The IL-7Ralpha pathway is quantitatively and functionally altered in cd8 t cells in multiple sclerosis. J Immunol 2012; 188: 1874-1883.
43. O'Doherty C, Alloza I, Rooney M, Vandenbroeck K. IL7RA polymorphisms and chronic inflammatory arthropathies. Tissue Antigen 2009; 74: 429-431.
44. Vudattu NK, Magalhaes I, Schmidt M, Seyfert-Margolis V, Maeurer MJ. Reduced numbers of IL-7 receptor (CD127) expressing immune cells and IL-7-signaling defects in peripheral blood from patients with breast cancer. Int J Cancer 2007; 121: 1512-1519.
45. van Leeuwen EM, de Bree GJ, Remmerswaal EB, Yong SL, Tesselaar K, ten Berge IJ et al. IL-7 receptor alpha chain expression distinguishes functional subsets of virusspecific human CD8\+ T cells. Blood 2005; 106: 2091-2098.
46. Wherry EJ, Day CL, Draenert R, Miller JD, Kiepiela P, Woodberry T et al. HIV-specific CD8 T cells express low levels of IL-7Ralpha: implications for HIV-specific T cell memory. Virology 2006; 353: 366-373.
47. Sauce D, Larsen M, Leese AM, Millar D, Khan N, Hislop AD et al. IL-7R alpha versus CCR7 and CD45 as markers of virus-specific CD8\+ T cell differentiation: contrasting pictures in blood and tonsillar lymphoid tissue. J Infect Dis 2007; 195: 268-278.
48. Golden-Mason L, Burton Jr JR, Castelblanco N, Klarquist J, Benlloch S, Wang C et al. Loss of IL-7 receptor alpha-chain (CD127) expression in acute HCV infection associated with viral persistence. Hepatology 2006; 44: 1098-1109.
49. Boutboul F, Puthier D, Appay V, Pelle O, Ait-Mohand H, Combadiere B et al. Modulation of interleukin-7 receptor expression characterizes differentiation of CD8 T cells specific for HIV, EBV and CMV. Aids 2005; 19: 1981-1986.
50. Colle JH, Moreau JL, Fontanet A, Lambotte O, Joussemet M, Delfraissy JF et al. 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 2006; 143: 398-403.
51. Koesters SA, Alimonti JB, Wachihi C, Matu L, Anzala O, Kimani J et al. IL-7Ralpha expression on CD4(\+) T lymphocytes decreases with HIV disease progression and inversely correlates with immune activation. Eur J Immunol 2006; 36: 336-344.
52. MacPherson PA, Fex C, Sanchez-Dardon J, Hawley-Foss N, Angel JB. 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 2001; 28: 454-457.
53. Mercier F, Boulassel MR, Yassine-Diab B, Tremblay C, Bernard NF, Sekaly RP et al. Persistent human immunodeficiency virus-1 antigenaemia affects the expression of interleukin-7Ralpha on central and effector memory CD4\+ and CD8\+ T cell subsets. Clin Exp Immunol 2008; 152: 72-80.
54. Paiardini M, Cervasi B, Albrecht H, Muthukumar A, Dunham R, Gordon S et al. Loss of CD127 expression defines an expansion of effector CD8\+ T cells in HIV-infected individuals. J Immunol 2005; 174: 2900-2909.
55. Rethi B, Fluur C, Atlas A, Krzyzowska M, Mowafi F, Grutzmeier S et al. Loss of IL-7Ralpha is associated with CD4 T-cell depletion, high interleukin-7 levels and CD28 down-regulation in HIV infected patients. Aids 2005; 19: 2077-2086.