IL-7 sustains CD31 expression in human naive CD4+ T cells and preferentially expands the CD31+ subset in a PI3K-dependent manner

Blood

Volumn 113, Issue 13, 2009, Pages 2999-3007

  Azevedo, Rita I ^a   Soares, Maria Vieira D ^a,b   Barata, João T ^a   Tendeiro, Rita ^a   Serra Caetano, Ana ^a   Victorino, Rui M M ^a   Sousa, Ana E ^a  

^a UNIVERSITY OF LISBON   (Portugal)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CD4 ANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE; RECOMBINANT INTERLEUKIN 7;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MALE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 64049104988     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-07-166223     Document Type: Article

References (39)

1. Kimmig S, Przybylski GK, Schmidt CA, et al. Two subsets of naive T helper cells with distinct T-cell receptor excision circle content in human adult peripheral blood. J Exp Med. 2002;195: 789-794.
2. Fry TJ, Mackall CL. The many faces of IL-7: from lymphopoiesis to peripheral T-cell maintenance. J Immunol. 2005;174:6571-6576.
3. Kong FK, Chen CL, Six A, Hockett RD, Cooper MD. T-cell receptor gene deletion circles identify recent thymic emigrants in the peripheral T-cell pool. Proc Natl Acad Sci USA. 1999;96:1536-1540.
4. Douek DC, McFarland RD, Keiser PH, et al. Changes in thymic function with age and during the treatment of HIV infection. Nature. 1998;396:690-695.
5. Kohler S, Wagner U, Pierer M, et al. Post-thymic in vivo proliferation of naive CD4+ T cells constrains the TCR repertoire in healthy human adults. Eur J Immunol. 2005;35:1987-1994.
6. Kilpatrick RD, Rickabaugh T, Hultin LE, et al. Homeostasis of the naive CD4+ T-cell compartment during aging. J Immunol. 2008;180:1499-1507.
7. Tan JT, Dudl E, LeRoy E, et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA. 2001;98:8732-8737.
8. Soares MV, Borthwick NJ, Maini MK, Janossy G, Salmon M, AkbarAN. IL-7-dependent extrathymic expansion of CD45RA+ T cells enables preservation of a naive repertoire. J Immunol. 1998;161:5909-5917.
9. Swainson L, Verhoeyen E, Cosset FL, Taylor N. IL-7Rα gene expression is inversely correlated with cell cycle progression in IL-7-stimulated T lymphocytes. J Immunol. 2006;176:6702-6708.
10. Seddon B, Zamoyska R. TCR and IL-7 receptor signals can operate independently or synergize to promote lymphopenia-induced expansion of naiveT cells. J Immunol. 2002;169:3752-3759.
11. Alpdogan O, Muriglan SJ, Eng JM, et al. IL-7 enhances peripheral T-cell reconstitution after allo-geneic hematopoietic stem cell transplantation. J Clin Invest. 2003;112:1095-1107.
12. Broers AE, Posthumus-van Sluijs SJ, Spits H, et al. Interleukin-7 improves T-cell recovery after experimental T-cell-depleted bone marrow transplantation in T-cell-deficient mice by strong expansion of recent thymic emigrants. Blood. 2003; 102:1534-1540.
13. Mackall CL, Fry TJ, Bare C, Morgan P, Galbraith A, Gress RE. IL-7 increases both thymic-depen-dent and thymic-independent T-cell regeneration after bone marrow transplantation. Blood. 2001; 97:1491-1497.
14. Moniuszko M, Fry T, Tsai WP, et al. Recombinant interleukin-7 induces proliferation of naive macaque CD4+ and CD8+ T cells in vivo. J Virol. 2004;78:9740-9749.
15. FryTJ, Moniuszko M, Creekmore S, et al. IL-7 therapy dramatically alters peripheral T-cell ho-meostasis in normal and SIV-infected nonhuman primates. Blood. 2003;101:2294-2299.
16. Albuquerque AS, Cortesao CS, Foxall RB, Soares RS, Victorino RM, Sousa AE. Rate of increase in circulating IL-7 and loss of IL-7Rα expression differ in HIV-1 and HIV-2 infections: two lymphopenic diseases with similar hyperimmune activation but distinct outcomes. J Immunol. 2007;178:3252-3259.
17. Bolotin E, Annett G, Parkman R, Weinberg K. Serum levels of IL-7 in bone marrow transplant recipients: relationship to clinical characteristics and lymphocyte count. Bone Marrow Transplant. 1999;23:783-788.
18. Napolitano LA, Grant RM, Deeks SG, et al. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: implications for T-cell homeostasis. Nat Med. 2001;7:73-79.
19. Fry TJ, Connick E, Falloon J, et al. A potential role for interleukin-7 in T-cell homeostasis. Blood. 2001;97:2983-2990.
20. Rosenberg SA, Sportes C, Ahmadzadeh M, et al. IL-7 administration to humans leads to expansion of CD8+ and CD4+ cells but a relative decrease of CD4+ T-regulatory cells. J Immunother. 2006;29:313-319.
21. Sportes C, Hakim FT, Memon SA, et al. Administration of rhIL-7 in humans increases in vivoTCR repertoire diversity by preferential expansion of naive T-cell subsets. J Exp Med. 2008;205:1701-1714.
22. Hassan J, Reen DJ. IL-7 promotes the survival and maturation but not differentiation of human post-thymic CD4+ T cells. Eur J Immunol. 1998; 28:3057-3065.
23. Swainson L, Kinet S, Mongellaz C, Sourisseau M, Henriques T, Taylor N. IL-7-induced proliferation of recent thymic emigrants requires activation of the PI3K pathway. Blood. 2007;109:1034-1042.
24. Hassan J, Reen DJ. Human recent thymic emigrants-identification, expansion, and survival characteristics. J Immunol. 2001;167:1970-1976.
25. Jaleco S, Swainson L, Dardalhon V, Burjanadze M, Kinet S, Taylor N. Homeostasis of naive and memory CD4+ T cells: IL-2 and IL-7 differentially regulate the balance between proliferation and Fas-mediated apoptosis. J Immunol. 2003;171:61-68.
26. Park JH, Yu Q, Erman B, et al. Suppression of IL7Ralpha transcription by IL-7 and other prosur-vival cytokines: a novel mechanism for maximizing IL-7-dependent T-cell survival. Immunity. 2004;21:289-302.
27. Barata JT, Silva A, Brandao JG, Nadler LM, Cardoso AA, Boussiotis VA. Activation of PI3K is indispensable for interleukin 7-mediated viability, proliferation, glucose use, and growth of T-cell acute lympho-blastic leukemia cells. J Exp Med. 2004;200:659-669.
28. Leonard WJ, O'Shea JJ. Jaks and STATs: biological implications. Annu Rev Immunol. 1998;16:293-322.
29. Rathmell JC, Farkash EA, GaoW, Thompson CB. IL-7 enhances the survival and maintains the size of naiveT cells. J Immunol. 2001;167:6869-6876.
30. Crawley JB, Rawlinson L, Lali FV, PageTH, Saklatvala J, Foxwell BM. T-cell proliferation in response to interleukins 2 and 7 requires p38MAP kinase activation. J Biol Chem. 1997; 272:15023-15027.
31. Barata JT, Silva A, Abecasis M, Carlesso N, Cumano A, Cardoso AA. Molecular and functional evidence for activity of murine IL-7 on human lymphocytes. Exp Hematol. 2006;34:1133-1142.
32. Kovanen PE, Rosenwald A, Fu J, et al. Analysis of gamma c-family cytokine target genes. Identification of dual-specificity phosphatase 5(DUSP5) as a regulator of mitogen-activated protein kinase activity in interleukin-2 signaling. J Biol Chem. 2003;278:5205-5213.
33. Deaglio S, Morra M, Mallone R, et al. Human CD38(ADP-ribosyl cyclase) is a counter-receptor of CD31, an Ig superfamily member. J Immunol.1998;160:395- 402.
34. Ernst B, Lee DS, Chang JM, Sprent J, Surh CD. The peptide ligands mediating positive selection in the thymus control T-cell survival and homeo-static proliferation in the periphery. Immunity. 1999;11:173-181.
35. Demeure CE, Byun DG, Yang LP, Vezzio N, Delespesse G. CD31(PECAM-1) is adifferentiation antigen lost during human CD4 T-cell maturation into Th1 or Th2 effector cells. Immunology. 1996; 88:110-115.
36. Verschelde C, Walzer T, Galia P, et al. A1/Bfl-1 expression is restricted to TCR engagement in T lymphocytes. Cell Death Differ. 2003;10:1059-1067.
37. Newton-Nash DK, Newman PJ. A new role for platelet-endothelial cell adhesion molecule-1(CD31): inhibition of TCR-mediated signal trans-duction. J Immunol. 1999;163:682-688.
38. Prager E, Staffler G, Majdic O, et al. Induction of hyporesponsiveness and impaired T lymphocyte activation by the CD31 receptor:ligand pathway in T cells. J Immunol. 2001;166:2364-2371.
39. Dittel BN, LeBien TW. The growth response to IL-7 during normal human B-cell ontogeny is restricted to B-lineage cells expressing CD34. J Immunol. 1995;154:58-67.