The interaction of LCK and the CD4 co-receptor alters the dose response of T-cells to interleukin-7

Immunology Letters

Volumn 131, Issue 2, 2010, Pages 170-181

  Kittipatarin, Christina ^a   Tschammer, Nuska ^a   Khaled, Annette R ^a  

^a UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Cytokine; Lymphocytes; Signal transduction

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; INTERLEUKIN 7; PROTEIN KINASE LCK; STAT5 PROTEIN; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ASSAY; CONCENTRATION RESPONSE; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL LINE; CELL PROLIFERATION; COMPARATIVE STUDY; DOSE RESPONSE; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR CLONING; PATHOLOGY; PHOSPHORYLATION; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD4; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE; CELL PROLIFERATION; CLONING, MOLECULAR; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; INTERLEUKIN-7; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; TRANSGENES;

EID: 77953711887     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2010.04.007     Document Type: Article

References (47)

1. Tsujino S., Di Santo J.P., Takaoka A., McKernan T.L., Noguchi S., Taya C., et al. Differential requirement of the cytoplasmic subregions of gamma c chain in T cell development and function. Proc Natl Acad Sci USA 2000, 97:10514-10519.
2. Sugamura K., Asao H., Kondo M., Tanaka N., Ishii N., Ohbo K., et al. The interleukin-2 receptor gamma chain: its role in the multiple cytokine receptor complexes and T cell development in XSCID. Annu Rev Immunol 1996, 14:179-205.
3. von-Freeden-Jeffry U., Vieira P., Lucian L.A., McNeil T., Burdach S.E., Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J Exp Med 1995, 181:1519-1526.
4. Peschon J.J., Gliniak B.C., Morrissey P.J., Maraskovsky E. Lymphoid development and function in IL-7R-deficient mice. Cytokine knockouts 1998, 37-52. Humana Press Inc., Totowa, NJ. S.K. Durum, K. Muegge (Eds.).
5. Park S.Y., Saijo K., Takahashi T., Osawa M., Arase H., Hirayama N., et al. Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity 1995, 3:771-782.
6. Yao Z., Cui Y., Watford W.T., Bream J.H., Yamaoka K., Hissong B.D., et al. Stat5a/b are essential for normal lymphoid development and differentiation. Proc Natl Acad Sci USA 2006, 103:1000-1005.
7. Puel A., Ziegler S.F., Buckley R.H., Leonard W.J. Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency. Nat Genet 1998, 20:394-397.
8. Fry T.J., Connick E., Falloon J., Lederman M.M., Liewehr D.J., Spritzler J., et al. A potential role for interleukin-7 in T-cell homeostasis. Blood 2001, 97:2983-2990.
9. Napolitano L.A., Grant R.M., Deeks S.G., Schmidt D., De Rosa S.C., Herzenberg L.A., 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.
10. Sawa Y., Arima Y., Ogura H., Kitabayashi C., Jiang J.-J., Fukushima T., et al. Hepatic interleukin-7 expression regulates T cell responses. Immunity 2009, 30:447-457.
11. Fisher A.G., Burdet C., LeMeur M., Haasner D., Gerber P., Ceredig R. Lymphoproliferative disorders in an IL-7 transgenic mouse line. Leukemia 1993, 7(Suppl 2):S66-S68.
12. El K.N., Lucas P.J., Klug D.B., Zamisch M., Merchant M., Bare C.V., et al. A dose effect of IL-7 on thymocyte development. Blood 2004, 104:1419-1427.
13. Kittipatarin C., Li W.Q., Bulavin D.V., Durum S.K., Khaled A.R. Cell cycling through Cdc25A: transducer of cytokine proliferative signals. Cell Cycle 2006, 5.
14. Kittipatarin C., Khaled A.R. Ex vivo expansion of memory CD8 T cells from lymph nodes or spleen through in vitro culture with interleukin-7. J Immunol Methods 2009, 344:45-57.
15. Swainson L., Verhoeyen E., Cosset F.L., 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.
16. Bosco N., Agenes F., Ceredig R. Effects of increasing IL-7 availability on lymphocytes during and after lymphopenia-induced proliferation. J Immunol 2005, 175:162-170.
17. Geiselhart L.A., Humphries C.A., Gregorio T.A., Mou S., Subleski J., Komschlies K.L. IL-7 administration alters the CD4:CD8 ratio, increases T cell numbers, and increases T cell function in the absence of activation. J Immunol 2001, 166:3019-3027.
18. Ingley E., Klinken S.P. Cross-regulation of JAK and Src kinases. Growth Factors 2006, 24:89-95.
19. Chin H., Arai A., Wakao H., Kamiyama R., Miyasaka N., Miura O. Lyn physically associates with the erythropoietin receptor and may play a role in activation of the Stat5 pathway. Blood 1998, 91:3734-3745.
20. Shi M., Cooper J.C., Yu C.L. A constitutively active Lck kinase promotes cell proliferation and resistance to apoptosis through signal transducer and activator of transcription 5b activation. Mol Cancer Res 2006, 4:39-45.
21. Burchill M.A., Goetz C.A., Prlic M., O'Neil J.J., Harmon I.R., Bensinger S.J., et al. Distinct effects of STAT5 activation on CD4+ and CD8+ T cell homeostasis: development of CD4+CD25+ regulatory T cells versus CD8+ memory T cells. J Immunol 2003, 171:5853-5864.
22. Tan J.T., Dudl E., LeRoy E., Murray R., Sprent J., Weinberg K.I., et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proc Natl Acad Sci USA 2001, 98:8732-8737.
23. Seddon B., Zamoyska R. TCR signals mediated by Src family kinases are essential for the survival of naive T cells. J Immunol 2002, 169:2997-3005.
24. Guimond M., Veenstra R.G., Grindler D.J., Zhang H., Cui Y., Murphy R.D., et al. Interleukin 7 signaling in dendritic cells regulates the homeostatic proliferation and niche size of CD4+ T cells. Nat Immunol 2009, 10:149-157.
25. Kim K., Khaled A.R., Reynolds D., Young H.A., Lee C.K., Durum S.K. Characterization of an interleukin-7-dependent thymic cell line derived from a p53(-/-) mouse. J Immunol Methods 2003, 274:177-184.
26. Van De Wiele C.J., Marino J.H., Murray B.W., Vo S.S., Whetsell M.E., Teague T.K. Thymocytes between the beta-selection and positive selection checkpoints are nonresponsive to IL-7 as assessed by STAT-5 phosphorylation. J Immunol 2004, 172:4235-4244.
27. Sportes C., Hakim F.T., Memon S.A., Zhang H., Chua K.S., Brown M.R., et al. Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J Exp Med 2008, 205:1701-1714.
28. Veillette A., Bookman M.A., Horak E.M., Bolen J.B. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 1988, 55:301-308.
29. Veillette A., Bookman M.A., Horak E.M., Samelson L.E., Bolen J.B. Signal transduction through the CD4 receptor involves the activation of the internal membrane tyrosine-protein kinase p56lck. Nature 1989, 338:257-259.
30. Veillette A., Zuniga-Pflucker J.C., Bolen J.B., Kruisbeek A.M. Engagement of CD4 and CD8 expressed on immature thymocytes induces activation of intracellular tyrosine phosphorylation pathways. J Exp Med 1989, 170:1671-1680.
31. Julius M., Maroun C.R., Haughn L. Distinct roles for CD4 and CD8 as co-receptors in antigen receptor signalling. Immunol Today 1993, 14:177-183.
32. Tomita K., Saijo K., Yamasaki S., Iida T., Nakatsu F., Arase H., et al. Cytokine-independent Jak3 activation upon T cell receptor (TCR) stimulation through direct association of Jak3 and the TCR complex. J Biol Chem 2001, 276:25378-25385.
33. Garcia R., Bowman T.L., Niu G., Yu H., Minton S., Muro-Cacho C.A., et al. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 2001, 20:2499-2513.
34. Seckinger P., Fougereau M. Activation of Src family kinases in human pre-B cells by IL-7. J Immunol 1994, 153:97-109.
35. Page T.H., Lali F.V., Foxwell B.M. Interleukin-7 activates p56lck and p59fyn, two tyrosine kinases associated with the p90 interleukin-7 receptor in primary human T cells. Eur J Immunol 1995, 25:2956-2960.
36. Seddon B., Zamoyska R. TCR and IL-7 receptor signals can operate independently or synergize to promote lymphopenia-induced expansion of naive T cells. J Immunol 2002, 169:3752-3759.
37. Sicheri F., Kuriyan J. Structures of Src-family tyrosine kinases. Curr Opin Struct Biol 1997, 7:777-785.
38. Brdicka T., Pavlistova D., Leo A., Bruyns E., Korinek V., Angelisova P., et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J Exp Med 2000, 191:1591-1604.
39. Xu S., Huo J., Tan J.E., Lam K.P. Cbp deficiency alters Csk localization in lipid rafts but does not affect T-cell development. Mol Cell Biol 2005, 25:8486-8495.
40. Parolini I., Topa S., Sorice M., Pace A., Ceddia P., Montesoro E., et al. Phorbol ester-induced disruption of the CD4-Lck complex occurs within a detergent-resistant microdomain of the plasma membrane. Involvement of the translocation of activated protein kinase C isoforms. J Biol Chem 1999, 274:14176-14187.
41. Kim P.W., Sun Z.Y., Blacklow S.C., Wagner G., Eck M.J. A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8. Science 2003, 301:1725-1728.
42. Molina T.J., Kishihara K., Siderovski D.P., van Ewijk W., Narendran A., Timms E., et al. Profound block in thymocyte development in mice lacking p56lck. Nature 1992, 357:161-164.
43. Nyakeriga A.M., Fichtenbaum C.J., Goebel J., Nicolaou S.A., Conforti L., Chougnet C.A. Engagement of the CD4 receptor affects the redistribution of Lck to the immunological synapse in primary T cells: implications for T-cell activation during human immunodeficiency virus type 1 infection. J Virol 2009, 83:1193-1200.
44. Van L.F., Sarafova S.D., Park J.H., Tai X., Pobezinsky L., Guinter T.I., et al. Deletion of CD4 and CD8 coreceptors permits generation of alphabetaT cells that recognize antigens independently of the MHC. Immunity 2007, 27:735-750.
45. Li W.Q., Jiang Q., Aleem E., Kaldis P., Khaled A.R., Durum S.K. IL-7 promotes T cell proliferation through destabilization of p27Kip1. J Exp Med 2006, 203:573-582.
46. Khaled A.R., Bulavin D.V., Kittipatarin C., Li W.Q., Alvarez M., Kim K., et al. Cytokine-driven cell cycling is mediated through Cdc25A. J Cell Biol 2005, 169:755-763.
47. Sportes C., Babb R.R., Krumlauf M.C., Hakim F.T., Steinberg S.M., Chow C.K., et al. Phase I study of recombinant human interleukin-7 administration in subjects with refractory malignancy. Clin Cancer Res 2010, 16:727-735.