CD45 down-regulates Lck-mediated CD44 signaling and modulates actin rearrangement in T cells

Journal of Immunology

Volumn 181, Issue 10, 2008, Pages 7033-7043

  Wong, Nelson K Y ^a   Lai, Jacqueline C Y ^a   Birkenhead, Darlene ^a   Shaw, Andrey S ^b   Johnson, Pauline ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CD45 ANTIGEN; HERMES ANTIGEN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE LCK; PROTEIN TYROSINE KINASE; TYROSINE; CD44 PROTEIN, MOUSE; PTPRC PROTEIN, MOUSE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL POLARITY; CELL SPREADING; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; ANIMAL; C57BL MOUSE; CELL CULTURE; CONFOCAL MICROSCOPY; IMAGE PROCESSING; IMMUNOLOGY; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; WESTERN BLOTTING;

ACTINS; ANIMALS; ANTIGENS, CD44; ANTIGENS, CD45; BLOTTING, WESTERN; CELLS, CULTURED; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOPRECIPITATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 58149182887     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.10.7033     Document Type: Article

References (74)

1. Alexander, D. R. 2000. The CD45 tyrosine phosphatase: a positive and negative regulator of immune cell function. Semin. Immunol. 12: 349-359.
2. Hermiston, M. L., Z. Xu, and A. Weiss. 2003. CD45: a critical regulator of signaling thresholds in immune cells. Annu. Rev. Immunol. 21: 107-137.
3. Huntington, N. D., and D. M. Tarlinton. 2004. CD45: direct and indirect government of immune regulation. Immunol. Lett. 94: 167-174.
4. Ostergaard, H. L., D. A. Shackelford, T. R. Hurley, P. Johnson, R. Hyman, B. M. Sefton, and I. S. Trowbridge. 1989. Expression of CD45 alters phosphorylation of the Lck-encoded tyrosine protein kinase in murine lymphoma T-cell lines. Proc. Natl. Acad. Sci. USA 86: 8959-8963.
5. lck by the CD45 phosphotyrosine phosphatase. Proc. Natl. Acad. Sci. USA 86: 6302-6306.
6. fyn protein tyrosine kinase by the CD45 phosphotyrosine phosphatase. Eur. J. Immunol. 22: 1173-1178.
7. Shiroo, M., L. Goff, M. Biffen, E. Shivnan, and D. Alexander. 1992. CD45 tyrosine phosphatase-activated p59fyn couples the T cell antigen receptor to pathways of diacylglycerol production, protein kinase C activation and calcium influx. EMBO J. 11: 4887-4897.
8. Brown, V. K., E. W. Ogle, A. L. Burkhardt, R. B. Rowley, J. B. Bolen, and L. B. Justement. 1994. Multiple components of the B cell antigen receptor complex associate with the protein tyrosine phosphatase, CD45. J. Biol. Chem. 269: 17238-17244.
9. Burg, D. L., M. T. Furlong, M. L. Harrison, and R. L. Geahlen. 1994. Interactions of Lyn with the antigen receptor during B cell activation. J. Biol. Chem. 269: 28136-28142.
10. Katagiri, T., M. Ogimoto, K. Hasegawa, K. Mizuno, and H. Yakura. 1995. Selective regulation of Lyn tyrosine kinase by CD45 in immature B cells. J. Biol. Chem. 270: 27987-27990.
11. Yanaga, S., H. Sugawara, M. Kurosaki, H. Sabe, H. Yamaura, and T. Kurosaki. 1996. CD45 modulates phosphorylation of both autophosphorylation and negative regulatory tyrosines of Lyn in B cells. J. Biol. Chem. 271: 30487-30492.
12. Roach, T., S. Slater, M. Koval, L. White, E. Cahir McFarland, M. Okumura, M. Thomas, and E. Brown. 1997. CD45 regulates Src family member kinase activity associated with macrophage integrin-mediated adhesion. Curr. Biol. 7: 408-417.
13. Sicheri, F., I. Moarefi, and J. Kuriyan. 1997. Crystal structure of the Src family tyrosine kinase Hck. Nature 385: 602-609.
14. Xu, W. Q., S. C. Harrison, and M. J. Eck. 1997. Three-dimensional structure of the tyrosine kinase c-Src. Nature 385: 595-602.
15. Brown, M. T., and J. A. Cooper. 1996. Regulation, substrates and functions of Src. Biochim. Biophys. Acta 1287: 121-149.
16. Williams, J. C., R. K. Wierenga, and M. Saraste. 1998. Insights into Src kinase functions - structural comparisons. Trends Biochem. Sci. 23: 179-184.
17. Ashwell, J. D., and U. D'Oro. 1999. CD45 and Src-family kinases: and now for something completely different. Immunol. Today 20: 412-416.
18. Thomas, M. L., and E. J. Brown. 1999. Positive and negative regulation of Src-family membrane kinases by CD45. Immunol. Today 20: 406-411.
19. D'Oro, U., and J. D. Ashwell. 1999. Cutting edge: The CD45 tyrosine phosphatase is an inhibitor of Lck activity in thymocytes. J. Immunol. 162: 1879-1883.
20. D'Oro, U., K. Sakaguchi, E. Appella, and J. D. Ashwell. 1996. Mutational analysis of lck in CD45-negative T cells: dominant role of tyrosine 394 phosphorylation in kinase activity. Mol. Cell Biol. 16: 4996-5003.
21. Li, R. H., N. Wong, M. D. Jabali, and P. Johnson. 2001. CD44-initiated cell spreading induces Pyk2 phosphorylation, is mediated by Src family kinases, and is negatively regulated by CD45. J. Biol. Chem. 276: 28767-28773. (Pubitemid 37451953)
22. Shenoi, H., J. Seavitt, A. Zheleznyak, M. L. Thomas, and E. J. Brown. 1999. Regulation of integrin-mediated T cell adhesion by the transmembrane protein tyrosine phosphatase CD45. J. Immunol. 162: 7120-7127. (Pubitemid 29277681)
23. Irie-Sasaki, J., T. Sasaki, W. Matsumoto, A. Opavsky, M. Cheng, G. Welstead, E. Griffiths, C. Krawczyk, C. D. Richardson, K. Aitken, et al. 2001. CD45 is a JAK phosphatase and negatively regulates cytokine receptor signalling. Nature 409: 349-354. (Pubitemid 32151240)
24. Petricoin, E. F., S. Ito, B. L. Williams, S. Audet, L. F. Stancato, A. Gamero, K. Clouse, P. Grimley, A. Weiss, J. Beeler, et al. 1997. Antiproliferative action of interferon-α requires components of T-cell-receptor signalling. Nature 390: 629-632.
25. Lesley, J., R. Hyman, N. English, J. B. Catterall, and G. A. Turner. 1997. CD44 in inflammation and metastasis. Glycoconj. J. 14: 611-622.
26. Johnson, P., A. Maiti, K. L. Brown, and R. Li. 2000. A role for the cell adhesion molecule CD44 and sulfation in leukocyte-endothelial cell adhesion during an inflammatory response? Biochem. Pharm. 59: 455-465.
27. Pure, E., and C. A. Cuff. 2001. A crucial role for CD44 in inflammation. Trends Mol. Med. 7: 213-221.
28. Ponta, H., L. Sherman, and P. A. Herrlich. 2003. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 4: 33-45. (Pubitemid 36077255)
29. Lesley, J., N. Howes, A. Perschl, and R. Hyman. 1994. Hyaluronan binding function of CD44 is transiently activated on T cells during an in vivo immune response. J. Exp. Med. 180: 383-387. (Pubitemid 24181089)
30. Kohda, D., C. J. Morton, A. A. Parkar, H. Hatanaka, F. M. Inagaki, I. D. Campbell, and A. J. Day. 1996. Solution structure of the link module: a hyaluronan-binding domain involved in extracellular matrix stability and cell migration. Cell 86: 767-775. (Pubitemid 26303445)
31. DeGrendele, H. C., P. Estess, L. J. Picker, and M. H. Siegelman. 1996. CD44 and its ligand hyaluronate mediate rolling under physiologic flow - a novel lymphocyte-endothelial cell primary adhesion pathway. J. Exp. Med. 183: 1119-1130.
32. Brenner, B., E. Gulbins, K. Schlottmann, U. Koppenhoefer, G. L. Busch, B. Walzog, M. Steinhausen, K. M. Coggeshall, O. Linderkamp, and F. Lang. 1996. L-selectin activates the Ras pathway via the tyrosine kinase p56lck. Proc. Natl. Acad. Sci. USA 93: 15376-15381. (Pubitemid 27009608)
33. lck in T lymphocytes. J. Biol. Chem. 271: 2863-2867.
34. Volkov, Y., A. Long, S. McGrath, D. Ni Eidhin, and D. Kelleher. 2001. Crucial importance of PKC-β(I) in LFA-1-mediated locomotion of activated T cells. Nat Immunol. 2: 508-514. (Pubitemid 33705852)
35. Fanning, A., Y. Volkov, M. Freeley, D. Kelleher, and A. Long. 2005. CD44 cross-linking induces protein kinase C-regulated migration of human T lymphocytes. Int. Immunol. 17: 449-458. (Pubitemid 40568120)
36. Bourguignon, L. Y. W., V. B. Lokeshwar, X. Chen, and W. G. L. Kerrick. 1993. Hyaluronic acid-induced lymphocyte signal transduction and HA receptor (GP85/CD44)-cytoskeleton interaction. J. Immunol. 151: 6634-6644. (Pubitemid 24001038)
37. Ilangumaran, S., A. Briol, and D. C. Hoessli. 1998. CD44 selectively associates with active src family protein tyrosine kinases Lck and Fyn in glycosphingolipidrich plasma membrane domains of human peripheral blood lymphocytes. Blood 91: 3901-3908.
38. lck associated with glycolipid-enriched membrane domains. J. Cell Biol. 135: 1515-1523.
39. Johnson, K. G., S. K. Bromley, M. L. Dustin, and M. L. Thomas. 2000. A supramolecular basis for CD45 tyrosine phosphatase regulation in sustained T cell activation. Proc. Natl. Acad. Sci. USA 97: 10138-10143. (Pubitemid 30680868)
40. Edmonds, S. D., and H. L. Ostergaard. 2002. Dynamic association of CD45 with detergent-insoluble microdomains in T lymphocytes. J. Immunol. 169: 5036-5042.
41. lck and the cytoplasmic domain of CD45 in vitro. J. Biol. Chem. 271: 1295-1300.
42. Ng, D. H. W., M. D. Jabali, A. Maiti, P. Borodchak, K. Harder, T. Brocker, B. Malissen, F. R. Jirik, and P. Johnson. 1997. CD45 and RPTPα display different protein tyrosine phosphatase activities in T lymphocytes. Biochem. J. 327: 867-876.
43. Holdorf, A. D., K. H. Lee, W. R. Burack, P. M. Allen, and A. S. Shaw. 2002. Regulation of Lck activity by CD4 and CD28 in the immunological synapse. Nat. Immunol. 3: 259-264.
44. Trowbridge, I. S. 1978. Interspecies spleen-myeloma hybrid producing monoclonal antibodies against mouse lymphocyte surface glycoprotein, T200. J. Exp. Med. 148: 313-323.
45. Wegener, A. M. K., F. Letourneur, A. Hoeveler, T. Brocker, F. Luton, and B. Malissen. 1992. The T cell receptor/CD3 complex is composed of at least two autonomous transduction modules. Cell 68: 83-95.
46. Byth, K. F., L. A. Conroy, S. Howlett, A. J. H. Smith, J. May, D. R. Alexander, and N. Holmes. 1996. CD45-null transgenic mice reveal a positive regulatory role for CD45 in early thymocyte development, in the selection of CD4+CD8+ thymocytes, and in B cell maturation. J. Exp. Med. 183: 1707-1718.
47. Kelleher, D., A. Murphy, C. Feighery, and E. B. Casey. 1995. Leukocyte function-associated antigen 1 (Lfa-1) and CD44 are signalling molecules for cytoskeleton- dependent morphological changes in activated T cells. J. Leukocyte Biol. 58: 539-546.
48. Hardwick, J. S., and B. M. Sefton. 1997. The activated form of the lck tyrosine protein kinase in cells exposed to hydrogen peroxide is phosphorylated at both Tyr-394 and Tyr-505. J. Biol. Chem. 272: 25429-25432.
49. Yamaguchi, H., and W. A. Hendrickson. 1996. Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384: 484-489.
50. von Willebrand, M., G. Baier, C. Couture, P. Burn, and T. Mustelin. 1994. Activation of phosphatidylinositol-3-kinase in Jurkat T cells depends on the presence of the p56lck tyrosine kinase. Eur. J. Immunol. 24: 234-238. (Pubitemid 24014705)
51. Weber, J. R., G. M. Bell, M. Y. Han, T. Pawson, and J. B. Imboden. 1992. Association of the tyrosine kinase LCK with phospholipase C-γ1 after stimulation of the T cell antigen receptor. J. Exp. Med. 176: 373-379.
52. Gupta, S., A. Weiss, G. Kumar, S. Wang, and A. Nel. 1994. The T-cell antigen receptor utilizes Lck, Raf-1, and MEK-1 for activating mitogen-activated protein kinase: evidence for the existence of a second protein kinase C-dependent pathway in an Lck-negative Jurkat cell mutant. J. Biol. Chem. 269: 17349-17357. (Pubitemid 24978726)
53. Finco, T. S., T. Kadlecek, W. G. Zhang, L. E. Samelson, and A. Weiss. 1998. LAT is required for TCR-mediated activation of PLCγ1 and the Ras pathway. Immunity 9: 617-626.
54. Lefebvre, D. C., J. Felberg, J. L. Cross, and P. Johnson. 2003. The non-catalytic domains of Lck regulate its dephosphorylation by CD45. Biochim. Biophys. Acta 1650: 40-49.
55. Mariathasan, S., A. Zakarian, D. Bouchard, A. M. Michie, J. C. Zuniga-Pflucker, and P. S. Ohashi. 2001. Duration and strength of extracellular signal-regulated kinase signals are altered during positive versus negative thymocyte selection. J. Immunol. 167: 4966-4973. (Pubitemid 33009727)
56. Starr, T. K., S. C. Jameson, and K. A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21: 139-176.
57. Iezzi, G., K. Karjalainen, and A. Lanzavecchia. 1998. The duration of antigenic stimulation determines the fate of naive and effector T cells. Immunity 8: 89-95. (Pubitemid 28097826)
58. Weiss, A., R. Shields, M. Newton, B. Manger, and J. Imboden. 1987. Ligand-receptor interactions required for commitment to the activation of the interleukin 2 gene. J. Immunol. 138: 2169-2176. (Pubitemid 17046269)
59. Koike, T., H. Yamagishi, Y. Hatanaka, A. Fukushima, J. W. Chang, Y. Xia, M. Fields, P. Chandler, and M. Iwashima. 2003. A novel ERK-dependent signaling process that regulates interleukin-2 expression in a late phase of T cell activation. J. Biol. Chem. 278: 15685-15692. (Pubitemid 36799679)
60. Tsukamoto, H., A. Irie, and Y. Nishimura. 2004. B-Raf contributes to sustained extracellular signal-regulated kinase activation associated with interleukin-2 production stimulated through the T cell receptor. J. Biol. Chem. 279: 48457-48465. (Pubitemid 39541004)
61. Qian, D. P., S. Lev, N. S. C. Vanoers, I. Dikic, J. Schlessinger, and A. Weiss. 1997. Tyrosine phosphorylation of Pyk2 is selectively regulated by fyn during TCR signaling. J. Exp. Med. 185: 1253-1259.
62. Ostergaard, H. L., and T. L. Lysechko. 2005. Focal adhesion kinase-related protein tyrosine kinase pyk2 in T-cell activation and function. Immunol. Res. 31: 267-282.
63. Griffiths, E. K., C. Krawczyk, Y. Y. Kong, M. Raab, S. J. Hyduk, D. Bouchard, V. S. Chan, I. Kozieradzki, A. J. Oliveira-Dos-Santos, A. Wakeham, et al. 2001. Positive regulation of T cell activation and integrin adhesion by the adapter Fyb/Slap. Science 293: 2260-2263.
64. Filipp, D., J. Zhang, B. L. Leung, A. Shaw, S. D. Levin, A. Veillette, and M. Julius. 2003. Regulation of fyn through translocation of activated lck into lipid rafts. J. Exp. Med. 197: 1221-1227. (Pubitemid 36570078)
65. Bunnell, S. C., V. Kapoor, R. P. Trible, W. Zhang, and L. E. Samelson. 2001. Dynamic actin polymerization drives T cell receptor-induced spreading: a role for the signal transduction adaptor LAT. Immunity 14: 315-329.
66. Barda-Saad, M., A. Braiman, R. Titerence, S. C. Bunnell, V. A. Barr, and L. E. Samelson. 2005. Dynamic molecular interactions linking the T cell antigen receptor to the actin cytoskeleton. Nat. Immunol. 6: 80-89. (Pubitemid 40136699)
67. Chung, C. Y., S. Funamoto, and R. A. Firtel. 2001. Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem Sci. 26: 557-566. (Pubitemid 32823441)
68. Rickert, P., O. D. Weiner, F. Wang, H. R. Bourne, and G. Servant. 2000. Leukocytes navigate by compass: roles of PI3Kγ and its lipid products. Trends Cell Biol. 10: 466-473. (Pubitemid 30767764)
69. Ward, S. G. 2004. Do phosphoinositide 3-kinases direct lymphocyte navigation? Trends Immunol. 25: 67-74.
70. Jones, N. P., J. Peak, S. Brader, S. A. Eccles, and M. Katan. 2005. PLCγ1 is essential for early events in integrin signalling required for cell motility. J. Cell Sci. 118: 2695-2706.
71. Seveau, S., R. J. Eddy, F. R. Maxfield, and L. M. Pierini. 2001. Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell. 12: 3550-3562. (Pubitemid 33108486)
72. Cannon, J. L., and J. K. Burkhardt. 2002. The regulation of actin remodeling during T-cell-APC conjugate formation. Immunol. Rev. 186: 90-99.
73. Sechi, A. S., and J. Wehland. 2004. Interplay between TCR signalling and actin cytoskeleton dynamics. Trends Immunol. 25: 257-265. (Pubitemid 38501672)
74. Haynes, B. F., M. J. Telen, L. P. Hale, and S. M. Denning. 1989. CD44-a molecule involved in leukocyte adherence and T-cell activation. Immunol. Today 10: 423-428.