Age-related changes in lck-Vav signaling pathways in mouse CD4 T cells

Cellular Immunology

Volumn 259, Issue 1, 2009, Pages 100-104

  Garcia, Gonzalo G ^a   Miller, Richard A ^a,b,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

Aging; Cellular activation; Cytoskeleton; Signal transduction; T lymphocytes; TCR signaling; Tyrosine kinases

Indexed keywords

CYTOSKELETON PROTEIN; EZRIN; GUANOSINE TRIPHOSPHATASE; MOESIN; PROTEIN KINASE LCK; RAC1 PROTEIN; TYROSINE DERIVATIVE; VAV PROTEIN;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME ACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

AGING; ANIMALS; ANTIGENS, CD3; CD4-POSITIVE T-LYMPHOCYTES; DNA-BINDING PROTEINS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MALE; MICE; NEUROPEPTIDES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-VAV; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

MUS;

EID: 68549094231     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2009.06.001     Document Type: Article

References (60)

1. Charrin S., and Alcover A. Role of ERM (ezrin-radixin-moesin) proteins in T lymphocyte polarization, immune synapse formation and in T cell receptor-mediated signaling. Front. Biosci. 11 (2006) 1987-1997
2. Huang Y., and Burkhardt J.K. T-cell-receptor-dependent actin regulatory mechanisms. J. Cell Sci. 120 (2007) 723-730
3. Krawczyk C., and Penninger J.M. Molecular motors involved in T cell receptor clusterings. J. Leukoc. Biol. 69 (2001) 317-330
4. Zamoyska R., Basson A., Filby A., Legname G., Lovatt M., and Seddon B. The influence of the src-family kinases, Lck and Fyn, on T cell differentiation, survival and activation. Immunol. Rev. 191 (2003) 107-118
5. Mustelin T., and Tasken K. Positive and negative regulation of T-cell activation through kinases and phosphatases. Biochem. J. 371 (2003) 15-27
6. Sefton B.M., and Taddie J.A. Role of tyrosine kinases in lymphocyte activation. Curr. Opin. Immunol. 6 (1994) 372-379
7. Roskoski Jr. R. Src protein-tyrosine kinase structure and regulation. Biochem. Biophys. Res. Commun. 324 (2004) 1155-1164
8. Eck M.J., Atwell S.K., Shoelson S.E., and Harrison S.C. Structure of the regulatory domains of the Src-family tyrosine kinase Lck. Nature 368 (1994) 764-769
9. Nika K., Tautz L., Arimura Y., Vang T., Williams S., and Mustelin T. A weak Lck tail bite is necessary for Lck function in T cell antigen receptor signaling. J. Biol. Chem. 282 (2007) 36000-36009
10. D'Oro U., Sakaguchi K., Appella E., and Ashwell J.D. Mutational analysis of Lck in CD45-negative T cells: dominant role of tyrosine 394 phosphorylation in kinase activity. Mol. Cell. Biol. 16 (1996) 4996-5003
11. Palacios E.H., and Weiss A. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene 23 (2004) 7990-8000
12. Fischer K.D., Tedford K., and Penninger J.M. Vav links antigen-receptor signaling to the actin cytoskeleton. Semin. Immunol. 10 (1998) 317-327
13. Hornstein I., Alcover A., and Katzav S. Vav proteins, masters of the world of cytoskeleton organization. Cell. Signal. 16 (2004) 1-11
14. Romero F., and Fischer S. Structure and function of vav. Cell. Signal. 8 (1996) 545-553
15. Tybulewicz V.L., Ardouin L., Prisco A., and Reynolds L.F. Vav1: a key signal transducer downstream of the TCR. Immunol. Rev. 192 (2003) 42-52
16. Miletic A.V., Sakata-Sogawa K., Hiroshima M., Hamann M.J., Gomez T.S., Ota N., Kloeppel T., Kanagawa O., Tokunaga M., Billadeau D.D., and Swat W. Vav1 acidic region tyrosine 174 is required for the formation of T cell receptor-induced microclusters and is essential in T cell development and activation. J. Biol. Chem. 281 (2006) 38257-38265
17. Kuhne M.R., Ku G., and Weiss A. A guanine nucleotide exchange factor-independent function of Vav1 in transcriptional activation. J. Biol. Chem. 275 (2000) 2185-2190
18. Amarasinghe G.K., and Rosen M.K. Acidic region tyrosines provide access points for allosteric activation of the autoinhibited Vav1 Dbl homology domain. Biochemistry 44 (2005) 15257-15268
19. Allenspach E.J., Cullinan P., Tong J., Tang Q., Tesciuba A.G., Cannon J.L., Takahashi S.M., Morgan R., Burkhardt J.K., and Sperling A.I. ERM-dependent movement of CD43 defines a novel protein complex distal to the immunological synapse. Immunity 15 (2001) 739-750
20. Shaw A.S. FERMing up the synapse. Immunity 15 (2001) 683-686
21. Niggli V., and Rossy J. Ezrin/radixin/moesin: versatile controllers of signaling molecules and of the cortical cytoskeleton. Int. J. Biochem. Cell Biol. 40 (2008) 344-349
22. Yonemura S., Matsui T., Tsukita S., and Tsukita S. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115 (2002) 2569-2580
23. Miletic A.V., Swat M., Fujikawa K., and Swat W. Cytoskeletal remodeling in lymphocyte activation. Curr. Opin. Immunol. 15 (2003) 261-268
24. Turner M., and Billadeau D.D. VAV proteins as signal integrators for multi-subunit immune-recognition receptors. Nat. Rev. Immunol. 2 (2002) 476-486
25. Bustelo X.R. Regulation of Vav proteins by intramolecular events. Front. Biosci. 7 (2002) d24-d30
26. Garcia G.G., and Miller R.A. Age-related defects in CD4+ T cell activation reversed by glycoprotein endopeptidase. Eur. J. Immunol. 33 (2003) 3464-3472
27. Garcia G.G., and Miller R.A. Age-dependent defects in TCR-triggered cytoskeletal rearrangement in CD4+ T cells. J. Immunol. 169 (2002) 5021-5027
28. Garcia G.G., and Miller R.A. Single-cell analyses reveal two defects in peptide-specific activation of naive T cells from aged mice. J. Immunol. 166 (2001) 3151-3157
29. Tamir A., Eisenbraun M.D., Garcia G.G., and Miller R.A. Age-dependent alterations in the assembly of signal transduction complexes at the site of T cell/APC interaction. J. Immunol. 165 (2000) 1243-1251
30. Garcia G.G., Sadighi Akha A.A., and Miller R.A. Age-related defects in moesin/ezrin cytoskeletal signals in mouse CD4 T cells. J. Immunol. 179 (2007) 6403-6409
31. Garcia G.G., and Miller R.A. Increased Zap-70 association with CD3zeta in CD4 T cells from old mice. Cell. Immunol. 190 (1998) 91-100
32. Garcia G.G., and Miller R.A. Differential tyrosine phosphorylation of zeta chain dimers in mouse CD4 T lymphocytes: effect of age. Cell. Immunol. 175 (1997) 51-57
33. Han J., Das B., Wei W., Van A.L., Mosteller R.D., Khosravi-Far R., Westwick J.K., Der C.J., and Broek D. Lck regulates Vav activation of members of the Rho family of GTPases. Mol. Cell. Biol. 17 (1997) 1346-1353
34. Tybulewicz V.L. Vav-family proteins in T-cell signalling. Curr. Opin. Immunol. 17 (2005) 267-274
35. van Leeuwen J.E., and Samelson L.E. T cell antigen-receptor signal transduction. Curr. Opin. Immunol. 11 (1999) 242-248
36. D.J. Morre, D.M. Morre, Preparation of mammalian plasma membranes by aqueous two-phase partition, Biotechniques 7 (1989) 946-8, 950-4, 956-8.
37. Mangeat P., Roy C., and Martin M. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9 (1999) 187-192
38. Bretscher A. Regulation of cortical structure by the ezrin-radixin-moesin protein family. Curr. Opin. Cell Biol. 11 (1999) 109-116
39. Bretscher A., Chambers D., Nguyen R., and Reczek D. ERM-Merlin and EBP50 protein families in plasma membrane organization and function. Annu. Rev. Cell Dev. Biol. 16 (2000) 113-143
40. Bretscher A., Edwards K., and Fehon R.G. ERM proteins and merlin: integrators at the cell cortex. Nat. Rev. Mol. Cell Biol. 3 (2002) 586-599
41. Engen J.R., Wales T.E., Hochrein J.M., Meyn III M.A., Banu O.S., Bahar I., and Smithgall T.E. Structure and dynamic regulation of Src-family kinases. Cell. Mol. Life Sci. 65 (2008) 3058-3073
42. Salojin K.V., Zhang J., and Delovitch T.L. TCR and CD28 are coupled via ZAP-70 to the activation of the Vav/Rac-1-/PAK-1/p38 MAPK signaling pathway. J. Immunol. 163 (1999) 844-853
43. Larbi A., Dupuis G., Khalil A., Douziech N., Fortin C., and Fulop Jr. T. Differential role of lipid rafts in the functions of CD4+ and CD8+ human T lymphocytes with aging. Cell. Signal. 18 (2006) 1017-1030
44. Fulop Jr. T., Gagne D., Goulet A.C., Desgeorges S., Lacombe G., Arcand M., and Dupuis G. Age-related impairment of p56lck and ZAP-70 activities in human T lymphocytes activated through the TcR/CD3 complex. Exp. Gerontol. 34 (1999) 197-216
45. Guidi L., Antico L., Bartoloni C., Costanzo M., Errani A., Tricerri A., Vangeli M., Doria G., Gatta L., Goso C., Mancino L., and Frasca D. Changes in the amount and level of phosphorylation of p56(lck) in PBL from aging humans. Mech. Ageing Dev. 102 (1998) 177-186
46. Tinkle C.W., Lipschitz D., and Ponnappan U. Decreased association of p56lck with CD4 may account for lowered tyrosine kinase activity in mitogen-activated human T lymphocytes during aging. Cell. Immunol. 186 (1998) 154-160
47. Whisler R.L., Bagenstose S.E., Newhouse Y.G., and Carle K.W. Expression and catalytic activities of protein tyrosine kinases (PTKs) Fyn and Lck in peripheral blood T cells from elderly humans stimulated through the T cell receptor (TCR)/CD3 complex. Mech. Ageing Dev. 98 (1997) 57-73
48. Larbi A., Dupuis G., Douziech N., Khalil A., and Fulop Jr. T. Low-grade inflammation with aging has consequences for T-lymphocyte signaling. Ann. NY Acad. Sci. 1030 (2004) 125-133
49. Larbi A., Douziech N., Khalil A., Dupuis G., Gherairi S., Guerard K.P., and Fulop Jr. T. Effects of methyl-beta-cyclodextrin on T lymphocytes lipid rafts with aging. Exp. Gerontol. 39 (2004) 551-558
50. Larbi A., Douziech N., Dupuis G., Khalil A., Pelletier H., Guerard K.P., and Fulop Jr. T. Age-associated alterations in the recruitment of signal-transduction proteins to lipid rafts in human T lymphocytes. J. Leukoc. Biol. 75 (2004) 373-381
51. Fulop Jr. T., Douziech N., Goulet A.C., Desgeorges S., Linteau A., Lacombe G., and Dupuis G. Cyclodextrin modulation of T lymphocyte signal transduction with aging. Mech. Ageing Dev. 122 (2001) 1413-1430
52. Whisler R.L., Chen M., Liu B., and Newhouse Y.G. Age-related impairments in TCR/CD3 activation of ZAP-70 are associated with reduced tyrosine phosphorylations of zeta-chains and p59fyn/p56lck in human T cells. Mech. Ageing Dev. 111 (1999) 49-66
53. Dornan S., Sebestyen Z., Gamble J., Nagy P., Bodnar A., Alldridge L., Doe S., Holmes N., Goff L.K., Beverley P., Szollosi J., and Alexander D.R. Differential association of CD45 isoforms with CD4 and CD8 regulates the actions of specific pools of p56lck tyrosine kinase in T cell antigen receptor signal transduction. J. Biol. Chem. 277 (2002) 1912-1918
54. Biffen M., Michael-Phillips D., Larson T., Venkitaraman A., and Alexander D. The CD45 tyrosine phosphatase regulates specific pools of antigen receptor-associated p59fyn and CD4-associated p56lck tyrosine in human T-cells. EMBO J. 13 (1994) 1920-1929
55. Garcia G.G., Berger S.B., Sadighi Akha A.A., and Miller R.A. Age-associated changes in glycosylation of CD43 and CD45 on mouse CD4 T cells. Eur. J. Immunol. 35 (2005) 622-631
56. Hardwick J.S., and Sefton B.M. Activation of the Lck tyrosine protein kinase by hydrogen peroxide requires the phosphorylation of Tyr-394. Proc. Natl. Acad. Sci. USA 92 (1995) 4527-4531
57. Hardwick J.S., and Sefton B.M. 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 (1997) 25429-25432
58. Nakamura K., Sasada T., Sono H., and Yodoi J. Inhibition of protein kinase C-mediated CD4 down-regulation by oxidative stress in T lymphocytes. J. Immunol. 157 (1996) 5339-5349
59. Nakamura K., Hori T., and Yodoi J. Alternative binding of p56lck and phosphatidylinositol 3-kinase in T cells by sulfhydryl oxidation: implication of aberrant signaling due to oxidative stress in T lymphocytes. Mol. Immunol. 33 (1996) 855-865
60. Nakamura K., Hori T., Sato N., Sugie K., Kawakami T., and Yodoi J. Redox regulation of a src family protein tyrosine kinase p56lck in T cells. Oncogene 8 (1993) 3133-3139