Specific subdomains of Vav differentially affect T cell and NK cell activation

Journal of Immunology

Volumn 164, Issue 8, 2000, Pages 3971-3981

  Billadeau, Daniel D ^a   Mackie, Stacy M ^a   Schoon, Renee A ^a   Leibson, Paul J ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM; INTERLEUKIN 2; IONOMYCIN; MUTANT PROTEIN; ONCOPROTEIN; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG; VAV PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE ACTIVATION; GENE FUNCTION; HUMAN; HUMAN CELL; LEUKOCYTE ACTIVATION; LYMPHOCYTOTOXICITY; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTO ONCOGENE; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION REGULATION;

EID: 0034655104     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.8.3971     Document Type: Article

References (76)

1. Cantrell, D. 1996. T cell antigen receptor signal transduction pathways. Annu. Rev. Immunol. 14:259.
2. Trinchieri, G. 1989. Biology of natural killer cells. Adv. Immunol. 47:187.
3. Alberola-Ila, J., S. Takaki, J. D. Kerner, and R. M. Perlmutter. 1997. Differential signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 15:25.
4. Daeron, M. 1997. Fc receptor biology. Annu. Rev. Immunol. 15:203.
5. Holsinger, L. J., D. M. Spencer, D. J. Austin, S. L. Schreiber, and G. R. Crabtree. 1995. Signal transduction in T lymphocytes using a conditional allele of Sos. Proc. Natl. Acad. Sci. USA 92:9810.
6. Wu, J., S. Katzav, and A. Weiss. 1995. A functional T-cell receptor signaling pathway is required for p95vav activity. Mol. Cell. Biol. 15:4337.
7. Billadeau, D. D., K. M. Brumbaugh, C. J. Dick, R. A. Schoon, X. R. Bustelo, and P. J. Leibson. 1998. The Vav-Rac1 pathway in cytotoxic lymphocytes regulates the generation of cell-mediated killing. J Exp. Med. 188:549.
8. Katzav, S., D. Martin-Zanca, and M. Barbacid. 1989. vav, a novel human oncogene from a locus ubiquitously expressed in hematopoietic cells. EMBO J. 8:2283.
9. Bustelo, X. R., J. A. Ledbetter, and M. Barbacid. 1992. Product of vav proto-oncogene defines a new class of tyrosine protein kinase substrates. Nature 356:68.
10. Margolis, B., P. Hu, S. Katzav, W. Li, J.M. Oliver, A. Ullrich, A. Weiss, and J. Schlessinger. 1992. Tyrosine phosphorylation of vav proto-oncogene product containing SH2 domain and transcription factor motifs. Nature 356:71.
11. Darby, C., R. L. Geahlen, and A. D. Schreiber. 1994. Stimulation of macrophage FcγRIIIA activates the receptor-associated protein tyrosine kinase Syk and induces phosphorylation of multiple proteins including p95Vav and p62/GAP-associated protein. J. Immunol. 152:5429.
12. Xu, X., and S.-F. Chong. 1996. Vav in natural killer cells is tyrosine phosphorylated upon cross-linking of FcγRIIIA and is constitutively associated with a serine/threonine kinase. Biochem. J. 318:527.
13. + thymocytes. Nature 374:474.
14. Tarakhovsky, A., M. Turner, S. Schaal, P. J. Mee, L. P. Duddy, K. Rajewsky, and V. J. L. Tybulewicz. 1995. Defective antigen receptor-mediated proliferation of B and T cells in the absence of Vav. Nature 374:467.
15. Zhang, R., F. W. Alt, L. Davidson, S. H. Orkin, and W. Swat. 1995. Defective signalling through the T-and B-cell antigen receptors in lymphoid cell lacking the vav proto-oncogene. Nature 374:470.
16. Turner, M., P. J. Mee, A. E. Walters, M. E. Quinn, A. L. Mellor, R. Zamoyska., and V. J. L. Tybulewicz. 1997. A requirement for the Rho-family GTP exchange factor Vav in positive and negative selection of thymocytes. Immunity 7:451.
17. Fischer, K.-D., Y.-Y. Kong, H. Nishina, K. Tedford, L. E. M. Marengere, I. Kozieradzki, T. Sasaki, M. Starr, G. Chan, S. Gardener, et al. 1998. Vav is a regulator of TCR-mediated cytoskeleton reorganization required for proliferation, interleukin 2 production, and T cell maturation. Curr. Biol. 8:554.
18. Holsinger, L. J., I. A. Graef, W. Swat, T. Chi, D. M. Baustista, L. Davidson, R. S. Lewis, F. W. Alt, and G. R. Crabtree. 1998. Defects in actin-cap formation in Vav-deficient mice implicate an actin requirement for lymphocyte signal transduction. Curr. Biol. 8:563.
19. Kong, Y.-Y., K.-D. Fischer, M. F. Bachmann, S. Mariathasan, I. Kozieradzki, M. P. Nghiem, D. Bouchard, A. Berstein, P. S. Ohashi, and J. M. Penninger. 1998. Vav regulates peptide-specific apoptosis in thymocytes. J. Exp. Med. 188:2099.
20. Costello, P. S., A. E. Walters, P. J. Mee, M. Turner, L. F. Reynolds, A. Prisco, N. Sarner, R. Zamoyska, and V. J. L. Tybulewicz. 1999. The Rho-family GTP exchange factor Vav is a critical transducer of T cell receptor signals to the calcium, ERK, and NF-κB pathways. Proc. Natl. Acad. Sci. USA 96:3035.
21. Olson, M. F., N. G. Pasteris, J. L. Gorski, and A. Hall. 1996. Faciogenital dysplasia protein (FGD1) and Vav, two related proteins required for normal embryonic development, are upstream regulators of Rho GTPases. Curr. Biol. 6:1628.
22. Crespo, P., K. E. Schuebel, A. A. Ostrom, S. J. Gutkind, and X. R. Bustelo, 1997. Phosphotyrosine-dependent activation of Rac-1 GDP/GTP exchange by vav proto-oncogene product. Nature 385:169.
23. Man, J., B. Das, W. Wei, L. Van Aelst, R. D. Mosteller, R. Khosravi-Far, J. K. Westwick, C. J. Der, and D. Brock. 1997. Lck regulates Vav activation of members of the Rho family of GTPases. Mol. Cell. Biol. 17:1346.
24. Adams, J. M., H. Houston, J. Allen, T. Lints, and R. Harvey. 1992. The hematopoietically expressed vav proto-oncogene shares homology with the dbl GDP-GTP exchange factor, the bcr gene and a yeast gene (CDC24) involved in cytoskeletal organization. Oncogene 7:611.
25. Hart, M. J., A. Eva, D. Zangrill, S. A. Aaronson, T. Evans, R. A. Cerione, and Y. Zheng. 1994. Cellular transformation and guanine nucleotide exchange activity are catalyzed by a common domain on the dbl oncogene product. J. Biol. Chem. 269:62.
26. Katzav, S. 1995. Vav: Captain Hook for signal transduction? Crit. Rev. Oncog. 6:87.
27. Bustelo, X. R. 1996. The Vav family of signal transduction molecules. Crit. Rev. Oncog. 7:65.
28. Katzav, S. 1993. Single point mutations in the SH2 domain impair the transforming potential of vav and fail to activate proto-vav. Oncogene 8:1757.
29. Wu, J., D. G. Motto, G. A. Koretzky, and A. Weiss. 1996. Vav and SLP-76 interact and functionally cooperate in IL-2 gene activation. Immunity 4:593.
30. Katzav, S., J. L. Cleveland, H. E. Helsop, and D. Pulido. 1991. Loss of the amino-terminal helix-loop-helix domain of the vav proto-oncogene activates its transforming potential. Mol. Cell. Biol. 11:1912.
31. Castresana, J., and M. Saraste. 1995. Does Vav bind to F-actin through a CH domain? FEBS Lett. 374:149.
32. Han, J., K. Luby-Phelps, K. Das, X. Shu, Y. Xia, R. D. Mosteller, U. M. Krishna, J. R. Falck, M. A. White, and D. Brock. 1998. Role of substrates and products of PI3-kinase in regulating activation of rac-related guanosine triphospriates by Vav. Science 279:558.
33. Ma, A. D., A. Metjian, S. Bagrodia, S. Taylor, and C. S. Abrams. 1998. Cytoskeletal reorganization by G protein-coupled receptors is dependent on phosphoinositide 3-kinase γ, a rac guanosine exchange factor, and Rac. Mol. Cell. Biol. 18:4744.
34. Windehank, K. P., R. T. Abraham, G. Powis, R. A. Olsen, T. J. Barna, and P. J. Leibson. 1988. Signal transduction during human natural killer cell activation: inositol phosphate generation and regulation by cyclic AMP. J. Immunol. 141:3951.
35. Perussia, B., and G. Trinchieri. 1984. Antibody 3G8, specific for the human neutrophil Fc receptor, reacts with natural killer cells. J. Immunol. 132:1410.
36. Ting, A. T., C. J. Dick, R. A. Schoon, L. M. Karnitz, R. T. Abraham, and P. J. Leibson, 1995. Interaction between lck and syk family tyrosine kinases in Fcγ receptor-initiated activation of natural killer cells. J. Biol. Chem. 270:16415.
37. Manser, E., T. H. Loo, C.-G. Koh, Z.-S. Zhao, X.-Q. Chen, L. Tan, I. Tan, T. Leung, and L. Lim. 1998. PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1:183.
38. Billadeau, D., D. F. Jelinek, N. Shah, T. W. LeBien, and B. Van Ness. 1995. Introduction of an activated N-ras oncogene alters the growth characteristics of the interleukin-6-dependent myeloma cell line ANBL6. Can. Res. 55:3640.
39. Hedin, K. E., M. P. Bell, K. R. Kalli, C. J. Huntoon, B. M. Sharp, and D. J. McKean. 1997. δ-Opioid receptors expressed by Jurkal T cells enhance IL-2 secretion by increasing AP-1 complexes and activity of the NF-AT/AP-1-binding promoter element. J. Immunol. 159:5431.
40. Pross, H. F., M. G. Baines, P. Rubin, P. Shragge, and M. S. Patterson. 1981. Spontaneous human lymphocyte-mediated cytotoxicity against tumor target cells. IX. The quantitation of natural killer cell activity. J. Clin. Immunol. 1:51.
41. Leibson, P. J., D. E. Midthun, K. P. Windebank, and R. T. Abraham. 1990. Transmembrane signaling during natural killer cell-mediated cytotoxicity: regulation by protein kinase C activation. J. Immunol. 145:1498.
42. Stradal, T., W. Kranewitter, S. J. Winder, and M. Gimona. 1998. CH domains revisited. FEBS Lett. 431:134.
43. Deckert, M., S. Tartare-Deckert, C. Couture, T. Mustelin, and A. Altmon. 1996. Functional and physical interactions of Syk family kinases with the Vav proto-oncogene product. Immunity 5:591.
44. Loh, C., K. T.-Y. Shaw, J. Carew, J. P. B. Viola, C. Luo, B. A. Perrino, and A. Rao. 1996. Calcineurin binds the transcription factor NFAT1 and reversibly regulates its activity. J. Biol. Chem. 271:10884.
45. Loh, C., J. A. Carew, J. Kim, P. J. Hogan, and A. Rao. 1996. T-cell receptor stimulation elicits an early phase of activation and a later phase of deactivation of the transcription factor NFAT1. Mol. Cell. Biol. 16:3945.
46. Rao, A., C. Luo, and P. Hogan. 1997. Transcription factors of the NFAT family: regulation and function. Annu. Rev. Immunol. 15:707.
47. 2+, calcineurin and NF-AT Cell 96:611.
48. Argov, S., A. Poros, and E. Klein. 1979. Cation requirement of natural, in-vitro generated and antibody dependent killing exerted by human lymphocytes. Immunobiology 156:25.
49. Clipstone, N. A., and G. R. Crabtree. 1992. Identification of calcineurin as a key signalling enzyme in T-lymphocylc activation. Nature 357:695.
50. Jain, J., P. G. McCaffrey, Z. Miner, T. K. Kerppola, J. N. Lambert, G. L. Verdine, T. Curran, and A. Rao. 1993. The T-cell transcription factor NFATp is a substrate for calcineurin and interacts with Fos and Jun. Nature 365:352.
51. Ruff, V. A., and K. L. Leach. 1995. Direct demonstration of NFATp dephosphorylation and nuclear localization in activated HT-2 cells using a specific NFATp polyclonal antibody. J. Biol. Chem. 270:22602.
52. Shibasaki, F., E. R. Price, D. Milan, and F. McKeon. 1996. Role of kinases and the phosphatase calcineurin in the nuclear shuttling of transcription factor NFAT. Nature 382:370.
53. Beak, C. R., N. A. Clipstone, S. N. Ho, and G. R. Crabtree. 1997. Nuclear localization of NF-ATc by a calcineurin-dependent, cyclosporin A-sensitive intramolecular interaction. Genes Dev. 11:824.
54. ras and calcineurin synergize to regulate the nuclear factor of activated T cells. J. Exp. Med. 178:1517.
55. Genot, E. M., P. J. Parker, and D. A. Cantrell. 1995. Analysis of the role of protein kinase Cα -∈, and ζ in T cell activation. J. Biol. Chem. 270:9833.
56. ras effector pathways regulate nuclear factor of activated T cells. EMBO J. 15:3923.
57. Turner, H., M. Gomez, E. McKenzie, A. Kirchem, A. Lennard, and D. A. Cantrell. 1998. Rac-1 regulates nuclear factor of activated T cells (NFAT) C1 nuclear translocation in response to Fc∈ receptor type I stimulation of Mast cells. J. Exp. Med. 188:527.
58. Fang, N., and G. A. Koretzky. 1999. SLP-76 and Vav function in separate, but overlapping pathways to augment interleukin-2 promoter activity. J. Biol. Chem. 274:16206.
59. Avots, A., M. Buttman, S. Chuvpilo, C. Escher, U. Smola, A. J. Bannister, U. R. Rapp, T. Kouzarides, and E. Serfling. 1999. CBP/p300 integrates Raf/Rac-signaling pathways in the transcriptional induction of NF-ATc during T cell activation. Immunity 10:515.
60. Gimona, M., and R. Mital. 1998. The single CH domain of calponin is neither sufficient nor necessary for F-actin binding. J. Cell Sci. 111:1813.
61. Fukami, K., N. Sawada, T. Endo, and T. Takenawa. 1996. Identification of a phosphatidylinositol 4.5-bisphosphate-binding site in chicken skeletal muscle a-actinin. J. Biol. Chem. 271:2646.
62. Chong, L. D., A. Traynor-Kaplan, G. M. Bokoch, and M. A. Schwartz. 1994. The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79:507.
63. Hartwig, J. H., G. M. Bokoch, C. L. Carpenter, P. A. Janmey, L. A. Taylor, A. Toker, and T. P. Stossel. 1995. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82:643.
64. Tolias, K. F., L. C. Cantley, and C. L. Carpenter. 1995. Rho family GTPases bind to phosphoinositide kinases. J. Biol. Chem. 270:17656.
65. Ren, X. D., G. M. Bokoch, A. Traynor-Kaplan, G. H. Jenkins, R. A. Anderson, and M. A. Schwartz. 1996. Physical association of the small GTPase Rho with a 68-kDa phosphatidylinositol 4-phosphate 5-kinase in Swiss 3T3 cells. Mol. Cell. Biol. 7:435.
66. O'Rourke, L. M., R. Tooze, M. Turner, D. M. Sandoval, R. H. Carter, V. J. L. Tybulewicz, and D. T. Fearon. 1998. CD19 as a membrane-anchored adaptor protein of B lymphocytes: costimulation of lipid and protein kinases by recruitment of Vav. Immunity 8:635.
67. Moon, T. D., J. E. Morley, R. L. Vessella, and P. H. Lange. 1983. The role of calmodulin in human natural killer cell activity. Scand. J. Immunol. 18:255.
68. Ng, J., B. B. Fredholm, and M. Jondal. 1987. Studies on the calcium dependence of human NK cell killing. Biochem. Pharmacol. 36:3943.
69. 2+ of human NK cells. J. Immunol. 143:1058.
70. Richards, A. L., and J. Y. Djeu. 1990. Calcium-dependent natural killer and calcium-independent natural cytotoxic activities in an IL-2-dependent cell line. J. Immunol. 145:3144.
71. Zhang, W., J. Sloan-Lancaster, J. Kitchen, R. P. Trible, and L. E. Samelson. 1998. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92:83.
72. Jevremovic, D., D. D. Billadeau, R. A. Schoon, C. J. Dick, B. J. Irvin, W. Zhang, L. E. Samelson, R. T. Abraham, and P. J. Leibson. 1999. A role for the adaptor protein LAT in human NK cell-mediated cytotoxicity. J. Immunol. 162:2453.
73. Trotta, R., K. A. Puorro, M. Paroli, L. Azzoni, B. Abebe, L. C. Eisenlohr, and B. Perussia. 1998. Dependence of both spontaneous and antibody-dependent, granule exocytosis-mediated NK cell cytotoxicity on extracellular-regulated kinases. J. Immunol. 161:6648.
74. Wei, S., A. M. Gamero, J. H. Liu, A. A. Daulton, N. I. Valkov, J. A. Trapani, A. C. Larner, M. J. Weber, and J. Y. Djeu. 1998. Control of lytic function by mitogen-activated protein kinase/extracellular regulatory kinase 2 (ERK2) in a human natural killer cell line: identitication of perform and granzyme B mobilization by functional ERK2. J. Exp. Med. 187:1753.
75. Yablonski, D., L. P. Kane, D. Qian, and A. Weiss. 1998. A Nck-Pak1 signaling module is required for T-cell receptor-mediated activation of NFAT, but not of JNK. EMBO J. 17:5647.
76. Bonnema, J. D., L. M. Karnitz, R. A. Schoon, R. T. Abraham, and P. J. Leibson. 1994. Fc receptor stimulation of phosphatidylinositol 3-kinase in natural killer cells is associated with protein kinase C-independent granule release and cell-mediated cytotoxicity. J. Exp. Med. 180:1427.