Knockouts of Src-family kinases: Stiff bones, wimpy T cells, and bad memories

Genes and Development

Volumn 10, Issue 15, 1996, Pages 1845-1857

  Lowell, Clifford A ^a   Soriano, Philippe ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PROTEIN KINASE P60;

BONE DEVELOPMENT; CELL DIFFERENTIATION; ENZYME REGULATION; GENE EXPRESSION; HUMAN; LYMPHOID TISSUE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; ONCOGENE SRC; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION;

EID: 0029786988     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.10.15.1845     Document Type: Review

References (121)

1. lck. J. Exp. Med. 173: 1421-1432.
2. Achen, M.G., M. Clauss, H. Schnurch, and W. Risau. 1995. The non-receptor tyrosine kinase Lyn is localised in the developing murine blood-brain barrier. Differentiation 59: 15-24.
3. Anderson, S.J. and R.M. Perlmutter. 1995. A signaling pathway governing early thymocyte maturation. Immunol. Today 16: 99-105.
4. lck controls allelic exclusion of T-cell receptor β-chain genes. Nature 365: 552-554.
5. Anderson, S.M. and B. Jorgensen. 1995. Activation of Src-related tyrosine kinases by IL-3. J. Immunol. 155: 1660-1670.
6. fyn. Cell 70: 751-763.
7. fyn T in interleukin-5 receptor signaling. J. Exp. Med. 182: 811-820.
8. lck tyrosine kinase and activates the phosphatase. Mol. Cell. Biol. 14: 1308-1321.
9. Barone, M.V. and S.A. Courtneidge. 1995. Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src. Nature 378: 509-512.
10. Beggs, H., P. Soriano, and P. Maness. 1994. NCAM-dependent neurite outgrowth is inhibited in neurons from fyn-minus mice. J. Cell Biol. 127: 825-833.
11. lck at Tyr-505 and down regulates its catalytic activity. EMBO J. 11:2919-2924.
12. Berton, G., L. Fumagalli, C. Laudanna, and C. Sorio. 1994. β2 integrin-dependent protein tyrosine phosphorylation and activation of the FGR protein tyrosine kinase in human neutrophils. J. Cell. Biol. 126: 1111-1121.
13. Bolen, J.B. 1995. Protein tyrosine kinases in the initiation of antigen receptor signaling. Curr. Opin. Immunol. 7: 306-311.
14. c-src expression for osteoclasts to form ruffled borders and to resorb bone in mice. J. Clin. Invest. 90: 1622-1627.
15. Brown, M.T. and J.A. Cooper. 1996. Regulation, substrates, and functions of Src. Biochem. Biophys. Acta Rev. Cancer (in press].
16. Burden-Gulley, S., H. Payne, and V. Lemmon. 1995. Growth cones are actively influenced by substrate-bound adhesion molecules. J. Neurosci. 15: 4370-4381.
17. Calautti, E., C. Missero, P.L. Stein, R.M. Ezzell, and G.P. Dotto. 1995. Fyn tyrosine kinase is involved in keratinocyte differentiation control. Genes & Dev, 9: 2279-2291.
18. Cance, W., R. Craven, M. Bergman, L. Xu, K. Alitalo, and E. Liu. 1994. Rak, a novel nuclear tyrosine kinase expressed in epithelial cells. Cell Growth Differ. 5: 1347-1355.
19. c-src expression in the developing rat brain. Proc. Natl. Acad. Sci. 85:3348-3352.
20. c-fyn is capable of complex formation with the middle-T antigen of polyoma virus. EMBO J. 7: 3845-3855.
21. Chow, L.M., C. Jarvis, Q. Hu, S.H. Nye, F.G. Gervais, A. Veillette, and L.A. Matis. 1994. Ntk: A Csk-related protein-tyrosine kinase expressed in brain and T lymphocytes. Proc. Natl. Acad. Sci. 91: 4975-4979.
22. Clark, E.A. and J.S. Brugge. 1995. Integrins and signal transduction pathways: The road taken. Science 268: 233-239.
23. FAK. Mol. Cell. Biol. 14: 147-155.
24. Cooke, M.P. and R.M. Perlmutter. 1989. Expression of a novel form of the fyn proto-oncogene in hematopoietic cells. New Biol. 1: 66-74.
25. Corey, S., A. Eguinoa, K. Puyana-Theall, J.B. Bolen, L. Cantley, F. Mollinedo, T.R. Jackson, P.T. Hawkins, and L.R. Stephens. 1993. Granulocyte macrophage-colony stimulating factor stimulates both association and activation of phosphoinositide 3OH-kinase and Src-related tyrosine kinase(s) in human myeloid derived cells. EMBO J. 12: 2681-2690.
26. Corey, S.J., A.L. Burkhardt, J.B. Bolen, R.L. Geahlen, L.S. Tkatch, and D.J. Tweardy. 1994. Granulocyte colony-stimulating factor receptor signaling involves the formation of a three-component complex with Lyn and Syk protein-tyrosine kinases. Proc. Natl. Acad. Sci. 91: 4683-4687.
27. Courtneidge, S.A. and A.E. Smith. 1983. Polyoma virus transforming protein associates with the product of the c-src gene. Nature 303: 435-439.
28. Courtneidge, S.A., R. Dhand, D. Pilat, G.M. Twamley, M.D. Waterfield, and M.F. Roussel. 1993. Activation of Src-family kinases by colony stimulating factor-1, and their association with its receptor. EMBO J. 12: 943-950.
29. Dixon, J.E. 1995. Structure and catalytic properties of protein tyrosine phosphatases. Ann. N.Y. Acad. Sci. 766: 18-22.
30. Eiseman, E. and J.B. Bolen. 1992. Engagement of the high-affinity IgE receptor activates src protein-related tyrosine kinases. Nature 355: 78-80.
31. Erpel, T. and S.A. Courtneidge. 1995. Src family protein tyrosine kinases and cellular signal transduction pathways. Curr. Opin. Cell. Biol. 7: 176-182.
32. Filvaroff, E., D.F. Stern, and G.P. Dotto. 1990. Tyrosine phosphorylation is an early and specific event involved in primary keratinocyte differentiation. Mol. Cell. Biol. 10: 1164-1173.
33. Gluecksohn-Schoenheimer, S. 1944, The development of normal and homozygous Brachyury (T/ T) mouse embryos in the extraembryonic coelom of the chick. Proc. Natl. Acad. Sci. 30: 134-140.
34. Grant, S.G., T.J. O'Dell, K.A. Karl, P.L. Stein, P. Soriano, and E.R. Kandel. 1992. Impaired long-term potentiation, spatial learning, and hippocampal development in Fyn mutant mice. Science 258: 1903-1910.
35. Grant, S.G., K.A. Karl, M.A. Kiebler, and E.R. Kandel. 1995. Focal adhesion kinase in the brain: Novel subcellular localization and specific regulation by Fyn tyrosine kinase in mutant mice. Genes & Dev. 9: 1909-1921.
36. Green, M.C. 1989. Catalog of mutant genes and polymorphic loci. In Genetic variants and strain of the laboratory mouse (ed. M.F. Lyon and A.G. Searle), pp. 12-403. Oxford University Press, Oxford, UK.
37. 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.
38. Guy, C.T., R.D. Cardiff, and W.J. Muller. 1992. Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12: 954-961.
39. Guy, C.T., S.K. Muthuswamy, R.D. Cardiff, P. Soriano, and W.J. Muller. 1994. Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice. Genes & Dev. 8: 23-32.
40. Hamada, F., M. Aoki, T. Akiyama, and K. Toyoshima. 1993. Association of immunoglobulin G Fc receptor II with Src-like protein-tyrosine kinase Fgr in neutrophils. Proc. Natl. Acad. Sci. 90: 6305-6309.
41. Hemesath, T., E. Steingrimsson, G. McGill, M. Hansen, J. Vaught, C. Hodgkinson, H. Arnheiter, N. Copeland, N. Jenkins, and D. Fisher. 1994. Microphthalmia, a critical factor in melanocyte development, defines a discrete transcription factor family. Genes & Dev. 8: 2770-2780.
42. Hennings, H., D. Michael, C. Cheng, P. Steinen, K. Holbrook, and S.H. Yuspa. 1990. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 19: 245-254.
43. Hibbs, M.L., D.M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S.A. Stacker, and A.R. Dunn. 1995. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83: 301-311.
44. c-src in association with intracellular membranes. J. Cell. Biol. 119: 1003-1013.
45. Howell, B.W. and J.A. Cooper. 1994. Csk suppression of Src involves movement of Csk to sites of Src activity. Mol. Cell. Biol. 14: 5402-5411.
46. Hunter, S., M.M. Huang, Z.K. Indik, and A.D. Schreiber. 1993. FcγRIIA-mediated phagocytosis and receptor phosphorylation in cells deficient in the protein tyrosine kinase Src. Exp. Hematol. 21: 1492-1497.
47. Ignelzi, M.A., D.R. Miller, P. Soriano, and P.P. Maness. 1994. Impaired neurite outgrowth of Src-minus neurons on the cell adhesion molecule LI. Neuron 12: 873-884.
48. Ilic, D., Y. Furuta, S. Kanazawa, N. Takeda, K. Sobue, N. Nakatsuji, S. Nomura, J. Fujimoto, M. Okada, T. Yamamoto, and S. Aizawa. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377: 539-544.
49. Imamoto, A. and P. Soriano. 1993. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell 73: 1117-1124.
50. Johnson, R.S., B.M. Spiegelman, and V. Papaioannou. 1992. Pleiotropic effects of a null mutation in the c-fos proto- oncogene. Cell 71: 577-586.
51. + thymocytes. Blood 87: 865-870.
52. c-src with endosomal membranes in mammalian fibroblasts. J. Cell. Biol. 118: 321-333.
53. Kaplan, K.B., K.B. Bibbins, J.R. Swedlow, M. Arnaud, D.O. Morgan, and H.E. Varmus. 1994. Association of the amino-terminal half of c-Src with focal adhesions alters their properties and is regulated by phosphorylation of tyrosine 527. EMBO J. 13: 4745-4756.
54. Kaplan, K.B., J.R. Swedlow, D.O. Morgan, and H.E. Varmus. 1995. c-Src enhances the spreading of src fibroblasts on fibronectin by a kinase-independent mechanism. Genes & Dev. 9: 1505-1517.
55. Kiefer, F., I. Anhauser, P. Soriano, A. Aguzzi, S.A. Courtneidge, and E.F. Wagner. 1994. Endothelial cell transformation by polyomavirus middle T antigen in mice lacking Src-related kinases. Cure. Biol. 4: 100-109.
56. Klages, S., D. Adam, K. Class, J. Fargnoli, J.B. Bolen, and R.C. Penhallow. 1994. Ctk: A protein-tyrosine kinase related to Csk that defines an enzyme family. Proc. Natl. Acad. Sci. 91: 2597-2601.
57. Kornbluth, S., M. Sudol, and H. Hanafusa. 1987. Association of the polyomavirus middle T antigen with c-yes protein. Nature 325: 171-173.
58. Kypta, R.M., Y. Goldber, E.T. Ulug, and S.A. Courtneidge. 1990. Association between the PDGF receptor and members of the Src-family of tyrosine kinases. Cell 62: 481-492.
59. Lancki, D.W., P. Fields, D. Qian, and F.W. Fitch. 1995a. Induction of lytic pathways in T cell clones derived from wild-type or protein tyrosine kinase Fyn mutant mice. Immunol. Rev. 146: 117-144.
60. Lancki, D.W., D. Qian, P. Fields, T. Gajewski, and F.W. Fitch. 1995b. Differential requirement for protein tyrosine kinase Fyn in the functional activation of antigen-specific T lymphocyte clones through the TCR or Thy-1. J. Immunol. 154: 4363-4370.
61. lck in thymopoiesis. EMBO J. 12: 1671-1680.
62. Lock, P., S. Ralph, E. Stanley, I. Boulet, R. Ramsay, and A.R. Dunn. 1991. Two isoforms of murine Hck, generated by utilization of alternative translational initiation codons, exhibit different patterns of subcellular localization. Mol. Cell. Biol. 11: 4363-4370.
63. Lowe, C, T. Yoneda, B.F. Boyce, H. Chen, G.R. Mundy, and P. Soriano. 1993. Osteopetrosis in Src-deficient mice is due to an autonomous defect of osteoclasts. Proc. Natl. Acad. Sci. 90: 4485-4489.
64. Lowell, C.A., P. Soriano, and H.E. Varmus. 1994. Functional overlap in the src gene family: Inactivation of hck and fgr impairs natural immunity. Genes & Dev. 8: 387-398.
65. c-fgr results in defective adhesion-dependent neutrophil functions. J. Cell Biol. 133: 895-910.
66. Lowell, C.A., M. Niwa, P. Soriano, and H.E. Varmus. 1996b. Deficiency of the Hck and Src tyrosine kinases results in extreme levels of extramedullary hematopoiesis. Blood 87: 1780-1792.
67. Markland, W.D. and A.E. Smith. 1987. Mutants of polyomavirus middle-T antigen. Biochim. Biophys. Acta 907: 299-321.
68. c-src contains a six-amino acid insertion relative to its non-neuronal counterpart. Science 237: 411-415.
69. lck. Nature 357: 161-164.
70. lck do not express significant antiviral effector functions. J. Immunol. 151: 699-706.
71. Mombaerts, P., S.J. Anderson, R.M. Perlmutter, T.W. Mak, and S. Tonegawa. 1994. An activated lck transgene promotes thymocyte development in RAG-1 mutant mice. Immunity 1: 261-267.
72. c-src. Nature 351: 69-72.
73. Nada, S., T. Yagi, H. Takeda, T. Tokunaga, H. Nakagawa, Y. Ikawa, M. Okada, and S. Aizawa. 1993. Constitutive activation of Src family kinases in mouse embryos that lack Csk. Cell 73: 1125-1135.
74. Nada, S., M. Okada, S. Aizawa, and H. Nakagawa. 1994. Identification of major tyrosine-phosphorylated proteins in Csk-deficient cells. Oncogene 9: 3571-3578.
75. Nishizumi, H., I. Taniuchi, Y. Yamanashi, D. Kitamura, D. Ilic, S. Mori, T. Watanabe, and T. Yamamoto. 1995. Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 3: 549-560.
76. Penhallow, R.C., K. Class, H. Sonoda, J.B. Bolen, and R.B. Rowley. 1995. Temporal activation of nontransmembrane protein-tyrosine kinases following mast cell FcεRI engagement. J. Biol. Chem. 270: 23362-23365.
77. Pyper, J.M. and J.B. Bolen. 1990. Identification of a novel neuronal C-SRC exon expressed in human brain. Mol. Cell. Biol. 10: 2035-2040.
78. Resh, M.D. 1994. Myristylation and palmitylation of Src family members: The fats of the matter. Cell 76: 411-413.
79. Richardson, A. and J. Parsons. 1995. Signal transduction through integrins: A central role for focal adhesion kinase? BioEssays 17: 229-236.
80. Robbins, S.M., N.A. Quintrell, and J.M. Bishop. 1995. Myristoylation and differential palmitoylation of the HCK protein-tyrosine kinases govern their attachment to membranes and association with caveolae. Mol. Cell. Biol. 15: 3507-3515.
81. Rohrschneider, L.R. 1980. Adhesion plaques of Rous sarcoma virus-transformed cells contain the Src gene product. Proc. Natl. Acad. Sci. 77: 3514-3518.
82. Ross, C.A., G.E. Wright, M.D. Resh, R.C. Pearson, and S.H. Snyder. 1988. Brain-specific src oncogene mRNA mapped in rat brain by in situ hybridization. Proc. Natl. Acad. Sci. 85: 9831-9835.
83. fyn-1 mice. J. Leukoc. Biol. 56: 812-816.
84. Soriano, P., C. Montgomery, R. Geske, and A. Bradley. 1991. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64: 693-702.
85. Stanley, E., S. Ralph, S. McEwen, I. Boulet, D.A. Holtzman, P. Lock, and A.R. Dunn. 1991. Alternatively spliced murine lyn mRNAs code distinct proteins. Mol. Cell. Biol. 11: 3399-3406.
86. lyn. J. Biol. Chem. 268: 20725-20728.
87. Stehelin, D., H.E. Varmus, J.M. Bishop, and P.K. Vogt. 1976. DNA related to the transforming gene|s| of avian sarcoma viruses is present in normal avian DNA. Nature 260: 170-173.
88. lvn mutant mice display differential signaling in thymocytes and peripheral T cells. Cell 70: 741-750.
89. Stein, P.L., H. Vogel, and P. Soriano. 1994. Combined deficiencies of Src, Fyn, and Yes tyrosine kinases in mutant mice. Genes & Dev. 8: 1999-2007.
90. Sudol, M., A. Alvarez-Buylla, and H. Hanafusa. 1988. Differential developmental expression of cellular Yes and cellular Src proteins in cerebellum. Oncogene Res. 2: 345-355.
91. Sudol, M., H. Greulich, L. Newman, A. Sarkar, J. Sukegawa, and T. Yamamoto. 1993. A novel Yes-related kinase, Yrk, is expressed at elevated levels in neural and hematopoietic tissues. Oncogene 8: 823-831.
92. c-src(1), in rat brain. J. Neuroscience 10: 2513-2527.
93. Superti-Furga, G. 1995. Regulation of the Src protein tyrosine kinase. FEES Lett. 369: 62-66.
94. Thomas, J.E., P. Soriano, and J.S. Brugge. 1991. Phosphorylation of c-Src on tyrosine 527 by another protein tyrosine kinase. Science 254: 568-571.
95. Thomas, J.E., A. Aguzzi, P. Soriano, E.F. Wagner, and J.S. Brugge. 1993. Induction of tumor formation and cell transformation by polyoma middle T antigen in the absence of Src. Oncogene 8: 2521-2529.
96. Thomas, J.H. 1993. Thinking about genetic redundancy. Trends Genet. 9: 395-399.
97. Thomas, S., P. Soriano and A. Imamoto. 1995. Specific and redundant roles of Src and Fyn in organizing the cytoskeleton. Nature 376: 267-271.
98. Tsygankov, A. and J. Bolen. 1993. The Src family of tyrosine protein kinases in hemopoietic signal transduction. Stem Cells 11:371-380.
99. Twamley-Stein, G.M., R. Pepperkok, W. Ansorge, and S.A. Courtneidge. 1993. The Src family tyrosine kinases are required for platelet-derived growth factor-mediated signal transduction in NIH 3T3 cells. Proc. Natl. Acad. Sci. 90: 7696-7700.
100. Umemori, H., A. Wanaka, H. Kato, M. Takeuchi, M. Tohyama, and T. Yamamoto. 1992. Specific expressions of Fyn and Lyn, lymphocyte antigen receptor-associated tyrosine kinases, in the central nervous system. Brain Res. Mol. Brain Res. 16: 303-310.
101. Umemori, H., S. Sato, T. Yagi, S. Aizawa, and T. Yamamoto. 1994. Initial events of myelmation involve Fyn tyrosine kinase signalling. Nature 367: 572-576.
102. Veillette, A. and D. Davidson. 1992. Src-related protein tyrosine kinases and T-cell receptor signalling. Trends Genet. 8: 61-66.
103. lck deficient mice: Allelic exclusion of the TcR β-locus is incomplete but thymocyte development is not restored by TcR β or TcR αβ transgenes. Eur. J. Immunol. 25: 1312-1318.
104. Wang, A.V., P.R. Scholl, and R.S. Geha. 1994. Physical and functional association of the high affinity immunoglobulin G receptor (FcγRI) with the kinases Hck and Lyn. J. Exp. Med. 180: 1165-1170.
105. Wang, Z.-Q., C. Ovitt, A.E. Grigoriadis, U. Möhle-Steinlein, U. Rüther, and E.F. Wagner. 1992. Bone and haematopoietic defects in mice lacking c-fos. Nature 360: 741-745.
106. fgr. J. Immunol. 154: 1919-1929.
107. Weil, R. and A. Veillette. 1996. Signal transduction by the lymphocyte-specific tyrosine protein kinase p561ck. Curr. Top. Microbiol Immunol. 205: 63-87.
108. Weiss, A. 1993. T cell antigen receptor signal transduction: A tale of tails and cytoplasmic protein-tyrosine kinases. Cell 73: 209-212.
109. Weiss, A. and D.R. Littman. 1994. Signal transduction by lymphocyte antigen receptors. Cell 76: 263-274.
110. lck. Eur. J. Immunol. 25: 3155-3159.
111. Wiktor-Jedrzejczak, W., A. Bartocci, A. Ferrante, A. Ahmed-Ansari, K. Sell, J. Pollard, and E. Stanley. 1990. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse. Proc. Natl. Acad. Sci. 87: 4828-4832.
112. Williams, E., J. Furness, F. Walsh, and P. Doherty. 1994. Activation of the FGF receptor underlies neurite outgrowth stimulated by LI, N-CAM, and N-cadherin. Neuron 13: 583-594.
113. Williams, R.L., S.A. Courtneidge, and E.F. Wagner. 1988. Embryonic lethalies and endothelial tumors in chimeric mice expressing polyoma virus middle T oncogene. Cell 52: 121-131.
114. src substrate, is a filamentous actin-binding protein enriched in the cell cortex. J. Cell. Biol. 120: 1417-1426.
115. Xu, H. and D.R. Littman. 1993. A kinase-independent function of Lck in potentiating antigen-specific T cell activation. Cell 74: 633-643.
116. Yagi, T., S. Aizawa, T. Tokunaga, Y. Shigetani, N. Takeda, and Y. Ikawa. 1993a. A role for Fyn tyrosine kinase in the suckling behaviour of neonatal mice. Nature 366: 742-745.
117. Yagi, T., Y. Shigetani, N. Okado, T. Tokunaga, Y. Ikawa, and S. Aizawa. 1993b. Regional localization of Fyn in adult brain: Studies with mice in which fyn gene was replaced by lacZ. Oncogene 8: 3343-3351.
118. lyn in adherent human neutrophils: Evidence for a role of divalent cations in regulation of neutrophil adhesion and protein tyrosine kinase activities. J. Inflammation 45: 297-331.
119. Yasunaga, M., T. Yagi, N. Hanzawa, M. Yasuda, Y. Yamanashi, T. Yamamoto, S. Aizawa, Y. Miyauchi, and S. Nishikawa. 1996. Involvement of Fyn tyrosine kinase in progression of cytokinesis of B lymphocyte progenitor. J. Cell. Biol. 132: 91-99.
120. Yi, T., J.B. Bolen, and J.N. Ihle. 1991. Hematopoietic cells express two forms of Lyn kinase differing by 21 amino acids in the amino terminus. Mol. Cell. Biol. 11: 2391-2398.
121. Yoshida, H., S.-I. Hayashi, T. Kunisada, M. Ogawa, S. Nishikawa, H. Okumura, T. Sudo, L.D. Shults, and S.-I. Nishikawa. 1990. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345: 442-444.