The Tec29 tyrosine kinase is required during Drosophila embryogenesis and interacts with Src64 in ring canal development

Molecular Cell

Volumn 1, Issue 6, 1998, Pages 819-829

  Roulier, Erica M ^a   Panzer, Scott ^a,b   Beckendorf, Steven K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Experimental Station   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN BINDING PROTEIN; CALMODULIN BINDING PROTEIN; CARRIER PROTEIN; DROSOPHILA PROTEIN; HU LI TAI SHAO PROTEIN, DROSOPHILA; INSECT PROTEIN; KEL PROTEIN, DROSOPHILA; ONCOPROTEIN; PROTEIN TYROSINE KINASE; SRC64B PROTEIN, DROSOPHILA; TEC PROTEIN TYROSINE KINASE; TEC PROTEIN-TYROSINE KINASE; TEC29 PROTEIN TYROSINE KINASE; TEC29 PROTEIN-TYROSINE KINASE;

ANIMAL; ANIMAL ANATOMY; ARTICLE; CHEMISTRY; DROSOPHILA; ENZYMOLOGY; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; OOCYTE; PHYSIOLOGY; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VERTEBRATE;

ACTINS; ANIMAL STRUCTURES; ANIMALS; BASE SEQUENCE; CALMODULIN-BINDING PROTEINS; CARRIER PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; INSECT PROTEINS; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; VERTEBRATES;

EID: 0032062412     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80081-7     Document Type: Article

References (62)

1. Afar, D.E.H., Park, H., Howell, B.W., Rawlings, D.J., Cooper, J., and Witte, O.N. (1996). Regulation of Btk by Src family tyrosine kinases. Mol. Cell. Biol. 16, 3465-3471.
2. Alexandropoulos, K., Cheng, G., and Baltimore, D. (1995). Proline-rich sequences that bind to Src homology 3 domains with individual specificities. Proc. Natl. Acad. Sci. USA 92, 3110-3114.
3. August, A., Sadra, A., Dupont, B., and Hanafusa, H. (1997). Src-induced activation of inducible T cell kinase (ITK) requires phosphatidylinositol 3-kinase activity and the Pleckstrin homology domain of inducibleT cell kinase. Proc. Natl. Acad. Sci. USA 94, 11227-11232.
4. Bunnell, S.C., Henry, P.A., Kolluri, R., Kirchhausen, T., Rickles, R.J., and Berg, L.J. (1996). Identification of Itk/Tsk Src homology 3 domain ligands. J. Biol. Chem. 271, 25646-25656.
5. Campos-Ortega, J.A., and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster (Berlin: Springer-Verlag).
6. Cant, K., Knowles, B.A., Mooseker, M.S., and Cooley, L. (1994). Drosophila singed, a Fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J. Cell Biol. 125, 369-380.
7. Cheng, G., Ye, Z.S., and Baltimore, D. (1994). Binding of Bruton's tyrosine kinase to Fyn, Lyn, or Hck through a Src homology 3 domain-mediated interaction. Proc. Natl. Acad. Sci. USA 91, 8152-8155.
8. Chou, T.-B., and Perrimon, N. (1992). Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 642-653.
9. Cooley, L., and Theurkauf, W.E. (1994). Cytoskeletal functions during Drosophila oogenesis. Science 266, 590-596.
10. Cory, G.O.C., Lovering, R.C., Hinshelwood, S., MacCarthy-Morrogh, L., Levinsky, R.J., and Kinnon, C. (1995). The protein product of the c-cbl protooncogene is phosphorylated after B cell receptor stimulation and binds the SH3 domain of Bruton's tyrosine kinase. J. Exp. Med. 182, 611-615.
11. de Weers, M., Brouns, G.S., Hinshelwood, S., Kinnon, C., Schuurman, R.K., Hendriks, R.W., and Borst, J. (1994). B-cell antigen receptor stimulation activates the human Bruton's tyrosine kinase, which is deficient in X-linked agammaglobulinemia. J. Biol. Chem. 269, 23857-23860.
12. Dodson, G.S., Guarnieri, D.J., and Simon, M.A. (1998). Src64 is required for ovarian ring canal morphogenesis during Drosophila oogenesis. Development, in press.
13. Frohman, M.A., and Martain, G.R. (1989). Rapid amplification of cDNA ends using nested primers. Tech 1, 165-170.
14. Gregory, R.J., Kammermeyer, K.L., Vincent, W.S., III, and Wadsworth, S.G. (1987). Primary sequence and developmental expression of a novel Drosophila melanogaster src gene. Mol. Cell. Biol. 7, 2119-2127.
15. Guarnieri, D.J., Dodson, G.S., and Simon, M.A. (1998). SRC64 regulates the localization of a Tec family kinase required for Drosophila ring canal growth. Mol. Cell, this issue, 1, 831-840.
16. Guinamard, R., Fougereau, M., and Seckinger, P. (1997). The SH3 domain of Bruton's tyrosine kinase interacts with Vav, Sam68 and EWS. Scand. J. Immunol. 45, 587-595.
17. Haire, R.N., Ohta, Y., Lewis, J.E., Fu, S.M., Kroisel, P., and Litman, G.W. (1994). TXK, a novel human tyrosine kinase expressed in T cells shares sequence identity with Tec family kinases and maps to 4p12. Hum. Mol. Genet. 3, 897-901.
18. Harlan, J.E., Hajduk, P.J., Yoon, H.S., and Fesik, S.W. (1994). Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371, 168-170.
19. Harland, R.M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
20. Hartl, D.L., Nurminsky, D.I., Jones, R.W., and Lozovskaya, E.R. (1994). Genome structure and evolution in Drosophila: applications of the framework P1 map. Proc. Natl. Acad. Sci. USA 91, 6824-6829.
21. Heyeck, S.D., Wilcox, H.M., Bunnell, S.C., and Berg, L.J. (1997). Lck phosphorylates the activation loop tyrosine of the Itk kinase domain and activates Itk kinase activity. J. Biol. Chem. 272, 25401-25408.
22. Jürgens, G., Lehmann, R., Schardin, M., and Nusslein-Volhard, C. (1986). Segmental organization of the head in the embryo of Drosophila melanogaster. Roux's Arch. Dev. Biol. 195, 359-377.
23. Katzen, A.L., Kornberg, T., and Bishop, J.M. (1990). Diverse expression of dsrc29A, a gene related to src, during the life cycle of Drosophila melanogaster. Development 110, 1169-1183.
24. Lowell, C.A., and Soriano, P. (1996). Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev. 10, 1845-1857.
25. Mahowald, A.P., and Strassheim, J.M. (1970). Intercellular migration of centrioles in the germarium of Drosophila melanogaster: an electron microscopic study. J. Cell Biol. 45, 306-320.
26. Mano, H., Ishikawa, F., Nishida, J., Hirai, H., and Takaku, F. (1990). A novel protein-tyrosine kinase, tec, is preferentially expressed in liver. Oncogene 5, 1781-1786.
27. Mano, H., Yamashita, Y., Miyazato, A., Miura, Y., and Ozawa, K. (1996). Tec protein tyrosine-kinase is an effector molecule of Lyn protein-tyrosine kinase. FASEB J. 10, 637-642.
28. Matsubara, M., Kusubata, M., Ishiguro, K., Uchida, T., Titani, K., and Taniguchi, H. (1996). Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J. Biol. Chem. 271, 21108-21113.
29. Ono, S., Yamakita, Y., Yamashiro, S., Matsudaira, P.T., Gnarra, J.R., Obinata, T., and Matsumura, F. (1997). Identification of an actin binding region and a protein kinase C phosphorylation site on human fascin. J. Biol. Chem. 272, 2527-2533.
30. Rawlings, D.J., Saffran, D.C., Tsukada, S., Largaespada, D.A., Grimaldi, J.C., Cohen, L., Mohr, R.N., Bazan, J.F., Howard, M., Copeland, N.G., et al. (1993). Mutation of unique region of Bruton's tyrosine kinase in immunodeficient XID mice. Science 261, 358-361.
31. Rawlings, D.J., Scharenberg, A.M., Park, H., Wahl, M.I., Lin, S., Kato, R.M., Fluckiger, A.C., Witte, O.N., and Kinet, J.P. (1996). Activation of BTK by a phosphorylation mechanism initiated by SRC family kinases. Science 271, 822-825.
32. Robinson, D., Cant, K., and Cooley, L. (1994). Morphogenesis of Drosophila ovarian ring canals. Development 120, 2015-2025.
33. Robinson, D.N., and Cooley, L. (1997). Drosophila Kelch is an oligomeric ring canal Actin organizer. J. Cell Biol. 138, 799-810.
34. Robinson, D.N., Smith-Leiker, T.A., Sokol, N.S., Hudson, A.M., and Cooley, L. (1997). Formation of the Drosophila ovarian ring canal inner rim depends on cheerio. Genetics 145, 1063-1072.
35. Rubin, G.M., and Spradling, A.C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
36. Salim, K., Bottomley, M.J., Querfurth, E., Zvelebil, M.J., Gout, I., Scaife, R., Margolis, R.L., Gigg, R., Smith, G.I., Driscoll, P.C., et al. (1996). Distinct specificity in the recognition of phosphoinositides by the pleckstrin homology domains of dynamin and Bruton's tyrosine kinase. EMBO J. 15, 6241-6250.
37. Saouaf, S., Mahajan, S., Rowley, R., Kut, S., Fargnoli, J., Burkhardt, A., Tsukada, S., Witte, O., and Bolen, J. (1994). Temporal differences in the activation of three classes of non-transmembrane protein tyrosine kinases following B-cell antigen receptor surface engagement. Proc. Natl. Acad. Sci. USA 91, 9524-9528.
38. Sato, K., Mano, H., Ariyama, T., Inazawa, J., Yazaki, Y., and Hirai, H. (1994). Molecular cloning and analysis of the human Tec protein-tyrosine kinase. Leukemia 8, 1663-1672.
39. Siliciano, J.D., Morrow, T.A., and Desiderio, S.V. (1992). itk, a T-cell-specific tyrosine kinase gene inducible by interleukin 2. Proc. Natl. Acad. Sci. USA 89, 11194-11198.
40. Simon, M.A., Kornberg, T.B., and Bishop, J.M. (1983). Three loci related to the src oncogene and tyrosine-specific protein kinase activity in Drosophila. Nature 302, 837-839.
41. Simon, M.A., Drees, B., Kornerg, T., and Bishop, J.M. (1985). The nucleotide sequence and the tissue-specific expression of Drosophila c-src. Cell 42, 831-840.
42. Sommers, C.L., Huang, K., Shores, E.W., Grinberg, A., Charlick, D.A., Kozak, C.A., and Love, P.E. (1995). Murine txk: a protein tyrosine kinase gene regulated by T cell activation. Oncogene 11, 245-251.
43. Spradling, A. (1993). Developmental Genetics of Oogenesis. In The Development of Drosophila melanogaster, M. Bate and A. Martinez-Arias, eds. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory), pp. 1-70.
44. Spradling, A.C., Stern, D.M., Kiss, I., Roote, J., Laverty, T., and Rubin, G.M. (1995). Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA 92, 10824-10830.
45. Takahashi, F., Endo, S., Kojima, T., and Saigo, K. (1996) Regulation of cell-cell contacts in developing Drosophila eyes by Dsrc41, a new, close relative of vertebrate c-src. Genes Dev. 10, 1645-1656.
46. Takahashi-Tezuka, M., Hibi, M., Fujitani, Y., Fukada, T., Yamaguchi, T., and Hirano, T. (1997). Tec tyrosine kinase links the cytokine receptors to PI-3 kinase probably through JAK. Oncogene 14, 2273-2282.
47. Tamagnone, L., Lahtinen, I., Mustonen, T., Virtaneva, K., Francis, F., Muscatelli, F., Alitalo, R., Smith, C.I.E., Larsson, C., and Alitalo, K. (1994). BMX, a novel nonreceptor tyrosine kinase gene of the BTK/ITK/TEC/TXK family located in chromosome Xp22.2. Oncogene 9, 3683-3688.
48. Tautz, D., and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81-85.
49. Tilney, L., Tilney, M., and Guild, G. (1996). Formation of actin filament bundles in the ring canals of developing Drosophila follicles. J. Cell Biol. 133, 61-74.
50. Torok, T., Tick, G., Alvarado, M., and Kiss, I. (1993). P-lacW insertional mutagenesis on the second chromosome of Drosophila melanogaster: isolation of lethals with different overgrowth phenotypes. Genetics 135, 71-80.
51. Tsukada, S., Saffran, D.C., Rawlings, D.J., Parolini, O., Allen, R.C., Klisak, I., Sparkes, R.S., Kubagawa, H., Mohandas, T., Quan, S., et al. (1993). Deficient expression of a B cell cytoplasmic tyrosine kinase in human X-linked agammaglobulinemia. Cell 72, 279-290.
52. Tsukada, S., Simon, M.I., Witte, O.N., and Katz, A. (1994). Binding of beta gamma subunits of heterotrimeric G proteins to the PH domain of Bruton tyrosine kinase. Proc. Natl. Acad. Sci. USA 91, 11256-11260.
53. Verheyen, E., and Cooley, L. (1994). Looking at Oogenesis. In Methods in Cell Biology, L.S.B. Golstein and E.A. Fyrberg, eds. (San Diego, CA: Academic Press, Inc.), pp. 545-561.
54. Vetrie, D., Vorechovsky, I., Sideras, P., Holland, J., Davies, A., Flinter, F., Hammarstrom, L., Kinnon, C., Levinsky, R., Bobrow, M., et al. (1993). The gene involved in X-linked agammaglobulinemia is a member of the src family of protein-tyrosine kinases. Nature 361, 226-233.
55. Vihinen, M., Nilsson, L., and Smith, C.I. (1994). Tec homology (TH) adjacent to the PH domain. FEBS Lett. 350, 263-265.
56. Vincent, W.S., Gregory, R.J., and Wadsworth, S.C. (1989). Embryonic expression of a Drosophila src gene: alternate forms of the protein are expressed in segmental stripes and in the nervous system. Genes Dev. 3, 334-347.
57. Wadsworth, S., Muckenthaler, F.A., and Vincent, W.S. (1990). Differential expression of alternate forms of a Drosophila src protein during embryonic and larval tissue differentiation. Dev. Biol. 138, 296-312.
58. Wustmann, G., Szidonya, J., Taubert, H., and Reuter, G. (1989). The genetics of position-effect variegation modifying loci in Drosophila melanogaster. Mol. Gen. Genet. 217, 520-527.
59. Xue, F., and Cooley, L. (1993). kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 72, 681-693.
60. Yang, W., Malek, S.N., and Desiderio, S. (1995). An SH3-binding site conserved in Bruton's tyrosine kinase and related tyrosine kinases mediates specific interactions in vitro and in vivo. J. Biol. Chem. 270, 20832-20840.
61. Yue, L., and Spradling, A.C. (1992). hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 6, 2443-2454.
62. Zinn, K., McAllister, L., and Goodman, C.S. (1988). Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell 53, 577-587.