Drosophila C-terminal Src kinase negatively regulates organ growth and cell proliferation through inhibition of the Src, Jun N-terminal kinase, and STAT pathways

Molecular and Cellular Biology

Volumn 24, Issue 15, 2004, Pages 6676-6689

  Read, Renee D ^a   Bach, Erika A ^b   Cagan, Ross L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PROTEIN TYROSINE KINASE; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

APOPTOSIS; ARTICLE; CANCER INHIBITION; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENZYME REGULATION; NONHUMAN; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FAMILY; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE; CELL DIVISION; DNA-BINDING PROTEINS; DROSOPHILA; EXPRESSED SEQUENCE TAGS; FLOW CYTOMETRY; GENOTYPE; IMMUNOHISTOCHEMISTRY; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LARVA; MICROSCOPY, ELECTRON, SCANNING; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTATION; PHENOTYPE; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR; TIME FACTORS; TRANS-ACTIVATORS;

DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 3242700398     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.15.6676-6689.2004     Document Type: Article

References (78)

1. Abram, C. L., and S. A. Courtneidge. 2000. Src family tyrosine kinases and growth factor signaling. Exp. Cell Res. 254:1-13.
2. Aligayer, H., D. D. Boyd, M. M. Heiss, E. K. Abdalla, S. A. Curley, and G. E. Gallick. 2002. Activation of Src kinase in primary colorectal carcinoma: an indicator of poor clinical prognosis. Cancer 94:344-351.
3. Baba, K., A. Takeshita, K. Majima, R. Ueda, S. Kondo, N. Juni, and D. Yamamoto. 1999. The Drosophila Bruton's tyrosine kinase (Btk) homolog is required for adult survival and male genital formation. Mol. Cell. Biol. 19:4405-4413.
4. Bach, E., S. Vincent, M. P. Zeidler, and N. Perrimon. 2003. A sensitized genetic screen to identify novel regulators and components of the Drosophila JAK-STAT pathway. Genetics 165:1149-1166.
5. Betz, A., N. Lampen, S. Martinek, M. W. Young, and J. E. Darnell, Jr. 2001. A Drosophila PIAS homologue negatively regulates stat92E. Proc. Natl. Acad. Sci. USA 98:9563-9568.
6. Bjorge, J. D., A. Jakymiw, and D. J. Fujita. 2000. Selected glimpses into the activation and function of Src kinase. Oncogene 19:5620-5635.
7. Bolen, J. B., A. Veillette, A. M. Schwartz, V. DeSeau, and N. Rosen. 1987. Activation of pp60c-src protein kinase activity in human colon carcinoma. Proc. Natl. Acad. Sci. USA 84:2251-2255.
8. Bromberg, J. F., C. M. Horvath, D. Besser, W. W. Lathem, and J. E. Darnell, Jr. 1998. Stat3 activation is required for cellular transformation by v-src. Mol. Cell. Biol 18:2553-2558.
9. Bromberg, J. F., M. H. Wrzeszczynska, G. Devgan, Y. Zhao, R. G. Pestell, C. Albanese, and J. E. Darnell, Jr. 1999. Stat3 as an oncogene. Cell 98:295-303.
10. Bryant, P. J., and P. Levinson. 1985. Intrinsic growth control in the imaginal primordia of Drosophila, and the autonomous action of a lethal mutation causing overgrowth. Dev. Biol. 107:355-363.
11. Buratovich, M. A., and P. J. Bryant. 1997. Enhancement of overgrowth by gene interactions in lethal(2)giant discs imaginal discs from Drosophila melanogaster. Genetics 147:657-670.
12. Cam, W. R., T. Masaki, Y. Shiratori, N. Kato, T. Ikenoue, M. Okamoto, K. Igarashi, T. Sano, and M. Omata. 2001. Reduced C-terminal Src kinase activity is correlated inversely with pp60(c-src) activity in colorectal carcinoma. Cancer 92:61-70.
13. Cao, X., A. Tay, G. R. Guy, and Y. H. Tan. 1996. Activation and association of Stat3 with Src in v-Src-transformed cell lines. Mol. Cell. Biol. 16:1595-1603.
14. Cartwright, C. A., M. P. Kamps, A. I. Meisler, J. M. Pipas, and W. Eckhart. 1989. pp60c-src activation in human colon carcinoma. J. Clin. Investig. 83:2025-2033.
15. Chen, H. W., X. Chen, S. W. Oh, M. J. Marinissen, J. S. Gutkind, and S. X. Hou. 2002. mom identifies a receptor for the Drosophila JAK/STAT signal transduction pathway and encodes a protein distantly related to the mammalian cytokine receptor family. Genes Dev. 16:388-398.
16. Chen, Y. R., and T. H. Tan. 2000. The c-Jun N-terminal kinase pathway and apoptotic signaling. Int. J. Oncol. 16:651-662.
17. Cooper, J. A., K. L. Gould, C. A. Cartwright, and T. Hunter. 1986. Tyr527 is phosphorylated in pp60c-src: implications for regulation. Science 231:1431-1434.
18. Deak, P., M. M. Omar, R. D. Saunders, M. Pal, O. Komonyi, J. Szidonya, P. Maroy, Y. Zhang, M. Ashburner, P. Benos, C. Savakis, I. Siden-Kiamos, C. Louis, V. N. Bolshakov, F. C. Kafatos, E. Madueno, J. Modolell, and D. M. Glover. 1997. P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics 147:1697-1722.
19. De Angelis, P. M., O. P. Clausen, A. Schjolberg, and T. Stokke. 1999. Chromosomal gains and losses in primary colorectal carcinomas detected by CGH and their associations with tumour DNA ploidy, genotypes and phenotypes. Br. J. Cancer 80:526-535.
20. Dodson, G. S., D. J. Guarnieri, and M. A. Simon. 1998. Src64 is required for ovarian ring canal morphogenesis during Drosophila oogenesis. Development 125:2883-2892.
21. Dong, X., L. Tsuda, K. H. Zavitz, M. Lin, S. Li, R. W. Carthew, and S. L. Zipursky. 1999. ebi regulates epidermal growth factor receptor signaling pathways in Drosophila. Genes Dev. 13:954-965.
22. Fan, G., S. E. Merritt, M. Kortenjann, P. E. Shaw, and L. B. Holzman. 1996. Dual leucine zipper-bearing kinase (DLK) activates p46SAPK and p38mapk but not ERK2. J. Biol. Chem. 271:24788-24793.
23. Garcia, R., T. L. Bowman, G. Niu, H. Yu, S. Minton, C. A. Muro-Cacho, C. E. Cox, R. Falcone, R. Fairclough, S. Parsons, A. Laudano, A. Gazit, A. Levitzki, A. Kraker, and R. Jove. 2001. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20:2499-2513.
24. Guarnieri, D. J., G. S. Dodson, and M. A. Simon. 1998. SRC64 regulates the localization of a Tec-family kinase required for Drosophila ring canal growth. Mol. Cell 1:831-840.
25. Halfar, K., C. Rommel, H. Stocker, and E. Hafen. 2001. Ras controls growth, survival and differentiation in the Drosophila eye by different thresholds of MAP kinase activity. Development 128:1687-1696.
26. Hamaguchi, I., N. Yamaguchi, J. Suda, A. Iwama, A. Hirao, M. Hashiyama, S. Aizawa, and T. Suda. 1996. Analysis of CSK homologous kinase (CHK/HYL) in hematopoiesis by utilizing gene knockout mice. Biochem. Biophys. Res. Commun. 224:172-179.
27. Harrison, D. A., R. Binari, T. S. Nahreini, M. Gilman, and N. Perrimon. 1995. Activation of a Drosophila Janus kinase (JAK) causes hematopoietic neoplasia and developmental defects. EMBO J. 14:2857-2865.
28. Hay, B. A., T. Wolff, and G. M. Rubin. 1994. Expression of baculovirus P35 prevents cell death in Drosophila. Development 120:2121-2129.
29. Huang, H., C. J. Potter, W. Tao, D. M. Li, W. Brogiolo, E. Halen, H. Sun, and T. Xu. 1999. PTEN affects cell size, cell proliferation and apoptosis during Drosophila eye development. Development 126:5365-5372.
30. 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.
31. Irby, R. B., W. Mao, D. Coppola, J. Kang, J. M. Loubeau, W. Trudeau, R. Karl, D. J. Fujita, R. Jove, and T. J. Yeatman. 1999. Activating SRC mutation in a subset of advanced human colon cancers. Nat. Genet. 21:187-190.
32. Irby, R. B., and T. J. Yeatman. 2000. Role of Src expression and activation in human cancer. Oncogene 19:5636-5642.
33. Johansen, K. A., D. D. Iwaki, and J. A. Lengyel. 2003. Localized JAK/STAT signaling is required for oriented cell rearrangement in a tubular epithelium. Development 130:135-145.
34. Kango-Singh, M., R. Nolo, C. Tao, P. Verstreken, P. R. Hiesinger, H. J. Bellen, and G. Halder. 2002. Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development 129:5719-5730.
35. Karim, F. D., H. C. Chang, M. Tberrien, D. A. Wassarman, T. Laverty, and G. M. Rubin. 1996. A screen for genes that function downstream of Ras1l during Drosophila eye development. Genetics 143:315-329.
36. Karim, F. D., and G. M. Rubin. 1998. Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 125:1-9.
37. Klinghoffer, R. A., C. Sachsenmaier, J. A. Cooper, and P. Soriano. 1999. Src family kinases are required for integrin but not PDGFR signal transduction. EMBO J. 18:2459-2471.
38. Kmiecik, T. E., and D. Shalloway. 1987. Activation and suppression of pp60c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell 49:65-73.
39. Kockel, L., J. Zietlinger, L. M. Staszewski, M. Mlodzik, and D. Bohmann. 1997. Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev. 11:1748-1758.
40. Kurada, P., and K. White. 1998. Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95:319-329.
41. Kussick, S. J., K. Basler, and J. A. Cooper. 1993. Ras1-dependent signaling by ectopically-expressed Drosophila src gene product in the embryo and developing eye. Oncogene 8:2791-2803.
42. Kussick, S. J., and J. A. Cooper. 1992. Overexpressed Drosophila src 64B is phosphorylated at its carboxy-terminal tyrosine, but is not catalytically repressed, in cultured Drosophila cells. Oncogene 7:2461-2470.
43. 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. USA 90:4485-4489.
44. Luo, H., H. Asha, L. Kockel, T. Parke, M. Mlodzik, and C. R. Dearolf. 1999. The Drosophila Jak kinase hopscotch is required for multiple developmental processes in the eye. Dev. Biol. 213:432-441.
45. Masaki, T., M. Okada, M. Tokuda, Y. Shiratori, O. Hatase, M. Shirai, M. Nishioka, and M. Omata. 1999. Reduced C-terminal Src kinase (Csk) activities in hepatocellular carcinoma. Hepatology 29:379-384.
46. Minden, A., A. Lin, F. X. Claret, A. Abo, and M. Karin. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81:1147-1157.
47. Mora, L. B., R. Buettner, J. Seigne, J. Diaz, N. Ahmad, R. Garcia, T. Bowman, R. Falcone, R. Fairclough, A. Cantor, C. Muro-Cacho, S. Livingston, J. Karras, J. Pow-Sang, and R. Jove. 2002. Constitutive activation of Stat3 in human prostate tumors and cell lines: direct inhibition of Stat3 signaling induces apoptosis of prostate cancer cells. Cancer Res. 62:6659-6666.
48. Morrison, D. K., M. S. Murakami, and V. Cleghon. 2000. Protein kinases and phosphatases in the Drosophila genome. J. Cell Biol. 150:F57-62.
49. 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.
50. Nagao, M., Y. Kaziro, and H. Itoh. 1999. The Src family tyrosine kinase is involved in Rho-dependent activation of c-Jun N-terminal kinase by Galpha12. Oncogene 18:4425-4434.
51. Neufeld, T. P., A. F. de la Cruz, L. A. Johnston, and B. A. Edgar. 1998. Coordination of growth and cell division in the Drosophila wing. Cell 93:1183-1193.
52. Piwnica-Worms, H., K. B. Saunders, T. M. Roberts, A. E. Smith, and S. H. Cheng. 1987. Tyrosine phosphorylation regulates the biochemical and biological properties of pp60c-src. Cell 49:75-82.
53. Potter, C. J., G. S. Turenchalk, and T. Xu. 2000. Drosophila in cancer research. An expanding role. Trends Genet. 16:33-39.
54. Prober, D. A., and B. A. Edgar. 2000. Ras1 promotes cellular growth in the Drosophila wing. Cell 100:435-446.
55. Ram, P. T., C. M. Horvath, and R. Iyengar. 2000. Stat3-mediated transformation of NIH-3T3 cells by the constitutively active Q205L Galphao protein. Science 287:142-144.
56. Rooney, P. H., A. Boonsong, J. A. McKay, S. Marsh, D. A. Stevenson, G. I. Murray, S. Curran, N. E. Haites, J. Cassidy, and H. L. McLeod. 2001. Colorectal cancer genomics: evidence for multiple genotypes which influence survival. Br. J. Cancer 85:1492-1498.
57. Roulier, E. M., S. Panzer, and S. K. Beckendorf. 1998. The Tec29 tyrosine kinase is required during Drosophila embryogenesis and interacts with Src64 in ring canal development. Mol. Cell 1:819-829.
58. Samokhvalov, I., J. Hendrikx, J. Visser, A. Belyavsky, D. Sotiropolous, and H. Gu. 1997. Mice lacking a functional chk gene have no apparent defects in the hematopoietic system. Biochem. Mol. Biol. Int. 43:115-122.
59. Saouaf, S. J., S. Mahajan, R. B. Rowley, S. A. Kut, J. Fargnoli, A. L. Burkhardt, S. Tsukada, O. N. Witte, and J. B. Bolen. 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.
60. Schlaepfer, D. D., and T. Hunter. 1996. Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein-tyrosine kinases. Mol. Cell. Biol. 16:5623-5633.
61. Secombe, J., J. Pispa, R. Saint, and H. Richardson. 1998. Analysis of a Drosophila cyclin E hypomorphic mutation suggests a novel role for cyclin E in cell proliferation control during eye imaginal disc development. Genetics 149:1867-1882.
62. Simon, M. A., D. D. Bowtell, G. S. Dodson, T. R. Laverty, and G. M. Rubin. 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell 67:701-716.
63. 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.
64. Stewart, R. A., D.-M. Li, H. Huang, and T. Xu. 2003. A genetic screen for modifiers of the lats tumor suppressor gene identifies C-terminal Src kinase as a regulator of cell proliferation in Drosophila. Oncogene 22:6436-6444.
65. Stowers, R. S., and T. L. Schwarz. 1999. A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152:1631-1639.
66. Takahashi, F., S. Endo, T. Kojima, and K. Saigo. 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.
67. Tapon, N., K. F. Harvey, D. W. Bell, D. C. Wahrer, T. A. Schiripo, D. A. Haber, and I. K. Hariharan. 2002. salvador promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 110:467-478.
68. Tateno, M., Y. Nishida, and T. Adachi-Yamada. 2000. Regulation of JNK by Src during Drosophila development. Science 287:324-327.
69. Tautz, D., and C. Pfeifle. 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.
70. Thomas, B. J., K. H. Zavitz, X. Dong, M. E. Lane, K. Weigmann, R. L. Finley, Jr., R. Brent, C. F. Lehner, and S. L. Zipursky. 1997. roughex down-regulates G2 cyclins in G1. Genes Dev. 11:1289-1298.
71. Tseng, A. S., and I. K. Hariharan. 2002. An overexpression screen in Drosophila for genes that restrict growth or cell-cycle progression in the developing eye. Genetics 162:229-243.
72. Turkson, J., T. Bowman, J. Adnane, Y. Zhang, J. Y. Djeu, M. Sekharam, D. A. Frank, L. B. Holzman, J. Wu, S. Sebti, and R. Jove. 1999. Requirement for Ras/Rac1-mediated p38 and c-Jun N-terminal kinase signaling in Stat3 transcriptional activity induced by the Src oncoprotein. Mol. Cell. Biol. 19:7519-7528.
73. Watanabe, N., S. Matsuda, S. Kuramochi, J. Tsuzuku, T. Yamamoto, and K. Endo. 1995. Expression of C-terminal src kinase in human colorectal cancer cell lines. Jpn. J. Clin. Oncol. 25:5-9.
74. Xu, T., W. Wang, S. Zhang, R. A. Stewart, and W. Yu. 1995. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121:1053-1063.
75. Yu, C. L., D. J. Meyer, G. S. Campbell, A. C. Larner, C. Carter-Su, J. Schwartz, and R. Jove. 1995. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269:81-83.
76. Zeidler, M. P., N. Perrimon, and D. I. Strutt. 1999. Polarity determination in the Drosophila eye: a novel role for unpaired and JAK/STAT signaling. Genes Dev. 13:1342-1353.
77. Zheng, Z., and S. X. Hou. 2002. Dynamic expression of STAT92E protein and function in JAK/STAT signal transduction pathway in Drosophila development. Annu. Drosoph. Res. Conf. 43:512B.
78. Zitnan, D., F. Sehnal, and P. J. Bryant. 1993. Neurons producing specific neuropeptides in the central nervous system of normal and pupariation-delayed Drosophila. Dev. Biol. 156:117-135.