Drosophila activated Cdc42 kinase has an anti-apoptotic function

PLoS Genetics

Volumn 8, Issue 5, 2012, Pages

  Schoenherr, Jessica A ^a   Drennan, J Michelle ^a   Martinez, Juan S ^a   Chikka, Madhusudana Rao ^a,b   Hall, Mark C ^a   Chang, Henry C ^a   Clemens, James C ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED CDC42 KINASE; ADAPTOR PROTEIN; DRK PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOTRANSFERASE; RAS PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; YORKIE PROTEIN; ACK PROTEIN, DROSOPHILA; CDC42 PROTEIN, DROSOPHILA; DRK PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROPEPTIDE; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE; TRANSACTIVATOR PROTEIN; WRINKLED PROTEIN, DROSOPHILA; YORKIE PROTEIN, DROSOPHILA;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; ENZYME LOCALIZATION; FEMALE; MALE; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; ANIMAL; CELL PROLIFERATION; CYTOLOGY; DROSOPHILA MELANOGASTER; EYE; FORELIMB; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTP-BINDING PROTEINS; MAP KINASE SIGNALING SYSTEM; MUTATION; NEUROPEPTIDES; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION; WING;

EID: 84863657989     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002725     Document Type: Article

References (61)

1. Manser E, Leung T, Salihuddin H, Tan L, Lim L, (1993) A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42. Nature 363: 364-367.
2. Yokoyama N, Miller WT, (2003) Biochemical properties of the Cdc42-associated tyrosine kinase ACK1. Substrate specificity, authphosphorylation, and interaction with Hck. J Biol Chem 278: 47713-47723.
3. Cotteret S, Chernoff J, (2002) The evolutionary history of effectors downstream of Cdc42 and Rac. Genome Biol 3: REVIEWS0002.
4. Sem KP, Zahedi B, Tan I, Deak M, Lim L, et al. (2002) ACK family tyrosine kinase activity is a component of Dcdc42 signaling during dorsal closure in Drosophila melanogaster. Mol Cell Biol 22: 3685-3697.
5. Shen F, Lin Q, Gu Y, Childress C, Yang W, (2007) Activated Cdc42-associated kinase 1 is a component of EGF receptor signaling complex and regulates EGF receptor degradation. Mol Biol Cell 18: 732-742.
6. Chan W, Tian R, Lee YF, Sit ST, Lim L, et al. (2009) Down-regulation of Active ACK1 Is Mediated by Association with the E3 Ubiquitin Ligase Nedd4-2. J Biol Chem 284: 8185-8194.
7. Lin Q, Wang J, Childress C, Sudol M, Carey DJ, et al. (2010) HECT E3 ubiquitin ligase Nedd4-1 ubiquitinates ACK and regulates epidermal growth factor (EGF)-induced degradation of EGF receptor and ACK. Mol Cell Biol 30: 1541-1554.
8. Yang W, Lin Q, Zhao J, Guan JL, Cerione RA, (2001) The nonreceptor tyrosine kinase ACK2, a specific target for Cdc42 and a negative regulator of cell growth and focal adhesion complexes. J Biol Chem 276: 43987-43993.
9. Yang W, Lo CG, Dispenza T, Cerione RA, (2001) The Cdc42 target ACK2 directly interacts with clathrin and influences clathrin assembly. J Biol Chem 276: 17468-17473.
10. Mahajan K, Coppola D, Challa S, Fang B, Chen YA, et al. (2010) Ack1 mediated AKT/PKB tyrosine 176 phosphorylation regulates its activation. PLoS ONE 5: e9646 doi:10.1371/journal.pone.0009646.
11. Mahajan NP, Liu Y, Majumder S, Warren MR, Parker CE, et al. (2007) Activated Cdc42-associated kinase Ack1 promotes prostate cancer progression via androgen receptor tyrosine phosphorylation. Proc Natl Acad Sci U S A 104: 8438-8443.
12. Prieto-Echague V, Gucwa A, Brown DA, Miller WT, (2010) Regulation of Ack1 localization and activity by the amino-terminal SAM domain. BMC Biochem 11: 42.
13. van der Horst EH, Degenhardt YY, Strelow A, Slavin A, Chinn L, et al. (2005) Metastatic properties and genomic amplification of the tyrosine kinase gene ACK1. Proc Natl Acad Sci U S A 102: 15901-15906.
14. Howlin J, Rosenkvist J, Andersson T, (2008) TNK2 preserves epidermal growth factor receptor expression on the cell surface and enhances migration and invasion of human breast cancer cells. Breast Cancer Res 10: R36.
15. Liu Z, Adams HC 3rd, Whitehead IP, (2009) The rho-specific guanine nucleotide exchange factor Dbs regulates breast cancer cell migration. J Biol Chem 284: 15771-15780.
16. Mahajan NP, Whang YE, Mohler JL, Earp HS, (2005) Activated tyrosine kinase Ack1 promotes prostate tumorigenesis: role of Ack1 in polyubiquitination of tumor suppressor Wwox. Cancer Res 65: 10514-10523.
17. Bednarek AK, Laflin KJ, Daniel RL, Liao Q, Hawkins KA, et al. (2000) WWOX, a novel WW domain-containing protein mapping to human chromosome 16q23.3-24.1, a region frequently affected in breast cancer. Cancer Res 60: 2140-2145.
18. Finnis M, Dayan S, Hobson L, Chenevix-Trench G, Friend K, et al. (2005) Common chromosomal fragile site FRA16D mutation in cancer cells. Hum Mol Genet 14: 1341-1349.
19. Ried K, Finnis M, Hobson L, Mangelsdorf M, Dayan S, et al. (2000) Common chromosomal fragile site FRA16D sequence: identification of the FOR gene spanning FRA16D and homozygous deletions and translocation breakpoints in cancer cells. Hum Mol Genet 9: 1651-1663.
20. Bednarek AK, Keck-Waggoner CL, Daniel RL, Laflin KJ, Bergsagel PL, et al. (2001) WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. Cancer Res 61: 8068-8073.
21. Bellacosa A, Kumar CC, Di Cristofano A, Testa JR, (2005) Activation of AKT kinases in cancer: implications for therapeutic targeting. Adv Cancer Res 94: 29-86.
22. Grossmann ME, Huang H, Tindall DJ, (2001) Androgen receptor signaling in androgen-refractory prostate cancer. J Natl Cancer Inst 93: 1687-1697.
23. Chen CD, Welsbie DS, Tran C, Baek SH, Chen R, et al. (2004) Molecular determinants of resistance to antiandrogen therapy. Nat Med 10: 33-39.
24. Hoare K, Hoare S, Smith OM, Kalmaz G, Small D, et al. (2003) Kos1, a nonreceptor tyrosine kinase that suppresses Ras signaling. Oncogene 22: 3562-3577.
25. Hoare S, Hoare K, Reinhard MK, Lee YJ, Oh SP, et al. (2008) Tnk1/Kos1 knockout mice develop spontaneous tumors. Cancer Res 68: 8723-8732.
26. May WS, Hoare K, Hoare S, Reinhard MK, Lee YJ, et al. (2010) Tnk1/Kos1: a novel tumor suppressor. Trans Am Clin Climatol Assoc 121: 281-292; discussion 292-283.
27. Lierman E, Van Miegroet H, Beullens E, Cools J, (2009) Identification of protein tyrosine kinases with oncogenic potential using a retroviral insertion mutagenesis screen. Haematologica 94: 1440-1444.
28. Gu TL, Cherry J, Tucker M, Wu J, Reeves C, et al. (2010) Identification of activated Tnk1 kinase in Hodgkin's lymphoma. Leukemia 24: 861-865.
29. Zahedi B, Shen W, Xu X, Chen X, Mahey M, et al. (2008) Leading edge-secreted Dpp cooperates with ACK-dependent signaling from the amnioserosa to regulate myosin levels during dorsal closure. Dev Dyn 237: 2936-2946.
30. Bellen HJ, Levis RW, Liao G, He Y, Carlson JW, et al. (2004) The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167: 761-781.
31. Arama E, Agapite J, Steller H, (2003) Caspase activity and a specific cytochrome C are required for sperm differentiation in Drosophila. Dev Cell 4: 687-697.
32. Santel A, Blumer N, Kampfer M, Renkawitz-Pohl R, (1998) Flagellar mitochondrial association of the male-specific Don Juan protein in Drosophila spermatozoa. J Cell Sci 111 (Pt 22): 3299-3309.
33. Santel A, Winhauer T, Blumer N, Renkawitz-Pohl R, (1997) The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech Dev 64: 19-30.
34. Grether ME, Abrams JM, Agapite J, White K, Steller H, (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev 9: 1694-1708.
35. Bergmann A, Agapite J, McCall K, Steller H, (1998) The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95: 331-341.
36. White K, Grether ME, Abrams JM, Young L, Farrell K, et al. (1994) Genetic control of programmed cell death in Drosophila. Science 264: 677-683.
37. Chen P, Nordstrom W, Gish B, Abrams JM, (1996) grim, a novel cell death gene in Drosophila. Genes Dev 10: 1773-1782.
38. Goyal L, McCall K, Agapite J, Hartwieg E, Steller H, (2000) Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. Embo J 19: 589-597.
39. Bergmann A, Yang AY, Srivastava M, (2003) Regulators of IAP function: coming to grips with the grim reaper. Curr Opin Cell Biol 15: 717-724.
40. Zachariou A, Tenev T, Goyal L, Agapite J, Steller H, et al. (2003) IAP-antagonists exhibit non-redundant modes of action through differential DIAP1 binding. Embo J 22: 6642-6652.
41. Ready DF, Hanson TE, Benzer S, (1976) Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53: 217-240.
42. Wolff T, Ready DF, (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113: 825-839.
43. Srivastava M, Scherr H, Lackey M, Xu D, Chen Z, et al. (2007) ARK, the Apaf-1 related killer in Drosophila, requires diverse domains for its apoptotic activity. Cell Death Differ 14: 92-102.
44. Fan Y, Bergmann A, (2010) The cleaved-Caspase-3 antibody is a marker of Caspase-9-like DRONC activity in Drosophila. Cell Death Differ 17: 534-539.
45. Smith-Bolton RK, Worley MI, Kanda H, Hariharan IK, (2009) Regenerative growth in Drosophila imaginal discs is regulated by Wingless and Myc. Dev Cell 16: 797-809.
46. Kurada P, White K, (1999) Epidermal growth factor receptor: its role in Drosophila eye differentiation and cell survival. Apoptosis 4: 239-243.
47. Grovdal LM, Johannessen LE, Rodland MS, Madshus IH, Stang E, (2008) Dysregulation of Ack1 inhibits down-regulation of the EGF receptor. Exp Cell Res 314: 1292-1300.
48. Sawamoto K, Taguchi A, Hirota Y, Yamada C, Jin M, et al. (1998) Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway. Cell Death Differ 5: 548.
49. Gaul U, Mardon G, Rubin GM, (1992) A putative Ras GTPase activating protein acts as a negative regulator of signaling by the Sevenless receptor tyrosine kinase. Cell 68: 1007-1019.
50. Galisteo ML, Yang Y, Urena J, Schlessinger J, (2006) Activation of the nonreceptor protein tyrosine kinase Ack by multiple extracellular stimuli. Proc Natl Acad Sci U S A 103: 9796-9801.
51. Satoh T, Kato J, Nishida K, Kaziro Y, (1996) Tyrosine phosphorylation of ACK in response to temperature shift-down, hyperosmotic shock, and epidermal growth factor stimulation. FEBS Lett 386: 230-234.
52. Mahajan K, Mahajan NP, (2010) Shepherding AKT and androgen receptor by Ack1 tyrosine kinase. J Cell Physiol 224: 327-333.
53. Hopper NA, Lee J, Sternberg PW, (2000) ARK-1 inhibits EGFR signaling in C. elegans. Mol Cell 6: 65-75.
54. Wu S, Liu Y, Zheng Y, Dong J, Pan D, (2008) The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 14: 388-398.
55. Zhang L, Ren F, Zhang Q, Chen Y, Wang B, et al. (2008) The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev Cell 14: 377-387.
56. Badouel C, Gardano L, Amin N, Garg A, Rosenfeld R, et al. (2009) The FERM-domain protein Expanded regulates Hippo pathway activity via direct interactions with the transcriptional activator Yorkie. Dev Cell 16: 411-420.
57. Huang J, Wu S, Barrera J, Matthews K, Pan D, (2005) The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122: 421-434.
58. Oh H, Irvine KD, (2008) In vivo regulation of Yorkie phosphorylation and localization. Development 135: 1081-1088.
59. Zhao B, Ye X, Yu J, Li L, Li W, et al. (2008) TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22: 1962-1971.
60. Sandu C, Ryoo HD, Steller H, (2010) Drosophila IAP antagonists form multimeric complexes to promote cell death. J Cell Biol 190: 1039-1052.
61. Clemens JC, Worby CA, Simonson-Leff N, Muda M, Maehama T, et al. (2000) Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc Natl Acad Sci U S A 97: 6499-6503.