Drosophila melanogaster MNK/Chk2 and p53 Regulate Multiple DNA Repair and Apoptotic Pathways following DNA Damage

Molecular and Cellular Biology

Volumn 24, Issue 3, 2004, Pages 1219-1231

  Brodsky, Michael H ^a,b   Weinert, Brian T ^b   Tsang, Garson ^b,c   Rong, Yikang S ^d   McGinnis, Nadine M ^a   Golic, Kent G ^c   Rio, Donald C ^b   Rubin, Gerald M ^b,c  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF UTAH   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; HEAD INVOLUTION DEFECTIVE PROTEIN; KU ANTIGEN; PROTEIN MDM2; PROTEIN MNK; PROTEIN P53; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR EIGER; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; DNA DAMAGE; DNA MICROARRAY; DNA REPAIR; DNA TRANSCRIPTION; DROSOPHILA MELANOGASTER; GENE DELETION; GENE INDUCTION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; IONIZING RADIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REAPER GENE; SEQUENCE HOMOLOGY; SICKLE GENE;

ANIMALS; APOPTOSIS; DNA DAMAGE; DNA REPAIR; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MEMBRANE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 1642540218     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.3.1219-1231.2004     Document Type: Article

References (80)

1. Abdu, U., M. Brodsky, and T. Schupbach. 2002. Activation of a meiotic checkpoint during Drosophila oogenesis regulates the translation of Gurken through Chk2/Mnk. Curr. Biol. 12:1645.
2. Abraham, R. T. 2001. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2177-2196.
3. Abrams, J. M., K. White, L. I. Fessler, and H. Steller. 1993. Programmed cell death during Drosophila embryogenesis. Development 117:29-43.
4. Amundson, S. A., M. Bittner, P. Meltzer, J. Trent, and A. J. Fornace, Jr. 2001. Physiological function as regulation of large transcriptional programs: the cellular response to genotoxic stress. Comp. Biochem. Physiol. B 129:703-710.
5. Barlow, C., K. D. Brown, C. X. Deng, D. A. Tagle, and A. Wynshaw-Boris. 1997. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17:453-456.
6. Bergmann, A., J. Agapite, K. McCall, and H. Steller. 1998. The Drosophila gene hid is a direct molecular target of Ras-dependent survival signaling. Cell 95:331-341.
7. Bergmann, A., M. Tugentman, B. Z. Shilo, and H. Steller. 2002. Regulation of cell number by MAPK-dependent control of apoptosis: a mechanism for trophic survival signaling. Dev. Cell 2:159-170.
8. Bhat, M. A., A. V. Philp, D. M. Glover, and H. J. Bellen. 1996. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II. Cell 87:1103-1114.
9. Braastad, C. D., M. Leguia, and E. A. Hendrickson. 2002. Ku86 autoantigen related protein-1 transcription initiates from a CpG island and is induced by p53 through a nearby p53 response element. Nucleic Acids Res. 30:1713-1724.
10. Brennecke, J., D. R. Hipfner, A. Stark, R. B. Russell, and S. M. Cohen. 2003. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cel1. 13:25-36.
11. Brodsky, M. H., W. Nordstrom, G. Tsang, E. Kwan, G. M. Rubin, and J. M. Abrams. 2000. Drosophila p53 binds a damage response element at the reaper locus. Cell 101:103-113.
12. Brodsky, M. H., J. J. Sekelsky, G. Tsang, R. S. Hawley, and G. M. Rubin. 2000. mus3O4 encodes a novel DNA damage checkpoint protein required during Drosophila development. Genes Dev. 14:666-678.
13. 1 by stabilizing p53. Genes Dev. 14:278-288.
14. Christich, A., S. Kauppila, P. Chen, N. Sogame, S. I. Ho, and J. M. Abrams. 2002. The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, and hid. Curr. Biol. 12:137-140.
15. Cook, W. D., and B. J. McCaw. 2000. Accommodating haploinsufficient tumor suppressor genes in Knudson's model. Oncogene 19:3434-3438.
16. Cortez, D., S. Guntuku, J. Qin, and S. J. Elledge. 2001. ATR and ATRIP: partners in checkpoint signaling. Science 294:1713-1716.
17. D'Amours, D., and S. P. Jackson. 2002. The Mrc11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3:317-327.
18. Derry, W. B., A. P. Putzke, and J. H. Rothman. 2001. Caenorhabditis elegans p53: role in apoptosis, meiosis, and stress resistance. Science 294:591-595.
19. el-Deiry, W. S. 1998. Regulation of p53 downstream genes. Semin. Cancer Biol. 8:345-357.
20. Flores, E. R., K. Y. Tsai, D. Crowley, S. Sengupta, A. Yang, F. McKeon, and T. Jacks. 2002. p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 416:560-564.
21. Fogarty, P., S. D. Campbell, R. Abu-Shumays, B. S. Phalle, K. R. Yu, G. L. Uy, M. L. Goldberg, and W. Sullivan. 1997. The Drosophila grapes gene is related to checkpoint gene chk1/rad27 and is required for late syncytial division lidelity. Curr. Biol. 7:418-426.
22. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis. ASM Press, Washington, D.C.
23. Gasch, A. P., M. Huang, S. Metzner, D. Botstein, S. J. Elledge, and P. O. Brown. 2001. Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell 12:2987-3003.
24. Ghabrial, A., and T. Schupbach. 1999. Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat. Cell Biol. 1:354-357.
25. Goyal, L., K. McCall, J. Agapite, E. Hartwieg, and H. Steller. 2000. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 19:589-597.
26. Grether, M. E., J. M. Abrams, J. Agapite, K. White, and H. Steller. 1995. The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes Dev. 9:1694-1708.
27. Hari, K. L., A. Santerre, J. J. Sekelsky, K. S. McKim, J. B. Boyd, and R. S. Hawley. 1995. The mei-41 gene of D. melanogaster is a structural and functional homolog of the human ataxia telangiectasia gene. Cell 82:815-821.
28. 2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348-360.
29. Hirao, A., A. Cheung, G. Duncan, P. M. Girard, A. J. Elia, A. Wakeham, H. Okada, T. Sarkissian, J. A. Wong, T. Sakai, E. De Stanchina, R. G. Bristow, T. Suda, S. W. Lowe, P. A. Jeggo, S. J. Elledge, and T. W. Mak. 2002. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol. Cell. Biol. 22:6521-6532.
30. Hirao, A., Y. Y. Kong, S. Matsuoka, A. Wakeham, J. Ruland, H. Yoshida, D. Liu, S. J. Elledge, and T. W. Mak. 2000. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287:1824-1827.
31. Igaki, T., H. Kanda, Y. Yamamoto-Goto, H. Kanuka, E. Kuranaga, T. Aigaki, and M. Miura. 2002. Eiger, a TNF superfamily ligand that triggers the Drosophila JNK pathway. EMBO J. 21:3009-3018.
32. Jackson, S. P. 2001. Detecting, signalling and repairing DNA double-strand breaks. Biochem. Soc. Trans. 29:655-661.
33. Jackson, S. P. 2002. Sensing and repairing DNA double-strand breaks. Carcinogenesis 23:687-696.
34. Jin, S., M. Kalkum, M. Overholtzer, A. Stoffel, B. T. Chait, and A. J. Levine. 2003. CIAP1 and the serine protease HTRA2 are involved in a novel p53-dependent apoptosis pathway in mammals. Genes Dev. 17:359-367.
35. Kanda, H., T. Igaki, H. Kanuka, T. Yagi, and M. Miura. 2002. Wengen, a member of the Drosophila tumor necrosis factor receptor superfamily, is required for Eiger signaling. J. Biol. Chem. 277:28372-28375.
36. Kastan, M. B., Q. Zhan, W. S. elI-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fornace, Jr. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71:587-597.
37. Kurada, P., and K. White. 1998. Ras promotes cell survival in Drosophila by downregulating hid expression. Cell 95:319-329.
38. Laurencon, A., A. Purdy, J. Sekelsky, R. S. Hawley, and T. T. Su. 2003. Phenotypic analysis of separation-of-function alleles of MEI-41, Drosophila ATM/ATR. Genetics 164:589-601.
39. Li, C., and W. H. Wong. 2001. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc. Natl. Acad. Sci. USA 98:31-36.
40. Martin, S. J. 2002. Destabilizing influences in apoptosis: sowing the seeds of IAP destruction. Cell 109:793-796.
41. McCurrach, M. E., T. M. Connor, C. M. Knudson, S. J. Korsmeyer, and S. W. Lowe. 1997. bax-deficiency promotes drug resistance and oncogenic transformation by attenuating p53-dependent apoptosis. Proc. Natl. Acad. Sci. USA 94:2345-2349.
42. Mills, A. A., B. Zheng, X. J. Wang, H. Vogel, D. R. Roop, and A. Bradley. 1999. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398:708-713.
43. Moreno, E., M. Yan, and K. Basler. 2002. Evolution of TNF signaling mechanisms. JNK-dependent apoptosis triggered by Eiger, the Drosophila homolog of the TNF superfamily. Curr. Biol. 12:1263.
44. Myung, K., C. Braastad, D. M. He, and E. A. Hendrickson. 1998. KARP-1 is induced by DNA damage in a p53- and ataxia telangiectasia mutated-dependent fashion. Proc. Natl. Acad. Sci. USA 95:7664-7669.
45. Nghiem, P., P. K. Park, Y. S. Kim, B. N. Desai, and S. L. Schreiber. 2002. ATR is not required for p53 activation but synergizes with p53 in the replication checkpoint. J. Biol. Chem. 277:4428-4434.
46. Nordstrom, W., P. Chen, H. Steller, and J. M. Abrams. 1996. Activation of the reaper gene during ectopic cell killing in Drosophila. Dev. Biol. 180:213-226.
47. Oishi, I., S. Sugiyama, H. Otani, H. Yamamura, Y. Nishida, and Y. Minami. 1998. A novel Drosophila nuclear protein serine/threonine kinase expressed in the germline during its establishment. Mech. Dev. 71:49-63.
48. Ollmann, M., L. M. Young, C. J. Di Como, F. Karim, M. Belvin, S. Robertson, K. Whittaker, M. Demsky, W. W. Fisher, A. Buchman, G. Duyk, L. Friedman, C. Prives, and C. Kopczynski. 2000. Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 101:91-101.
49. Owen-Schaub, L. B., W. Zhang, J. C. Cusack, L. S. Angelo, S. M. Santee, T. Fujiwara, J. A. Roth, A. B. Deisseroth, W. W. Zhang, E. Kruzel, et al. 1995. Wild-type human p53 and a temperature-sensitive mutant induce Fas/APO-1 expression. Mol. Cell. Biol. 15:3032-3040.
50. Peters, M., C. DeLuca, A. Hirao, V. Stambolic, J. Potter, L. Zhou, J. Liepa, B. Snow, S. Arya, J. Won, D. Bouchard, R. Binari, A. S. Manoukian, and T. W. Mak. 2002. Chk2 regulates irradiation-induced, p53-mediated apoptosis in Drosophila. Proc. Natl. Acad. Sci. USA 99:11305-11310.
51. Peterson, C., G. E. Carney, B. J. Taylor, and K. White. 2002. reaper is required for neuroblast apoptosis during Drosophila development. Development 129:1467-1476.
52. Rong, Y. S., S. W. Titen, H. B. Xie, M. M. Golic, M. Bastiani, P. Bandyopadhyay, B. M. Olivera, M. Brodsky, G. M. Rubin, and K. G. Golic. 2002. Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 16:1568-1581.
53. Rouse, J., and S. P. Jackson. 2002. Interfaces between the detection, signaling, and repair of DNA damage. Science 297:547-551.
54. Sawamoto, K., A. Taguchi, Y. Hirota, C. Yamada, M. H. Jin, and H. Okano. 1998. Argos induces programmed cell death in the developing Drosophila eye by inhibition of the Ras pathway. Cell Death Differ. 5:262-270.
55. Sax, J. K., P. Fei, M. E. Murphy, E. Bernhard, S. J. Korsmeyer, and W. S. El-Deiry. 2002. BID regulation by p53 contributes to chemosensitivity. Nat. Cell Biol. 4:842-849.
56. Schumacher, B., K. Hofmann, S. Boulton, and A. Gartner. 2001. The C. elegans homolog of the p53 tumor suppressor is required for DNA damage-induced apoptosis. Curr. Biol. 11:1722-1727.
57. Sekelsky, J. J., M. H. Brodsky, and K. C. Burtis. 2000. DNA repair in Drosophila: insights from the Drosophila genome sequence. J. Cell Biol. 150:F31-F36.
58. Sheikh, M. S., and A. J. Fornace, Jr. 2000. Death and decoy receptors and p53-mediated apoptosis. Leukemia 14:1509-1513.
59. Sihon, O. C., A. Laurencon, R. Hawley, and W. E. Theurkauf. 1999. The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 9:302-312.
60. Sihon, O. C., V. A. Stevenson, and W. E. Theurkauf. 1997. DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388:93-97.
61. Sogame, N., M. Kim, and J. M. Abrams. 2003. Drosophila p53 preserves genomic stability by regulating cell death. Proc. Natl. Acad. USA 100: 4696-4701.
62. Srinivasula, S. M., P. Datta, M. Kohayashi, J. W. Wu, M. Fujioka, R. Hegde, Z. Zhang, R. Mukattash, T. Fernandes-Alnemri, Y. Shi, J. B. Jaynes, and E. S. Alnemri. 2002. sickle, a novel Drosophila death gene in the reaper/hid/ grim region, encodes an IAP-inhibitory protein. Curr. Biol. 12:125-130.
63. Sutton, M. D., B. T. Smith, V. G. Godoy, and G. C. Walker. 2000. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance. Annu. Rev. Genet. 34:479-497.
64. Takada, S., A. Kelkar, and W. E. Theurkauf. 2003. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113:87-99.
65. Tibbetts, R. S., K. M. Brumbaugh, J. M. Williams, J. N. Sarkaria, W. A. Cliby, S. Y. Shieb, Y. Taya, C. Prives, and R. T. Abraham. 1999. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13:152-157.
66. +/- mouse model in carcinogenicity testing. Toxicol. Pathol. 29(Suppl.):147-154.
67. Vousden, K. H. 2002. Activation of the p53 tumor suppressor protein. Biochim. Biophys. Acta 1602:47-59.
68. Vousden, K. H., and X. Lu. 2002. Live or let die: the cell's response to p53. Nat. Rev. Cancer 2:594-604.
69. Wahl, G. M., and A. M. Carr. 2001. The evolution of diverse biological responses to DNA damage: insights from yeast and p53. Nat. Cell Biol. 3:E277-E286.
70. Wang, S. L., C. J. Hawkins, S. J. Yoo, H. A. Muller, and B. A. Hay. 1999. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 98:453-463.
71. White, K., M. E. Grether, J. M. Abrams, L. Young, K. Farrell, and H. Steller. 1994. Genetic control of programmed cell death in Drosophila. Science 264:677-683.
72. White, K., E. Tahaoglu, and H. Steller. 1996. Cell killing by the Drosophila gene reaper. Science 271:805-807.
73. Wing, J. P., J. S. Karres, J. L. Ogdahl, L. Zhou, L. M. Schwartz, and J. R. Nambu. 2002. Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 12:131-135.
74. Wu, G. S., K. Kim, and W. S. el-Deiry. 2000. KILLER/DR5, a novel DNA-damage inducible death receptor gene, links the p53-tumor suppressor to caspase activation and apoptotic death. Adv. Exp. Med. Biol. 465:143-151.
75. Xu, J., S. Xin, and W. Du. 2001. Drosophila Chk2 is required for DNA damage-mediated cell cycle arrest and apoptosis. FEBS Lett. 508:394-398.
76. -/- mice. Mol. Cell. Biol. 18:4385-4390.
77. Yang, A., R. Schweitzer, D. Sun, M. Kaghad, N. Walker, R. T. Bronson, C. Tabin, A. Sharpe, D. Caput, C. Crum, and F. McKeon. 1999. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714-718.
78. Yang, A., N. Walker, R. Bronson, M. Kaghad, M. Oosterwegel, J. Bonnin, C. Vagner, H. Bonnet, P. Dikkes, A. Sharpe, F. McKeon, and D. Caput. 2000. p73-deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404:99-103.
79. Zhou, L., Z. Song, J. Tittel, and H. Steller. 1999. HAC-1, a Drosophila homolog of APAF-1 and CED-4 functions in developmental and radiation-induced apoptosis. Mol. Cell 4:745-755.
80. Zhou, L., and H. Steller. 2003. Distinct pathways mediate UV-induced apoptosis in Drosophila embryos. Dev. Cell 4:599-605.