Multiple isoforms of CDC25 oppose ATM activity to maintain cell proliferation during vertebrate development

Molecular Cancer Research

Volumn 10, Issue 11, 2012, Pages 1451-1461

  Verduzco, Daniel ^a,b   Dovey, Jennifer Shepard ^c,d   Shukla, Abhay A ^a,b   Kodym, Elisabeth ^a,b   Skaug, Brian A ^a,b   Amatruda, James F ^a,b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; PROTEIN TYROSINE PHOSPHATASE;

ANIMAL TISSUE; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; EMBRYO DEVELOPMENT; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE INACTIVATION; GENE MUTATION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STANDSTILL GENE; VERTEBRATE; ZEBRA FISH;

ANIMALS; CDC25 PHOSPHATASES; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DNA-BINDING PROTEINS; EMBRYONIC DEVELOPMENT; G2 PHASE; HUMANS; MICE; MUTATION; PROTEIN ISOFORMS; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS; ZEBRAFISH;

ATAXIA TELANGIECTASIA; DANIO RERIO; MUS; VERTEBRATA;

EID: 84869209717     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-12-0072     Document Type: Article

References (52)

1. Friedberg EC, McDaniel LD, Schultz RA. The role of endogenous and exogenous DNA damage and mutagenesis. Curr Opin Genet Dev 2004;14:5-10. (Pubitemid 38167472)
2. Burcham PC. Internal hazards: baseline DNA damage by endogenous products of normal metabolism. Mutat Res 1999;443:11-36. (Pubitemid 29327264)
3. Xiao W, Samson L. In vivo evidence for endogenous DNA alkylation damage as a source of spontaneous mutation in eukaryotic cells. Proc Natl Acad Sci U S A 1993;90:2117-21. (Pubitemid 23078576)
4. Ames BN. Endogenous DNA damage as related to cancer and aging. Mutat Res 1989;214:41-6. (Pubitemid 19220285)
5. Giglia-Mari G, Zotter A, Vermeulen W. DNA damage response. Cold Spring Harb Perspect Biol 2011;3:a000745.
6. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004;432:316-23. (Pubitemid 39551659)
7. Smith J, Tho LM, Xu N, Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv Cancer Res 2010;108:73-112.
8. Siliciano JD, Canman CE, Taya Y, Sakaguchi K, Appella E, Kastan MB. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev 1997;11:3471-81. (Pubitemid 28023968)
9. Matsuoka S, Huang M, Elledge SJ. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998;282: 1893-7. (Pubitemid 28555269)
10. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, et al. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 1996;86:159-71. (Pubitemid 26259926)
11. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immunedefects, and thymic lymphoma. Genes Dev 1996;10:2411-22. (Pubitemid 26341877)
12. Zha S, Sekiguchi J, Brush JW, Bassing CH, Alt FW. Complementary functions of ATM and H2AX in development and suppression of genomic instability. Proc Natl Acad Sci U S A 2008;105: 9302-6.
13. Gurley KE, Kemp CJ. Synthetic lethality between mutation in Atm and DNA-PK(cs) during murine embryogenesis. Curr Biol 2001;11:191-4. (Pubitemid 32152105)
14. Aressy B, Ducommun B. Cell cycle control by the CDC25 phosphatases. Anticancer Agents Med Chem 2008;8:818-24.
15. Mailand N, Podtelejnikov AV, Groth A, Mann M, Bartek J, Lukas J. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J 2002;21:5911-20. (Pubitemid 35315288)
16. Busino L, Chiesa M, Draetta GF, Donzelli M. Cdc25A phosphatase: combinatorial phosphorylation, ubiquitylation and proteolysis. Oncogene 2004;23:2050-6. (Pubitemid 38496734)
17. Lee G, White LS, Hurov KE, Stappenbeck TS, Piwnica-Worms H. Response of small intestinal epithelial cells to acute disruption of cell division through CDC25 deletion. Proc Natl Acad Sci U S A 2009;106:4701-6.
18. Ferguson AM, White LS, Donovan PJ, Piwnica-Worms H. Normal cell cycle and checkpoint responses in mice and cells lacking Cdc25B and Cdc25C protein phosphatases. Mol Cell Biol 2005;25:2853-60. (Pubitemid 40381646)
19. Nogare DE, Arguello A, Sazer S, Lane ME. Zebrafish cdc25a is expressed during early development and limiting for post-blastoderm cell cycle progression. Dev Dyn 2007;236:3427-35. (Pubitemid 350276399)
20. Dalle Nogare DE, Pauerstein PT, Lane ME. G2 acquisition by transcription- independent mechanism at the zebrafish midblastula transition. Dev Biol 2009;326:131-42.
21. Shepard JL, Amatruda JF, Stern HM, Subramanian A, Finkelstein D, Ziai J, et al. A zebrafish bmyb mutation causes genome instability and increased cancer susceptibility. Proc Natl Acad Sci U S A 2005;102:13194-9. (Pubitemid 41325000)
22. Westerfield M. The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). 4th ed. Eugene, OR: University of Oregon Press; 2000.
23. Sidi S, Sanda T, Kennedy RD, Hagen AT, Jette CA, Hoffmans R, et al. Chk1 suppresses a caspase-2 apoptotic response to DNA damage that bypasses p53, Bcl-2, and caspase-3. Cell 2008;133:864-77. (Pubitemid 351715394)
24. Verduzco D, Amatruda JF. Analysis of cell proliferation, senescence, and cell death in Zebrafish embryos. In: Westerfield M, Zon L, Detrich HW III, editors. Essential Zebrafish Methods. London, UK: Elsevier; 2009.
25. Davuluri G, Gong W, Yusuff S, Lorent K, Muthumani M, Dolan AC, et al. Mutation of the zebrafish nucleoporin elys sensitizes tissue progenitors to replication stress. PLoS Genet 2008;4:e1000240.
26. Link BA, Kainz PM, Ryou T, Dowling JE. The perplexed and confused mutations affect distinct stages during the transition from proliferating to post-mitotic cells within the zebrafish retina. Dev Biol 2001;236:436-53. (Pubitemid 32756996)
27. Shepard JL, Stern HM, Pfaff KL, Amatruda JF. Analysis of the cell cycle in zebrafish embryos. Methods Cell Biol 2004;76:109-25.
28. Kodym E, Kodym R, Choy H, Saha D. Sustained metaphase arrest in response to ionizing radiation in a non-small cell lung cancer cell line. Radiat Res 2008;169:46-58. (Pubitemid 351295092)
29. Imamura S, Kishi S. Molecular cloning and functional characterization of zebrafish ATM. Int J Biochem Cell Biol 2005;37:1105-16. (Pubitemid 40311749)
30. Shepard JL, Amatruda JF, Finkelstein D, Ziai J, Finley KR, Stern HM, et al. A mutation in separase causes genome instability and increased susceptibility to epithelial cancer. Genes Dev 2007;21:55-9. (Pubitemid 46089707)
31. Sauve DM, Anderson HJ, Ray JM, James WM, Roberge M. Phosphorylation- induced rearrangement of the histone H3NH2-terminal domain during mitotic chromosome condensation. J Cell Biol 1999;145:225-35. (Pubitemid 29198297)
32. Xu D, Bai J, Duan Q, Costa M, Dai W. Covalent modifications of histones during mitosis and meiosis. Cell Cycle 2009;8:3688-94.
33. Kurki P, Vanderlaan M, Dolbeare F, Gray J, Tan EM. Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle. Exp Cell Res 1986;166:209-19. (Pubitemid 16030469)
34. Bahary N, Davidson A, Ransom D, Shepard J, Stern H, Trede N, et al. The Zon laboratory guide to positional cloning in zebrafish. Methods Cell Biol 2004;77:305-29.
35. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, Fletcher CD, et al. tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci U S A 2005;102:407-12. (Pubitemid 40116780)
36. Olive PL, Banath JP. The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 2006;1:23-9.
37. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA doublestranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998;273:5858-68. (Pubitemid 28124064)
38. Cangi MG, Piccinin S, Pecciarini L, Talarico A, Dal Cin E, Grassi S, et al. Constitutive overexpression of CDC25A in primary human mammary epithelial cells results in both defective DNA damage response and chromosomal breaks at fragile sites. Int J Cancer 2008; 123:1466-71.
39. Durocher D, Jackson SP. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr Opin Cell Biol 2001;13: 225-31. (Pubitemid 32209224)
40. Yang J, Yu Y, Hamrick HE, Duerksen-Hughes PJ. ATM, ATR and DNA-PK: initiators of the cellular genotoxic stress responses. Carcinogenesis 2003;24:1571-80. (Pubitemid 37304662)
41. Lavin MF, Kozlov S. ATM activation and DNA damage response. Cell Cycle 2007;6:931-42. (Pubitemid 46658748)
42. Chen Y, Poon RY. The multiple checkpoint functions of CHK1 and CHK2 in maintenance of genome stability. Front Biosci 2008;13: 5016-29. (Pubitemid 351599655)
43. Reinhardt HC, Yaffe MB. Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2. Curr Opin Cell Biol 2009; 21:245-55.
44. Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 2008;9:759-69.
45. Ahmed M, Rahman N. ATM and breast cancer susceptibility. Oncogene 2006;25:5906-11. (Pubitemid 44453446)
46. Shechter D, Costanzo V, Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat Cell Biol 2004;6:648-55. (Pubitemid 38960923)
47. Kramer A, Mailand N, Lukas C, Syljuasen RG, Wilkinson CJ, Nigg EA, et al. Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 2004;6:884-91. (Pubitemid 39207253)
48. MacPhail SH, Banath JP, Yu Y, Chu E, Olive PL. Cell cycle-dependent expression of phosphorylated histone H2AX: reduced expression in unirradiated but not X-irradiated G1-phase cells. Radiat Res 2003;159:759-67. (Pubitemid 36676868)
49. Huang X, Halicka HD, Traganos F, Tanaka T, Kurose A, Darzynkiewicz Z. Cytometric assessment of DNA damage in relation to cell cycle phase and apoptosis. Cell Prolif 2005;38:223-43. (Pubitemid 41176576)
50. Tanaka T, Halicka HD, Huang X, Traganos F, Darzynkiewicz Z. Constitutive histone H2AX phosphorylation and ATM activation, the reporters of DNA damage by endogenous oxidants. Cell Cycle 2006;5: 1940-5. (Pubitemid 44435299)
51. McManus KJ, Hendzel MJ. ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol Biol Cell 2005;16:5013-25. (Pubitemid 41416478)
52. Ichijima Y, Sakasai R, Okita N, Asahina K, Mizutani S, Teraoka H. Phosphorylation of histone H2AX at M phase in human cells without DNA damage response. Biochem Biophys Res Commun 2005;336:807-12. (Pubitemid 41338340)