Mutation of the zebrafish nucleoporin elys sensitizes tissue progenitors to replication stress

PLoS Genetics

Volumn 4, Issue 10, 2008, Pages

  Davuluri, Gangarao ^a   Gong, Weilong ^a   Yusuff, Shamila ^a   Lorent, Kristin ^a   Muthumani, Manimegalai ^a   Dolan, Amy C ^a   Pack, Michael ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; DOUBLE STRANDED DNA; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 3; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 7; NUCLEOPORIN; PROTEIN ELYS; PROTEIN P53; UNCLASSIFIED DRUG; ELYS PROTEIN, ZEBRAFISH; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS INHIBITION; ENZYME ACTIVATION; ENZYME INHIBITION; GENE MUTATION; LARVAL STAGE; NONHUMAN; NUCLEAR PORE COMPLEX; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CELL CYCLE; CHEMISTRY; CYTOLOGY; DNA DAMAGE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTESTINE; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGY; PRENATAL DEVELOPMENT; RETINA; TUMOR SUPPRESSOR GENE;

AMPHIBIA; DANIO RERIO; MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CELL CYCLE; DNA DAMAGE; DNA REPLICATION; GENES, P53; INTESTINES; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PORE COMPLEX PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RETINA; RNA, MESSENGER; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 55449091773     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000240     Document Type: Article

References (70)

1. Manova K, Tomihara-Newberger C, Wang S, Godelman A, Kalantry S, et al. (1998) Apoptosis in mouse embryos: elevated levels in pregastrulae and in the distal anterior region of gastrulae of normal and mutant mice. Dev Dyn 213: 293-308.
2. Abud HE (2004) Shaping developing tissues by apoptosis. Cell Death Differ 11: 797-799.
3. Poelmann RE, Gittenberger-de Groot AC (2005) Apoptosis as an instrument in cardiovascular development. Birth Defects Res C Embryo Today 5: 305-313.
4. Zhu J, Petersen S, Tessarollo L, Nussenzweig A (2001) Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr Biol 11: 105-109.
5. Luo G, Yao MS, Bender CF, Mills M, Bladl AR, et al. (1999) Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc Natl Acad Sci 96: 7376-7381.
6. Liu CY, Flesken-Nikitin A, Li S, Zeng Y, Lee WH (1996) Inactivation of the mouse Brca1 gene leads to failure in the morphogenesis of the egg cylinder in early postimplantation development. Genes and Dev 10: 1835-1843.
7. Hakem R, de la Pompa JL, Sirard C, Mo R, Woo M, et al. (1996) The tumor suppressor gene Brca1 is required for embryonic cellular proliferation in the mouse. Cell 85: 1009-1023.
8. Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, et al. (1997) Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 386: 804-810.
9. Lim DS, Hasty P (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol Cell Biol 16: 7133-7143.
10. Tebbs RS, Flannery ML, Meneses JJ, Hartmann A, Tucker JD, et al. (1999) Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev Biol 208: 513-529.
11. Brown EJ, Baltimore D (2000) ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes and Dev 14: 397-402.
12. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, et al. (2000) Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes and Dev 15: 1448-1459.
13. Dobles M, Liberal V, Scott ML, Benezra R, Sorger PK (2000) Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2. Cell 101: 635-645.
14. Frappart PO, Tong WM, Demuth I, Radovanovic I, Herceg Z, et al. (2005) An essential function for NBS1 in the prevention of ataxia and cerebellar defects. Nat Med 11: 538-544.
15. Lam MH, Liu Q, Elledge SJ, Rosen JM (2004) Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell 6: 45-59.
16. Okita K, Kiyonari H, Nobuhisa I, Kimura N, Aizawa S, et al. (2004) Targeted disruption of the mouse ELYS gene results in embryonic death at periimplantation development. Genes Cells 9: 1083-1091.
17. Kimura N, Takizawa M, Okita K, Natori O, Igarashi K, et al. (2002) Identification of a novel transcription factor, ELYS, expressed predominantly in mouse foetal haematopoietic tissues. Genes Cells 7: 435-446.
18. Fernandez AG, Piano F (2006) Network analysis of C. elegans early embryogenesis identifies MEL-28 as a central coordinator of chromatin maintenance and nuclear envelope function. Curr Biol 16: 1757-1763.
19. Galy V, Askjaer P, Franz C, López-Iglesias C, Mattaj IW (2006) MEL-28, a novel nuclear envelope and kinetochore protein essential for zygotic nuclear envelope assembly in C. elegans. Curr Biol 16: 1748-1756.
20. Rasala BA, Orjalo AV, Shen Z, Briggs S, Forbes DJ (2006) ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division. Proc Natl Acad Sci 103: 17801-17806.
21. Franz C, Walczak R, Yavuz S, Santarella R, Gentzel M, et al. (2007) MEL-28/ELYS is required for the recruitment of nucleoporins to chromatin and postmitotic nuclear pore complex assembly. EMBO Rep 8: 165-172.
22. Gillespie PJ, Khoudoli GA, Stewart G, Swedlow JR, Blow JJ (2007) ELYS/MEL-28 Chromatin Association Coordinates Nuclear Pore Complex Assembly and Replication Licensing. Curr Biol 17: 1-6.
23. Chen JN, Haffter P, Odenthal J, Vogelsang E, Brand M, et al. (1996) Mutations affecting the cardiovascular system and other internal organs in zebrafish. Development 123: 293-302.
24. Wallace KN, Akhter S, Smith EM, Lorent K, Pack M (2005a) Intestinal growth and differentiation in zebrafish. Mech Dev 122: 157-173.
25. Yee NS, Lorent K, Pack M (2005) Exocrine pancreas development in zebrafish. Dev Biol 284: 84-101.
26. Ng AN, de Jong-Curtain TA, Mawdsley DJ, White SJ, Shin J, et al. (2005) Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev Biol 286: 114-135.
27. Chen J, Ruan H, Ng SM, Gao C, Soo HM, et al. (2005) Loss of function of def selectively up-regulates Delta113p53 expression to arrest expansion growth of digestive organs in zebrafish. Genes and Dev 19: 2900-2911.
28. Ahn J, Urist M, Prives C (2004) The Chk2 protein kinase. DNA Repair 3: 1039-1047.
29. Takahashi A, Ohnishi T (2005) Does gammaH2AX foci formation depend on the presence of DNA double strand breaks? Cancer Lett 229: 171-179.
30. Lowndes NF, Toh GW (2005) DNA repair: the importance of phosphorylating histone H2AX. Curr Biol 15: R99-R102.
31. Baker KE, Parker R (2004) Nonsense-mediated mRNA decay: terminating erroneous gene expression. Curr Opin Cell Biol 16: 293-299.
32. Crosnier C, Vargesson N, Gschmeissner S, Ariza-McNaughton L, Morrison A, et al. (2005) Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 132: 1093-1104.
33. Loeb-Hennard C, Kremmer E, Bally-Cuif L (2005) Prominent transcription of zebrafish N-myc (nmyc1) in tectal and retinal growth zones during embryonic and early larval development. Gene Expr Patterns 5: 341-347.
34. Li Z, Hu M, Ochocinska MJ, Joseph NM, Easter SS Jr (2000) Modulation of cell proliferation in the embryonic retina of zebrafish. Dev Dyn 219: 391-401.
35. Ryu S, Holzschuh J, Erhardt S, Ettl AK, Driever W (2005) Depletion of minichromosome maintenance protein 5 in the zebrafish retina causes cell-cycle defect and apoptosis. Proc Natl Acad Sci 102: 18467-18472.
36. Suntharalingam M, Wente SR (2003) Peering through the pore: nuclear pore complex structure, assembly, and function. Dev Cell 4: 775-789.
37. Davis LI, Blobel G (1987) Nuclear pore complex contains a family of glycoproteins that includes p62: glycosylation through a previously unidentified cellular pathway. Proc Natl Acad Sci 84: 7552-7556.
38. Plaster N, Sonntag C, Busse CE, Hammerschmidt M (2006) p53 deficiency rescues apoptosis and differentiation of multiple cell types in zebrafish flathead mutants deficient for zygotic DNA polymerase delta1. Cell Death Differ 13: 223-235.
39. Langheinrich U, Hennen E, Stott G, Vacun G (2002) Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling. Curr Biol 12: 2023-2028.
40. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, et al. (2005) tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci 102: 407-412.
41. Pommier Y, Weinstein JN, Aladjem MI, Kohn KW (2006) Chk2 molecular interaction map and rationale for Chk2 inhibitors. Clin Cancer Res 12: 2657-2661.
42. Carlessi L, Buscemi G, Larson G, Hong Z, Wu JZ, et al. (2007) Biochemical and cellular characterization of VRX0466617, a novel and selective inhibitor for the checkpoint kinase Chk2. Mol Cancer Ther 6: 935-944.
43. Yee NS, Gong W, Huang Y, Lorent K, Dolan AC, et al. (2007) Mutation of RNA Pol III subunit rpc2/polr3b Leads to Deficiency of Subunit Rpc11 and disrupts zebrafish digestive development. Plos Biol 5: e312.
44. Ho CC, Siu WY, Lau A, Chan WM, Arooz T, et al. (2006) Stalled replication induces p53 accumulation through distinct mechanisms from DNA damage checkpoint pathways. Cancer Res 15: 2233-2241.
45. Ishimi Y, Komamura-Kohno Y, Kwon HJ, Yamada K, Nakanishi M (2003) Identification of MCM4 as a target of the DNA replication block checkpoint system. J Biol Chem 278: 24644-24650.
46. Bailis JM, Luche DD, Hunter T, Forsburg SL (2008) Minichromosome maintenance proteins interact with checkpoint and recombination proteins to promote s-phase genome stability. Mol Cell Biol 28: 1724-1738.
47. Tran EJ, Wente SR (2006) Dynamic nuclear pore complexes: life on the edge. Cell 125: 1041-1053.
48. Rusche LN, Kirchmaier AL, Rine J (2003) The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 72: 481-516.
49. Burke B, Ellenberg J (2002) Remodelling the walls of the nucleus. Nat Rev Mol Cell Biol 3: 487-497.
50. Lambert S, Froget B, Carr AM (2007) Arrested replication fork processing: interplay between checkpoints and recombination. DNA Repair 6: 1042-1061.
51. Paulsen RD, Cimprich KA (2007) The ATR pathway: fine-tuning the fork. DNA Repair 6: 953-966.
52. D'Arpa P, Liu LF (1989) Topoisomerase-targeting antitumor drugs. Biochim Biophys Acta 989: 163-177.
53. Woodward AM, Gohler T, Luciani MG, Oehlmann M, Ge X, et al. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 5: 673-683.
54. Ge XQ, Jackson DA, Blow JJ (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes and Dev 21: 3331-3341.
55. Iizuka M, Sarmento OF, Sekiya T, Scrable H, Allis CD, et al. (2008) Hbo1 Links p53-dependent stress signaling to DNA replication licensing. Mol Cell Biol 28: 140-153.
56. Sun W, Hola M, Pedley K, Tada S, Blow JJ, et al. (2000) The replication capacity of intact mammalian nuclei in Xenopus egg extracts declines with quiescence, but the residual DNA synthesis is independent of Xenopus MCM proteins. J Cell Sci 113: 683-695.
57. Stoeber K, Tlsty TD, Happerfield L, Thomas GA, Romanov S, et al. (2001) DNA replication licensing and human cell proliferation. J Cell Sci 114: 2027-2041.
58. Pruitt SC, Bailey KJ, Freeland A (2007) Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells 5: 3121-3132.
59. Bochman ML, Schwacha A (2007) Differences in the single-stranded DNA binding activities of MCM2-7 and MCM467: MCM2 and MCM5 define a slow ATP-dependent step. J Biol Chem 282: 33795-33804.
60. O'Keefe K, Li H, Zhang Y (2003) Nucleocytoplasmic shuttling of p53 is essential for MDM2-mediated cytoplasmic degradation but not ubiquitination. Mol Cell Biol 23: 6396-6405.
61. Inoue T, Wu L, Stuart J, Maki CG (2005) Control of p53 nuclear accumulation in stressed cells. FEBS Lett 579: 4978-4984.
62. Hirano M, Furiya Y, Asai H, Yasui A, Ueno S (2006) ALADINI482S causes selective failure of nuclear protein import and hypersensitivity to oxidative stress in triple A syndrome. Proc Natl Acad Sci 103: 2298-2303.
63. Therizols P, Fairhead C, Cabal GG, Genovesio A, Olivo-Marin JC, et al. (2006) Telomere tethering at the nuclear periphery is essential for efficient DNA double strand break repair in subtelomeric region. J Cell Biol 172: 189-199.
64. Bennett CB, Lewis LK, Karthikeyan G, Lobachev KS, Jin YH, et al. (2001) Genes required for ionizing radiation resistance in yeast. Nat Genet 29: 426-434.
65. Chang M, Bellaoui M, Boone C, Brown GW (2002) A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc Natl Acad Sci 99: 16934-16939.
66. De Souza CP, Hashmi SB, Horn KP, Osmani SA (2006) A point mutation in the Aspergillus nidulans sonBNup98 nuclear pore complex gene causes conditional DNA damage sensitivity. Genetics 174: 1881-1893.
67. Loeillet SB, Palancade M, Cartron A, Thierry GF, Richard B, et al. (2005) Genetic network interactions among replication, repair and nuclear pore deficiencies in yeast. DNA Repair 4: 459-468.
68. Wallace KN, Dolan AC, Seiler C, Smith EM, Yusuff S, et al. (2005b) Mutation of smooth muscle myosin causes epithelial invasion and cystic expansion of the zebrafish intestine. Dev Cell 8: 717-726.
69. Matthews RP, Lorent K, Russo P, Pack M (2004) The zebrafish onecut gene hnf-6 functions in an evolutionarily conserved genetic pathway that regulates biliary development. Dev Biol 274: 245-259.
70. Geiger GA, Parker SE, Beothy AP, Tucker JA, Mullins MC, et al. (2006) Zebrafish as a "biosensor"? Effects of ionizing radiation and amifostine on embryonic viability and development. Cancer Res 66: 8172-8181.