The ENU-induced cetus mutation reveals an essential role of the DNA helicase DDX11 for mesoderm development during early mouse embryogenesis

Developmental Dynamics

Volumn 241, Issue 8, 2012, Pages 1249-1259

  Cota, Christina D ^a   García García, María J ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

DDX11; Embryo; Genome instability; Somites

Indexed keywords

AMINO ACID; HELICASE; N ETHYL N NITROSUREA; NITROSOUREA; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; APOPTOSIS; ARTICLE; CLONE; DNA DAMAGE; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENOMIC INSTABILITY; LETHALITY; MESODERM; MORPHOGENESIS; MUTATION; NEURAL TUBE; NONHUMAN; NULL ALLELE; PHENOTYPE; PLACENTA; PRIORITY JOURNAL; SISTER CHROMATID; SOMITE;

AMINO ACID MOTIFS; ANIMALS; APOPTOSIS; DEAD-BOX RNA HELICASES; EMBRYONIC DEVELOPMENT; GENOMIC INSTABILITY; MESODERM; MICE; MUTATION;

EID: 84864003996     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23810     Document Type: Article

References (61)

1. Amann J, Kidd VJ, Lahti JM. 1997. Characterization of putative human homologues of the yeast chromosome transmission fidelity gene, CHL1. J Biol Chem 272: 3823-3832.
2. Belo JA, Bouwmeester T, Leyns L, Kertesz N, Gallo M, Follettie M, De Robertis EM. 1997. Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula. Mech Dev 68:45-57.
3. Bolton VN, Oades PJ, Johnson MH. 1984. The relationship between cleavage, DNA replication, and gene expression in the mouse 2-cell embryo. J Embryol Exp Morphol 79: 139-163.
4. Candia AF, Hu J, Crosby J, Lalley PA, Noden D, Nadeau JH, Wright CV. 1992. Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116: 1123-1136.
5. 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 U S A 99: 16934-16939.
6. Chapman DL, Garvey N, Hancock S, Alexiou M, Agulnik SI, Gibson-Brown JJ, Cebra-Thomas J, Bollag RJ, Silver LM, Papaioannou VE. 1996. Expression of the T-box family genes, Tbx1-Tbx5, during early mouse development. Dev Dyn 206: 379-390.
7. Collignon J, Sockanathan S, Hacker A, Cohen-Tannoudji M, Norris D, Rastan S, Stevanovic M, Goodfellow PN, Lovell-Badge R. 1996. A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122: 509-520.
8. Fairman-Williams ME, Guenther U-P, Jankowsky E. 2010. SF1 and SF2 helicases: family matters. Curr Opin Struct Biol 20: 313-324.
9. Fan L, Fuss JO, Cheng QJ, Arvai AS, Hammel M, Roberts VA, Cooper PK, Tainer JA. 2008. XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell 133: 789-800.
10. Farina A, Shin JH, Kim DH, Bermudez VP, Kelman Z, Seo YS, Hurwitz J. 2008. Studies with the Human Cohesin Establishment Factor, ChlR1: association of ChlR1 with Ctf18-RFC AND Fen1. J Biol Chem 283: 20925-20936.
11. Garcia-Garcia MJ, Anderson KV. 2003. Essential role of glycosaminoglycans in Fgf signaling during mouse gastrulation. Cell 114: 727-737.
12. Garcia-Garcia MJ, Eggenschwiler JT, Caspary T, Alcorn HL, Wyler MR, Huangfu D, Rakeman AS, Lee JD, Feinberg EH, Timmer JR, Anderson KV. 2005. Analysis of mouse embryonic patterning and morphogenesis by forward genetics. Proc Natl Acad Sci U S A 102: 5913-5919.
13. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119: 493-501.
14. George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079-1091.
15. Gerring SL, Spencer F, Hieter P. 1990. The CHL 1 (CTF 1) gene product of Saccharomyces cerevisiae is important for chromosome transmission and normal cell cycle progression in G2/M. EMBO J 9: 4347-4358.
16. Graves-Woodward KL, Gottlieb J, Challberg MD, Weller SK. 1997. Biochemical analyses of mutations in the HSV-1 helicase-primase that alter ATP hydrolysis, DNA unwinding, and coupling between hydrolysis and unwinding. J Biol Chem 272: 4623-4630.
17. Hall MC, Matson SW. 1999. Helicase motifs: the engine that powers DNA unwinding. Mol Microbiol 34: 867-877.
18. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD. 1997. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360.
19. Heyer BS, MacAuley A, Behrendtsen O, Werb Z. 2000. Hypersensitivity to DNA damage leads to increased apoptosis during early mouse development. Genes Dev 14: 2072-2084.
20. Hirota Y, Lahti JM. 2000. Characterization of the enzymatic activity of hChlR1, a novel human DNA helicase. Nucleic Acids Res 28: 917-924.
21. Hsu DS, Kim ST, Sun Q, Sancar A. 1995. Structure and function of the UvrB protein. J Biol Chem 270: 8319-8327.
22. Inoue A, Li T, Roby SK, Valentine MB, Inoue M, Boyd K, Kidd VJ, Lahti JM. 2007. Loss of ChlR1 helicase in mouse causes lethality due to the accumulation of aneuploid cells generated by cohesion defects and placental malformation. Cell Cycle 6: 1646-1654.
23. Kauffman SL. 1968. Lengthening of the generation cycle during embryonic differentiation of the mouse neural tube. Exp Cell Res 49: 420-424.
24. Kerr JF, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257.
25. Korolev S, Hsieh J, Gauss GH, Lohman TM, Waksman G. 1997. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90: 635-647.
26. Laha S, Das SP, Hajra S, Sau S, Sinha P. 2006. The budding yeast protein Chl1p is required to preserve genome integrity upon DNA damage in S-phase. Nucleic Acids Res 34: 5880-5891.
27. Lee JD, Silva-Gagliardi NF, Tepass U, McGlade CJ, Anderson KV. 2007. The FERM protein Epb4.1l5 is required for organization of the neural plate and for the epithelial-mesenchymal transition at the primitive streak of the mouse embryo. Development 134: 2007-2016.
28. Leman AR, Noguchi C, Lee CY, Noguchi E. 2010. Human Timeless and Tipin stabilize replication forks and facilitate sister-chromatid cohesion. J Cell Sci 123: 660-670.
29. Liras P, McCusker J, Mascioli S, Haber JE. 1978. Characterization of a mutation in yeast causing nonrandom chromosome loss during mitosis. Genetics 88: 651-671.
30. Luijsterburg MS, van Attikum H. 2011. Chromatin and the DNA damage response: the cancer connection. Mol Oncol 5: 349-367.
31. Mac Auley A, Werb Z, Mirkes PE. 1993. Characterization of the unusually rapid cell cycles during rat gastrulation. J Embryol Exp Morphol 117: 873-883.
32. Mahlapuu M, Ormestad M, Enerback S, Carlsson P. 2001. The forkhead transcription factor Foxf1 is required for differentiation of extra-embryonic and lateral plate mesoderm. Development 128: 155-166.
33. Mannini L, Musio A. 2011. The dark side of cohesin: the carcinogenic point of view. Mutat Res 728: 81-87.
34. Moolenaar GF, Visse R, Ortiz-Buysse M, Goosen N, van de Putte P. 1994. Helicase motifs V and VI of the Escherichia coli UvrB protein of the UvrABC endonuclease are essential for the formation of the preincision complex. J Mol Biol 240: 294-307.
35. Ogiwara H, Ui A, Lai MS, Enomoto T, Seki M. 2007. Chl1 and Ctf4 are required for damage-induced recombinations. Biochem Biophys Res Commun 354: 222-226.
36. Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD. 2006. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
37. Parish JL, Rosa J, Wang X, Lahti JM, Doxsey SJ, Androphy EJ. 2006. The DNA helicase ChlR1 is required for sister chromatid cohesion in mammalian cells. J Cell Sci 119: 4857-4865.
38. Petronczki M. 2004. Sister-chromatid cohesion mediated by the alternative RF-CCtf18/Dcc1/Ctf8, the helicase Chl1 and the polymerase-associated protein Ctf4 is essential for chromatid disjunction during meiosis II. J Cell Sci 117: 3547-3559.
39. Poelmann R. 1980. Differential mitosis and degeneration patterns in relation to the alterations in the shape of the embryonic ectoderm of early post-implantation mouse embryos. J Embryol Exp Morphol 55: 33-51.
40. Power MA, Tam PP. 1993. Onset of gastrulation, morphogenesis and somitogenesis in mouse embryos displaying compensatory growth. Anat Embryol (Berl) 187: 493-504.
41. Rantakari P, Nikkila J, Jokela H, Ola R, Pylkas K, Lagerbohm H, Sainio K, Poutanen M, Winqvist R. 2010. Inactivation of Palb2 gene leads to mesoderm differentiation defect and early embryonic lethality in mice. Hum Mol Genet 19: 3021-3029.
42. Rieder CL. 2011. Mitosis in vertebrates: the G2/M and M/A transitions and their associated checkpoints. Chromosome Res 19: 291-306.
43. Sawicki W, Abramczuk J, Blaton O. 1978. DNA synthesis in the second and third cell cycles of mouse preimplantation development. A cytophotometric study. Exp Cell Res 112: 199-205.
44. Sherwood R, Takahashi TS, Jallepalli PV. 2010. Sister acts: coordinating DNA replication and cohesion establishment. Genes Dev 24: 2723-2731.
45. Shibata M, Garcia-Garcia MJ. 2011. The mouse KRAB zinc-finger protein CHATO is required in embryonic-derived tissues to control yolk sac and placenta morphogenesis. Dev Biol 349: 331-341.
46. Skibbens RV. 2004. Chl1p, a DNA helicase-like protein in budding yeast, functions in sister-chromatid cohesion. Genetics 166: 33-42.
47. Solter D, Skreb N, Damjanov I. 1971. Cell cycle analysis in the mouse EGG-cylinder. Exp Cell Res 64: 331-334.
48. Spencer F, Gerring SL, Connelly C, Hieter P. 1990. Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124: 237-249.
49. Ström L, Lindroos HB, Shirahige K, Sjögren C. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16: 1003-1015.
50. Ström L, Karlsson C, Lindroos HB, Wedahl S, Katou Y, Shirahige K, Sjögren C. 2007. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317: 242-245.
51. Suzuki A, la Pompa de JL, Hakem R, Elia A, Yoshida R, Mo R, Nishina H, Chuang T, Wakeham A, Itie A, Koo W, Billia P, Ho A, Fukumoto M, Hui CC, Mak TW. 1997. Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev 11: 1242-1252.
52. Tuteja N, Tuteja R. 2004. Unraveling DNA helicases. Motif, structure, mechanism and function. Eur J Biochem 271: 1849-1863.
53. Uhlmann F. 2009. A matter of choice: the establishment of sister chromatid cohesion. EMBO Rep 10: 1095-1102.
54. Unal E, Heidinger-Pauli JM, Koshland D. 2007. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317: 245-248.
55. van der Lelij P, Chrzanowska KH, Godthelp BC, Rooimans MA, Oostra AB, Stumm M, Zdzienicka MZ, Joenje H, de Winter JP. 2010. Warsaw Breakage Syndrome, a Cohesinopathy Associated with Mutations in the XPD Helicase Family Member DDX11/ChlR1. Am J Hum Genet 86: 262-266.
56. Watson ED, Cross JC. 2005. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20: 180-193.
57. Weiss RS, Enoch T, Leder P. 2000. Inactivation of mouse Hus1 results in genomic instability and impaired responses to genotoxic stress. Genes Dev 14: 1886-1898.
58. Wilkinson DG, Bhatt S, Herrmann BG. 1990. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343: 657-659.
59. Wu Y, Suhasini AN, Brosh RM. 2008. Welcome the Family of FANCJ-like Helicases to the Block of Genome Stability Maintenance Proteins. Cell Mol Life Sci 66: 1209-1222.
60. Wu Y, Sommers JA, Khan I, de Winter JP, Brosh RM. 2012. Biochemical characterization of Warsaw breakage syndrome helicase. J Biol Chem 287: 1007-1021.
61. Yang JT, Rayburn H, Hynes RO. 1993. Embryonic mesodermal defects in alpha 5 integrin-deficient mice. Development 119: 1093-1105.