MCM8- and MCM9-Deficient Mice Reveal Gametogenesis Defects and Genome Instability Due to Impaired Homologous Recombination

Molecular Cell

Volumn 47, Issue 4, 2012, Pages 523-534

  Lutzmann, Malik ^a   Grey, Corinne ^a   Traver, Sabine ^a   Ganier, Olivier ^a   Maya Mendoza, Apolinar ^a   Ranisavljevic, Noemie ^a   Bernex, Florence ^b   Nishiyama, Atsuya ^a   Montel, Nathalie ^a   Gavois, Elodie ^a   Forichon, Luc ^a   de Massy, Bernard ^a   Méchali, Marcel ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RAD51 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CHROMATIN; CHROMOSOME DAMAGE; CONTROLLED STUDY; DNA REPAIR; FEMALE; FEMALE STERILITY; FIBROBLAST; GAMETOGENESIS; GENE; GENOMIC INSTABILITY; GONAD; HOMOLOGOUS RECOMBINATION; MALE; MCM8 GENE; MCM9 GENE; MEIOTIC PROPHASE I; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY TUMOR; PHENOTYPE; SPERMATOCYTE; SPERMATOZOON;

ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; FEMALE; FIBROBLASTS; GAMETOGENESIS; GENOMIC INSTABILITY; GERM CELLS; HOMOLOGOUS RECOMBINATION; MALE; MEIOTIC PROPHASE I; MICE; MICE, INBRED C57BL; OVARY; SPERMATOCYTES;

MUS;

EID: 84865368229     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.05.048     Document Type: Article

References (43)

1. Ahmed E.A., van der Vaart A., Barten A., Kal H.B., Chen J., Lou Z., Minter-Dykhouse K., Bartkova J., Bartek J., de Boer P., de Rooij D.G. Differences in DNA double strand breaks repair in male germ cell types: lessons learned from a differential expression of Mdc1 and 53BP1. DNA Repair (Amst.) 2007, 6:1243-1254.
2. Arnaudeau C., Lundin C., Helleday T. DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 2001, 307:1235-1245.
3. Barlow C., Liyanage M., Moens P.B., Tarsounas M., Nagashima K., Brown K., Rottinghaus S., Jackson S.P., Tagle D., Ried T., Wynshaw-Boris A. Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development 1998, 125:4007-4017.
4. Blanton H.L., Radford S.J., McMahan S., Kearney H.M., Ibrahim J.G., Sekelsky J. REC, Drosophila MCM8, drives formation of meiotic crossovers. PLoS Genet. 2005, 1:e40.
5. Byun T.S., Pacek M., Yee M.C., Walter J.C., Cimprich K.A. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 2005, 19:1040-1052.
6. Chan K.L., Palmai-Pallag T., Ying S., Hickson I.D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 2009, 11:753-760.
7. Collis S.J., Barber L.J., Clark A.J., Martin J.S., Ward J.D., Boulton S.J. HCLK2 is essential for the mammalian S-phase checkpoint and impacts on Chk1 stability. Nat. Cell Biol. 2007, 9:391-401.
8. Crossan G.P., van der Weyden L., Rosado I.V., Langevin F., Gaillard P.H., McIntyre R.E., Gallagher F., Kettunen M.I., Lewis D.Y., Brindle K., et al. Disruption of mouse Slx4, a regulator of structure-specific nucleases, phenocopies Fanconi anemia. Nat. Genet. 2011, 43:147-152. Sanger Mouse Genetics Project.
9. de Vries F.A., de Boer E., van den Bosch M., Baarends W.M., Ooms M., Yuan L., Liu J.G., van Zeeland A.A., Heyting C., Pastink A. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 2005, 19:1376-1389.
10. Dobson M.J., Pearlman R.E., Karaiskakis A., Spyropoulos B., Moens P.B. Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 1994, 107:2749-2760.
11. Donovan S., Harwood J., Drury L.S., Diffley J.F. Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast. Proc. Natl. Acad. Sci. USA 1997, 94:5611-5616.
12. Ekholm-Reed S., Mendez J., Tedesco D., Zetterberg A., Stillman B., Reed S.I. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J Cell Biol. 2004, 165:789-800.
13. Eot-Houllier G., Fulcrand G., Watanabe Y., Magnaghi-Jaulin L., Jaulin C. Histone deacetylase 3 is required for centromeric H3K4 deacetylation and sister chromatid cohesion. Genes Dev. 2008, 22:2639-2644.
14. Forand A., Fouchet P., Lahaye J.B., Chicheportiche A., Habert R., Bernardino-Sgherri J. Similarities and differences in the in vivo response of mouse neonatal gonocytes and spermatogonia to genotoxic stress. Biol. Reprod. 2009, 80:860-873.
15. Gozuacik D., Chami M., Lagorce D., Faivre J., Murakami Y., Poch O., Biermann E., Knippers R., Bréchot C., Paterlini-Bréchot P. Identification and functional characterization of a new member of the human Mcm protein family: hMcm8. Nucleic Acids Res. 2003, 31:570-579.
16. Groth A., Ray-Gallet D., Quivy J.P., Lukas J., Bartek J., Almouzni G. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 2005, 17:301-311.
17. Handel M.A., Schimenti J.C. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility. Nat. Rev. Genet. 2010, 11:124-136.
18. Harrison J.C., Haber J.E. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 2006, 40:209-235.
19. Hartford S.A., Luo Y., Southard T.L., Min I.M., Lis J.T., Schimenti J.C. Minichromosome maintenance helicase paralog MCM9 is dispensible for DNA replication but functions in germ-line stem cells and tumor suppression. Proc. Natl. Acad. Sci. USA 2011, 108:17702-17707.
20. Hartge P. Genetics of reproductive lifespan. Nat. Genet. 2009, 41:637-638.
21. He C., Kraft P., Chen C., Buring J.E., Paré G., Hankinson S.E., Chanock S.J., Ridker P.M., Hunter D.J., Chasman D.I. Genome-wide association studies identify loci associated with age at menarche and age at natural menopause. Nat. Genet. 2009, 41:724-728.
22. Holloway J.K., Mohan S., Balmus G., Sun X., Modzelewski A., Borst P.L., Freire R., Weiss R.S., Cohen P.E. Mammalian BTBD12 (SLX4) protects against genomic instability during mammalian spermatogenesis. PLoS Genet. 2011, 7:e1002094.
23. Jackson D.A., Pombo A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol. 1998, 140:1285-1295.
24. Li X., Heyer W.D. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 2008, 18:99-113.
25. Liang Y., Gao H., Lin S.Y., Peng G., Huang X., Zhang P., Goss J.A., Brunicardi F.C., Multani A.S., Chang S., Li K. BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice. PLoS Genet. 2010, 6:e1000826.
26. Liu Y., Richards T.A., Aves S.J. Ancient diversification of eukaryotic MCM DNA replication proteins. BMC Evol. Biol. 2009, 9:60.
27. Lutzmann M., Méchali M. MCM9 binds Cdt1 and is required for the assembly of prereplication complexes. Mol. Cell 2008, 31:190-200.
28. Maiorano D., Lemaître J.M., Méchali M. Stepwise regulated chromatin assembly of MCM2-7 proteins. J. Biol. Chem. 2000, 275:8426-8431.
29. Maiorano D., Cuvier O., Danis E., Méchali M. MCM8 is an MCM2-7-related protein that functions as a DNA helicase during replication elongation and not initiation. Cell 2005, 120:315-328.
30. Maiorano D., Lutzmann M., Méchali M. MCM proteins and DNA replication. Curr. Opin. Cell Biol. 2006, 18:130-136.
31. Maya-Mendoza A., Petermann E., Gillespie D.A., Caldecott K.W., Jackson D.A. Chk1 regulates the density of active replication origins during the vertebrate S phase. EMBO J. 2007, 26:2719-2731.
32. Moens P.B., Chen D.J., Shen Z., Kolas N., Tarsounas M., Heng H.H., Spyropoulos B. Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 1997, 106:207-215.
33. Naim V., Rosselli F. The FANC pathway and mitosis: a replication legacy. Cell Cycle 2009, 8:2907-2911.
34. Petermann E., Helleday T. Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 2010, 11:683-687.
35. Petermann E., Orta M.L., Issaeva N., Schultz N., Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37:492-502.
36. Peters A.H., Plug A.W., van Vugt M.J., de Boer P. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 1997, 5:66-68.
37. Pierce A.J., Johnson R.D., Thompson L.H., Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999, 13:2633-2638.
38. Pittman D.L., Cobb J., Schimenti K.J., Wilson L.A., Cooper D.M., Brignull E., Handel M.A., Schimenti J.C. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1998, 1:697-705.
39. Stolk L., Zhai G., van Meurs J.B., Verbiest M.M., Visser J.A., Estrada K., Rivadeneira F., Williams F.M., Cherkas L., Deloukas P., et al. Loci at chromosomes 13, 19 and 20 influence age at natural menopause. Nat. Genet. 2009, 41:645-647.
40. Takubo K., Hirao A., Ohmura M., Azuma M., Arai F., Nagamatsu G., Suda T. Premeiotic germ cell defect in seminiferous tubules of Atm-null testis. Biochem. Biophys. Res. Commun. 2006, 351:993-998.
41. Volkening M., Hoffmann I. Involvement of human MCM8 in prereplication complex assembly by recruiting hcdc6 to chromatin. Mol. Cell. Biol. 2005, 25:1560-1568.
42. Yang W.L., Cai K.Q., Smedberg J.L., Smith E.R., Klein-Szanto A., Hamilton T.C., Xu X.X. A reduction of cyclooxygenase 2 gene dosage counters the ovarian morphological aging and tumor phenotype in Wv mice. Am. J. Pathol. 2007, 170:1325-1336.
43. Zhang Y.W., Otterness D.M., Chiang G.G., Xie W., Liu Y.C., Mercurio F., Abraham R.T. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 2005, 19:607-618.