Genome instability and embryonic developmental defects in RMI1 deficient mice

DNA Repair

Volumn 12, Issue 10, 2013, Pages 835-843

  Guiraldelli, Michel F ^a   Eyster, Craig ^a   Pezza, Roberto J ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

DNA repair; Genome instability; Homologous recombination

Indexed keywords

PROTEIN RMI1; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL PROLIFERATION; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DNA CONTENT; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; EMBRYO DEVELOPMENT; FIBROBLAST; GENOMIC INSTABILITY; LETHALITY; MICRONUCLEUS; MITOSIS INDEX; MOUSE; NONHUMAN; PRIORITY JOURNAL;

DNA REPAIR; GENOME INSTABILITY; HOMOLOGOUS RECOMBINATION;

ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; FEMALE; GENOMIC INSTABILITY; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOTIC INDEX; NUCLEAR PROTEINS;

MUS;

EID: 84885371004     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.07.004     Document Type: Article

References (48)

1. Myung K., Datta A., Chen C., Kolodner R.D. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nature Genetics 2001, 27:113-116.
2. Chaganti R.S., Schonberg S., German J. A manyfold increase in sister chromatid exchanges in Bloom's syndrome lymphocytes. Proceedings of the National Academy of Sciences of the USA 1974, 71:4508-4512.
3. Wang W., Seki M., Narita Y., Sonoda E., Takeda S., Yamada K., Masuko T., Katada T., Enomoto T. Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO Journal 2000, 19:3428-3435.
4. Mankouri H.W., Hickson I.D. Understanding the roles of RecQ helicases in the maintenance of genome integrity and suppression of tumorigenesis. Biochemical Society Transactions 2004, 32:957-958.
5. German J. Cytological evidence for crossing-over in vitro in human lymphoid cells. Science 1964, 144:298-301.
6. Jessop L., Rockmill B., Roeder G.S., Lichten M. Meiotic chromosome synapsis-promoting proteins antagonize the anti-crossover activity of sgs1. PLoS Genetics 2006, 2:e155.
7. Dayani Y., Simchen G., Lichten M. Meiotic recombination intermediates are resolved with minimal crossover formation during return-to-growth, an analogue of the mitotic cell cycle. PLoS Genetics 2011, 7:e1002083.
8. De Muyt A., Jessop L., Kolar E., Sourirajan A., Chen J., Dayani Y., Lichten M. BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Molecular Cell 2012, 46:43-53.
9. Ellis N.A., Groden J., Ye T.Z., Straughen J., Lennon D.J., Ciocci S., Proytcheva M., German J. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 1995, 83:655-666.
10. German J. Bloom syndrome: a Mendelian prototype of somatic mutational disease. Medicine (Baltimore) 1993, 72:393-406.
11. Payne M., Hickson I.D. Genomic instability and cancer: lessons from analysis of Bloom's syndrome. Biochemical Society Transactions 2009, 37:553-559.
12. Babbe H., Chester N., Leder P., Reizis B. The Bloom's syndrome helicase is critical for development and function of the alphabeta T-cell lineage. Molecular and Cellular Biology 2007, 27:1947-1959.
13. Yin J., Sobeck A., Xu C., Meetei A.R., Hoatlin M., Li L., Wang W. BLAP75, an essential component of Bloom's syndrome protein complexes that maintain genome integrity. EMBO Journal 2005, 24:1465-1476.
14. Chester N., Kuo F., Kozak C., O'Hara C.D., Leder P. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes & Development 1998, 12:3382-3393.
15. Wu L., Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 2003, 426:870-874.
16. Plank J.L., Wu J., Hsieh T.S. Topoisomerase IIIalpha and Bloom's helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proceedings of the National Academy of Sciences of the USA 2006, 103:11118-11123.
17. Hickson I.D. RecQ helicases: caretakers of the genome. Nature Reviews Cancer 2003, 3:169-178.
18. Bugreev D.V., Yu X., Egelman E.H., Mazin A.V. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes & Development 2007, 21:3085-3094.
19. Bugreev D.V., Mazina O.M., Mazin A.V. Bloom syndrome helicase stimulates RAD51 DNA strand exchange activity through a novel mechanism. Journal of Biological Chemistry 2009, 284:26349-26359.
20. Raynard S., Bussen W., Sung P. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. Journal of Biological Chemistry 2006, 281:13861-13864.
21. Raynard S., Zhao W., Bussen W., Lu L., Ding Y.Y., Busygina V., Meetei A.R., Sung P. Functional role of BLAP75 in BLM-topoisomerase IIIalpha-dependent Holliday junction processing. Journal of Biological Chemistry 2008, 283:15701-15708.
22. Bussen W., Raynard S., Busygina V., Singh A.K., Sung P. Holliday junction processing activity of the BLM-Topo IIIalpha-BLAP75 complex. Journal of Biological Chemistry 2007, 282:31484-31492.
23. Daley J.M., Niu H., Sung P. Roles of DNA helicases in the mediation and regulation of homologous recombination. Advances in Experimental Medicine and Biology 2013, 767:185-202.
24. Xu D., Guo R., Sobeck A., Bachrati C.Z., Yang J., Enomoto T., Brown G.W., Hoatlin M.E., Hickson I.D., Wang W. RMI, a new OB-fold complex essential for Bloom syndrome protein to maintain genome stability. Genes & Development 2008, 22:2843-2855.
25. Meetei A.R., Sechi S., Wallisch M., Yang D., Young M.K., Joenje H., Hoatlin M.E., Wang W. A multiprotein nuclear complex connects Fanconi anemia and Bloom syndrome. Molecular and Cellular Biology 2003, 23:3417-3426.
26. Singh T.R., Ali A.M., Busygina V., Raynard S., Fan Q., Du C.H., Andreassen P.R., Sung P., Meetei A.R. BLAP18/RMI2, a novel OB-fold-containing protein, is an essential component of the Bloom helicase-double Holliday junction dissolvasome. Genes & Development 2008, 22:2856-2868.
27. Mullen J.R., Nallaseth F.S., Lan Y.Q., Slagle C.E., Brill S.J. Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Molecular and Cellular Biology 2005, 25:4476-4487.
28. Cejka P., Plank J.L., Bachrati C.Z., Hickson I.D., Kowalczykowski S.C. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nature Structural & Molecular Biology 2010, 17:1377-1382.
29. Yang J., Bachrati C.Z., Ou J., Hickson I.D., Brown G.W. Human topoisomerase IIIalpha is a single-stranded DNA decatenase that is stimulated by BLM and RMI1. Journal of Biological Chemistry 2010, 285:21426-21436.
30. Chang M., Bellaoui M., Zhang C., Desai R., Morozov P., Delgado-Cruzata L., Rothstein R., Freyer G.A., Boone C., Brown G.W. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO Journal 2005, 24:2024-2033.
31. Yang J., O'Donnell L., Durocher D., Brown G.W. RMI1 promotes DNA replication fork progression and recovery from replication fork stress. Molecular and Cellular Biology 2012.
32. Ralf C., Hickson I.D., Wu L. The Bloom's syndrome helicase can promote the regression of a model replication fork. Journal of Biological Chemistry 2006, 281:22839-22846.
33. Hoadley K.A., Xue Y., Ling C., Takata M., Wang W., Keck J.L. Defining the molecular interface that connects the Fanconi anemia protein FANCM to the Bloom syndrome dissolvasome. Proceedings of the National Academy of Sciences of the USA 2012, 109:4437-4442.
34. Deans A.J., West S.C. FANCM connects the genome instability disorders Bloom's syndrome and Fanconi anemia. Molecular Cell 2009, 36:943-953.
35. Li W., Wang J.C. Mammalian DNA topoisomerase IIIalpha is essential in early embryogenesis. Proceedings of the National Academy of Sciences of the USA 1998, 95:1010-1013.
36. Suwa A., Yoshino M., Yamazaki C., Naitou M., Fujikawa R., Matsumoto S., Kurama T., Shimokawa T., Aramori I. RMI1 deficiency in mice protects from diet and genetic-induced obesity. FEBS Journal 2010, 277:677-686.
37. Chen H., You M.J., Jiang Y., Wang W., Li L. RMI1 attenuates tumor development and is essential for early embryonic survival. Molecular Carcinogenesis 2011, 50:80-88.
38. Darzynkiewicz Z. Critical aspects in analysis of cellular DNA content. Current Protocols in Cytometry 2011, Chapter7, Unit 7.2.
39. Wang R.H., Sengupta K., Li C., Kim H.S., Cao L., Xiao C., Kim S., Xu X., Zheng Y., Chilton B., Jia R., Zheng Z.M., Appella E., Wang X.W., Ried T., Deng C.X. Impaired DNA damage response, genome instability, and tumorigenesis in SIRT1 mutant mice. Cancer Cell 2008, 14:312-323.
40. Ghosh S., Schroeter D., Paweletz N. Okadaic acid overrides the S-phase check point and accelerates progression of G2-phase to induce premature mitosis in HeLa cells. Experimental Cell Research 1996, 227:165-169.
41. Wiltshire T., Park C., Caldwell K.A., Handel M.A. Induced premature G2/M-phase transition in pachytene spermatocytes includes events unique to meiosis. Developmental Biology 1995, 169:557-567.
42. Chu W.K., Hickson I.D. RecQ helicases: multifunctional genome caretakers. Nature Reviews Cancer 2009, 9:644-654.
43. Fenech M. The micronucleus assay determination of chromosomal level DNA damage. Methods in Molecular Biology 2008, 410:185-216.
44. Guo R., Xu D., Wang W. Identification and analysis of new proteins involved in the DNA damage response network of Fanconi anemia and Bloom syndrome. Methods 2009, 48:72-79.
45. Chen C.F., Brill S.J. Binding and activation of DNA topoisomerase III by the Rmi1 subunit. Journal of Biological Chemistry 2007, 282:28971-28979.
46. Wu L., Bachrati C.Z., Ou J., Xu C., Yin J., Chang M., Wang W., Li L., Brown G.W., Hickson I.D. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proceedings of the National Academy of Sciences of the USA 2006, 103:4068-4073.
47. Ashton T.M., Mankouri H.W., Heidenblut A., McHugh P.J., Hickson I.D. Pathways for Holliday junction processing during homologous recombination in Saccharomyces cerevisiae. Molecular and Cellular Biology 2011, 31:1921-1933.
48. Rosin M.P., German J. Evidence for chromosome instability in vivo in Bloom syndrome: increased numbers of micronuclei in exfoliated cells. Human Genetics 1985, 71:187-191.