Mammalian CNTD1 is critical for meiotic crossover maturation and deselection of excess precrossover sites

Journal of Cell Biology

Volumn 205, Issue 5, 2014, Pages 633-641

  Holloway, J Kim ^a   Sun, Xianfei ^a   Yokoo, Rayka ^b   Villeneuve, Anne M ^b   Cohen, Paula E ^a  

^a Department of Obstetrics Gynecology   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN N TERMINAL DOMAIN CONTAINING 1; CYCLINE; HEI10 PROTEIN; MUTL GAMMA PROTEIN; MUTS GAMMA PROTEIN; PROTEIN MUTL; PROTEIN MUTS; RING FINGER PROTEIN; RNF212 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CROSSING OVER; FEMALE; GENE CONTROL; GENE DISRUPTION; MALE; MEDIATOR RELEASE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALS; CELL DIFFERENTIATION; CHROMOSOME SEGREGATION; CHROMOSOMES; CROSSING OVER, GENETIC; CYCLINS; DNA BREAKS, DOUBLE-STRANDED; LIGASES; MALE; MEIOSIS; MICE; MICE, TRANSGENIC; MUTATION; PHENOTYPE; RECOMBINATION, GENETIC; SPERM COUNT; SPERMATOCYTES; UBIQUITIN-PROTEIN LIGASES;

EID: 84902324306     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201401122     Document Type: Article

References (42)

1. Ashley, T., D. Walpita, and D.G. de Rooij. 2001. Localization of two mammalian cyclin dependent kinases during mammalian meiosis. J. Cell Sci. 114:685-693.
2. Baker, S.M., A.W. Plug, T.A. Prolla, C.E. Bronner, A.C. Harris, X. Yao, D.M. Christie, C. Monell, N. Arnheim, A. Bradley, et al. 1996. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13:336-342. http://dx.doi.org/10.1038/ng0796-336
3. Baudat, F., K. Manova, J.P. Yuen, M. Jasin, and S. Keeney. 2000. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol. Cell. 6:989-998. http://dx.doi.org/10.1016/S1097-2765(00)00098-8
4. Chelysheva, L., D. Vezon, A. Chambon, G. Gendrot, L. Pereira, A. Lemhemdi, N. Vrielynck, S. Le Guin, M. Novatchkova, and M. Grelon. 2012. The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet. 8:e1002799. http://dx.doi.org/10.1371/journal.pgen.1002799
5. Cohen, P.E., S.E. Pollack, and J.W. Pollard. 2006. Genetic analysis of chromosome pairing, recombination, and cell cycle control during first meiotic prophase in mammals. Endocr. Rev. 27:398-426. http://dx.doi.org/10.1210/er.2005-0017
6. Cole, F., L. Kauppi, J. Lange, I. Roig, R. Wang, S. Keeney, and M. Jasin. 2012. Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat. Cell Biol. 14:424-430. http://dx.doi.org/10.1038/ncb2451
7. Dezso, Z., Y. Nikolsky, E. Sviridov, W. Shi, T. Serebriyskaya, D. Dosymbekov, A. Bugrim, E. Rakhmatulin, R.J. Brennan, A. Guryanov, et al. 2008. A comprehensive functional analysis of tissue specificity of human gene expression. BMC Biol. 6:49. http://dx.doi.org/10.1186/1741-7007-6-49
8. Eaker, S., J. Cobb, A. Pyle, and M.A. Handel. 2002. Meiotic prophase abnormalities and metaphase cell death in MLH1-deficient mouse spermatocytes: insights into regulation of spermatogenic progress. Dev. Biol. 249:85-95. http://dx.doi.org/10.1006/dbio.2002.0708
9. Edelmann, W., P.E. Cohen, M. Kane, K. Lau, B. Morrow, S. Bennett, A. Umar, T. Kunkel, G. Cattoretti, R. Chaganti, et al. 1996. Meiotic pachytene arrest in MLH1-deficient mice. Cell. 85:1125-1134. http://dx.doi.org/10.1016/S0092-8674(00)81312-4
10. Evans, E.P., G. Breckon, and C.E. Ford. 1964. An air-drying method for meiotic preparations from mammalian testes. Cytogenetics. 3:289-294. http://dx.doi.org/10.1159/000129818
11. Holloway, J.K., J. Booth, W. Edelmann, C.H. McGowan, and P.E. Cohen. 2008. MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet. 4:e1000186. http://dx.doi.org/10.1371/journal.pgen.1000186
12. Holloway, J.K., M.A. Morelli, P.L. Borst, and P.E. Cohen. 2010. Mammalian BLM helicase is critical for integrating multiple pathways of meiotic recombination. J. Cell Biol. 188:779-789. http://dx.doi.org/10.1083/jcb.200909048
13. Holloway, J.K., S. Mohan, G. Balmus, X. Sun, A. Modzelewski, P.L. Borst, R. Freire, R.S. Weiss, and P.E. Cohen. 2011. Mammalian BTBD12 (SLX4) protects against genomic instability during mammalian spermatogenesis. PLoS Genet. 7:e1002094. http://dx.doi.org/10.1371/journal.pgen.1002094
14. Hunter, N., and N. Kleckner. 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell. 106:59-70. http://dx.doi.org/10.1016/S0092-8674(01)00430-5
15. Hunter, N., G.V. Börner, M. Lichten, and N. Kleckner. 2001. Gamma-H2AX illuminates meiosis. Nat. Genet. 27:236-238. http://dx.doi.org/10.1038/85781
16. Kneitz, B., P.E. Cohen, E. Avdievich, L. Zhu, M.F. Kane, H. Hou Jr., R.D. Kolodner, R. Kucherlapati, J.W. Pollard, and W. Edelmann. 2000. MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev. 14:1085-1097.
17. Kolas, N.K., L. Yuan, C. Hoog, H.H. Heng, E. Marcon, and P.B. Moens. 2004. Male mouse meiotic chromosome cores deficient in structural proteins SYCP3 and SYCP2 align by homology but fail to synapse and have possible impaired specificity of chromatin loop attachment. Cytogenet. Genome Res. 105:182-188. http://dx.doi.org/10.1159/000078188
18. Kolas, N.K., A. Svetlanov, M.L. Lenzi, F.P. Macaluso, S.M. Lipkin, R.M. Liskay, J. Greally, W. Edelmann, and P.E. Cohen. 2005. Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I. J. Cell Biol. 171:447-458. http://dx.doi.org/10.1083/jcb.200506170
19. Lipkin, S.M., P.B. Moens, V. Wang, M. Lenzi, D. Shanmugarajah, A. Gilgeous, J. Thomas, J. Cheng, J.W. Touchman, E.D. Green, et al. 2002. Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31:385-390.
20. Lyndaker, A.M., P.X. Lim, J.M. Mleczko, C.E. Diggins, J.K. Holloway, R.J. Holmes, R. Kan, D.H. Schlafer, R. Freire, P.E. Cohen, and R.S. Weiss. 2013. Conditional inactivation of the DNA damage response gene Hus1 in mouse testis reveals separable roles for components of the RAD9-RAD1-HUS1 complex in meiotic chromosome maintenance. PLoS Genet. 9: e1003320. http://dx.doi.org/10.1371/journal.pgen.1003320
21. Mahadevaiah, S.K., J.M. Turner, F. Baudat, E.P. Rogakou, P. de Boer, J. Blanco-Rodríguez, M. Jasin, S. Keeney, W.M. Bonner, and P.S. Burgoyne. 2001. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27:271-276. http://dx.doi.org/10.1038/85830
22. Marcon, E., and P. Moens. 2003. MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics. 165:2283-2287.
23. Moens, P.B., D.J. Chen, Z. Shen, N.K. Kolas, M. Tarsounas, H.H. Heng, and B. Spyropoulos. 1997. Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma. 106:207-215. http://dx.doi.org/10.1007/s004120050241
24. Peters, A.H., A.W. Plug, M.J. van Vugt, and P. de Boer. 1997. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5:66-68. http://dx.doi.org/10.1023/A:1018445520117
25. Pittman, D.L., J. Cobb, K.J. Schimenti, L.A. Wilson, D.M. Cooper, E. Brignull, M.A. Handel, and J.C. Schimenti. 1998. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germlinespecific RecA homolog. Mol. Cell. 1:697-705. http://dx.doi.org/10.1016/S1097-2765(00)80069-6
26. Qiao, H., H.B. Prasada Rao, Y. Yang, J.H. Fong, J.M. Cloutier, D.C. Deacon, K.E. Nagel, R.K. Swartz, E. Strong, J.K. Holloway, et al. 2014. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat. Genet. 46:194-199. http://dx.doi.org/10.1038/ng.2858
27. Reynolds, A., H. Qiao, Y. Yang, J.K. Chen, N. Jackson, K. Biswas, J.K. Holloway, F. Baudat, B. de Massy, J. Wang, et al. 2013. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45:269-278. http://dx.doi.org/10.1038/ng.2541
28. Santucci-Darmanin, S., D. Walpita, F. Lespinasse, C. Desnuelle, T. Ashley, and V. Paquis-Flucklinger. 2000. MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB J. 14:1539-1547. http://dx.doi.org/10.1096/fj.14.11.1539
29. Schalk, J.A., A.J. Dietrich, A.C. Vink, H.H. Offenberg, M. van Aalderen, and C. Heyting. 1998. Localization of SCP2 and SCP3 protein molecules within synaptonemal complexes of the rat. Chromosoma. 107:540-548. http://dx.doi.org/10.1007/s004120050340
30. Schmekel, K., R.L. Meuwissen, A.J. Dietrich, A.C. Vink, J. van Marle, H. van Veen, and C. Heyting. 1996. Organization of SCP1 protein molecules within synaptonemal complexes of the rat. Exp. Cell Res. 226:20-30. http://dx.doi.org/10.1006/excr.1996.0198
31. Singh, M.K., E. Nicolas, W. Gherraby, D. Dadke, S. Lessin, and E.A. Golemis. 2007. HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene. 26:4825-4832. http://dx.doi.org/10.1038/sj.onc.1210282
32. -/- mice. Exp. Hematol. 36:273-282. http://dx.doi.org/10.1016/j.exphem.2007.11.006
33. Strong, E.R., and J.C. Schimenti. 2010. Evidence implicating CCNB1IP1, a RING domain-containing protein required for meiotic crossing over in mice, as an E3 SUMO ligase. Genes (Basel). 1:440-451. http://dx.doi.org/10.3390/genes1030440
34. Svetlanov, A., F. Baudat, P.E. Cohen, and B. de Massy. 2008. Distinct functions of MLH3 at recombination hot spots in the mouse. Genetics. 178:1937-1945. http://dx.doi.org/10.1534/genetics.107.084798
35. Thorrez, L., K. Van Deun, L.C. Tranchevent, L. Van Lommel, K. Engelen, K. Marchal, Y. Moreau, I. Van Mechelen, and F. Schuit. 2008. Using ribosomal protein genes as reference: a tale of caution. PLoS ONE. 3:e1854. http://dx.doi.org/10.1371/journal.pone.0001854
36. Toby, G.G., W. Gherraby, T.R. Coleman, and E.A. Golemis. 2003. A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol. Cell. Biol. 23:2109-2122. http://dx.doi.org/10.1128/MCB.23.6.2109-2122.2003
37. Uroz, L., O. Rajmil, and C. Templado. 2008. Premature separation of sister chromatids in human male meiosis. Hum. Reprod. 23:982-987. http://dx.doi.org/10.1093/humrep/dem427
38. Wang, K., M. Wang, D. Tang, Y. Shen, C. Miao, Q. Hu, T. Lu, and Z. Cheng. 2012. The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genet. 8:e1002809. http://dx.doi.org/10.1371/journal.pgen.1002809
39. Ward, J.O., L.G. Reinholdt, W.W. Motley, L.M. Niswander, D.C. Deacon, L.B. Griffin, K.K. Langlais, V.L. Backus, K.J. Schimenti, M.J. O'Brien, et al. 2007. Mutation in mouse hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet. 3:e139. http://dx.doi.org/10.1371/journal.pgen.0030139
40. Yokoo, R., K.A. Zawadzki, K. Nabeshima, M. Drake, S. Arur, and A.M. Villeneuve. 2012. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 149:75-87. http://dx.doi.org/10.1016/j.cell.2012.01.052
41. Yoshida, K., G. Kondoh, Y. Matsuda, T. Habu, Y. Nishimune, and T. Morita. 1998. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell. 1:707-718. http://dx.doi.org/10.1016/S1097-2765(00)80070-2
42. Yuan, L., J.G. Liu, J. Zhao, E. Brundell, B. Daneholt, and C. Höög. 2000. The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility. Mol. Cell. 5:73-83. http://dx.doi.org/10.1016/S1097-2765(00)80404-9