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Published online February 20, 2007
doi:10.1083/jcb.200608130
The Journal of Cell Biology, Vol. 176, No. 5, 581-592
The Rockefeller University Press, 0021-9525 $30.00
© 2007 Kuznetsov et al.
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Article

 RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females

Sergey Kuznetsov1, Manuela Pellegrini2, Kristy Shuda3, Oscar Fernandez-Capetillo2, Yilun Liu4, Betty K. Martin1, Sandra Burkett1, Eileen Southon1, Debananda Pati5, Lino Tessarollo1, Stephen C. West4, Peter J. Donovan6, Andre Nussenzweig2, and Shyam K. Sharan1

1 Mouse Cancer Genetics Program, Center for Cancer Research, National Cancer Institute at Frederick, Frederick, MD 21702
2 Experimental Immunology Branch, National Cancer Institute, Bethesda, MD 20892
3 Kimmel Cancer Center, Thomas Jefferson University, Philadelphia, PA 19107
4 Cancer Research UK, London Research Institute, Clare Hall Laboratories, South Mimms, Herts EN6 3LD, England, UK
5 Department of Pediatrics, Texas Children's Cancer Center, Baylor College of Medicine, Houston, TX 77030
6 Institute for Cell Engineering, Johns Hopkins University, Baltimore, MD 21205

Correspondence to Shyam K. Sharan: ssharan{at}mail.ncifcrf.gov

RAD51C is a member of the RecA/RAD51 protein family, which is known to play an important role in DNA repair by homologous recombination. In mice, it is essential for viability. Therefore, we have generated a hypomorphic allele of Rad51c in addition to a null allele. A subset of mice expressing the hypomorphic allele is infertile. This infertility is caused by sexually dimorphic defects in meiotic recombination, revealing its two distinct functions. Spermatocytes undergo a developmental arrest during the early stages of meiotic prophase I, providing evidence for the role of RAD51C in early stages of RAD51-mediated recombination. In contrast, oocytes can progress normally to metaphase I after superovulation but display precocious separation of sister chromatids, aneuploidy, and broken chromosomes at metaphase II. These defects suggest a possible late role of RAD51C in meiotic recombination. Based on the marked reduction in Holliday junction (HJ) resolution activity in Rad51c-null mouse embryonic fibroblasts, we propose that this late function may be associated with HJ resolution.

M. Pellegrini, K. Shuda, and O. Fernandez-Capetillo contributed equally to this paper.

O. Fernandez-Capetillo's present address is Spanish National Cancer Center, 28029 Madrid, Spain.

P.J. Donovan's present address is Stem Cell Program and Dept. of Biological Chemistry and Developmental and Cell Biology, University of California, Irvine, Irvine, CA 92697.

Abbreviations used in this paper: DSB, double strand break; GV, germinal vesicle; hCG, human chorionic gonadotropin; HJ, Holliday junction; MEF, mouse embryonic fibroblast; neo, neomycin; PGK, phosphoglycerate kinase; PMS, pregnant mare serum; PSSC, precocious separation of sister chromatids; RPA, replication protein A.


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