The DNA damage checkpoint protein RAD9A is essential for male meiosis in the mouse

Journal of Cell Science

Volumn 126, Issue 17, 2013, Pages 3927-3938

  Vasileva, Ana ^a,b   Hopkins, Kevin M ^a   Wang, Xiangyuan ^b   Weisbach, Melissa M ^b   Friedman, Richard A ^b   Wolgemuth, Debra J ^b   Lieberman, Howard B ^a,c  

^a Columbia University Medical Center ^*  (United States)

^b NewYork Presbyterian Hospital   (United States)

^c NONE   (United States)

Author keywords

Double strand breaks; Meiosis; RAD9A; Spermatogenesis

Indexed keywords

BINDING PROTEIN; CELL DNA; CELL PROTEIN; DNA TOPOISOMERASE 2BETA BINDING PROTEIN 1; DOUBLE STRANDED DNA; HISTONE H2AX; RAD9A PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; DIPLOTENE; DOUBLE STRANDED DNA BREAK; GENE DELETION; GERM LINE; MALE; MALE FERTILITY; MEIOSIS; MEIOTIC PROPHASE I; MOUSE; NONHUMAN; PACHYTENE; PRIORITY JOURNAL; PROPHASE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPERMATOCYTE; SPERMATOGONIUM;

DOUBLE-STRAND BREAKS; MEIOSIS; RAD9A; SPERMATOGENESIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; CARRIER PROTEINS; CELL CYCLE CHECKPOINTS; CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; FERTILITY; HISTONES; MALE; MEIOTIC PROPHASE I; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; RECOMBINATIONAL DNA REPAIR; SEQUENCE DELETION; SPERMATOCYTES; SPERMATOGENESIS; TESTIS;

EID: 84883292683     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.126763     Document Type: Article

References (68)

1. Abdu, U., Klovstad, M., Butin-Israeli, V., Bakhrat, A. and Schüpbach, T. (2007). An essential role for Drosophila hus1 in somatic and meiotic DNA damage responses. J. Cell Sci. 120, 1042-1049.
2. Adelfalk, C., Janschek, J., Revenkova, E., Blei, C., Liebe, B., Göb, E., Alsheimer, M., Benavente, R., de Boer, E., Novak, I. et al. (2009). Cohesin SMC1beta protects telomeres in meiocytes. J. Cell Biol. 187, 185-199.
3. Andrews, N. C. and Faller, D. V. (1991). A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19, 2499.
4. Barchi, M., Mahadevaiah, S., Di Giacomo, M., Baudat, F., de Rooij, D. G., Burgoyne, P. S., Jasin, M. and Keeney, S. (2005). Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage. Mol. Cell. Biol. 25, 7203-7215.
5. Bastos, H., Lassalle, B., Chicheportiche, A., Riou, L., Testart, J., Allemand, I. and Fouchet, P. (2005). Flow cytometric characterization of viable meiotic and postmeiotic cells by Hoechst 33342 in mouse spermatogenesis. Cytometry 65A, 40- 49.
6. Batourina, E., Gim, S., Bello, N., Shy, M., Clagett-Dame, M., Srinivas, S., Costantini, F. and Mendelsohn, C. (2001). Vitamin A controls epithelial/ mesenchymal interactions through Ret expression. Nat. Genet. 27, 74-78.
7. Bellani, M. A., Romanienko, P. J., Cairatti, D. A. and Camerini-Otero, R. D. (2005). SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-/- spermatocytes. J. Cell Sci. 118, 3233-3245.
8. Bellvé, A. R., Cavicchia, J. C., Millette, C. F., O'Brien, D. A., Bhatnagar, Y. M. and Dym, M. (1977). Spermatogenic cells of the prepuberal mouse. Isolation and morphological characterization. J. Cell Biol. 74, 68-85.
9. Bolcun-Filas, E., Hall, E., Speed, R., Taggart, M., Grey, C., de Massy, B., Benavente, R. and Cooke, H. J. (2009). Mutation of the mouse Syce1 gene disrupts synapsis and suggests a link between synaptonemal complex structural components and DNA repair. PLoS Genet. 5, e1000393.
10. Broustas, C. G. and Lieberman, H. B. (2012). Contributions of Rad9 to tumorigenesis. J. Cell. Biochem. 113, 742-751.
11. Chang, D. Y. and Lu, A. L. (2005). Interaction of checkpoint proteins Hus1/Rad1/Rad9 with DNA base excision repair enzyme MutY homolog in fission yeast, Schizosaccharomyces pombe. J. Biol. Chem. 280, 408-417.
12. Chung, S. S., Sung, W., Wang, X. and Wolgemuth, D. J. (2004). Retinoic acid receptor alpha is required for synchronization of spermatogenic cycles and its absence results in progressive breakdown of the spermatogenic process. Dev. Dyn. 230, 754- 766.
13. Chung, S. S., Zhu, L. J., Mo, M. Y., Silvestrini, B., Lee, W. M. and Cheng, C. Y. (1998). Evidence for cross-talk between Sertoli and germ cells using selected cathepsins as markers. J. Androl. 19, 686-703.
14. Edelmann, W., Cohen, P. E., Kneitz, B., Winand, N., Lia, M., Heyer, J., Kolodner, R., Pollard, J. W. and Kucherlapati, R. (1999). Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet. 21, 123-127.
15. Eichinger, C. S. and Jentsch, S. (2010). Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1. Proc. Natl. Acad. Sci. USA 107, 11370-11375.
16. Flaggs, G., Plug, A. W., Dunks, K. M., Mundt, K. E., Ford, J. C., Quiggle, M. R., Taylor, E. M., Westphal, C. H., Ashley, T., Hoekstra, M. F. et al. (1997). Atmdependent interactions of a mammalian chk1 homolog with meiotic chromosomes. Curr. Biol. 7, 977-986.
17. Freire, R., Murguýá, J. R., Tarsounas, M., Lowndes, N. F., Moens, P. B. and Jackson, S. P. (1998). Human and mouse homologs of Schizosaccharomyces pombe rad1(+) and Saccharomyces cerevisiae RAD17: linkage to checkpoint control and mammalian meiosis. Genes Dev. 12, 2560-2573.
18. Furuya, K., Poitelea, M., Guo, L., Caspari, T. and Carr, A. M. (2004). Chk1 activation requires Rad9 S/TQ-site phosphorylation to promote association with Cterminal BRCT domains of Rad4TOPBP1. Genes Dev. 18, 1154-1164.
19. Gembka, A., Toueille, M., Smirnova, E., Poltz, R., Ferrari, E., Villani, G. and Hübscher, U. (2007). The checkpoint clamp, Rad9-Rad1-Hus1 complex, preferentially stimulates the activity of apurinic/apyrimidinic endonuclease 1 and DNA polymerase beta in long patch base excision repair. Nucleic Acids Res. 35, 2596-2608.
20. Greer, D. A., Besley, B. D., Kennedy, K. B. and Davey, S. (2003). hRad9 rapidly binds DNA containing double-strand breaks and is required for damage-dependent topoisomerase II beta binding protein 1 focus formation. Cancer Res. 63, 4829-4835.
21. Grushcow, J. M., Holzen, T. M., Park, K. J., Weinert, T., Lichten, M. and Bishop, D. K. (1999). Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics 153, 607-620.
22. Guan, X., Madabushi, A., Chang, D. Y., Fitzgerald, M. E., Shi, G., Drohat, A. C. and Lu, A. L. (2007). The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates DNA repair enzyme TDG glycosylase. Nucleic Acids Res. 35, 6207-6218.
23. Hamer, G., Novak, I., Kouznetsova, A. and Höög, C. (2008a). Disruption of pairing and synapsis of chromosomes causes stage-specific apoptosis of male meiotic cells. Theriogenology 69, 333-339.
24. Hamer, G., Wang, H., Bolcun-Filas, E., Cooke, H. J., Benavente, R. and Höög, C. (2008b). Progression of meiotic recombination requires structural maturation of the central element of the synaptonemal complex. J. Cell Sci. 121, 2445-2451.
25. He, W., Zhao, Y., Zhang, C., An, L., Hu, Z., Liu, Y., Han, L., Bi, L., Xie, Z., Xue, P. et al. (2008). Rad9 plays an important role in DNA mismatch repair through physical interaction with MLH1. Nucleic Acids Res. 36, 6406-6417.
26. Hobbs, R. M., Fagoonee, S., Papa, A., Webster, K., Altruda, F., Nishinakamura, R., Chai, L. and Pandolfi, P. P. (2012). Functional antagonism between Sall4 and Plzf defines germline progenitors. Cell Stem Cell 10, 284-298.
27. Hofmann, E. R., Milstein, S., Boulton, S. J., Ye, M., Hofmann, J. J., Stergiou, L., Gartner, A., Vidal, M. and Hengartner, M. O. (2002). Caenorhabditis elegans HUS-1 is a DNA damage checkpoint protein required for genome stability and EGL- 1-mediated apoptosis. Curr. Biol. 12, 1908-1918.
28. Hong, E. J. and Roeder, G. S. (2002). A role for Ddc1 in signaling meiotic doublestrand breaks at the pachytene checkpoint. Genes Dev. 16, 363-376.
29. Hopkins, K. M., Auerbach, W., Wang, X. Y., Hande, M. P., Hang, H., Wolgemuth, D. J., Joyner, A. L. and Lieberman, H. B. (2004). Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol. Cell. Biol. 24, 7235-7248.
30. Hu, Z., Liu, Y., Zhang, C., Zhao, Y., He, W., Han, L., Yang, L., Hopkins, K. M., Yang, X., Lieberman, H. B. et al. (2008). Targeted deletion of Rad9 in mouse skin keratinocytes enhances genotoxin-induced tumor development. Cancer Res. 68, 5552- 5561.
31. Kleiman, N. J., David, J., Elliston, C. D., Hopkins, K. M., Smilenov, L. B., Brenner, D. J., Worgul, B. V., Hall, E. J. and Lieberman, H. B. (2007). Mrad9 and atm haploinsufficiency enhance spontaneous and X-ray-induced cataractogenesis in mice. Radiat. Res. 168, 567-573.
32. Kobayashi, M., Hirano, A., Kumano, T., Xiang, S. L., Mihara, K., Haseda, Y., Matsui, O., Shimizu, H. and Yamamoto, K. (2004). Critical role for chicken Rad17 and Rad9 in the cellular response to DNA damage and stalled DNA replication. Genes Cells 9, 291-303.
33. Lee, J., Kumagai, A. and Dunphy, W. G. (2007). The Rad9-Hus1-Rad1 checkpoint clamp regulates interaction of TopBP1 with ATR. J. Biol. Chem. 282, 28036-28044.
34. Li, T., Wang, Z., Zhao, Y., He, W., An, L., Liu, S., Liu, Y., Wang, H. and Hang, H. (2013). Checkpoint protein Rad9 plays an important role in nucleotide excision repair. DNA Repair (Amst.) 12, 284-292.
35. Lieberman, H. B. (2006). Rad9, an evolutionarily conserved gene with multiple functions for preserving genomic integrity. J. Cell. Biochem. 97, 690-697.
36. Liu, D., Matzuk, M. M., Sung, W. K., Guo, Q., Wang, P. and Wolgemuth, D. J. (1998). Cyclin A1 is required for meiosis in the male mouse. Nat. Genet. 20, 377-380.
37. Mahadevaiah, S. K., Turner, J. M., Baudat, F., Rogakou, E. P., de Boer, P., Blanco-Rodrýǵuez, J., Jasin, M., Keeney, S., Bonner, W. M. and Burgoyne, P. S. (2001). Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27, 271-276.
38. Mahadevaiah, S. K., Bourc'his, D., de Rooij, D. G., Bestor, T. H., Turner, J. M. and Burgoyne, P. S. (2008). Extensive meiotic asynapsis in mice antagonises meiotic silencing of unsynapsed chromatin and consequently disrupts meiotic sex chromosome inactivation. J. Cell Biol. 182, 263-276.
39. Mäkiniemi, M., Hillukkala, T., Tuusa, J., Reini, K., Vaara, M., Huang, D., Pospiech, H., Majuri, I., Westerling, T., Mäkelä, T. P. et al. (2001). BRCT domain-containing protein TopBP1 functions in DNA replication and damage response. J. Biol. Chem. 276, 30399-30406.
40. Moens, P. B., Kolas, N. K., Tarsounas, M., Marcon, E., Cohen, P. E. and Spyropoulos, B. (2002). The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. J. Cell Sci. 115, 1611-1622.
41. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
42. Niida, H. and Nakanishi, M. (2006). DNA damage checkpoints in mammals. Mutagenesis 21, 3-9.
43. Pandita, R. K., Sharma, G. G., Laszlo, A., Hopkins, K. M., Davey, S., Chakhparonian, M., Gupta, A., Wellinger, R. J., Zhang, J., Powell, S. N. et al. (2006). Mammalian Rad9 plays a role in telomere stability, S- and G2-phase-specific cell survival, and homologous recombinational repair. Mol. Cell. Biol. 26, 1850-1864.
44. Park, M. J., Park, J. H., Hahm, S. H., Ko, S. I., Lee, Y. R., Chung, J. H., Sohn, S. Y., Cho, Y., Kang, L. W. and Han, Y. S. (2009). Repair activities of human 8- oxoguanine DNA glycosylase are stimulated by the interaction with human checkpoint sensor Rad9-Rad1-Hus1 complex. DNA Repair (Amst.) 8, 1190-1200.
45. Perera, D., Perez-Hidalgo, L., Moens, P. B., Reini, K., Lakin, N., Syväoja, J. E., San-Segundo, P. A. and Freire, R. (2004). TopBP1 and ATR colocalization at meiotic chromosomes: role of TopBP1/Cut5 in the meiotic recombination checkpoint. Mol. Biol. Cell 15, 1568-1579.
46. Peretz, G., Arie, L. G., Bakhrat, A. and Abdu, U. (2009). The Drosophila hus1 gene is required for homologous recombination repair during meiosis. Mech. Dev. 126, 677- 686.
47. Peters, A. H., Plug, A. W., van Vugt, M. J. and de Boer, P. (1997). A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res. 5, 66-68.
48. Pittman, D. L., Cobb, J., Schimenti, K. J., Wilson, L. A., Cooper, D. M., Brignull, E., Handel, M. A. and Schimenti, J. C. (1998). Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell 1, 697-705.
49. Revenkova, E., Eijpe, M., Heyting, C., Gross, B. and Jessberger, R. (2001). Novel meiosis-specific isoform of mammalian SMC1. Mol. Cell. Biol. 21, 6984-6998.
50. Revenkova, E., Eijpe, M., Heyting, C., Hodges, C. A., Hunt, P. A., Liebe, B., Scherthan, H. and Jessberger, R. (2004). Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination. Nat. Cell Biol. 6, 555-562.
51. Rogers, R. S., Inselman, A., Handel, M. A. and Matunis, M. J. (2004). SUMO modified proteins localize to the XY body of pachytene spermatocytes. Chromosoma 113, 233-243.
52. Royo, H., Polikiewicz, G., Mahadevaiah, S. K., Prosser, H., Mitchell, M., Bradley, A., de Rooij, D. G., Burgoyne, P. S. and Turner, J. M. (2010). Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr. Biol. 20, 2117-2123.
53. Russell, L. D., Ettlin, R. A., Sinha Hikim, A. P. and Clegg, E. D. (1990). Histological and Histopathological Evaluation of the Testis. Clearwater, FL: Cache River Press.
54. Sadate-Ngatchou, P. I., Payne, C. J., Dearth, A. T. and Braun, R. E. (2008). Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 46, 738-742.
55. Salazar, G., Joshi, A., Liu, D., Wei, H., Persson, J. L. and Wolgemuth, D. J. (2005). Induction of apoptosis involving multiple pathways is a primary response to cyclin A1-deficiency in male meiosis. Dev. Dyn. 234, 114-123.
56. Shi, S. R., Key, M. E. and Kalra, K. L. (1991). Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39, 741-748.
57. Smirnova, E., Toueille, M., Markkanen, E. and Hübscher, U. (2005). The human checkpoint sensor and alternative DNA clamp Rad9-Rad1-Hus1 modulates the activity of DNA ligase I, a component of the long-patch base excision repair machinery. Biochem. J. 389, 13-17.
58. Sotomayor, R. E. and Handel, M. A. (1986). Failure of acrosome assembly in a male sterile mouse mutant. Biol. Reprod. 34, 171-182.
59. Toueille, M., El-Andaloussi, N., Frouin, I., Freire, R., Funk, D., Shevelev, I., Friedrich-Heineken, E., Villani, G., Hottiger, M. O. and Hü bscher, U. (2004). The human Rad9/Rad1/Hus1 damage sensor clamp interacts with DNA polymerase beta and increases its DNA substrate utilisation efficiency: implications for DNA repair. Nucleic Acids Res. 32, 3316-3324.
60. Vasileva, A., Tiedau, D., Firooznia, A., Müller-Reichert, T. and Jessberger, R. (2009). Tdrd6 is required for spermiogenesis, chromatoid body architecture, and regulation of miRNA expression. Curr. Biol. 19, 630-639.
61. Wang, Y. (2003). Epididymal sperm count. Curr. Protoc. Toxicol. 14, 16.6.1-16.6.5.
62. Wang, W., Brandt, P., Rossi, M. L., Lindsey-Boltz, L., Podust, V., Fanning, E., Sancar, A. and Bambara, R. A. (2004). The human Rad9-Rad1-Hus1 checkpoint complex stimulates flap endonuclease 1. Proc. Natl. Acad. Sci. USA 101, 16762- 16767
63. Woolveridge, I., de Boer-Brouwer, M., Taylor, M. F., Teerds, K. J., Wu, F. C. and Morris, I. D. (1999). Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biol. Reprod. 60, 461-470.
64. Yabuta, Y., Ohta, H., Abe, T., Kurimoto, K., Chuma, S. and Saitou, M. (2011). TDRD5 is required for retrotransposon silencing, chromatoid body assembly, and spermiogenesis in mice. J. Cell Biol. 192, 781-795.
65. Yang, F., Wei, Q., Adelstein, R. S. and Wang, P. J. (2012). Non-muscle myosin IIB is essential for cytokinesis during male meiotic cell divisions. Dev. Biol. 369, 356-361.
66. Yu, Q., Brain, J., Laneuville, P. and Osmond, D. G. (2001). Suppressed apoptosis of pre-B cells in bone marrow of pre-leukemic p190bcr/abl transgenic mice. Leukemia 15, 819-827.
67. Zhu, A., Zhou, H., Leloup, C., Marino, S. A., Geard, C. R., Hei, T. K. and Lieberman, H. B. (2005). Differential impact of mouse Rad9 deletion on ionizing radiation-induced bystander effects. Radiat. Res. 164, 655-661.
68. Zhu, A., Zhang, C. X. and Lieberman, H. B. (2008). Rad9 has a functional role in human prostate carcinogenesis. Cancer Res. 68, 1267-1274.