This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Baarends, W. M.
Right arrow Articles by Grootegoed, J. A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Baarends, W. M.
Right arrow Articles by Grootegoed, J. A.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, February 2003, p. 1151-1162, Vol. 23, No. 4
0270-7306/03/$08.00+0     DOI: 10.1128/MCB.23.4.1151-1162.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Loss of HR6B Ubiquitin-Conjugating Activity Results in Damaged Synaptonemal Complex Structure and Increased Crossing-Over Frequency during the Male Meiotic Prophase

Willy M. Baarends,1* Evelyne Wassenaar,1 Jos W. Hoogerbrugge,1 Gert van Cappellen,1 Henk P. Roest,2 Jan Vreeburg,1 Marja Ooms,1 Jan H. J. Hoeijmakers,2 and J. Anton Grootegoed1

Department of Reproduction and Development,1 Department of Cell Biology and Genetics, Erasmus University Rotterdam, 3000 DR Rotterdam, The Netherlands2

Received 9 July 2002/ Returned for modification 9 August 2002/ Accepted 19 November 2002

The ubiquitin-conjugating enzymes HR6A and HR6B are the two mammalian homologs of Saccharomyces cerevisiae RAD6. In yeast, RAD6 plays an important role in postreplication DNA repair and in sporulation. HR6B knockout mice are viable, but spermatogenesis is markedly affected during postmeiotic steps, leading to male infertility. In the present study, increased apoptosis of HR6B knockout primary spermatocytes was detected during the first wave of spermatogenesis, indicating that HR6B performs a primary role during the meiotic prophase. Detailed analysis of HR6B knockout pachytene nuclei showed major changes in the synaptonemal complexes. These complexes were found to be longer. In addition, we often found depletion of synaptonemal complex proteins from near telomeric regions in the HR6B knockout pachytene nuclei. Finally, we detected an increased number of foci containing the mismatch DNA repair protein MLH1 in these nuclei, reflecting a remarkable and consistent increase (20 to 25%) in crossing-over frequency. The present findings reveal a specific requirement for the ubiquitin-conjugating activity of HR6B in relation to dynamic aspects of the synaptonemal complex and meiotic recombination in spermatocytes.


* Corresponding author. Mailing address: Department of Reproduction and Development, Erasmus University Rotterdam, P.O. Box 1738, 3000 DR Rotterdam, The Netherlands. Phone: 31-10-4087976. Fax: 31-10-4089461. E-mail: baarends{at}endov.fgg.eur.nl.


Molecular and Cellular Biology, February 2003, p. 1151-1162, Vol. 23, No. 4
0022-538X/03/$08.00+0     DOI: 10.1128/MCB.23.4.1151-1162.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.




This article has been cited by other articles:

  • Suryavathi, V., Khattri, A., Gopal, K., Rani, D. S., Panneerdoss, S., Gupta, N. J., Chakravarty, B., Deenadayal, M., Singh, L., Thangaraj, K. (2008). Novel Variants in UBE2B Gene and Idiopathic Male Infertility. J Androl 29: 564-571 [Abstract] [Full Text]  
  • Zamudio, N. M, Chong, S., O'Bryan, M. K (2008). Epigenetic regulation in male germ cells. Reproduction 136: 131-146 [Abstract] [Full Text]  
  • Jantsch, V., Tang, L., Pasierbek, P., Penkner, A., Nayak, S., Baudrimont, A., Schedl, T., Gartner, A., Loidl, J. (2007). Caenorhabditis elegans prom-1 Is Required for Meiotic Prophase Progression and Homologous Chromosome Pairing. Mol. Biol. Cell 18: 4911-4920 [Abstract] [Full Text]  
  • Baarends, W. M., Wassenaar, E., Hoogerbrugge, J. W., Schoenmakers, S., Sun, Z.-W., Grootegoed, J. A. (2007). Increased phosphorylation and dimethylation of XY body histones in the Hr6b-knockout mouse is associated with derepression of the X chromosome. J. Cell Sci. 120: 1841-1851 [Abstract] [Full Text]  
  • Rathke, C., Baarends, W. M., Jayaramaiah-Raja, S., Bartkuhn, M., Renkawitz, R., Renkawitz-Pohl, R. (2007). Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila. J. Cell Sci. 120: 1689-1700 [Abstract] [Full Text]  
  • Sekiguchi, S., Kwon, J., Yoshida, E., Hamasaki, H., Ichinose, S., Hideshima, M., Kuraoka, M., Takahashi, A., Ishii, Y., Kyuwa, S., Wada, K., Yoshikawa, Y. (2006). Localization of Ubiquitin C-Terminal Hydrolase L1 in Mouse Ova and Its Function in the Plasma Membrane to Block Polyspermy. Am. J. Pathol. 169: 1722-1729 [Abstract] [Full Text]  
  • Egydio de Carvalho, C., Colaiacovo, M. P. (2006). SUMO-mediated regulation of synaptonemal complex formation during meiosis. Genes Dev. 20: 1986-1992 [Full Text]  
  • Escalier, D. (2006). Knockout mouse models of sperm flagellum anomalies. Hum Reprod Update 12: 449-461 [Abstract] [Full Text]  
  • Wesoly, J., Agarwal, S., Sigurdsson, S., Bussen, W., Van Komen, S., Qin, J., van Steeg, H., van Benthem, J., Wassenaar, E., Baarends, W. M., Ghazvini, M., Tafel, A. A., Heath, H., Galjart, N., Essers, J., Grootegoed, J. A., Arnheim, N., Bezzubova, O., Buerstedde, J.-M., Sung, P., Kanaar, R. (2006). Differential Contributions of Mammalian Rad54 Paralogs to Recombination, DNA Damage Repair, and Meiosis. Mol. Cell. Biol. 26: 976-989 [Abstract] [Full Text]  
  • Wang, S., Zheng, H., Esaki, Y., Kelly, F., Yan, W. (2006). Cullin3 Is a KLHL10-Interacting Protein Preferentially Expressed During Late Spermiogenesis. Biol. Reprod. 74: 102-108 [Abstract] [Full Text]  
  • Kwon, J., Mochida, K., Wang, Y.-L., Sekiguchi, S., Sankai, T., Aoki, S., Ogura, A., Yoshikawa, Y., Wada, K. (2005). Ubiquitin C-Terminal Hydrolase L-1 Is Essential for the Early Apoptotic Wave of Germinal Cells and for Sperm Quality Control During Spermatogenesis. Biol. Reprod. 73: 29-35 [Abstract] [Full Text]  
  • de Vries, F. A.T., 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. (2005). Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 19: 1376-1389 [Abstract] [Full Text]  
  • Siep, M., Sleddens-Linkels, E., Mulders, S., van Eenennaam, H., Wassenaar, E., Van Cappellen, W. A., Hoogerbrugge, J., Grootegoed, J. A., Baarends, W. M. (2004). Basic helix-loop-helix transcription factor Tcfl5 interacts with the Calmegin gene promoter in mouse spermatogenesis. Nucleic Acids Res 32: 6425-6436 [Abstract] [Full Text]  
  • Donaldson, T. D., Noureddine, M. A., Reynolds, P. J., Bradford, W., Duronio, R. J. (2004). Targeted Disruption of Drosophila Roc1b Reveals Functional Differences in the Roc Subunit of Cullin-dependent E3 Ubiquitin Ligases. Mol. Biol. Cell 15: 4892-4903 [Abstract] [Full Text]  
  • van der Laan, R., Uringa, E.-J., Wassenaar, E., Hoogerbrugge, J. W., Sleddens, E., Odijk, H., Roest, H. P., de Boer, P., Hoeijmakers, J. H. J., Grootegoed, J. A., Baarends, W. M. (2004). Ubiquitin ligase Rad18Sc localizes to the XY body and to other chromosomal regions that are unpaired and transcriptionally silenced during male meiotic prophase. J. Cell Sci. 117: 5023-5033 [Abstract] [Full Text]  
  • Kwon, J., Wang, Y.-L., Setsuie, R., Sekiguchi, S., Sakurai, M., Sato, Y., Lee, W.-W., Ishii, Y., Kyuwa, S., Noda, M., Wada, K., Yoshikawa, Y. (2004). Developmental Regulation of Ubiquitin C-Terminal Hydrolase Isozyme Expression During Spermatogenesis in Mice. Biol. Reprod. 71: 515-521 [Abstract] [Full Text]  
  • Roest, H. P., Baarends, W. M., de Wit, J., van Klaveren, J. W., Wassenaar, E., Hoogerbrugge, J. W., van Cappellen, W. A., Hoeijmakers, J. H. J., Grootegoed, J. A. (2004). The Ubiquitin-Conjugating DNA Repair Enzyme HR6A Is a Maternal Factor Essential for Early Embryonic Development in Mice. Mol. Cell. Biol. 24: 5485-5495 [Abstract] [Full Text]  
  • Tsai-Morris, C.-H., Sheng, Y., Lee, E., Lei, K.-J., Dufau, M. L. (2004). Gonadotropin-regulated testicular RNA helicase (GRTH/Ddx25) is essential for spermatid development and completion of spermatogenesis. Proc. Natl. Acad. Sci. USA 101: 6373-6378 [Abstract] [Full Text]  
  • Kwon, Y. T., Xia, Z., An, J. Y., Tasaki, T., Davydov, I. V., Seo, J. W., Sheng, J., Xie, Y., Varshavsky, A. (2003). Female Lethality and Apoptosis of Spermatocytes in Mice Lacking the UBR2 Ubiquitin Ligase of the N-End Rule Pathway. Mol. Cell. Biol. 23: 8255-8271 [Abstract] [Full Text]  
  • Escalier, D. (2003). New Insights into the Assembly of the Periaxonemal Structures in Mammalian Spermatozoa. Biol. Reprod. 69: 373-378 [Abstract] [Full Text]  
  • Walter, C. A., Walter, R. B., McCarrey, J. R. (2003). Germline Genomes--A Biological Fountain of Youth?. Sci Aging Knowl Environ 2003: pe4-4 [Abstract] [Full Text]