Mlh1 deficiency in zebrafish results in male sterility and aneuploid as well as triploid progeny in females

Genetics

Volumn 175, Issue 4, 2007, Pages 1561-1569

  Feitsma, Harma ^a   Leal, Marcelo C ^b   Moens, Peter B ^c   Cuppen, Edwin ^a   Schulz, Rüdiger W ^b  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PROTEIN MLH1;

ANEUPLOIDY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; FEMALE; FEMALE FERTILITY; GENOME; MALE; MALE STERILITY; MEIOSIS; METAPHASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROGENY; PROPHASE; SINGLE NUCLEOTIDE POLYMORPHISM; SPERMATOCYTE; SPERMATOGENESIS; TERATOLOGY; TESTIS WEIGHT; TRIPLOIDY; ZEBRA FISH;

ANEUPLOIDY; ANIMALS; BASE SEQUENCE; CROSSING OVER, GENETIC; DNA MISMATCH REPAIR; DNA PRIMERS; DNA REPAIR ENZYMES; FEMALE; INFERTILITY, MALE; MALE; MEIOSIS; MUTATION; PHENOTYPE; POLYPLOIDY; SEMINIFEROUS TUBULES; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; EUKARYOTA;

EID: 34249010580     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.106.068171     Document Type: Article

References (34)

1. BAKER, S. M., A. W. PLUG, T. A. PROLLA, C. E. BRONNER, A. C. HARRIS et al., 1996 Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13: 336-342.
2. CANNAVO, E., G. MARRA, J. SABATES- BELLVER, M. MENIGATTI, S. M. LIPKIN et al., 2005 Expression of the MutL homologue hMLH3 in human cells and its role in DNA mismatch repair. Cancer Res. 65: 10759-10766.
3. CARRASCO, L. A., S. DOROSHOV, D. J. PENMAN and N. BROMAGE, 1998 Long-term, quantitative analysis of gametogenesis in autotriploid rainbow trout, Oncorhynchus mykiss. J. Reprod. Fertil. 113: 197-210.
4. DEKENS, M. P., F. J. PELEGRI, H. M. MAISCHEIN and C. NUSSLEIN-VOLHARD, 2003 The maternal-effect gene futile cycle is essential for pronuclear congression and mitotic spindle assembly in the zebrafish zygote. Development 130: 3907-3916.
5. DE VRIES, S. S., E. B. BAART, M. DEKKER, A. SIEZEN, D. G. DE ROOIJ et al., 1999 Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 13: 523-531.
6. DE VRIES, F. A., E. DE BOER, M. VAN DEN BOSCH, W. M. BAARENDS, M. OOMS et al., 2005 Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 19: 1376-1389.
7. DUFFY, K. T., M. F. MCALEER, W. R. DAVIDSON, L. KARI, C. KARI et al., 2005 Coordinate control of cell cycle regulatory genes in zebra-fish development tested by cyclin D1 knockdown with morpholino phosphorodiamidates and hydroxyprolyl-phosphono peptide nucleic acids. Nucleic Acids Res. 33: 4914-4921.
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.
9. EDELMANN, W., P. E. COHEN, M. KANE, K. LAU, B. MORROW et al., 1996 Meiotic pachytene arrest in MLH1-deficient mice. Cell 85: 1125-1134.
10. EDELMANN, W., P. E. COHEN, B. KNEITZ, N. WINAND, M. LIA et al., 1999 Mammalian MutS homologue 5 is required for chromosome pairing in meiosis. Nat. Genet. 21: 123-127.
11. FELIP, A., F. PIFERRER, M. CARRILLO and S. ZANUY, 2001 Comparison of the gonadal development and plasma levels of sex steroid hormones in diploid and triploid sea bass, Dicentrarchus labrax L. J. Exp. Zool. 290: 384-395.
12. GUILLON, H., F. BAUDAT, C. GREY, R. M. LISKAY and B. DE MASSY, 2005 Crossover and noncrossover pathways in mouse meiosis. Mol. Cell 20: 563-573.
13. GURYEV, V., M. J. KOUDIJS, E. BEREZIKOV, S. L. JOHNSON, R. H. PLASTERK et al., 2006 Genetic variation in the zebrafish. Genome Res. 16: 491-497.
14. HARFE, B. D., B. K. MINESINGER and S. JINKS-ROBERTSON, 2000 Discrete in vivo roles for the MutL homologs Mlh2p and Mlh3p in the removal of frameshift intermediates in budding yeast. Curr. Biol. 10: 145-148.
15. HASEGAWA, T., N. HARADA, K. IKEDA, T. ISHII, I. HOKUTO et al., 1999 Digynic triploid infant surviving for 46 days. Am. J. Med. Genet. 87: 306-310.
16. HENRY, I. M., B. P. DILKES, K. YOUNG, B. WATSON, H. WU et al., 2005 Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics 170: 1979-1988.
17. HUNT, P. A., and T. J. HASSOLD, 2002 Sex matters in meiosis. Science 296: 2181-2183.
18. KELLY, K. O., A. F. DERNBURG, G. M. STANFIELD and A. M. VILLENEUVE, 2000 Caenorhabditis elegans msh-5 is required for both normal and radiation-induced meiotic crossing over but not for completion of meiosis. Genetics 156: 617-630.
19. KNEITZ, B., P. E. COHEN, E. AVDIEVICH, L. ZHU, M. F. KANE et al., 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.
20. KOLAS, N. K., A. SVETLANOV, M. L. LENZI, F. P. MACALUSO, S. M. LIPKIN et al., 2005 Localization of MMR proteins on meiotic chromosomes in mice indicates distinct functions during prophase I. J. Cell Biol. 171: 447-458.
21. KULIEV, A., and Y. VERLINSKY, 2004 Meiotic and mitotic nondisjunction: lessons from preimplantation genetic diagnosis. Hum. Reprod. Update 10: 401-407.
22. LIPKIN, S. M., P. B. MOENS, V. WANG, M. LENZI, D. SHANMUGARAJAH et al., 2002 Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat. Genet. 31: 385-390.
23. MARCON, E., and P. MOENS, 2003 MLH1p and MLH3p localize to precociously induced chiasmata of okadaic-acid-treated mouse spermatocytes. Genetics 165: 2283-2287.
24. MARCON, E., and P. B. MOENS, 2005 The evolution of meiosis: recruitment and modification of somatic DNA-repair proteins. Bio-Essays 27: 795-808.
25. MARIAN, L. A., 1997 Production of triploid transgenic zebrafish, Brachydanio rerio (Hamilton). Indian J. Exp. Biol. 35: 1237-1242.
26. MENEELY, P. M., 1994 Sex determination in polyploids of Caenorhabditis elegans. Genetics 137: 467-481.
27. MIZGIREUV, I. V., I. G. MAJOROVA, V. M. GORODINSKAYA, V. V. KHUDOLEY and S. Y. REVSKOY, 2004 Carcinogenic effect of N-nitrosodimethylamine on diploid and triploid zebrafish (Danio rerio). Toxicol. Pathol. 32: 514-518.
28. MOENS, P. B., 2006 Zebrafish: chiasmata and interference. Genome 49: 205-208.
29. WAGNER, D. S., R. DOSCH, K. A. MINTZER, A. P. WIEMELT and M. C. MULLINS, 2004 Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev. Cell 6: 781-790.
30. WEI, K., R. KUCHERLAPATI and W. EDELMANN, 2002 Mouse models for human DNA mismatch-repair gene defects. Trends Mol. Med. 8: 346-353.
31. WIENHOLDS, E., and R. H. PLASTERK, 2004 Target-selected gene inactivation in zebrafish. Methods Cell Biol. 77: 69-90.
32. WIENHOLDS, E., F. VAN EEDEN, M. KOSTERS, J. MUDDE, R. H. PLASTERK et al., 2003 Efficient target-selected mutagenesis in zebrafish. Genome Res. 13: 2700-2707.
33. WOODS, L. M., C. A. HODGES, E. BAART, S. M. BAKER, M. LISKAY et al., 1999 Chromosomal influence on meiotic spindle assembly: abnormal meiosis I in female Mlh1 mutant mice. J. Cell Biol. 145: 1395-1406.
34. ZALEVSKY, J., A. J. MACQUEEN, J. B. DUFFY, K. J. KEMPHUES and A. M. VILLENEUVE, 1999 Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast. Genetics 153: 1271-1283.