Caenorhabditis elegans prom-1 is required for meiotic prophase progression and homologous chromosome pairing

Molecular Biology of the Cell

Volumn 18, Issue 12, 2007, Pages 4911-4920

  Jantsch, Verena ^a   Tang, Lois ^a   Pasierbek, Pawel ^b   Penkner, Alexandra ^a   Nayak, Sudhir ^c   Baudrimont, Antoine ^a   Schedl, Tim ^c   Gartner, Anton ^d   Loidl, Josef ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; F BOX PROTEIN; PROTEIN PROM 1; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; CONTROLLED STUDY; GENE ISOLATION; GENE MUTATION; GENE SEQUENCE; MEIOTIC PROPHASE I; MITOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL;

ALLELES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; CHROMOSOME PAIRING; F-BOX PROTEINS; FERTILITY AGENTS, MALE; HUMANS; MALE; MUTATION; PHYLOGENY; PROPHASE;

CAENORHABDITIS ELEGANS; SYNAPSIS;

EID: 37049023879     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-03-0243     Document Type: Article

References (50)

1. Alpi, A., Pasierbek, P., Gartner, A., and Loidl, J. (2003). Genetic and cytological characterization of the recombination protein RAD-51 in Caenorhabditis elegans. Chromosoma 112, 6-16.
2. Baarends, W. M., Wassenaar, E., Hoogerbrugge, J. W., van Cappellen, G., Roest, H. P., Vreeburg, J., Ooms, M., Hoeijmakers, J.H.J., and Grootegoed, J. A. (2003). Loss of HR6B ubiquitin-conjugating activity results in damaged synaptonemal complex structure and increased crossing-over frequency during the male meiotic prophase. Mol. Cell Biol. 23, 1151-1162.
3. Bhalla, N., and Dernburg, A. F. (2005). A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310, 1683-1686.
4. Borts, R. H., Lichten, M., and Haber, J. E. (1986). Analysis of meiosis-defective mutations in yeast by physical monitoring of recombination. Genetics 113, 551-567.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Colaiácovo, M. P., MacQueen, A. J., Martinez-Perez, E., McDonald, K., Adamo, A., La Volpe, A., and Villeneuve, A. M. (2003). Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev. Cell 5, 463-474.
7. Couteau, F., Nabeshima, K., Villeneuve, A., and Zetka, M. (2004). A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr. Biol. 14, 585-592.
8. Couteau, F., and Zetka, M. (2005). HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 19, 2744-2756.
9. Crittenden, S. L., Leonhard, K. A., Byrd, D. T., and Kimble, J. (2006). Cellular analyses of the mitotic region in the Caenorhabditis elegans adult germ line. Mol. Biol. Cell 17, 3051-3061.
10. Dernburg, A. F., McDonald, K., Moulder, G., Barstead, R., Dresser, M., and Villeneuve, A. M. (1998). Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94, 387-398.
11. Felsenstein, J. (1989). PHYLIP: phylogeny inference package (version 3.2). Cladistics 5, 164-166.
12. Gartner, A., MacQueen, A. J., and Villeneuve, A. M. (2004). Methods for analyzing checkpoint responses in Caenorhabditis elegans. Methods Mol. Biol. 280, 257-274.
13. Gartner, A., Milstein, S., Ahmed, S., Hodgkin, J., and Hengartner, M. O. (2000). A conserved checkpoint pathway mediates DNA damage-induced apoptosis and cell cycle arrest in C. elegans. Mol. Cell 5, 435-443.
14. Hansen, D., Hubbard, E.J.A., and Schedl, T. (2004). Multi-pathway control of the proliferation versus meiotic development decision in the Caenorhabditis elegans germline. Dev. Biol. 268, 342-357
15. Harper, J. W., Burton, J. L., and Solomon, M. J. (2002). The anaphase-promoting complex: it's not just for mitosis any more. Genes Dev. 16, 2179-2206.
16. Henderson, K. A., Kee, K., Maleki, S., Santini, P. A., and Keeney, S. (2006). Cyclin-dependent kinase directly regulates initiation of meiotic recombination. Cell 125, 1321-1332.
17. Hillers, K. J., and Villeneuve, A. M. (2003). Chromosome-wide control of meiotic crossing over in C. elegans. Curr. Biol. 13, 1641-1647.
18. Hochstrasser, M. (2002). New proteases in a ubiquitin stew. Science 298, 250-252.
19. Jones, A. R., Francis, R., and Schedl, T. (1996). GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage- and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180, 165-183.
20. Kamath, R. S. et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237.
21. Kipreos, E. T., Lander, L. E., Wing, J. P., He, W. W., and Hedgecock, E. M. (1996). cul-1 is required for cell cycle exit in C. elegans and identifies a novel gene family. Cell 85, 829-839.
22. Kipreos, E. T., and Pagano, M. (2000). The F-box protein family. Genome Biol. 1, 3002.1-3002.7.
23. Loidl, J. (1991). Coming to grips with a complex matter. A multidisciplinary approach to the synaptonemal complex. Chromosoma 100, 289-292.
24. Loidl, J. (1994). Cytological aspects of meiotic recombination. Experientia 50, 285-294.
25. Loidl, J., and Jones, G. H. (1986). Synaptonemal complex spreading in Allium. I. Triploid A. sphaerocephalon. Chromosoma 93, 420-428.
26. MacQueen, A. J., Colaiácovo, M. P., McDonald, K., and Villeneuve, A. M. (2002). Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 16, 2428-2442.
27. MacQueen, A. J., and Villeneuve, A. M. (2001). Nuclear reorganization and homologous chromosome pairing during meiotic prophase require C. elegans chk-2. Genes Dev. 15, 1674-1687.
28. Martinez-Perez, E., and Villeneuve, A. M. (2005). HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 19, 2727-2743.
29. McKim, K. S. (2005). When size does not matter: pairing sites during meiosis. Cell 123, 989-992.
30. Mello, C. C., Kramer, J. M., Stinchcomb, D., and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
31. Nabeshima, K., Villeneuve, A. M., and Hillers, K. J. (2004). Chromosome-wide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168, 1275-1292.
32. Nayak, S., Santiago, F. E., Jin, H., Lin, D., Schedl, T., and Kipreos, E. T. (2002). The Caenorhabditis elegans Skp1-related gene family: diverse functions in cell proliferation, morphogenesis, and meiosis. Curr. Biol. 12, 277-287.
33. Pasierbek, P., Jantsch, M., Melcher, M., Schleiffer, A., Schweizer, D., and Loidl, J. (2001). A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 15, 1349-1360.
34. Penkner, A., Tang, L., Novatchkova, M., Ladurner, M., Fridkin, A., Gruenbaum, Y., Schweizer, D., Loidl, J., and Jantsch, V. (2007). The nuclear envelope protein matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev. Cell 12, 873-885.
35. Petronczki, M., Siomos, M. F., and Nasmyth, K. (2003). Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112, 423-440.
36. Phillips, C. M., and Dernburg, A. F. (2006). A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 11, 817-829.
37. Phillips, C. M., Wong, C., Bhalla, N., Carlton, P. M., Weiser, P., Meneely, P. M., and Dernburg, A. F. (2005). HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123, 1051-1063.
38. Piano, F., Schetter, A. J., Morton, D. G., Gunsalus, K. C., Reinke, V., Kim, S. K., and Kemphues, K. J. (2002). Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Science 1959-1964.
39. Reinke, V. et al. (2000). A global profile of germline gene expression in C. elegans. Mol. Cell 6, 605-616.
40. Rual, J.-F. et al. (2004). Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14, 2162-2168.
41. Schedl, T. (1997). Developmental Genetics of the Germ Line. In: C. elegans II, ed. D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess, Plainview, NY: Cold Spring Harbor Laboratory Press, 241-269.
42. Schulman, B. A., Carrano, A. C., Jeffrey, P. D., Bowen, Z., Kinnucan, E. R., Finnin, M. S., Elledge, S. J., Harper, J. W., Pagano, M., and Pavletich, N. P. (2000). Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408, 381-386.
43. Schumacher, B., Hanazawa, M., Lee, M.-H., Nayak, S., Volkmann, K., Hofmann, R., Hengartner, M., Schedl, T., and Gartner, A. (2005). Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 120, 357-368.
44. Shinohara, A., Ogawa, H., and Ogawa, T. (1992). Rad51 protein involved in repair and recombination in Saccharomyces cerevisiae is a RecA-like protein. Cell 69, 457-470.
45. Simon-Kayser, B., Seoul, C., Renaudin, K., Jezequel, P., Bouchot, O., Rigaud, J., and Bezieau, S. (2005). Molecular cloning and characterization of FBXO47, a novel gene containing an F-box domain, located in the 17q12 band deleted in papillary renal cell carcinoma. Genes Chromos. Cancer 43, 83-94.
46. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
47. Timmons, L., Court, D. L., and Fire, A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
48. Wang, Y. X., Wu, H., Liang, G. Q., and Yang, M. (2004). Defects in nucleolar migration and synapsis in male prophase I in the ask1-1 mutant of Arabidopsis. Sex. Plant Reprod. 16, 273-282.
49. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H., and Plasterk, R.H.A. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28, 160-164.
50. Zetka, M. C., Kawasaki, I., Strome, S., and Muller, F. (1999). Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 13, 2258-2270.