Mutations in Caenorhabditis elegans him-19 show meiotic defects that worsen with age

Molecular Biology of the Cell

Volumn 21, Issue 6, 2010, Pages 885-896

  Tang, Lois ^a,b   Machacek, Thomas ^a   Mamnun, Yasmine M ^a   Penkner, Alexandra ^a   Gloggnitzer, Jiradet ^a,c   Wegrostek, Christina ^a   Konrat, Robert ^a   Jantsch, Michael F ^a   Loidl, Josef ^a   Jantsch, Verena ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b KAROLINSKA INSTITUTE   (Sweden)

^c ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 2; RAD51 PROTEIN; RECF PROTEIN;

AGE DISTRIBUTION; AGING; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CHROMOSOME PAIRING; CONTROLLED STUDY; DEVELOPMENTAL GENE; DNA RECOMBINATION; DOUBLE STRANDED DNA BREAK; FEMALE; GENE MUTATION; HERMAPHRODITISM; HIM 19 GENE; MALE; MEIOSIS; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; SYNAPTONEMAL COMPLEX; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMOSOME PAIRING; DNA BREAKS, DOUBLE-STRANDED; DNA-BINDING PROTEINS; FEMALE; GONADS; HUMANS; MALE; MEIOSIS; MOLECULAR SEQUENCE DATA; MUTATION; OOGENESIS; PHENOTYPE; RECOMBINATION, GENETIC; RNA SPLICING;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 77949442379     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-09-0811     Document Type: Article

References (52)

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. Andux, S., and Ellis, R. E. (2008). Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females. PLoS Genet. 4, e1000295.
3. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
4. Cheng, Z., Coller, J., Parker, R., and Song, H. (2005). Crystal structure and functional analysis of DEAD-box protein Dhh1p. RNA 11, 1258-1270.
5. Colaiacovo, 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.
6. Colaiacovo, M. P., Stanfield, G. M., Reddy, K. C., Reinke, V., Kim, S. K., and Villeneuve, A. M. (2002). A targeted RNAi screen for genes involved in chromosome morphogenesis and nuclear organization in the Caenorhabditis elegans germline. Genetics 162, 113-128.
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. 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.
10. Dernburg, A. F., Zalevsky, J., Colaiacovo, M. P., and Villeneuve, A. M. (2000). Transgene-mediated cosuppression in the C. elegans germ line. Genes Dev. 14, 1578-1583.
11. Eckmann, C. R., Crittenden, S. L., Suh, N., and Kimble, J. (2004). GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168, 147-160.
12. Goodyer, W., Kaitna, S., Couteau, F., Ward, J. D., Boulton, S. J., and Zetka, M. (2008). HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev. Cell 14, 263-274.
13. Hansen, D., Wilson-Berry, L., Dang, T., and Schedl, T. (2004). Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131, 93-104.
14. Hassold, T., and Hunt, P. (2009). Maternal age and chromosomally abnormal pregnancies: what we know and what we wish we knew. Curr. Opin. Pediatr. 21, 703-708.
15. Hodgkin, J. (1986). Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 114, 15-52.
16. Hodgkin, J., Horvitz, H. R., and Brenner, S. (1979). Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91, 67-94.
17. Hubbard, E.J.A., and Greenstein, D. (2005). Introduction to the germ line. In: WormBook, ed. T.C.e.R. Community: WormBook. http://www.wormbook.org.
18. Hunt, P. A., and Hassold, T. J. (2008). Human female meiosis: what makes a good egg go bad? Trends Genet. 24, 86-93.
19. Jantsch, V., Tang, L., Pasierbek, P., Penkner, A., Nayak, S., Baudrimont, A., Schedl, T., Gartner, A., and Loidl, J. (2007). Caenorhabditis elegans prom-1 is required for meiotic prophase progression and homologous chromosome pairing. Mol. Biol. Cell 18, 4911-4920.
20. Kadyk, L. C., and Kimble, J. (1998). Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125, 1803-1813.
21. Kelly, K. O., Dernburg, A. F., Stanfield, G. M., and Villeneuve, A. M. (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.
22. Kimble, J., and Crittenden, S. L. (2007). Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 23, 405-433.
23. Konrat, R. (2009). The protein meta-structure: a novel concept for chemical and molecular biology. Cell Mol. Life Sci. 66, 3625-3639.
24. Loidl, J. (1994). Cytological aspects of meiotic recombination. Experientia 50, 285-294.
25. Loidl, J., Ehrendorfer, F., and Schweizer, D. (1990). EM analysis of meiotic chromosome pairing in a pentaploid Achillea hybrid. Heredity 65, 11-20.
26. MacQueen, A. J., Colaiacovo, 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., Phillips, C. M., Bhalla, N., Weiser, P., Villeneuve, A. M., and Dernburg, A. F. (2005). Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123, 1037-1050.
28. 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.
29. Mair, G. R., Braks, J. A., Garver, L. S., Wiegant, J. C., Hall, N., Dirks, R. W., Khan, S. M., Dimopoulos, G., Janse, C. J., and Waters, A. P. (2006). Regulation of sexual development of Plasmodium by translational repression. Science 313, 667-669.
30. Martinez-Perez, E., Schvarzstein, M., Barroso, C., Lightfoot, J., Dernburg, A. F., and Villeneuve, A. M. (2008). Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 22, 2886-2901.
31. 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.
32. Nabeshima, K., Villeneuve, A. M., and Colaiacovo, M. P. (2005). Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J. Cell Biol. 168, 683-689.
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. Peoples-Holst, T. L., and Burgess, S. M. (2005). Multiple branches of the meiotic recombination pathway contribute independently to homolog pairing and stable juxtaposition during meiosis in budding yeast. Genes Dev. 19, 863-874.
36. Petronczki, M., Siomos, M. F., and Nasmyth, K. (2003). Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112, 423-440.
37. 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.
38. Phillips, C. M., Meng, X., Zhang, L., Chretien, J. H., Urnov, F. D., and Dernburg, A. F. (2009). Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat. Cell Biol. 11, 934-942.
39. 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.
40. Rasmussen, S. W. (1986). Chromosome interlocking during synapsis - a transient disorder. Tokai J. Exp. Clin. Med. 11, 437-451.
41. Rinaldo, C., Bazzicalupo, P., Ederle, S., Hilliard, M., and La Volpe, A. (2002). Roles for Caenorhabditis elegans rad-51 in meiosis and in resistance to ionizing radiation during development. Genetics 160, 471-479.
42. Rinaldo, C., Ederle, S., Rocco, V., and La Volpe, A. (1998). The Caenorhabditis elegans RAD51 homolog is transcribed into two alternative mRNAs potentially encoding proteins of different sizes. Mol. Gen. Genet. 260, 289-294.
43. Rose, A. M., and Baillie, D. L. (1979). The effect of temperature and parental age on recombination and nondisjunction in Caenorhabditis elegans. Genetics 92, 409-418.
44. 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, New York: Cold Spring Harbor Laboratory Press, 241-269.
45. Smolikov, S., Eizinger, A., Hurlburt, A., Rogers, E., Villeneuve, A. M., and Colaiacovo, M. P. (2007a). Synapsis-defective mutants reveal a correlation between chromosome conformation and the mode of double-strand break repair during Caenorhabditis elegans meiosis. Genetics 176, 2027-2033.
46. Smolikov, S., Eizinger, A., Schild-Prufert, K., Hurlburt, A., McDonald, K., Engebrecht, J., Villeneuve, A. M., and Colaiacovo, M. P. (2007b). SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics 176, 2015-2025.
47. Smolikov, S., Schild-Prufert, K., and Colaiacovo, M. P. (2008). CRA-1 uncovers a double-strand break-dependent pathway promoting the assembly of central region proteins on chromosome axes during C. elegans meiosis. PLoS Genet. 4, e1000088.
48. Smolikov, S., Schild-Prufert, K., and Colaiacovo, M. P. (2009). A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet. 5, e1000669.
49. Subramanian, V. V., and Bickel, S. E. (2008). Aging predisposes oocytes to meiotic nondisjunction when the cohesin subunit SMC1 is reduced. PLoS Genet. 4, e1000263.
50. Wicks, S. R., Yeh, R. T., Gish, W. R., Waterston, R. H., and Plasterk, R. H. (2001). Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28, 160-164.
51. Zickler, D. (2006). From early homologue recognition to synaptonemal complex formation. Chromosoma 115, 158-174.
52. Zickler, D., and Kleckner, N. (1999). Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33, 603-754.