Meiotic HORMA domain proteins prevent untimely centriole disengagement during caenorhabditis elegans spermatocyte meiosis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 10, 2013, Pages

  Schvarzstein, Mara ^a   Pattabiraman, Divya ^a   Bembenek, Joshua N ^b   Villeneuve, Anne M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HIM 3 PROTEIN; HORMA DOMAIN PROTEIN; HTP 1 PROTEIN; HTP 2 PROTEIN; MEMBRANE PROTEIN; REC 8 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CELL ADHESION; CELLULAR PARAMETERS; CENTRIOLE DISENGAGEMENT; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; SISTER CHROMATID; SPERMATID; SPERMATOCYTE; ZYGOTE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL CYCLE PROTEINS; CENTRIOLES; CHROMOSOMAL PROTEINS, NON-HISTONE; FEMALE; GENES, HELMINTH; MALE; MEIOSIS; MODELS, BIOLOGICAL; MUTATION; SPERMATOCYTES; SPERMATOGENESIS;

EID: 84874608642     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213888110     Document Type: Article

References (45)

1. Manandhar G, Schatten H, Sutovsky P (2005) Centrosome reduction during gametogenesis and its significance. Biol Reprod 72(1):2-13.
2. Nigg EA, Stearns T (2011) The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol 13(10):1154-1160.
3. Wong C, Stearns T (2003) Centrosome number is controlled by a centrosome-intrinsic block to reduplication. Nat Cell Biol 5(6):539-544.
4. Tsou M-FB, et al. (2009) Polo kinase and separase regulate the mitotic licensing of centriole duplication in human cells. Dev Cell 17(3):344-354.
5. Tsou M-FB, Stearns T (2006) Mechanism limiting centrosome duplication to once per cell cycle. Nature 442(7105):947-951.
6. Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res 1(1):15-26.
7. Pelletier L, O'Toole E, Schwager A, Hyman AA, Müller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444(7119):619-623.
8. Leidel S, Gönczy P (2003) SAS-4 is essential for centrosome duplication in C elegans and is recruited to daughter centrioles once per cell cycle. Dev Cell 4(3):431-439.
9. O'Connell KF, et al. (2001) The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105(4):547-558.
10. Wolf N, Hirsh D, McIntosh JR (1978) Spermatogenesis in males of the free-living nematode, Caenorhabditis elegans. J Ultrastruct Res 63(2):155-169.
11. Albertson DG (1984) Formation of the first cleavage spindle in nematode embryos. Dev Biol 101(1):61-72.
12. Schvarzstein M, Wignall SM, Villeneuve AM (2010) Coordinating cohesion, co-orientation, and congression during meiosis: Lessons from holocentric chromosomes. Genes Dev 24(3): 219-228.
13. Couteau F, Zetka M (2005) HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev 19(22):2744-2756.
14. Martinez-Perez E, Villeneuve AM (2005) HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev 19(22):2727-2743.
15. Zetka MC, Kawasaki I, Strome S, Müller 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(17):2258-2270.
16. Couteau F, Goodyer W, Zetka M (2004) Finding and keeping your partner during meiosis. Cell Cycle 3(8):1014-1016.
17. Couteau F, Nabeshima K, Villeneuve A, 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(7):585-592.
18. Goodyer W, et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14(2):263-274.
19. Severson AF, Ling L, van Zuylen V, Meyer BJ (2009) The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev 23(15):1763-1778.
20. Martinez-Perez E, et al. (2008) Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev 22(20):2886-2901.
21. Kitajima TS, Kawashima SA, Watanabe Y (2004) The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427(6974):510-517.
22. Kitajima TS, Ohsugi M, Ellenberg J (2011) Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes. Cell 146(4):568-581.
23. Kateneva AV, Higgins JMG (2009) Shugoshin and PP2A: Collaborating to keep chromosomes connected. Dev Cell 17(3):303-305.
24. Kerrebrock AW, Miyazaki WY, Birnby D, Orr-Weaver TL (1992) The Drosophila mei- S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics 130(4):827-841.
25. Ishiguro T, Tanaka K, Sakuno T, Watanabe Y (2010) Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat Cell Biol 12(5):500-506.
26. de Carvalho CE, et al. (2008) LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes Dev 22(20):2869-2885.
27. Kirkham M, Müller-Reichert T, Oegema K, Grill S, Hyman AA (2003) SAS-4 is a C. elegans centriolar protein that controls centrosome size. Cell 112(4):575-587.
28. Kemp CA, Kopish KR, Zipperlen P, Ahringer J, O'Connell KF (2004) Centrosome maturation and duplication in C. elegans require the coiled-coil protein SPD-2. Dev Cell 6(4):511-523.
29. Pelletier L, et al. (2004) The Caenorhabditis elegans centrosomal protein SPD-2 is required for both pericentriolar material recruitment and centriole duplication. Curr Biol 14(10):863-873.
30. Zhu F, et al. (2008) The mammalian SPD-2 ortholog Cep192 regulates centrosome biogenesis. Curr Biol 18(2):136-141.
31. Shakes DC, et al. (2009) Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5(8):e1000611.
32. Dernburg AF, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94(3):387-398.
33. Colaiácovo MP, et al. (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5(3):463-474.
34. Guan J, Ekwurtzel E, Kvist U, Yuan L (2008) Cohesin protein SMC1 is a centrosomal protein. Biochem Biophys Res Commun 372(4):761-764.
35. Schöckel L, Möckel M, Mayer B, Boos D, Stemmann O (2011) Cleavage of cohesin rings coordinates the separation of centrioles and chromatids. Nat Cell Biol 13(8):966-972.
36. Hayashi M, Chin GM, Villeneuve AM (2007) C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet 3(11):e191.
37. Bembenek JN, White JG, Zheng Y (2010) A role for separase in the regulation of RAB-11-positive vesicles at the cleavage furrow and midbody. Curr Biol 20(3):259-264.
38. Nakamura A, Arai H, Fujita N (2009) Centrosomal Aki1 and cohesin function in separase-regulated centriole disengagement. J Cell Biol 187(5):607-614.
39. Tsou M-FB, Stearns T (2006) Controlling centrosome number: Licenses and blocks. Curr Opin Cell Biol 18(1):74-78.
40. Siomos MF, et al. (2001) Separase is required for chromosome segregation during meiosis I in Caenorhabditis elegans. Curr Biol 11(23):1825-1835.
41. Bembenek JN, et al. (2007) Cortical granule exocytosis in C. elegans is regulated by cell cycle components including separase. Development 134(21):3837-3848.
42. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77(1):71-94.
43. Gönczy P, et al. (1999) Dissection of cell division processes in the one cell stage Caenorhabditis elegans embryo by mutational analysis. J Cell Biol 144(5): 927-946.
44. Oegema K, Desai A, Rybina S, Kirkham M, Hyman AA (2001) Functional analysis of kinetochore assembly in Caenorhabditis elegans. J Cell Biol 153(6):1209-1226.
45. Delattre M, et al. (2004) Centriolar SAS-5 is required for centrosome duplication in C. elegans. Nat Cell Biol 6(7):656-664.