Coordinating cohesion, co-orientation, and congression during meiosis: Lessons from holocentric chromosomes

Genes and Development

Volumn 24, Issue 3, 2010, Pages 219-228

  Schvarzstein, Mara ^a   Wignall, Sarah M ^a   Villeneuve, Anne M ^a  

^a NONE

Author keywords

Co oriention; Cohesion; Congression; Meiosis

Indexed keywords

CAENORHABDITIS ELEGANS; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; GAMETE; HAPLOIDY; MEIOSIS; NONHUMAN; PLOIDY; PRIORITY JOURNAL; PROPHASE; REVIEW; SISTER CHROMATID;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIDS; CHROMOSOME PAIRING; CHROMOSOMES; MEIOSIS; MODELS, BIOLOGICAL;

CAENORHABDITIS ELEGANS;

EID: 76149146726     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1863610     Document Type: Review

References (46)

1. Albertson DG, Thomson JN. 1993. Segregation of holocentric chromosomes at meiosis in the nematode Caenorhabditis elegans. Chromosome Res 1: 15-26.
2. Albertson D, Rose A, Villeneuve A. 1997. Chromosome organization, mitosis and meiosis. In C. elegans II (eds. DL Riddle et al.), pp. 47-48. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Barnes TM, Kohara Y, Coulson A, Hekimi S. 1995. Meiotic recombination, noncoding DNA and genomic organization in Caenorhabditis elegans. Genetics 141: 159-179.
4. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF. 2008. ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4: e1000235. doi: 10.1371/journal.pgen. 1000235.
5. Brunet S, Maria AS, Guillaud P, Dujardin D, Kubiak JZ, Maro B. 1999. Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol 146: 1-12.
6. Chan RC, Severson AF, Meyer BJ. 2004. Condensin restructures chromosomes in preparation for meiotic divisions. J Cell Biol 167: 613-625.
7. Chelysheva L, Diallo S, Vezon D, Gendrot G, Vrielynck N, Belcram K, Rocques N, Marquez-Lema A, Bhatt AM, Horlow C, et al. 2005. AtREC8 and AtSCC3 are essential to the monopolar orientation of the kinetochores during meiosis. J Cell Sci 118: 4621-4632.
8. Couteau F, Zetka M. 2005. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes & Dev 19: 2744-2756.
9. 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: 585-592.
10. de Carvalho CE, Zaaijer S, Smolikov S, Gu Y, Schumacher JM, Colaiacovo MP. 2008. LAB-1 antagonizes the Aurora B kinase in C. elegans. Genes & Dev 22: 2869-2885.
11. d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R. 2009. Turning meiosis into mitosis. PLoS Biol 7: e1000124. doi: 10.1371/journal.pbio.1000124.
12. Ekwall K. 2004. The roles of histone modifications and small RNA in centromere function. Chromosome Res 12: 535-542.
13. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. 2008. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14: 263-274.
14. Hillers KJ. 2004. Crossover interference. Curr Biol 14: R1036-R1037. doi: 10.1016/j.cub.2004.11.038.
15. Howe M, McDonald KL, Albertson DG, Meyer BJ. 2001. HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans holocentric chromosomes. J Cell Biol 153: 1227-1238.
16. Jones GH. 1987. Chiasmata. In Meiosis (ed. EP Moens), pp. 213-244. Academic Press, Orlando, FL.
17. Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M. 2002. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous Chromosomes during meiosis. Curr Biol 12: 798-812.
18. Kitajima TS, Kawashima SA, Watanabe Y. 2004. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 427: 510-517.
19. Kudo NR, Wassmann K, Anger M, Schuh M, Wirth KG, Xu H, Helmhart W, Kudo H, McKay M, Maro B, et al. 2006. Resolution of chiasmata in oocytes requires separase-mediated proteolysis. Cell 126: 135-146.
20. MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF. 2005. Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123: 1037-1050.
21. 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: 2727-2743.
22. Martinez-Perez E, Schvarzstein M, Barroso C, Lightfoot J, Dernburg AF, Villeneuve AM. 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.
23. McNally KL, McNally FJ. 2005. Fertilization initiates the transition from anaphase I to metaphase II during female meiosis in C. elegans. Dev Biol 282: 218-230.
24. Monen J, Maddox PS, Hyndman F, Oegema K, Desai A. 2005. Differential role of CENP-A in the segregation of holocentric C. elegans chromosomes during meiosis and mitosis. Nat Cell Biol 7: 1248-1255.
25. Nabeshima K, Villeneuve AM, Hillers KJ. 2004. Chromosomewide regulation of meiotic crossover formation in Caenorhabditis elegans requires properly assembled chromosome axes. Genetics 168: 1275-1292.
26. Nabeshima K, Villeneuve AM, Colaiacovo MP. 2005. Crossing over is coupled to late meiotic prophase bivalent differentiation through asymmetric disassembly of the SC. J Cell Biol 168: 683-689.
27. Nonomura K, Nakano M, Eiguchi M, Suzuki T, Kurata N. 2006. PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J Cell Sci 119: 217-225.
28. Oegema K, Hyman AA. 2006. Cell division. In WormBook (ed. The C. elegans Research Community), WormBook. doi: 10.1895/wormbook.1.72.1; http://www.wormbook.org.
29. Page SL, Hawley RS. 2003. Chromosome choreography: The meiotic ballet. Science 301: 785-789.
30. Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J. 2001. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes & Dev 15: 1349-1360.
31. Pasierbek P, Fodermayr M, Jantsch V, Jantsch M, Schweizer D, Loidl J. 2003. The Caenorhabditis elegans SCC-3 homologue is required for meiotic synapsis and for proper chromosome disjunction in mitosis and meiosis. Exp Cell Res 289: 245-255.
32. Powers J, Rose DJ, Saunders A, Dunkelbarger S, Strome S, Saxton WM. 2004. Loss of KLP-19 polar ejection force causes misorientation and missegregation of holocentric chromosomes. J Cell Biol 166: 991-1001.
33. Resnick TD, Satinover DL, MacIsaac F, Stukenberg PT, Earnshaw WC, Orr-Weaver TL, Carmena M. 2006. INCENP and Aurora B promote meiotic sister chromatid cohesion through localization of the Shugoshin MEI-S332 in Drosophila. Dev Cell 11: 57-68.
34. Rogers E, Bishop JD, Waddle JA, Schumacher JM, Lin R. 2002. The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J Cell Biol 157: 219-229.
35. Ruchaud S, Carmena M, Earnshaw WC. 2007. Chromosomal passengers: Conducting cell division. Nat Rev Mol Cell Biol 8: 798-812.
36. Sakuno T,Watanabe Y. 2009. Studies of meiosis disclose distinct roles of cohesion in the core centromere and pericentromeric regions. Chromosome Res 17: 239-249.
37. Sakuno T, Tada K, Watanabe Y. 2009. Kinetochore geometry defined by cohesion within the centromere. Nature 458: 852-858.
38. 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: 1763-1778.
39. Shakes DC, Wu JC, Sadler PL, Laprade K, Moore LL, Noritake A, Chu DS. 2009. Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5: e1000611. doi: 10.1371/journal.pgen.1000611.
40. Smolikov S, Eizinger A, Schild-Prufert K, Hurlburt A, McDonald K, Engebrecht J, Villeneuve AM, Colaiacovo MP. 2007. SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics 176: 2015-2025.
41. Viera A, Gomez R, Parra MT, Schmiesing JA, Yokomori K, Rufas JS, Suja JA. 2007. Condensin I reveals new insights on mouse meiotic chromosome structure and dynamics. PLoS One 2: e783. doi: 10.1371/journal.pone.0000783.
42. Wang F, Yoder J, Antoshechkin I, Han M. 2003. Caenorhabditis elegans EVL-14/PDS-5 and SCC-3 are essential for sister chromatid cohesion in meiosis and mitosis. Mol Cell Biol 23: 7698-7707.
43. White MJD. 1973. Animal cytology and evolution. Cambridge University Press, London.
44. Wignall SM, Villeneuve AM. 2009. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat Cell Biol 11: 839-844.
45. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, Boonsanay V, Eckmann CR, Cooke HJ, Jasin M, Keeney S, et al. 2009. Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAA-ATPase. PLoS Genet 5: e1000702. doi: 10.1371/journal.pgen.1000702.
46. Yu HG, Koshland D. 2007. The Aurora kinase Ipl1 maintains the centromeric localization of PP2A to protect cohesin during meiosis. J Cell Biol 176: 911-918.