The synaptonemal complex protein Zip1 promotes bi-orientation of centromeres at meiosis I

PLoS Genetics

Volumn 5, Issue 12, 2009, Pages

  Gladstone, Mara N ^a,b,d   Obeso, David ^a,c   Chuong, Hoa ^a   Dawson, Dean S ^a,c  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b TUFTS UNIVERSITY   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN ZIP1; PROTEIN ZIP2; PROTEIN ZIP3; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; SLC39A1 PROTEIN, HUMAN;

ARTICLE; CENTROMERE; CHROMOSOME; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; INFERTILITY; MEIOSIS; MENTAL DEFICIENCY; MUSCLE SPINDLE AFFERENT NERVE; NONHUMAN; PACHYTENE; PROTEIN LOCALIZATION; SYNAPTONEMAL COMPLEX; HUMAN; PHYSIOLOGY;

CATION TRANSPORT PROTEINS; CENTROMERE; HUMANS; MEIOSIS;

EID: 74249084585     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000771     Document Type: Article

References (55)

1. Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477-487.
2. Pinsky BA, Biggins S (2005) The spindle checkpoint: tension versus attachment. Trends Cell Biol 15: 486-493.
3. Cheslock PS, Kemp BJ, Boumil RM, Dawson DS (2005) The roles of MAD1, MAD2 and MAD3 in meiotic progression and the segregation of nonexchange chromosomes. Nat Genet 37: 756-760.
4. Kouznetsova A, Lister L, Nordenskjold M, Herbert M, Hoog C (2007) Biorientation of achiasmatic chromosomes in meiosis I oocytes contributes to aneuploidy in mice. Nat Genet 39: 966-968.
5. LeMaire-Adkins R, Radke K, Hunt PA (1997) Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females. J Cell Biol 139: 1611-1619.
6. Stewart MN, Dawson DS (2004) Potential roles for centromere pairing in meiotic chromosome segregation. Cell Cycle 3: 1232-1234.
7. Stewart MN, Dawson DS (2008) Changing partners: moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet 24: 564-573.
8. Östergren G (1951) The mechanism of co-orientation in bivalents and multivalents. Hereditas 37: 85-156.
9. Dernburg AF, Sedat JW, Hawley RS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86: 135-146.
10. Ding DQ, Yamamoto A, Haraguchi T, Hiraoka Y (2004) Dynamics of homologous chromosome pairing during meiotic prophase in fission yeast. Dev Cell 6: 329-341.
11. Davis L, Smith GR (2003) Nonrandom homolog segregation at meiosis I in Schizosaccharomyces pombe mutants lacking recombination. Genetics 163: 857-874.
12. Kemp B, Boumil RM, Stewart MN, Dawson DS (2004) A role for centromere pairing in meiotic chromosome segregation. Genes Dev 18: 1946-1951.
13. Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308: 870-873.
14. Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72: 365-378.
15. Kaback DB, Guacci V, Barber D, Mahon JW (1992) Chromosome sizedependent control of meiotic recombination. Science 256: 228-232.
16. Maxfield Boumil R, Kemp B, Angelichio M, Nilsson-Tillgren T, Dawson DS (2003) Meiotic segregation of a homeologous chromosome pair. Mol Genet Genomics 268: 750-760.
17. Hayashi A, Ogawa H, Kohno K, Gasser SM, Hiraoka Y (1998) Meiotic behaviours of chromosomes and microtubules in budding yeast: relocalization of centromeres and telomeres during meiotic prophase. Genes Cells 3: 587-601.
18. Jin Q, Trelles-Sticken E, Scherthan H, Loidl J (1998) Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J Cell Biol 141: 21-29.
19. Aragon-Alcaide L, Strunnikov AV (2000) Functional dissection of in vivo interchromosome association in Saccharomyces cerevisiae. Nat Cell Biol 2: 812-818.
20. Agarwal S, Roeder GS (2000) Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102: 245-255.
21. Chua PR, Roeder GS (1998) Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93: 349-359.
22. Novak JE, Ross-Macdonald PB, Roeder GS (2001) The budding yeast Msh4 protein functions in chromosome synapsis and the regulation of crossover distribution. Genetics 158: 1013-1025.
23. Borner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117: 29-45.
24. Tsubouchi T, Macqueen AJ, Roeder GS (2008) Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22: 3217-3226.
25. Tsubouchi T, Zhao H, Roeder GS (2006) The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2. Dev Cell 10: 809-819.
26. Meluh PB, Koshland D (1997) Budding yeast centromere composition and assembly as revealed by in vivo cross-linking. Genes Dev 11: 3401-3412.
27. Chen SY, Tsubouchi T, Rockmill B, Sandler JS, Richards DR, et al. (2008) Global analysis of the meiotic crossover landscape. Dev Cell 15: 401-415.
28. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479-485.
29. Byers B, Goetsch L (1975) Electron microscopic observations on the meiotic karyotype of diploid and tetraploid Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 72: 5056-5060.
30. Dresser ME, Giroux CN (1988) Meiotic chromosome behavior in spread preparations of yeast. J Cell Biol 106: 567-573.
31. Goetsch L, Byers B (1982) Meiotic cytology of Saccharomyces cerevisiae in protoplast lysates. Mol Gen Genet 187: 54-60.
32. Benjamin KR, Zhang C, Shokat KM, Herskowitz I (2003) Control of landmark events in meiosis by the CDK Cdc28 and the meiosis-specific kinase Ime2. Genes Dev 17: 1524-1539.
33. Carlile TM, Amon A (2008) Meiosis I is established through division-specific translational control of a cyclin. Cell 133: 280-291.
34. Xu L, Ajimura M, Padmore R, Klein C, Kleckner N (1995) NDT80, a meiosisspecific gene required for exit from pachytene in Saccharomyces cerevisiae. Mol Cell Biol 15: 6572-6581.
35. Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK (1998) Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev 12: 2208-2221.
36. Kamieniecki RJ, Shanks RM, Dawson DS (2000) Slk19p is necessary to prevent separation of sister chromatids in meiosis I. Curr Biol 10: 1182-1190.
37. Shonn MA, McCarroll R, Murray AW (2000) Requirement of the spindle checkpoint for proper chromosome segregation in budding yeast meiosis. Science 289: 300-303.
38. Shonn MA, Murray AL, Murray AW (2003) Spindle checkpoint component Mad2 contributes to biorientation of homologous chromosomes. Curr Biol 13: 1979-1984.
39. Dawson DS, Murray AW, Szostak JW (1986) An alternative pathway for meiotic chromosome segregation in yeast. Science 234: 713-717.
40. Macqueen AJ, Roeder GS (2009) Fpr3 and Zip3 ensure that initiation of meiotic recombination precedes chromosome synapsis in budding yeast. Curr Biol 19: 1519-1526.
41. Loidl J, Scherthan H, Kaback DB (1994) Physical association between nonhomologous chromosomes precedes distributive disjunction in yeast. Proc Natl Acad Sci U S A 91: 331-334.
42. Lacefield S, Murray AW (2007) The spindle checkpoint rescues the meiotic segregation of chromosomes whose crossovers are far from the centromere. Nat Genet 39: 1273-1277.
43. Brinkley BR, Brenner SL, Hall JM, Tousson A, Balczon RD, et al. (1986) Arrangements of kinetochores in mouse cells during meiosis and spermiogenesis. Chromosoma 94: 309-317.
44. Xu H, Beasley M, Verschoor S, Inselman A, Handel MA, et al. (2004) A new role for the mitotic RAD21/SCC1 cohesin in meiotic chromosome cohesion and segregation in the mouse. EMBO Rep 5: 378-384.
45. Dobson MJ, Pearlman RE, Karaiskakis A, Spyropoulos B, Moens PB (1994) Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J Cell Sci 107(Pt 10): 2749-2760.
46. de la Fuente R, Parra MT, Viera A, Calvente A, Gomez R, et al. (2007) Meiotic pairing and segregation of achiasmate sex chromosomes in eutherian mammals: the role of SYCP3 protein. PLoS Genet 3: e198. doi:10.1371/journal. pgen.0030198.
47. Page J, Viera A, Parra MT, de la Fuente R, Suja JA, et al. (2006) Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genet 2: e136. doi:10.1371/journal.pgen. 0020136.
48. Rasmussen SW (1977) The transformation of the Synaptonemal Complex into the 'elimination chromatin' in Bombyx mori oocytes. Chromosoma 60: 205-221.
49. Page J, de la Fuente R, Gomez R, Calvente A, Viera A, et al. (2006) Sex chromosomes, synapsis, and cohesins: a complex affair. Chromosoma 115: 250-259.
50. Wolf KW (1994) How meiotic cells deal with non-exchange chromosomes. Bioessays 16: 107-114.
51. Hunt PA, Hassold TJ (2002) Sex matters in meiosis. Science 296: 2181-2183.
52. Nicolas A, Treco D, Schultes NP, Szostak JW (1989) An initiation site for meiotic gene conversion in the yeast Saccharomyces cerevisiae. Nature 338: 35-39.
53. Dresser ME, Ewing DJ, Harwell SN, Coody D, Conrad MN (1994) Nonhomologous synapsis and reduced crossing over in a heterozygous paracentric inversion in Saccharomyces cerevisiae. Genetics 138: 633-647.
54. Burke D, Dawson DS, Stearns T (2000) Methods in Yeast Genetics Cold Spring Harbor Laboratory Press.
55. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.