Rejuvenation of Meiotic Cohesion in Oocytes during Prophase I Is Required for Chiasma Maintenance and Accurate Chromosome Segregation

PLoS Genetics

Volumn 10, Issue 9, 2014, Pages

  Weng, Katherine A ^a,b   Jeffreys, Charlotte A ^a   Bickel, Sharon E ^a  

^a Dartmouth College ^*  (United States)

^b St George s University of Medicine   (Jamaica)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CELL CYCLE PROTEIN; COHESIN; DROSOPHILA PROTEIN; NONHISTONE PROTEIN; PROTEIN SUBUNIT;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL MATURATION; CELL REGENERATION; CHROMOSOME CHIASM; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; DROSOPHILA; FEMALE; GENETIC LINKAGE; HOMOLOGOUS RECOMBINATION; MALE; MEIOTIC PROPHASE I; NONHUMAN; OOCYTE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; GENE SILENCING; GENETICS; MEIOSIS; METABOLISM; PROTEIN SUBUNIT;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DNA BREAKS, DOUBLE-STRANDED; DROSOPHILA; DROSOPHILA PROTEINS; GENE KNOCKDOWN TECHNIQUES; MEIOSIS; MEIOTIC PROPHASE I; OOCYTES; PROTEIN SUBUNITS; S PHASE;

EID: 84907587766     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004607     Document Type: Article

References (70)

1. Nasmyth K, Haering CH, (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525–558.
2. Peters JM, Nishiyama T, (2012) Sister chromatid cohesion. Cold Spring Harb Perspect Biol 4: a011130.
3. McNicoll F, Stevense M, Jessberger R, (2013) Cohesin in gametogenesis. Curr Top Dev Biol 102: 1–34.
4. Bickel SE, Orr-Weaver T, Balicky EM, (2002) The sister-chromatid cohesion protein ORD is required for chiasma maintenance in Drosophila oocytes. Curr Biol 12: 925–929.
5. Buonomo SB, Clyne RK, Fuchs J, Loidl J, Uhlmann F, et al. (2000) Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin. Cell 103: 387–398.
6. Hodges CA, Revenkova E, Jessberger R, Hassold TJ, Hunt PA, (2005) SMC1beta-deficient female mice provide evidence that cohesins are a missing link in age-related nondisjunction. Nat Genet 37: 1351–1355.
7. Hunt PA, Hassold TJ, (2008) Human female meiosis: what makes a good egg go bad? Trends Genet 24: 86–93.
8. Nagaoka SI, Hassold TJ, Hunt PA, (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13: 493–504.
9. Duncan FE, Hornick JE, Lampson MA, Schultz RM, Shea LD, et al. (2012) Chromosome cohesion decreases in human eggs with advanced maternal age. Aging Cell 11: 1121–1124.
10. Angell RR, (1997) First-meiotic-division nondisjunction in human oocytes. Am J Hum Genet 61: 23–32.
11. Subramanian VV, Bickel SE, (2008) Aging predisposes oocytes to meiotic nondisjunction when the cohesin subunit SMC1 is reduced. PLoS Genet 4: e1000263.
12. Chiang T, Duncan FE, Schindler K, Schultz RM, Lampson MA, (2010) Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr Biol 20: 1522–1528.
13. Liu L, Keefe DL, (2008) Defective cohesin is associated with age-dependent misaligned chromosomes in oocytes. Reprod Biomed Online 16: 103–112.
14. Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, et al. (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20: 1511–1521.
15. Strom L, Karlsson C, Lindroos HB, Wedahl S, Katou Y, et al. (2007) Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317: 242–245.
16. Strom L, Lindroos HB, Shirahige K, Sjogren C, (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16: 1003–1015.
17. Unal E, Heidinger-Pauli JM, Koshland D, (2007) DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317: 245–248.
18. Lyons NA, Morgan DO, (2011) Cdk1-dependent destruction of Eco1 prevents cohesion establishment after S phase. Mol Cell 42: 378–389.
19. Lyons NA, Fonslow BR, Diedrich JK, Yates JR, 3rdMorgan DO, (2013) Sequential primed kinases create a damage-responsive phosphodegron on Eco1. Nat Struct Mol Biol 20: 194–201.
20. Gause M, Webber HA, Misulovin Z, Haller G, Rollins RA, et al. (2008) Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells. Chromosoma 117: 51–66.
21. Kuleszewicz K, Fu X, Kudo NR, (2013) Cohesin loading factor Nipbl localizes to chromosome axes during mammalian meiotic prophase. Cell Div 8: 12.
22. Visnes T, Giordano F, Kuznetsova A, Suja JA, Lander AD, et al. (2013) Localisation of the SMC loading complex Nipbl/Mau2 during mammalian meiotic prophase I. Chromosoma. 123: 239–252.
23. Ashburner M, Golic K, Hawley R (2005) Drosophila. A laboratory handbook. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
24. Williams BC, Garrett-Engele CM, Li Z, Williams EV, Rosenman ED, et al. (2003) Two putative acetyltransferases, san and deco, are required for establishing sister chromatid cohesion in Drosophila. Curr Biol 13: 2025–2036.
25. Januschke J, Gervais L, Dass S, Kaltschmidt JA, Lopez-Schier H, et al. (2002) Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. Curr Biol 12: 1971–1981.
26. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S, (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877–879.
27. Page SL, Hawley RS, (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525–558.
28. Webber HA, Howard L, Bickel SE, (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol 164: 819–829.
29. Khetani RS, Bickel SE, (2007) Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J Cell Sci 120: 3123–3137.
30. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, et al. (1999) A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98: 91–103.
31. Pasierbek P, Fodermayr M, Jantsch V, Jantsch M, Schweizer D, et al. (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. Murdoch B, Owen N, Stevense M, Smith H, Nagaoka S, et al. (2013) Altered cohesin gene dosage affects Mammalian meiotic chromosome structure and behavior. PLoS Genet 9: e1003241.
33. Llano E, Herran Y, Garcia-Tunon I, Gutierrez-Caballero C, de Alava E, et al. (2012) Meiotic cohesin complexes are essential for the formation of the axial element in mice. J Cell Biol 197: 877–885.
34. Brar GA, Hochwagen A, Ee LS, Amon A, (2009) The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. Mol Biol Cell 20: 1030–1047.
35. Tanneti NS, Landy K, Joyce EF, McKim KS, (2011) A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol 21: 1852–1857.
36. Page SL, Hawley RS, (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15: 3130–3143.
37. Carpenter ATC, (1975) Electron microscopy of meiosis in Drosophila melanogaster females. Chromosoma 51: 157–182.
38. Anderson LK, Royer SM, Page SL, McKim KS, Lai A, et al. (2005) Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of Drosophila synaptonemal complex. Proc Natl Acad Sci U S A 102: 4482–4487.
39. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, et al. (2011) A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods 8: 405–407.
40. Rorth P, (1998) Gal4 in the Drosophila female germline. Mech Dev 78: 113–118.
41. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, et al. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151–156.
42. Lee YS, Nakahara K, Pham JW, Kim K, He Z, et al. (2004) Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117: 69–81.
43. Van Doren M, Williamson AL, Lehmann R, (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8: 243–246.
44. Revenkova E, Jessberger R, (2006) Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins. Chromosoma 115: 235–240.
45. Stack SM, Anderson LK, (2001) A model for chromosome structure during the mitotic and meiotic cell cycles. Chromosome Res 9: 175–198.
46. Rollins RA, Morcillo P, Dorsett D, (1999) Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics 152: 577–593.
47. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, et al. (2000) Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243–254.
48. McKim KS, Hayashi-Hagihara A, (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev 12: 2932–2942.
49. McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, et al. (1998) Meiotic synapsis in the absence of recombination. Science 279: 876–878.
50. Voelkel-Meiman K, Moustafa SS, Lefrancois P, Villeneuve AM, MacQueen AJ, (2012) Full-length synaptonemal complex grows continuously during meiotic prophase in budding yeast. PLoS Genet 8: e1002993.
51. Kronja I, Orr-Weaver TL, (2011) Translational regulation of the cell cycle: when, where, how and why? Philos Trans R Soc Lond B Biol Sci 366: 3638–3652.
52. Zhang J, Shi X, Li Y, Kim BJ, Jia J, et al. (2008) Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol Cell 31: 143–151.
53. Ben-Shahar TR, Heeger S, Lehane C, East P, Flynn H, et al. (2008) Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321: 563–566.
54. Heidinger-Pauli JM, Unal E, Koshland D, (2009) Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage. Mol Cell 34: 311–321.
55. Koehler KE, Boulton CL, Collins HE, French RL, Herman KC, et al. (1996) Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nature Genet 14: 406–413.
56. Lamb NE, Feingold E, Savage A, Avramopoulos D, Freeman S, et al. (1997) Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21. Hum Mol Genet 6: 1391–1399.
57. Hassold T, Merrill M, Adkins K, Freeman S, Sherman S, (1995) Recombination and maternal age-dependent nondisjunction: Molecular studies of trisomy 16. Am J Hum Genet 57: 867–874.
58. Sherman SL, Petersen MB, Freeman SB, Hersey J, Pettay D, et al. (1994) Non-disjunction of chromosome 21 in maternal meiosis I: Evidence for a maternal age-dependent mechanism involving reduced recombination. Hum Mol Genet 3: 1529–1535.
59. Miyazaki WY, Orr-Weaver TL, (1992) Sister-chromatid misbehavior in Drosophila ord mutants. Genetics 132: 1047–1061.
60. Bickel SE, Wyman DW, Orr-Weaver TL, (1997) Mutational analysis of the Drosophila sister-chromatid cohesion protein ORD and its role in the maintenance of centromeric cohesion. Genetics 146: 1319–1331.
61. Chiang T, Schultz RM, Lampson MA, (2012) Meiotic origins of maternal age-related aneuploidy. Biol Reprod 86: 1–7.
62. Revenkova E, Herrmann K, Adelfalk C, Jessberger R, (2010) Oocyte cohesin expression restricted to predictyate stages provides full fertility and prevents aneuploidy. Curr Biol 20: 1529–1533.
63. Tachibana-Konwalski K, Godwin J, van der Weyden L, Champion L, Kudo NR, et al. (2010) Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes. Genes Dev 24: 2505–2516.
64. Laugsch M, Seebach J, Schnittler H, Jessberger R, (2013) Imbalance of SMC1 and SMC3 Cohesins Causes Specific and Distinct Effects. PLoS One 8: e65149.
65. Zeng Y, Li H, Schweppe NM, Hawley RS, Gilliland WD, (2010) Statistical analysis of nondisjunction assays in Drosophila. Genetics 186: 505–513.
66. Lantz V, Chang JS, Horabin JI, Bopp D, Schedl P, (1994) The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 8: 598–613.
67. Chandley AC, (1966) Studies on oogenesis in Drosophila melanogaster with 3-H-thymidine label. Exp Cell Res 44: 201–215.
68. Carpenter AT, (1981) EM autoradiographic evidence that DNA synthesis occurs at recombination nodules during meiosis in Drosophila melanogaster females. Chromosoma 83: 59–80.
69. King RC (1970) Ovarian development in Drosophila melanogaster. New York, NY: Academic Press. 227 p.
70. Morris LX, Spradling AC, (2011) Long-term live imaging provides new insight into stem cell regulation and germline-soma coordination in the Drosophila ovary. Development 138: 2207–2215.