Centromere proteins cenp-C and cal1 functionally interact in meiosis for centromere clustering, pairing, and chromosome segregation

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

Volumn 110, Issue 49, 2013, Pages 19878-19883

  Unhavaithaya, Yingdee ^a   Orr Weaver, Terry L ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

CENP A; CID

Indexed keywords

CENTROMERE PROTEIN C; CHROMOSOME ALIGNMENT 1 PROTEIN; CHROMOSOME PROTEIN; NUCLEAR PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CELL FUNCTION; CENTROMERE; CHROMOSOME ARM; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CONTROLLED STUDY; GENE INTERACTION; GENE MUTATION; HETEROZYGOTE; MEIOSIS; MUTANT DROSOPHILA; NONDISJUNCTION; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; SYNAPTONEMAL COMPLEX;

CENP-A; CID;

ANIMALS; CELL NUCLEOLUS; CENTROMERE; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MEIOSIS; MICROSCOPY, CONFOCAL; OVARY; STATISTICS, NONPARAMETRIC;

EID: 84889644216     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1320074110     Document Type: Article

References (46)

1. Gascoigne KE, Cheeseman IM (2011) Kinetochore assembly: If you build it, they will come. Curr Opin Cell Biol 23(1):102-108
2. Watanabe Y (2012) Geometry and force behind kinetochore orientation: Lessons from meiosis. Nat Rev Mol Cell Biol 13(6):370-382
3. Stewart MN, Dawson DS (2008) Changing partners: Moving from non-homologous to homologous centromere pairing in meiosis. Trends Genet 24(11):564-573
4. Obeso D, Dawson DS (2010) Temporal characterization of homology-independent centromere coupling in meiotic prophase. PLoS ONE 5(4):e10336
5. Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homologyindependent centromere coupling. Science 308(5723):870-873
6. Dernburg AF, Sedat JW, Hawley RS (1996) Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86(1):135-146
7. Gladstone MN, Obeso D, Chuong H, Dawson DS (2009) The synaptonemal complex protein Zip1 promotes bi-orientation of centromeres at meiosis 1. PLoS Genet 5(12): e1000771
8. Karpen GH, Le M-H, Le H (1996) Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science 273(5271):118-122
9. Takeo S, Lake CM, Morais-de-Sá E, Sunkel CE, Hawley RS (2011) Synaptonemal complex- dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr Biol 21(21):1845-1851
10. Tanneti NS, Landy K, Joyce EF, McKim KS (2011) A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr Biol 21(21):1852-1857
11. Newnham L, Jordan P, Rockmill B, Roeder GS, Hoffmann E (2010) The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis 1. Proc Natl Acad Sci USA 107(2):781-785
12. Bisig CG, et al. (2012) Synaptonemal complex components persist at centromeres and are required for homologous centromere pairing in mouse spermatocytes. PLoS Genet 8(6):e1002701
13. Qiao H, et al. (2012) Interplay between synaptonemal complex, homologous recombination, and centromeres during mammalian meiosis. PLoS Genet 8(6):e1002790
14. Webber HA, Howard L, Bickel SE (2004) The cohesion protein ORD is required for homologue bias during meiotic recombination. J Cell Biol 164(6):819-829
15. Zickler D, Kleckner N (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32:619-697
16. Carpenter ATC (1975) Electron microscopy of meiosis in Drosophila melanogaster females. 1. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51(2):157-182
17. Perpelescu M, Fukagawa T (2011) The ABCs of CENPs. Chromosoma 120(5):425-446
18. Orr B, Sunkel CE (2011) Drosophila CENP-C is essential for centromere identity. Chromosoma 120(1):83-96
19. Erhardt S, et al. (2008) Genome-wide analysis reveals a cell cycle-dependent mechanism controlling centromere propagation. J Cell Biol 183(5):805-818
20. Goshima G, et al. (2007) Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316(5823):417-421
21. Schittenhelm RB, Althoff F, Heidmann S, Lehner CF (2010) Detrimental incorporation of excess Cenp-A/Cid and Cenp-C into Drosophila centromeres is prevented by limiting amounts of the bridging factor Cal1. J Cell Sci 123(Pt 21):3768-3779
22. Schuh M, Lehner CF, Heidmann S (2007) Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr Biol 17(3):237-243
23. Mellone BG, et al. (2011) Assembly of Drosophila centromeric chromatin proteins during mitosis. PLoS Genet 7(5):e1002068
24. Tanaka K, Chang HL, Kagami A, Watanabe Y (2009) CENP-C functions as a scaffold for effectors with essential kinetochore functions inmitosis and meiosis. Dev Cell 17(3):334-343
25. Parra MT, et al. (2009) Sequential assembly of centromeric proteins in male mouse meiosis. PLoS Genet 5(3):e1000417
26. Dunleavy EM, et al. (2012) The cell cycle timing of centromeric chromatin assembly in Drosophila meiosis is distinct from mitosis yet requires CAL1 and CENP-C. PLoS Biol 10(12):e1001460
27. Raychaudhuri N, et al. (2012) Transgenerational propagation and quantitative maintenance of paternal centromeres depends on Cid/Cenp-A presence in Drosophila sperm. PLoS Biol 10(12):e1001434
28. Hawley RS (2002) Meiosis: How male flies do meiosis. Curr Biol 12(19):R660-R662
29. Koundakjian EJ, Cowan DM, Hardy RW, Becker AH (2004) The Zuker collection: A resource for the analysis of autosomal gene function in Drosophila melanogaster. Genetics 167(1):203-206
30. Unhavaithaya Y, Park EA, Royzman I, Orr-Weaver TL (2013) Drosophila embryonic cell cycle mutants. G3 (Bethesda) 3(10):1875-1880
31. Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15(23):3130-3143
32. Resnick TD, et al. (2009) Mutations in the chromosomal passenger complex and the condensin complex differentially affect synaptonemal complex disassembly and metaphase I configuration in Drosophila female meiosis. Genetics 181(3):875-887
33. Gilliland WD, Hughes SF, Vietti DR, Hawley RS (2009) Congression of achiasmate chromosomes to themetaphase plate in Drosophilamelanogaster oocytes. Dev Biol 325(1):122-128
34. de Cuevas M, Spradling AC (1998) Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125(15):2781-2789
35. Hawley RS, Gilliland WD (2006) Sometimes the result is not the answer: The truths and the lies that come from using the complementation test. Genetics 174(1):5-15
36. Heeger S, et al. (2005) Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog. Genes Dev 19(17):2041-2053
37. Chen CC, Greene E, Bowers SR, Mellone BG (2012) A role for the CAL1-partner Modulo in centromere integrity and accurate chromosome segregation in Drosophila. PLoS ONE 7(9):e45094
38. Padeken J, et al. (2013) The nucleoplasmin homolog NLP mediates centromere clustering and anchoring to the nucleolus. Mol Cell 50(2):236-249
39. 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
40. Gascoigne KE, et al. (2011) Induced ectopic kinetochore assembly bypasses the requirement for CENP-A nucleosomes. Cell 145(3):410-422
41. Przewloka MR, et al. (2011) CENP-C is a structural platform for kinetochore assembly. Curr Biol 21(5):399-405
42. Trazzi S, et al. (2009) The C-terminal domain of CENP-C displays multiple and critical functions for mammalian centromere formation. PLoS ONE 4(6):e5832
43. Screpanti E, et al. (2011) Direct binding of Cenp-C to the Mis12 complex joins the inner and outer kinetochore. Curr Biol 21(5):391-398
44. Lake CM, Hawley RS (2012) The molecular control of meiotic chromosomal behavior: Events in early meiotic prophase in Drosophila oocytes. Annu Rev Physiol 74:425-451
45. Walker MY, Hawley RS (2000) Hanging on to your homolog: The roles of pairing, synapsis and recombination in the maintenance of homolog adhesion. Chromosoma 109(1-2):3-9
46. Zeng Y, Li H, Schweppe NM, Hawley RS, Gilliland WD (2010) Statistical analysis of nondisjunction assays in Drosophila. Genetics 186(2):505-513