A single mutation results in diploid gamete formation and parthenogenesis in a Drosophila yemanuclein-alpha meiosis I defective mutant

BMC Genetics

Volumn 11, Issue , 2010, Pages

  Meyer, Régis E ^a,d   Delaage, Michèle ^b   Rosset, Roland ^b   Capri, Michèle ^a,b   Aït Ahmed, Ounissa ^a,b,c  

^a INSTITUTE OF HUMAN GENETICS   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c STANFORD UNIVERSITY   (United States)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; UNCLASSIFIED DRUG; YEMANUCLEIN ALPHA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; HISTONE; NUCLEAR PROTEIN; YEMALPHA PROTEIN, DROSOPHILA;

ALLELE; ARTICLE; CELL CYCLE; CENTROMERE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; DIPLOIDY; DROSOPHILA MELANOGASTER; FEMALE; FERTILIZATION; GAMETE; GENE; GENE MUTATION; GENETIC ANALYSIS; MALE; MEIOSIS; NONHUMAN; OOCYTE; PARTHENOGENESIS; PROGENY; AMINO ACID SEQUENCE; ANIMAL; CYTOLOGY; DROSOPHILA; FEMALE INFERTILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; CHROMOSOMES; DIPLOIDY; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; HISTONES; INFERTILITY, FEMALE; KINETOCHORES; MEIOSIS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NUCLEAR PROTEINS; OOCYTES; PARTHENOGENESIS;

EID: 78149493853     PISSN: None     EISSN: 14712156     Source Type: Journal    
DOI: 10.1186/1471-2156-11-104     Document Type: Article

References (53)

1. Petronczki M, Siomos MF, Nasmyth K. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 2003, 112(4):423-440. 10.1016/S0092-8674(03)00083-7, 12600308.
2. Lee JY, Orr-Weaver TL. The molecular basis of sister-chromatid cohesion. Annu Rev Cell Dev Biol 2001, 17:753-777. 10.1146/annurev.cellbio.17.1.753, 11687503.
3. Thomas SE, Soltani-Bejnood M, Roth P, Dorn R, Logsdon JM, McKee BD. Identification of two proteins required for conjunction and regular segregation of achiasmate homologs in Drosophila male meiosis. Cell 2005, 123(4):555-568. 10.1016/j.cell.2005.08.043, 16286005.
4. Theurkauf WE, Hawley RS. Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein. J Cell Biol 1992, 116(5):1167-1180. 10.1083/jcb.116.5.1167, 2289365, 1740471.
5. Kitajima TS, Yokobayashi S, Yamamoto M, Watanabe Y. Distinct cohesin complexes organize meiotic chromosome domains. Science 2003, 300(5622):1152-1155. 10.1126/science.1083634, 12750522.
6. Klein F, Mahr P, Galova M, Buonomo SB, Michaelis C, Nairz K, Nasmyth K. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 1999, 98(1):91-103. 10.1016/S0092-8674(00)80609-1, 10412984.
7. Toth A, Rabitsch KP, Galova M, Schleiffer A, Buonomo SB, Nasmyth K. Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis i. Cell 2000, 103(7):1155-1168. 10.1016/S0092-8674(00)00217-8, 11163190.
8. Watanabe Y. Sister chromatid cohesion along arms and at centromeres. Trends Genet 2005, 21(7):405-412. 10.1016/j.tig.2005.05.009, 15946764.
9. Yokobayashi S, Watanabe Y. The kinetochore protein Moa1 enables cohesion-mediated monopolar attachment at meiosis I. Cell 2005, 123(5):803-817. 10.1016/j.cell.2005.09.013, 16325576.
10. Baker BS, Carpenter AT. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster. Genetics 1972, 71(2):255-286. 1212782, 4625747.
11. Mason JM. Orientation disruptor (ord): a recombination-defective and disjunction-defective meiotic mutant in Drosophila melanogaster. Genetics 1976, 84(3):545-572. 1213594, 826453.
12. Sandler L, Lindsley DL, Nicoletti B, Trippa G. Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics 1968, 60(3):525-558. 1212059, 5728740.
13. McKim KS, Jang JK, Manheim EA. Meiotic recombination and chromosome segregation in Drosophila females. Annu Rev Genet 2002, 36:205-232. 10.1146/annurev.genet.36.041102.113929, 12429692.
14. Ait-Ahmed O, Bellon B, Capri M, Joblet C, Thomas-Delaage M. The yemanuclein-alpha: a new Drosophila DNA binding protein specific for the oocyte nucleus. Mech Dev 1992, 37(1-2):69-80. 10.1016/0925-4773(92)90016-D, 1606021.
15. Balaji S, Iyer LM, Aravind L. HPC2 and ubinuclein define a novel family of histone chaperones conserved throughout eukaryotes. Mol Biosyst 2009, 5(3):269-275. 10.1039/b816424j, 19225618.
16. Banumathy G, Somaiah N, Zhang R, Tang Y, Hoffmann J, Andrake M, Ceulemans H, Schultz D, Marmorstein R, Adams PD. Human UBN1 is an ortholog of yeast Hpc2p and has an essential role in the HIRA/ASF1a chromatin-remodeling pathway in senescent cells. Mol Cell Biol 2009, 29(3):758-770. 10.1128/MCB.01047-08, 2630694, 19029251.
17. Moshkin YM, Kan TW, Goodfellow H, Bezstarosti K, Maeda RK, Pilyugin M, Karch F, Bray SJ, Demmers JA, Verrijzer CP. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol Cell 2009, 35(6):782-793. 10.1016/j.molcel.2009.07.020, 19782028.
18. Ait-Ahmed O, Griffin-Shea R, Vola C, Capri M, Thomas-Cavallin M, Pardo D. Isolation of developmentally regulated genes in Drosophila melanogaster. Biol Cell 1988, 62(1):57-64. 10.1016/0248-4900(88)90044-5, 2452664.
19. Ait-Ahmed O, Thomas-Cavallin M, Rosset R. Isolation and characterization of a region of the Drosophila genome which contains a cluster of differentially expressed maternal genes (yema gene region). Dev Biol 1987, 122(1):153-162. 10.1016/0012-1606(87)90341-1, 2439394.
20. Lindsley DL, Sandler L, Baker BS, Carpenter AT, Denell RE, Hall JC, Jacobs PA, Miklos GL, Davis BK, Gethmann RC, et al. Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 1972, 71(1):157-184. 1212769, 4624779.
21. Callaini G, Riparbelli MG. Fertilization in Drosophila melanogaster: centrosome inheritance and organization of the first mitotic spindle. Dev Biol 1996, 176(2):199-208. 10.1006/dbio.1996.0127, 8660861.
22. Aho S, Buisson M, Pajunen T, Ryoo YW, Giot JF, Gruffat H, Sergeant A, Uitto J. Ubinuclein, a novel nuclear protein interacting with cellular and viral transcription factors. J Cell Biol 2000, 148(6):1165-1176. 10.1083/jcb.148.6.1165, 2174308, 10725330.
23. Capri M, Santoni MJ, Thomas-Delaage M, Ait-Ahmed O. Implication of a 5' coding sequence in targeting maternal mRNA to the Drosophila oocyte. Mech Dev 1997, 68(1-2):91-100. 10.1016/S0925-4773(97)00130-5, 9431807.
24. Gilliland WD, Hughes SF, Vietti DR, Hawley RS. Congression of achiasmate chromosomes to the metaphase plate in Drosophila melanogaster oocytes. Dev Biol 2009, 325(1):122-128. 10.1016/j.ydbio.2008.10.003, 18977343.
25. Riparbelli MG, Callaini G, Glover DM. Failure of pronuclear migration and repeated divisions of polar body nuclei associated with MTOC defects in polo eggs of Drosophila. J Cell Sci 2000, 113(Pt 18):3341-3350.
26. Jang JK, Messina L, Erdman MB, Arbel T, Hawley RS. Induction of metaphase arrest in Drosophila oocytes by chiasma-based kinetochore tension. Science 1995, 268(5219):1917-1919. 10.1126/science.7604267, 7604267.
27. McKim KS, Jang JK, Theurkauf WE, Hawley RS. Mechanical basis of meiotic metaphase arrest. Nature 1993, 362(6418):364-366. 10.1038/362364a0, 8455723.
28. Katis VL, Matos J, Mori S, Shirahige K, Zachariae W, Nasmyth K. Spo13 facilitates monopolin recruitment to kinetochores and regulates maintenance of centromeric cohesion during yeast meiosis. Curr Biol 2004, 14(24):2183-2196. 10.1016/j.cub.2004.12.020, 15620645.
29. Shonn MA, McCarroll R, Murray AW. Spo13 protects meiotic cohesin at centromeres in meiosis I. Genes Dev 2002, 16(13):1659-1671. 10.1101/gad.975802, 186364, 12101124.
30. Blower MD, Sullivan BA, Karpen GH. Conserved organization of centromeric chromatin in flies and humans. Dev Cell 2002, 2(3):319-330. 10.1016/S1534-5807(02)00135-1, 11879637.
31. Parra MT, Viera A, Gomez R, Page J, Benavente R, Santos JL, Rufas JS, Suja JA. Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 2004, 117(Pt 7):1221-1234. 10.1242/jcs.00947, 14970259.
32. Fuyama Y. Genetics of Parthenogenesis in DROSOPHILA MELANOGASTER. II. Characterization of a Gynogenetically Reproducing Strain. Genetics 1986, 114(2):495-509. 1202953, 17246347.
33. Fuyama Y. Genetics of Parthenogenesis in DROSOPHILA MELANOGASTER. I. the Modes of Diploidization in the Gynogenesis Induced by a Male-Sterile Mutant, ms(3)K81. Genetics 1986, 112(2):237-248. 1202699, 17246314.
34. Loppin B, Berger F, Couble P. The Drosophila maternal gene sesame is required for sperm chromatin remodeling at fertilization. Chromosoma 2001, 110(6):430-440. 10.1007/s004120100161, 11735001.
35. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004, 116(1):51-61. 10.1016/S0092-8674(03)01064-X, 14718166.
36. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Nature 2005, 437(7063):1386-1390. 10.1038/nature04059, 16251970.
37. Klapholz S, Esposito RE. Isolation of SPO12-1 and SPO13-1 from a natural variant of yeast that undergoes a single meiotic division. Genetics 1980, 96(3):567-588. 1214362, 7021311.
38. Marston AL, Lee BH, Amon A. The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation. Dev Cell 2003, 4(5):711-726. 10.1016/S1534-5807(03)00130-8, 12737806.
39. Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature 2004, 427(6974):510-517. 10.1038/nature02312, 14730319.
40. Rabitsch KP, Gregan J, Schleiffer A, Javerzat JP, Eisenhaber F, Nasmyth K. Two fission yeast homologs of Drosophila Mei-S332 are required for chromosome segregation during meiosis I and II. Curr Biol 2004, 14(4):287-301.
41. Kerrebrock AW, Miyazaki WY, Birnby D, Orr-Weaver TL. The Drosophila mei-S332 gene promotes sister-chromatid cohesion in meiosis following kinetochore differentiation. Genetics 1992, 130(4):827-841. 1204932, 1582560.
42. Bickel SE, Wyman DW, Miyazaki WY, Moore DP, Orr-Weaver TL. Identification of ORD, a Drosophila protein essential for sister chromatid cohesion. Embo J 1996, 15(6):1451-1459. 450050, 8635478.
43. Yan R, Thomas SE, Tsai JH, Yamada Y, McKee BD. SOLO: a meiotic protein required for centromere cohesion, coorientation, and SMC1 localization in Drosophila melanogaster. J Cell Biol 188(3):335-349. 10.1083/jcb.200904040, 2819681, 20142422.
44. Schittenhelm RB, Heeger S, Althoff F, Walter A, Heidmann S, Mechtler K, Lehner CF. Spatial organization of a ubiquitous eukaryotic kinetochore protein network in Drosophila chromosomes. Chromosoma 2007, 116(4):385-402. 10.1007/s00412-007-0103-y, 1950589, 17333235.
45. Przewloka MR, Zhang W, Costa P, Archambault V, D'Avino PP, Lilley KS, Laue ED, McAinsh AD, Glover DM. Molecular analysis of core kinetochore composition and assembly in Drosophila melanogaster. PLoS One 2007, 2(5):e478. 10.1371/journal.pone.0000478, 1868777, 17534428.
46. Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, Vale RD, Stuurman N. Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 2007, 316(5823):417-421. 10.1126/science.1141314, 2837481, 17412918.
47. Krude T. Chromatin assembly: the kinetochore connection. Curr Biol 2002, 12(7):R256-258. 10.1016/S0960-9822(02)00786-8, 11937044.
48. Sharp JA, Franco AA, Osley MA, Kaufman PD. Chromatin assembly factor I and Hir proteins contribute to building functional kinetochores in S. cerevisiae. Genes Dev 2002, 16(1):85-100. 10.1101/gad.925302, 155315,155315, 11782447.
49. Obuse C, Iwasaki O, Kiyomitsu T, Goshima G, Toyoda Y, Yanagida M. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat Cell Biol 2004, 6(11):1135-1141. 10.1038/ncb1187, 15502821.
50. Zhang R, Liu ST, Chen W, Bonner M, Pehrson J, Yen TJ, Adams PD. HP1 proteins are essential for a dynamic nuclear response that rescues the function of perturbed heterochromatin in primary human cells. Mol Cell Biol 2007, 27(3):949-962. 10.1128/MCB.01639-06, 1800672, 17101789.
51. Feiguin F, Llamazares S, Gonzalez C. Methods in Drosophila cell cycle biology. Curr Top Dev Biol 1998, 36:279-291. 10.1016/S0070-2153(08)60508-6, 9342534.
52. Lantz V, Chang JS, Horabin JI, Bopp D, Schedl P. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev 1994, 8(5):598-613. 10.1101/gad.8.5.598, 7523244.
53. Thomas-Cavallin M, Ait-Ahmed O. The random primer labeling technique applied to in situ hybridization on tissue sections. J Histochem Cytochem 1988, 36(10):1335-1340.