Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during drosophila meiosis

PLoS Genetics

Volumn 6, Issue 8, 2010, Pages

  Joyce, Eric F ^a   Mckim, Kim S ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DOUBLE STRANDED DNA; HISTONE DEACETYLASE; PROTEIN PCH2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE PROGRESSION; CHROMOSOME REARRANGEMENT; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; DNA STRAND BREAKAGE; DROSOPHILA MELANOGASTER; GENE MUTATION; GENETIC CONSERVATION; MEIOSIS; METAZOON; NONHUMAN; PACHYTENE; PROPHASE; SACCHAROMYCES CEREVISIAE;

ANIMALS; CHROMOSOME SEGREGATION; CHROMOSOMES; CROSSING OVER, GENETIC; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; MALE; MEIOSIS; PACHYTENE STAGE;

DROSOPHILA MELANOGASTER; METAZOA; SACCHAROMYCES CEREVISIAE;

EID: 77957336019     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001059     Document Type: Article

References (56)

1. Page SL, Hawley RS (2004) The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol 20: 525-558.
2. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33: 603-754.
3. 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.
4. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, et al. (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398.
5. Keeney S (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52: 1-53.
6. Muller HJ (1916) The mechanism of crossing-over. American Naturalist 50: 193-434.
7. Sturtevant AH (1915) The behavior of the chromosomes as studied through linkage. Z Induktive Abstammungs Vererbungslehre 13: 234-287.
8. Hillers KJ (2004) Crossover interference. Curr Biol 14: R1036-R1037.
9. Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101: 12592-12597.
10. Carpenter ATC, Sandler L (1974) On recombination-defective meiotic mutants in Drosophila melanogaster. Genetics 76: 453-475.
11. Lucchesi JC, Suzuki DT (1968) The interchromosomal control of recombination. Ann Rev Genet 2: 53-86.
12. Jang JK, Sherizen DE, Bhagat R, Manheim EA, McKim KS (2003) Relationship of DNA double-strand breaks to synapsis in Drosophila. J Cell Sci 116: 3069-3077.
13. Ghabrial A, Schupbach T (1999) Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat Cell Biol 1: 354-357.
14. Joyce EF, McKim KS (2009) Drosophila PCH2 Is Required for a Pachytene Checkpoint That Monitors Double-Strand-Break-Independent Events Leading to Meiotic Crossover Formation. Genetics 181: 39-51.
15. San-Segundo PA, Roeder GS (1999) Pch2 links chromatin silencing to meiotic checkpoint control. Cell 97: 313-324.
16. Bhalla N, Dernburg AF (2005) A conserved checkpoint monitors meiotic chromosome synapsis in Caenorhabditis elegans. Science 310: 1683-1686.
17. Mitra N, Roeder GS (2007) A novel nonnull ZIP1 allele triggers meiotic arrest with synapsed chromosomes in Saccharomyces cerevisiae. Genetics 176: 773-787.
18. Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes & Dev 15: 3130-3143.
19. McCaffrey R, St Johnston D, Gonzalez-Reyes A (2006) Drosophila mus301/spindle-C Encodes a Helicase With an Essential Role in Double-Strand DNA Break Repair and Meiotic Progression. Genetics 174: 1273-1285.
20. 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.
21. 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.
22. 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.
23. Khetani RS, Bickel SE (2007) Regulation of meiotic cohesion and chromosome core morphogenesis during pachytene in Drosophila oocytes. J Cell Sci 120: 3123-3137.
24. Novitski E, Braver G (1954) An analysis of crossing over within a heterozygous inversion in Drosophila melanogaster. Genetics 39: 197-209.
25. Sherizen D, Jang JK, Bhagat R, Kato N, McKim KS (2005) Meiotic recombination in Drosophila females depends on chromosome continuity between genetically defined boundaries. Genetics 169: 767-781.
26. Gong WJ, McKim KS, Hawley RS (2005) All Paired Up with No Place to Go: Pairing, Synapsis, and DSB Formation in a Balancer Heterozygote. PLoS Genet 1: e67. doi:10.1371/journal.pgen.0010067.
27. Lindsley DL, Zimm GG (1992) The Genome of Drosophila melanogaster. San DiegoCA: Academic Press, Inc.
28. Mehrotra S, McKim KS (2006) Temporal analysis of meiotic DNA doublestrand break formation and repair in Drosophila females. PLoS Genet 2: e200. doi:10.1371/journal.pgen.0020200.
29. Madigan JP, Chotkowski HL, Glaser RL (2002) DNA double-strand breakinduced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res 30: 3698-3705.
30. Radford SJ, Goley E, Baxter K, McMahan S, Sekelsky J (2005) Drosophila ERCC1 is required for a subset of MEI-9-dependent meiotic crossovers. Genetics 170: 1737-1745.
31. Joyce EF, Tanneti SN, McKim KS (2009) Drosophila Hold'em Is Required for a Subset of Meiotic Crossovers and Interacts With the DNA Repair Endonuclease Complex Subunits MEI-9 and ERCC1. Genetics 181: 335-340.
32. Szauter P (1984) An analysis of regional constraints on exchange in Drosophila melanogaster using recombination-defective meiotic mutants. Genetics 106: 45-71.
33. Carpenter ATC (1988) Thoughts on Recombination nodules, meiotic recombination, and chiasmata. In: Kucherlapati R, Smith G, eds. Genetic recombination. WashingtonD.C.: American Society of Microbiology. pp 529-548.
34. McKim KS, Jang JK, Manheim EA (2002) Meiotic recombination and chromosome segregation in Drosophila females. Annu Rev Genet 36: 205-232.
35. Tracey WD, Jr., Ning X, Klingler M, Kramer SG, Gergen JP (2000) Quantitative analysis of gene function in the Drosophila embryo. Genetics 154: 273-284.
36. Rorth P (1998) Gal4 in the Drosophila female germline. Mech Dev 78: 113-118.
37. Van Doren M, Williamson AL, Lehmann R (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8: 243-246.
38. Astrom SU, Cline TW, Rine J (2003) The Drosophila melanogaster sir2+ gene is nonessential and has only minor effects on position-effect variegation. Genetics 163: 931-937.
39. Rosenberg MI, Parkhurst SM (2002) Drosophila Sir2 is required for heterochromatic silencing and by euchromatic Hairy/E(Spl) bHLH repressors in segmentation and sex determination. Cell 109: 447-458.
40. Newman BL, Lundblad JR, Chen Y, Smolik SM (2002) A Drosophila homologue of Sir2 modifies position-effect variegation but does not affect life span. Genetics 162: 1675-1685.
41. 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.
42. Borner GV, Barot A, Kleckner N (2008) Yeast Pch2 promotes domainal axis organization, timely recombination progression, and arrest of defective recombinosomes during meiosis. Proc Natl Acad Sci U S A 105: 3327-3332.
43. Joshi N, Barot A, Jamison C, Borner GV (2009) Pch2 links chromosome axis remodeling at future crossover sites and crossover distribution during yeast meiosis. PLoS Genet 5: e1000557. doi:10.1371/journal.pgen.1000557.
44. Wojtasz L, Daniel K, Roig I, Bolcun-Filas E, Xu H, et al. (2009) Mouse HORMAD1 and HORMAD2, two conserved meiotic chromosomal proteins, are depleted from synapsed chromosome axes with the help of TRIP13 AAAATPase. PLoS Genet 5: e1000702. doi:10.1371/journal.pgen.1000702.
45. Phillips CM, Dernburg AF (2006) A Family of Zinc-Finger Proteins Is Required for Chromosome-Specific Pairing and Synapsis during Meiosis in C. elegans. Dev Cell 11: 817-829.
46. Penkner A, Tang L, Novatchkova M, Ladurner M, Fridkin A, et al. (2007) The nuclear envelope protein Matefin/SUN-1 is required for homologous pairing in C. elegans meiosis. Dev Cell 12: 873-885.
47. Ding X, Xu R, Yu J, Xu T, Zhuang Y, et al. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12: 863-872.
48. Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, et al. (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322: 597-602.
49. Blanton HL, Radford SJ, McMahan S, Kearney HM, Ibrahim JG, et al. (2005) REC, Drosophila MCM8, Drives Formation of Meiotic Crossovers. PLoS Genet 1: e40. doi:10.1371/journal.pgen.0010040.
50. Wakimoto BT, Hearn MG (1990) The effects of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster. Genetics 125: 141-154.
51. McKim K, Joyce EF, Jang JK, eds (2008) Cytological analysis of meiosis in fixed Drosophila ovaries Totowa, NJ: Humana Press.
52. Manheim EA, McKim KS (2003) The Synaptonemal Complex Component C(2)M Regulates Meiotic Crossing over in Drosophila. Curr Biol 13: 276-285.
53. 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.
54. Gonzalez-Reyes A, Elliot H, Johnston D St (1997) Oocyte determination and the origin of polarity in Drosophila: the role of the spindle genes. Development 124: 4927-4937.
55. Stapleton M, Liao G, Brokstein P, Hong L, Carninci P, et al. (2002) The Drosophila gene collection: identification of putative full-length cDNAs for 70% of D. melanogaster genes. Genome Res 12: 1294-1300.
56. King RC (1970) Ovarian development in Drosophila melanogaster. New York: Academic Press, Inc.