Vilya, a component of the recombination nodule, is required for meiotic double-strand break formation in Drosophila

eLife

Volumn 4, Issue OCTOBER2015, 2015, Pages

  Lake, Cathleen M ^a   Nielsen, Rachel J ^a   Guo, Fengli ^a   Unruh, Jay R ^a   Slaughter, Brian D ^a   Hawley, R Scott ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSING OVER; DNA STRAND; DNA STRAND BREAKAGE; ELECTRON MICROSCOPY; GENE DISRUPTION; MEIOSIS; PACHYTENE; SYNAPTONEMAL COMPLEX; ANIMAL; DOUBLE STRANDED DNA BREAK; DROSOPHILA; IMMUNOELECTRON MICROSCOPY; METABOLISM; PHYSIOLOGY;

CELL CYCLE PROTEIN; DROSOPHILA PROTEIN; MEI-P22 PROTEIN, DROSOPHILA; NONHISTONE PROTEIN; PROTEIN BINDING;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; CROSSING OVER, GENETIC; DNA BREAKS, DOUBLE-STRANDED; DROSOPHILA; DROSOPHILA PROTEINS; MEIOSIS; MICROSCOPY, IMMUNOELECTRON; PROTEIN BINDING;

EID: 84949921606     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08287     Document Type: Article

References (71)

1. Agarwal S, Roeder GS. 2000. Zip3 provides a link between recombination enzymes and synaptonemal complex proteins. Cell 102:245-255. doi:10.1016/S0092-8674(00)00029-5
2. Anderson LK, Royer SM, Page SL, Mckim KS, Lai A, Lilly MA, Hawley RS. 2005. Juxtaposition of C(2)M and the transverse filament protein C(3)G within the central region of drosophila synaptonemal complex. Proceedings of the National Academy of Sciences of the United States of America 102:4482-4487. doi:10.1073/pnas.0500172102
3. Baudat Frédéric, Manova K, Yuen JP, Jasin M, Keeney S. 2000. Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Molecular Cell 6:989-998. doi:10.1016/S1097-2765(00)00098-8
4. Bhagat R, Manheim EA, Sherizen DE, Mckim KS. 2004. Studies on crossover-specific mutants and the distribution of crossing over in drosophila females. Cytogenetic and Genome Research 107:160-171. doi:10.1159/000080594
5. Bhalla N, Wynne DJ, Jantsch V, Dernburg AF, Hawley RS, Dernburg AF. 2008. ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in c. elegans. PLoS Genetics 4:e1000235 doi:10.1371/journal.pgen.1000235.s002
6. Blumenstiel JP, Fu R, Theurkauf WE, Hawley RS. 2008. Components of the RNAi machinery that mediate long-distance chromosomal associations are dispensable for meiotic and early somatic homolog pairing in drosophila melanogaster. Genetics 180:1355-1365. doi:10.1534/genetics.108.092650
7. Carpenter AT. 1975a. Electron microscopy of meiosis in drosophila melanogaster females. Chromosoma 51:157-182. doi:10.1007/BF00319833
8. Carpenter AT. 1975b. Electron microscopy of meiosis in drosophila melanogaster females: II The Recombination Nodule-a Recombination-Associated Structure at Pachytene?. Proceedings of the National Academy of Sciences of the United States of America 72:3186-3189.
9. Chelysheva L, Vezon D, Chambon Aurélie, Gendrot G, Pereira L, Lemhemdi A, Vrielynck N, Le Guin S, Novatchkova M, Grelon M. 2012. The arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genetics 8:e1002799 doi:10.1371/journal.pgen.1002799.s010
10. Cheng C-H, Lo Y-H, Liang S-S, Ti S-C, Lin F-M, Yeh C-H, Huang H-Y, Wang T-F. 2006. SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of saccharomyces cerevisiae. Genes & Development 20:2067-2081. doi:10.1101/gad.1430406
11. Christophorou N, Rubin T, Huynh Jean-René. 2013. Synaptonemal complex components promote centromere pairing in pre-meiotic germ cells. PLoS Genetics 9:e1004012 doi:10.1371/journal.pgen.1004012
12. Chua PR, Roeder GS. 1998. Zip2, a meiosis-specific protein required for the initiation of chromosome synapsis. Cell 93:349-359. doi:10.1016/S0092-8674(00)81164-2
13. Collins KA, Callicoat JG, Lake CM, Mcclurken CM, Kohl KP, Hawley RS. 2012. A germline clone screen on the x chromosome reveals novel meiotic mutants in drosophila melanogaster. G3 (Bethesda) 2:1369-1377. doi:10.1534/g3.112.003723
14. Collins KA, Unruh JR, Slaughter BD, Yu Z, Lake CM, Nielsen RJ, Box KS, Miller DE, Blumenstiel JP, Perera AG, Malanowski KE, Hawley RS. 2014. Corolla is a novel protein that contributes to the architecture of the synaptonemal complex of drosophila. Genetics 198:219-228. doi:10.1534/genetics.114.165290
15. de Massy B. 2013. Initiation of meiotic recombination: how and where? conservation and specificities among eukaryotes. Annual Review of Genetics 47:563-599. doi:10.1146/annurev-genet-110711-155423
16. de Muyt A, Zhang L, Piolot T, Kleckner N, Espagne E, Zickler D. 2014. E3 ligase Hei10: a multifaceted structure-based signaling molecule with roles within and beyond meiosis. Genes & Development 28:1111-1123. doi:10.1101/gad.240408.114
17. Dernburg AF, Mcdonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. 1998. Meiotic recombination in c. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94: 387-398. doi:10.1016/S0092-8674(00)81481-6
18. Doren MV, Williamson AL, Lehmann R. 1998. Regulation of zygotic gene expression in drosophila primordial germ cells. Current Biology 8:243-246. doi:10.1016/S0960-9822(98)70091-0
19. Downs JA, Allard Stéphane, Jobin-Robitaille O, Javaheri A, Auger Andréanne, Bouchard N, Kron SJ, Jackson SP, Coˆ té J. 2004. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Molecular Cell 16:979-990. doi:10.1016/j.molcel.2004.12.003
20. Ghabrial A, Ray RP, Schupbach T. 1998. Okra and spindle-b encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in drosophila oogenesis. Genes & Development 12:2711-2723. doi:10.1101/gad.12.17.2711
21. Ghabrial A, Schüpbach T. 1999. Activation of a meiotic checkpoint regulates translation of gurken during drosophila oogenesis. Nature Cell Biology 1:354-357. doi:10.1038/14046
22. Hall BG. 2013. Building phylogenetic trees from molecular data with MEGA. Molecular Biology and Evolution 30: 1229-1235. doi:10.1093/molbev/mst012
23. Hawley RS, Irick H, Zitron AE, Haddox DA, Lohe A, New C, Whitley MD, Arbel T, Jang J, Mckim K. 1992. There are two mechanisms of achiasmate segregation in drosophila females, one of which requires heterochromatic homology. Developmental Genetics 13:440-467. doi:10.1002/dvg.1020130608
24. Hu Y, Flockhart I, Vinayagam A, Bergwitz C, Berger B, Perrimon N, Mohr SE. 2011. An integrative approach to ortholog prediction for disease-focused and other functional studies. BMC Bioinformatics 12:357 doi:10.1534/genetics.109.103630
25. Jang JK, Sherizen DE, Bhagat R, Manheim EA, Mckim KS. 2003. Relationship of DNA double-strand breaks to synapsis in drosophila. Journal of Cell Science 116:3069-3077. doi:10.1242/jcs.00614
26. Jantsch V, Pasierbek P, Mueller MM, Schweizer D, Jantsch M, Loidl J. 2004. Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in caenorhabditis elegans. Molecular and Cellular Biology 24:7998-8006. doi:10.1128/MCB.24.18.7998-8006.2004
27. Jeffress JK, Page SL, Royer SK, Belden ED, Blumenstiel JP, Anderson LK, Hawley RS. 2007. The formation of the central element of the synaptonemal complex may occur by multiple mechanisms: the roles of the n-and c-terminal domains of the drosophila C(3)G protein in mediating synapsis and recombination. Genetics 177: 2445-2456. doi:10.1534/genetics.107.078717
28. Joyce EF, Apostolopoulos N, Beliveau BJ, Wu C-Ting. 2013. Germline progenitors escape the widespread phenomenon of homolog pairing during drosophila development. PLoS Genetics 9:e1004013 doi:10.1371/journal.pgen.1004013
29. Keeney S, Giroux CN, Kleckner N. 1997. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375-384. doi:10.1016/S0092-8674(00)81876-0
30. King RC, Rubinson AC, Smith RF. 1956. Oogenesis in adult drosophila melanogaster. Growth 20:121-157.
31. Kong A, Thorleifsson G, Stefansson H, Masson G, Helgason A, Gudbjartsson DF, Jonsdottir GM, Gudjonsson SA, Sverrisson S, Thorlacius T, Jonasdottir A, Hardarson GA, Palsson ST, Frigge ML, Gulcher JR, Thorsteinsdottir U, Stefansson K. 2008. Sequence variants in the RNF212 gene associate with genome-wide recombination rate. Science 319:1398-1401. doi:10.1126/science.1152422
32. Lake CM, Holsclaw JK, Bellendir SP, Sekelsky J, Hawley RS. 2013. The development of a monoclonal antibody recognizing the drosophila melanogaster phosphorylated histone H2A variant (-H2AV). Genetics 3:1539-1543. doi:10.1534/g3.113.006833
33. Lake CM, Nielsen RJ, Hawley RS. 2011. The drosophila zinc finger protein trade embargo is required for double strand break formation in meiosis. PLoS Genetics 7:e1002005 doi:10.1371/journal.pgen.1002005
34. Lindsley DL, Sandler L, Counce SJ, Chandley AC, Lewis KR. 1977. The genetic analysis of meiosis in female drosophila melanogaster [and discussion]. Philosophical Transactions of the Royal Society B: Biological Sciences 277:295-312. doi:10.1098/rstb.1977.0019
35. Liu H, Jang JK, Kato N, Mckim KS. 2002. Mei-P22 encodes a chromosome-associated protein required for the initiation of meiotic recombination in drosophila melanogaster. Genetics 162:245-258.
36. Lupas A, van Dyke M, Stock J. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164. doi:10.1126/science.252.5009.1162
37. Martins T, Maia André F, Steffensen S, Sunkel CE. 2009. Sgt1, a co-chaperone of Hsp90 stabilizes polo and is required for centrosome organization. The EMBO Journal 28:234-247. doi:10.1038/emboj.2008.283
38. Matsubayashi H, Yamamoto M-T. 2003. REC, a new member of the MCM-related protein family, is required for meiotic recombination in drosophila. Genes & Genetic Systems 78:363-371. doi:10.1266/ggs.78.363
39. Mckim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R, Hawley RS. 1998. Meiotic synapsis in the absence of recombination. Science 279:876-878. doi:10.1126/science.279.5352.876
40. 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 & Development 12:2932-2942. doi:10.1101/gad.12.18.2932
41. Mehrotra S, Mckim KS. 2006. Temporal analysis of meiotic DNA double-strand break formation and repair in drosophila females. PLoS Genetics 2:e200 doi:10.1371/journal.pgen.0020200
42. Metzger MB, Pruneda JN, Klevit RE, Weissman AM. 2014. RING-type E3 ligases: master manipulators of E2 ubiquitin-conjugating enzymes and ubiquitination. Biochimica Et Biophysica Acta 1843:47-60. doi:10.1016/j.bbamcr.2013.05.026
43. Moens PB, Kolas NK, Tarsounas M, Marcon E, Cohen PE, Spyropoulos B. 2002. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination. Journal of Cell Science 115:1611-1622.
44. Murakami H, Keeney S. 2008. Regulating the formation of DNA double-strand breaks in meiosis. Genes & Development 22:286-292. doi:10.1101/gad.1642308
45. Ouspenski II, Elledge SJ, Brinkley BR. 1999. New yeast genes important for chromosome integrity and segregation identified by dosage effects on genome stability. Nucleic Acids Research 27:3001-3008. doi:10.1093/nar/27.15.3001
46. Page SL, Hawley RS. 2001. C(3)G encodes a drosophila synaptonemal complex protein. Genes & Development 15:3130-3143. doi:10.1101/gad.935001
47. Page SL, Hawley RS. 2003. Chromosome choreography: the meiotic ballet. Science 301:785-789. doi:10.1126/science.1086605
48. Page SL, Hawley RS. 2004. The genetics and molecular biology of the synaptonemal complex. Annual Review of Cell and Developmental Biology 20:525-558. doi:10.1146/annurev.cellbio.19.111301.155141
49. Page SL, Khetani RS, Lake CM, Nielsen RJ, Jeffress JK, Warren WD, Bickel SE, Hawley RS. 2008. Corona is required for higher-order assembly of transverse filaments into full-length synaptonemal complex in drosophila oocytes. PLoS Genetics 4:e1000194 doi:10.1371/journal.pgen.1000194
50. Qiao H, Prasada Rao HBD, Yang Y, Fong JH, Cloutier JM, Deacon DC, Nagel KE, Swartz RK, Strong E, Holloway JK, Cohen PE, Schimenti J, Ward J, Hunter N. 2014. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nature Genetics 46:194-199. doi:10.1038/ng.2858
51. Reynolds A, Qiao H, Yang Y, Chen JK, Jackson N, Biswas K, Holloway JK, Baudat Frédéric, de Massy B, Wang J, Höög C, Cohen PE, Hunter N. 2013. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nature Genetics 45:269-278. doi:10.1038/ng.2541
52. Roeder GS. 1997. Meiotic chromosomes: it takes two to tango. Genes & Development 11:2600-2621. doi:10.1101/gad.11.20.2600
53. Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. The Journal of Cell Biology 146:905-916. doi:10.1083/jcb.146.5.905
54. Romanienko PJ, Camerini-Otero RD. 2000. The mouse Spo11 gene is required for meiotic chromosome synapsis. Molecular Cell 6:975-987. doi:10.1016/S1097-2765(00)00097-6
55. Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, Dernburg AF, Villeneuve AM. 2013. The c. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genetics 9:e1003674 doi:10.1371/journal.pgen.1003674
56. Serrentino M-E, Chaplais E, Sommermeyer Vérane, Borde Valérie. 2013. Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genetics 9:e1003416 doi:10.1371/journal.pgen.1003416
57. Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM, Petrini JH, Haber JE, Lichten M. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Current Biology 14:1703-1711. doi:10.1016/j.cub.2004.09.047
58. Smolikov S, Schild-Prüfert K, Colaiácovo Mónica P. 2009. A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in caenorhabditis elegans meiosis. PLoS Genetics 5:e1000669 doi:10.1371/journal.pgen.1000669
59. Strong ER, Schimenti JC. 2010. Evidence implicating CCNB1IP1, a RING domain-containing protein required for meiotic crossing over in mice, as an E3 SUMO ligase. Genes 1:440-451. doi:10.3390/genes1030440
60. Sym M, Engebrecht J, Roeder GS. 1993. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365-378. doi:10.1016/0092-8674(93)90114-6
61. Takeo S, Hawley RS, Aigaki T. 2010. Calcineurin and its regulation by Sra/RCAN is required for completion of meiosis in drosophila. Developmental Biology 344:957-967. doi:10.1016/j.ydbio.2010.06.011
62. Takeo S, Lake CM, Morais-de-Sá E, Sunkel Cláudio E, Hawley RS. 2011. Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in drosophila oocytes. Current Biology 21:1845-1851. doi:10.1016/j.cub.2011.09.044
63. Tanneti NS, Landy K, Joyce EF, Mckim KS. 2011. A pathway for synapsis initiation during zygotene in drosophila oocytes. Current Biology 21:1852-1857. doi:10.1016/j.cub.2011.10.005
64. Thacker D, Mohibullah N, Zhu X, Keeney S. 2014. Homologue engagement controls meiotic DNA break number and distribution. Nature 510:241-246. doi:10.1038/nature13120
65. Toby GG, Gherraby W, Coleman TR, Golemis EA. 2003. A novel RING finger protein, human enhancer of invasion 10, alters mitotic progression through regulation of cyclin b levels. Molecular and Cellular Biology 23: 2109-2122. doi:10.1128/MCB.23.6.2109-2122.2003
66. Wang K, Wang M, Tang D, Shen Y, Miao C, Hu Q, Lu T, Cheng Z. 2012. The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genetics 8:e1002809 doi:10.1371/journal.pgen.1002809
67. Ward JO, Reinholdt LG, Motley WW, Niswander LM, Deacon DC, Griffin LB, Langlais KK, Backus VL, Schimenti KJ, O’Brien MJ, Eppig JJ, Schimenti JC. 2007. Mutation in mouse hei10, an e3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genetics 3:e139 doi:10.1371/journal.pgen.0030139
68. Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. 2012. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell 149:75-87. doi:10.1016/j.cell.2012.01.052
69. Zickler D, Kleckner N. 1999. Meiotic chromosomes: integrating structure and function. Annual Review of Genetics 33:603-754. doi:10.1146/annurev.genet.33.1.603
70. Zimmering S. 1976. Genetic and cytogenetic aspects of altered segregation phenomena in Drosophila. In: Ashburner M, Novitski E. eds, The genetics and biology of drosophila. vol 1a. New York: Academic Press
71. Zitron AE, Hawley RS. 1989. The genetic analysis of distributive segregation in drosophila melanogaster. I. isolation and characterization of aberrant x segregation (axs), a mutation defective in chromosome partner choice. Genetics 122:801-821. Lake