Drosophila ERCC1 is Required for a Subset of MEI-9-dependent Meiotic Crossovers

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 2005 Jun 10

PMID 15944364

Citations 27

Authors

Sarah J Radford

Elizabeth Goley

Kimberly Baxter

Susan McMahan

Jeff Sekelsky

Affiliations

Soon will be listed here.

Abstract

Drosophila MEI-9 is the catalytic subunit of a DNA structure-specific endonuclease required for nucleotide excision repair (NER). The enzymatic activity of this endonuclease during NER requires the presence of a second, noncatalytic subunit called ERCC1. In addition to its role in NER, MEI-9 is required for the generation of most meiotic crossovers. To better understand the role of MEI-9 in crossover formation, we report here the characterization of the Drosophila Ercc1 gene. We created an Ercc1 mutant through homologous gene targeting. We find that Ercc1 mutants are identical to mei-9 mutants in sensitivity to DNA-damaging agents, but have a less severe reduction in the number of meiotic crossovers. MEI-9 protein levels are reduced in Ercc1 mutants; however, overexpression of MEI-9 is not sufficient to restore meiotic crossing over in Ercc1 mutants. We conclude that MEI-9 can generate some meiotic crossovers in an ERCC1-independent manner.

Citing Articles

Divergence and conservation of the meiotic recombination machinery.

Arter M, Keeney S Nat Rev Genet. 2023; 25(5):309-325.

PMID: 38036793 DOI: 10.1038/s41576-023-00669-8.

Meiotic Crossover Patterning.

Pazhayam N, Turcotte C, Sekelsky J Front Cell Dev Biol. 2021; 9:681123.

PMID: 34368131 PMC: 8344875. DOI: 10.3389/fcell.2021.681123.

Genetic mechanisms of formation of radiation-induced instability of the genome and its transgenerational effects in the descendants of chronically irradiated individuals of Drosophila melanogaster.

Yushkova E Radiat Environ Biophys. 2020; 59(2):221-236.

PMID: 32076810 DOI: 10.1007/s00411-020-00833-2.

The XPF-ERCC1 Complex Is Essential for Genome Stability and Is Involved in the Mechanism of Gene Targeting in .

Guyon-Debast A, Rossetti P, Charlot F, Epert A, Neuhaus J, Schaefer D Front Plant Sci. 2019; 10:588.

PMID: 31143199 PMC: 6521618. DOI: 10.3389/fpls.2019.00588.

A virus-acquired host cytokine controls systemic aging by antagonizing apoptosis.

Mlih M, Khericha M, Birdwell C, Phillip West A, Karpac J PLoS Biol. 2018; 16(7):e2005796.

PMID: 30036358 PMC: 6072105. DOI: 10.1371/journal.pbio.2005796.

References

Rong Y, Golic K . A targeted gene knockout in Drosophila. Genetics. 2001; 157(3):1307-12. PMC: 1461559. DOI: 10.1093/genetics/157.3.1307. View

Rong Y, Titen S, Xie H, Golic M, Bastiani M, Bandyopadhyay P . Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev. 2002; 16(12):1568-81. PMC: 186348. DOI: 10.1101/gad.986602. View

Park C, Bessho T, Matsunaga T, Sancar A . Purification and characterization of the XPF-ERCC1 complex of human DNA repair excision nuclease. J Biol Chem. 1995; 270(39):22657-60. DOI: 10.1074/jbc.270.39.22657. View

Gloor G, Preston C, Nassif N, Phillis R, Benz W, Robertson H . Type I repressors of P element mobility. Genetics. 1993; 135(1):81-95. PMC: 1205629. DOI: 10.1093/genetics/135.1.81. View

Yildiz O, Majumder S, Kramer B, Sekelsky J . Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol Cell. 2002; 10(6):1503-9. PMC: 3206640. DOI: 10.1016/s1097-2765(02)00782-7. View

Sekelsky J, Hollis K, Eimerl A, Burtis K, Hawley R . Nucleotide excision repair endonuclease genes in Drosophila melanogaster. Mutat Res. 2000; 459(3):219-28. DOI: 10.1016/s0921-8777(99)00075-0. View

Pirrotta V . Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988; 10:437-56. DOI: 10.1016/b978-0-409-90042-2.50028-3. View

Oh J, Bailin T, Fukai K, Feng G, Ho L, Mao J . Positional cloning of a gene for Hermansky-Pudlak syndrome, a disorder of cytoplasmic organelles. Nat Genet. 1996; 14(3):300-6. DOI: 10.1038/ng1196-300. View

Davies A, Friedberg E, Tomkinson A, Wood R, West S . Role of the Rad1 and Rad10 proteins in nucleotide excision repair and recombination. J Biol Chem. 1995; 270(42):24638-41. DOI: 10.1074/jbc.270.42.24638. View

10.

James P, Halladay J, Craig E . Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 1996; 144(4):1425-36. PMC: 1207695. DOI: 10.1093/genetics/144.4.1425. View

11.

Donaldson T, Noureddine M, Reynolds P, Bradford W, Duronio R . Targeted disruption of Drosophila Roc1b reveals functional differences in the Roc subunit of Cullin-dependent E3 ubiquitin ligases. Mol Biol Cell. 2004; 15(11):4892-903. PMC: 524738. DOI: 10.1091/mbc.e04-03-0180. View

12.

Drysdale R, Crosby M . FlyBase: genes and gene models. Nucleic Acids Res. 2004; 33(Database issue):D390-5. PMC: 540000. DOI: 10.1093/nar/gki046. View

13.

Houtsmuller A, Rademakers S, Nigg A, Hoogstraten D, Hoeijmakers J, Vermeulen W . Action of DNA repair endonuclease ERCC1/XPF in living cells. Science. 1999; 284(5416):958-61. DOI: 10.1126/science.284.5416.958. View

14.

Bardwell A, Bardwell L, Tomkinson A, Friedberg E . Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science. 1994; 265(5181):2082-5. DOI: 10.1126/science.8091230. View

15.

Yildiz O, Kearney H, Kramer B, Sekelsky J . Mutational analysis of the Drosophila DNA repair and recombination gene mei-9. Genetics. 2004; 167(1):263-73. PMC: 1470841. DOI: 10.1534/genetics.167.1.263. View

16.

Ivanov E, Haber J . RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol Cell Biol. 1995; 15(4):2245-51. PMC: 230452. DOI: 10.1128/MCB.15.4.2245. View

17.

Rong Y, Golic K . Gene targeting by homologous recombination in Drosophila. Science. 2000; 288(5473):2013-8. DOI: 10.1126/science.288.5473.2013. View

18.

Sekelsky J, McKim K, Chin G, Hawley R . The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1. Genetics. 1995; 141(2):619-27. PMC: 1206761. DOI: 10.1093/genetics/141.2.619. View

19.

Ivanov E, Sugawara N, Haber J . Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics. 1996; 142(3):693-704. PMC: 1207011. DOI: 10.1093/genetics/142.3.693. View

20.

Prakash L, Dumais D, Polakowska R, Perozzi G, Prakash S . Molecular cloning of the RAD10 gene of Saccharomyces cerevisiae. Gene. 1985; 34(1):55-61. DOI: 10.1016/0378-1119(85)90294-x. View