NatB Domain-Containing CRA-1 Antagonizes Hydrolase ACER-1 Linking Acetyl-CoA Metabolism to the Initiation of Recombination during C. elegans Meiosis

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Gao, Jinmin ^a   Kim, Hyun Min ^a   Elia, Andrew E ^a   Elledge, Stephen J ^a   Colaiácovo, Monica P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A HYDROLASE; DOUBLE STRANDED DNA; PEPTIDE ALPHA N ACETYLTRANSFERASE B; PROTEIN ACER 1; PROTEIN CRA 1; PROTEIN NAA25; PROTEIN XND 1; REGULATOR PROTEIN; UNCLASSIFIED DRUG; ACER-1 PROTEIN, C ELEGANS; ACETYL COENZYME A; CAENORHABDITIS ELEGANS PROTEIN; CRA-1 PROTEIN, C ELEGANS; HISTONE;

ARTICLE; CAENORHABDITIS ELEGANS; DNA STRAND BREAKAGE; ENZYME METABOLISM; HISTONE ACETYLATION; MEIOTIC RECOMBINATION; NONHUMAN; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; ACETYLATION; ANIMAL; DOUBLE STRANDED DNA BREAK; GENETIC RECOMBINATION; GENETICS; METABOLISM; X CHROMOSOME;

CAENORHABDITIS ELEGANS;

ACETYL COENZYME A; ACETYL-COA HYDROLASE; ACETYLATION; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA BREAKS, DOUBLE-STRANDED; HISTONES; RECOMBINATION, GENETIC; X CHROMOSOME;

EID: 84926221647     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005029     Document Type: Article

References (52)

1. Hassold T, Hunt P, (2001) To err (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2: 280–291. 11283700
2. Garcia-Cruz R, Roig I, Caldes MG, (2009) Maternal origin of the human aneuploidies. Are homolog synapsis and recombination to blame? Notes (learned) from the underbelly. Genome Dyn 5: 128–136. doi: 10.1159/000166638 18948712
3. Keeney S, (2001) Mechanism and control of meiotic recombination initiation. Curr Top Dev Biol 52: 1–53. 11529427
4. Arora C, Kee K, Maleki S, Keeney S, (2004) Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 13: 549–559. 14992724
5. Li J, Hooker GW, Roeder GS, (2006) Saccharomyces cerevisiae Mer2, Mei4 and Rec114 form a complex required for meiotic double-strand break formation. Genetics 173: 1969–1981. 16783010
6. Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, et al. (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386: 414–417. 9121560
7. 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. 9039264
8. 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. 9708740
9. Blat Y, Protacio RU, Hunter N, Kleckner N, (2002) Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation. Cell 111: 791–802. 12526806
10. Kumar R, Bourbon HM, de Massy B, (2010) Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev 24: 1266–1280. doi: 10.1101/gad.571710 20551173
11. Panizza S, Mendoza MA, Berlinger M, Huang L, Nicolas A, et al. (2011) Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination. Cell 146: 372–383. doi: 10.1016/j.cell.2011.07.003 21816273
12. Sommermeyer V, Beneut C, Chaplais E, Serrentino ME, Borde V, (2013) Spp1, a Member of the Set1 Complex, Promotes Meiotic DSB Formation in Promoters by Tethering Histone H3K4 Methylation Sites to Chromosome Axes. Mol Cell 49: 43–54. doi: 10.1016/j.molcel.2012.11.008 23246437
13. Pan J, Keeney S, (2007) Molecular cartography: mapping the landscape of meiotic recombination. PLoS Biol 5: e333. 18092891
14. Petes TD, (2001) Meiotic recombination hot spots and cold spots. Nat Rev Genet 2: 360–369. 11331902
15. Borde V, Robine N, Lin W, Bonfils S, Geli V, et al. (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28: 99–111. doi: 10.1038/emboj.2008.257 19078966
16. Buard J, Barthes P, Grey C, de Massy B, (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28: 2616–2624. doi: 10.1038/emboj.2009.207 19644444
17. Brick K, Smagulova F, Khil P, Camerini-Otero RD, Petukhova GV, (2012) Genetic recombination is directed away from functional genomic elements in mice. Nature 485: 642–645. doi: 10.1038/nature11089 22660327
18. Tischfield SE, Keeney S, (2012) Scale matters: the spatial correlation of yeast meiotic DNA breaks with histone H3 trimethylation is driven largely by independent colocalization at promoters. Cell Cycle 11: 1496–1503. doi: 10.4161/cc.19733 22433953
19. Baker CL, Walker M, Kajita S, Petkov PM, Paigen K, (2014) PRDM9 binding organizes hotspot nucleosomes and limits Holliday junction migration. Genome Res 24: 724–732. doi: 10.1101/gr.170167.113 24604780
20. Yamada S, Ohta K, Yamada T, (2013) Acetylated Histone H3K9 is associated with meiotic recombination hotspots, and plays a role in recombination redundantly with other factors including the H3K4 methylase Set1 in fission yeast. Nucleic Acids Res 41: 3504–3517. doi: 10.1093/nar/gkt049 23382177
21. Galdieri L, Vancura A, (2012) Acetyl-CoA carboxylase regulates global histone acetylation. J Biol Chem 287: 23865–23876. doi: 10.1074/jbc.M112.380519 22580297
22. Takahashi H, McCaffery JM, Irizarry RA, Boeke JD, (2006) Nucleocytosolic acetyl-coenzyme a synthetase is required for histone acetylation and global transcription. Mol Cell 23: 207–217. 16857587
23. Colaiacovo MP, (2006) The many facets of SC function during C. elegans meiosis. Chromosoma 115: 195–211. 16555015
24. Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, et al. (2003) Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell 5: 463–474. 12967565
25. Mets DG, Meyer BJ, (2009) Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell 139: 73–86. doi: 10.1016/j.cell.2009.07.035 19781752
26. Nottke AC, Beese-Sims SE, Pantalena LF, Reinke V, Shi Y, et al. (2011) SPR-5 is a histone H3K4 demethylase with a role in meiotic double-strand break repair. Proc Natl Acad Sci U S A 108: 12805–12810. doi: 10.1073/pnas.1102298108 21768382
27. Saito TT, Mohideen F, Meyer K, Harper JW, Colaiacovo MP, (2012) SLX-1 is required for maintaining genomic integrity and promoting meiotic noncrossovers in the Caenorhabditis elegans germline. PLoS Genet 8: e1002888. doi: 10.1371/journal.pgen.1002888 22927825
28. Rosu S, Libuda DE, Villeneuve AM, (2011) Robust crossover assurance and regulated interhomolog access maintain meiotic crossover number. Science 334: 1286–1289. doi: 10.1126/science.1212424 22144627
29. Wagner CR, Kuervers L, Baillie DL, Yanowitz JL, (2010) xnd-1 regulates the global recombination landscape in Caenorhabditis elegans. Nature 467: 839–843. doi: 10.1038/nature09429 20944745
30. Smolikov S, Schild-Prufert K, Colaiacovo MP, (2008) CRA-1 uncovers a double-strand break-dependent pathway promoting the assembly of central region proteins on chromosome axes during C. elegans meiosis. PLoS Genet 4: e1000088. doi: 10.1371/journal.pgen.1000088 18535664
31. Starheim KK, Arnesen T, Gromyko D, Ryningen A, Varhaug JE, et al. (2008) Identification of the human N(alpha)-acetyltransferase complex B (hNatB): a complex important for cell-cycle progression. Biochem J 415: 325–331. doi: 10.1042/BJ20080658 18570629
32. Kelly WG, Schaner CE, Dernburg AF, Lee MH, Kim SK, et al. (2002) X-chromosome silencing in the germline of C. elegans. Development 129: 479–492. 11807039
33. Fong Y, Bender L, Wang W, Strome S, (2002) Regulation of the different chromatin states of autosomes and X chromosomes in the germ line of C. elegans. Science 296: 2235–2238. 12077420
34. Bender LB, Suh J, Carroll CR, Fong Y, Fingerman IM, et al. (2006) MES-4: an autosome-associated histone methyltransferase that participates in silencing the X chromosomes in the C. elegans germ line. Development 133: 3907–3917. 16968818
35. Sung P, (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265: 1241–1243. 8066464
36. Bessler JB, Andersen EC, Villeneuve AM, (2010) Differential localization and independent acquisition of the H3K9me2 and H3K9me3 chromatin modifications in the Caenorhabditis elegans adult germ line. PLoS Genet 6: e1000830. doi: 10.1371/journal.pgen.1000830 20107519
37. Meneely PM, McGovern OL, Heinis FI, Yanowitz JL, (2012) Crossover distribution and frequency are regulated by him-5 in Caenorhabditis elegans. Genetics 190: 1251–1266. doi: 10.1534/genetics.111.137463 22267496
38. Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, Janicki SM, Greenberg RA, (2010) ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141: 970–981. doi: 10.1016/j.cell.2010.04.038 20550933
39. Reddy KC, Villeneuve AM, (2004) C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell 118: 439–452. 15315757
40. Hodgkin J, Horvitz HR, Brenner S, (1979) Nondisjunction Mutants of the Nematode CAENORHABDITIS ELEGANS. Genetics 91: 67–94. 17248881
41. Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, et al. (2009) ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324: 1076–1080. doi: 10.1126/science.1164097 19461003
42. Wellen KE, Thompson CB, (2012) A two-way street: reciprocal regulation of metabolism and signalling. Nat Rev Mol Cell Biol 13: 270–276. doi: 10.1038/nrm3305 22395772
43. Morran LT, Cappy BJ, Anderson JL, Phillips PC, (2009) Sexual partners for the stressed: facultative outcrossing in the self-fertilizing nematode Caenorhabditis elegans. Evolution 63: 1473–1482. doi: 10.1111/j.1558-5646.2009.00652.x 19210536
44. Frokjaer-Jensen C, Davis MW, Hopkins CE, Newman BJ, Thummel JM, et al. (2008) Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40: 1375–1383. doi: 10.1038/ng.248 18953339
45. Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM, et al. (2013) Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10: 741–743. doi: 10.1038/nmeth.2532 23817069
46. MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM, (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16: 2428–2442. 12231631
47. Stergiou L, Eberhard R, Doukoumetzidis K, Hengartner MO, (2011) NER and HR pathways act sequentially to promote UV-C-induced germ cell apoptosis in Caenorhabditis elegans. Cell Death Differ 18: 897–906. doi: 10.1038/cdd.2010.158 21151025
48. Phillips CM, Wong C, Bhalla N, Carlton PM, Weiser P, et al. (2005) HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell 123: 1051–1063. 16360035
49. Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, et al. (2008) HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell 14: 263–274. doi: 10.1016/j.devcel.2007.11.016 18267094
50. Timmons L, Court DL, Fire A, (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103–112. 11223248
51. Witkowski A, Witkowska HE, Smith S, (1994) Reengineering the specificity of a serine active-site enzyme. Two active-site mutations convert a hydrolase to a transferase. J Biol Chem 269: 379–383. 8276823
52. Fleck CB, Brock M, (2009) Re-characterisation of Saccharomyces cerevisiae Ach1p: fungal CoA-transferases are involved in acetic acid detoxification. Fungal Genet Biol 46: 473–485. doi: 10.1016/j.fgb.2009.03.004 19298859