FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9087-9095

  Girard, Chloe ^a   Crismani, Wayne ^a,b   Froger, Nicole ^a   Mazel, Julien ^a   Lemhemdi, Afef ^a   Horlow, Christine ^a   Mercier, Raphael ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b Pioneer Dupont   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FANCM PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA GROUP E PROTEIN; FANCONI ANEMIA GROUP L PROTEIN; FANCONI ANEMIA PROTEIN; MHF1 PROTEIN; MHF2 PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ARABIDOPSIS; ARTICLE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CROSSING OVER; DNA REPAIR; FANCD2 GENE; FANCE GENE; FANCI GENE; FANCL GENE; GENE; GENE FUNCTION; GENE LOCUS; GENETIC DISTANCE; GENETIC SCREENING; GENOME ANALYSIS; MEIOTIC RECOMBINATION; METAPHASE; MHF1 GENE; MHF2 GENE; NONHUMAN; NONSENSE MUTATION; PLANT GENOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA BINDING; PROTEIN FUNCTION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA HELICASES; DNA-BINDING PROTEINS; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; MEIOSIS; MUTATION; RECOMBINATION, GENETIC;

EID: 84906233940     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku614     Document Type: Article

References (71)

1. Youds, J.L. and Boulton, S.J. (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J. Cell Sci., 124, 501-513.
2. Lynn, A., Soucek, R. and Börner, G.V. (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res., 15, 591-605.
3. Osman, K., Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J. and Franklin, F.C.H. (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol., 190, 523-544.
4. Berchowitz, L.E. and Copenhaver, G.P. (2010) Genetic interference: don't stand so close to me. Curr. Genomics, 11, 91-102.
5. Henderson, I.R. (2012) Control of meiotic recombination frequency in plant genomes. Curr. Opin. Plant Biol., 15, 556-561.
6. Crismani, W., Girard, C., Froger, N., Pradillo, M., Santos, J.L., Chelysheva, L., Copenhaver, G.P., Horlow, C. and Mercier, R. (2012) FANCM limits meiotic crossovers. Science, 336, 1588-1590.
7. Lorenz, A., Osman, F., Sun, W., Nandi, S., Steinacher, R. and Whitby, M.C. (2012) The fission yeast FANCM ortholog directs non-crossover recombination during meiosis. Science, 336, 1585-1588.
8. Deakyne, J.S. and Mazin, A. V. (2011) Fanconi anemia: at the crossroads of DNA repair. Biochemistry, 76, 36-48.
9. Kottemann, M.C. and Smogorzewska, A. (2013) Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature, 493, 356-363.
10. Yan, Z., Delannoy, M., Ling, C., Daee, D., Osman, F., Muniandy, P.A., Shen, X., Oostra, A.B., Du, H., Steltenpool, J. et al. (2010) A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol. Cell, 37, 865-878.
11. Singh, T.R., Saro, D., Ali, A.M., Zheng, X.-F., Du, C., Killen, M.W., Sachpatzidis, A., Wahengbam, K., Pierce, A.J., Xiong, Y. et al. (2010) MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell, 37, 879-886.
12. Ríos, G., Lossow, A., Hertel, B., Breuer, F., Schaefer, S., Broich, M., Kleinow, T., Jásik, J., Winter, J., Ferrando, A. et al. (2002) Rapid identification of Arabidopsis insertion mutants by non-radioactive detection of T-DNA tagged genes. Plant J., 32, 243-253.
13. Chelysheva, L., Gendrot, G., Vezon, D., Doutriaux, M.-P., Mercier, R. and Grelon, M. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet., 3, e83.
14. Macaisne, N., Novatchkova, M., Peirera, L., Vezon, D., Jolivet, S., Froger, N., Chelysheva, L., Grelon, M. and Mercier, R. (2008) SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers. Curr. Biol., 18, 1432-1437.
15. Higgins, J.D., Vignard, J., Mercier, R., Pugh, A.G., Franklin, F.C.H. and Jones, G.H. (2008) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J., 55, 28-39.
16. Berchowitz, L.E., Francis, K.E., Bey, A.L. and Copenhaver, G.P. (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet., 3, e132.
17. Stacey, N.J., Kuromori, T., Azumi, Y., Roberts, G., Breuer, C., Wada, T., Maxwell, A., Roberts, K. and Sugimoto-Shirasu, K. (2006) Arabidopsis SPO11-2 functions with SPO11-1 in meiotic recombination. Plant J., 48, 206-216.
18. Chelysheva, L., Vezon, D., Chambon, A., Gendrot, G., Pereira, L., Lemhemdi, A., Vrielynck, N., Le Guin, S., Novatchkova, M. and Grelon, M. (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet., 8, e1002799.
19. Berchowitz, L.E. and Copenhaver, G.P. (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat. Protoc., 3, 41-50.
20. Ross, K.J., Fransz, P. and Jones, G.H. (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosom. Res., 4, 507-516.
21. Chelysheva, L., Grandont, L., Vrielynck, N., le Guin, S., Mercier, R. and Grelon, M. (2010) An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res., 129, 143-153.
22. Malkova, A., Swanson, J., German, M., McCusker, J.H., Housworth, E.A., Stahl, F.W. and Haber, J.E. (2004) Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII. Genetics, 168, 49-63.
23. Perkins, D.D. (1949) Biochemical mutants in the smut fungus ustilago maydis. Genetics, 34, 607-626.
24. McCauley, J., Masand, N., McGowan, R., Rajagopalan, S., Hunter, A., Michaud, J.L., Gibson, K., Robertson, J., Vaz, F., Abbs, S. et al. (2011) X-linked VACTERL with hydrocephalus syndrome: further delineation of the phenotype caused by FANCB mutations. Am. J. Med. Genet. A, 155A, 2370-2380.
25. De Winter, J.P., Rooimans, M.A., van Der Weel, L., van Berkel, C.G., Alon, N., Bosnoyan-Collins, L., de Groot, J., Zhi, Y., Waisfisz, Q., Pronk, J.C. et al. (2000) The Fanconi anaemia gene FANCF encodes a novel protein with homology to ROM. Nat. Genet., 24, 15-16.
26. Meetei, A.R., Yan, Z. and Wang, W. (2004) FANCL replaces BRCA1 as the likely ubiquitin ligase responsible for FANCD2 monoubiquitination. Cell Cycle, 3, 179-181.
27. Marek, L.R. and Bale, A.E. (2006) Drosophila homologs of FANCD2 and FANCL function in DNA repair. DNA Repair (Amst)., 5, 1317-1326.
28. Knoll, A., Higgins, J.D., Seeliger, K., Reha, S.J., Dangel, N.J., Bauknecht, M., Schröpfer, S., Franklin, F.C.H. and Puchta, H. (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell, 24, 1448-1464.
29. Scheller, J., Schürer, A., Rudolph, C., Hettwer, S. and Kramer, W. (2000) MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics, 7, 1069-1081.
30. Prakash, R., Satory, D., Dray, E., Papusha, A., Scheller, J., Kramer, W., Krejci, L., Klein, H., Haber, J.E., Sung, P. et al. (2009) Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev., 23, 67-79.
31. Sun, W., Nandi, S., Osman, F., Ahn, J.S., Jakovleska, J., Lorenz, A. and Whitby, M.C. (2008) The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell, 32, 118-128.
32. Lee, K.Y., Chung, K.Y. and Koo, H.-S. (2010) The involvement of FANCM, FANCI, and checkpoint proteins in the interstrand DNA crosslink repair pathway is conserved in C. elegans. DNA Repair (Amst)., 9, 374-382.
33. Youds, J.L., Barber, L.J. and Boulton, S.J. (2009) C. elegans: a model of Fanconi anemia and ICL repair. Mutat. Res., 668, 103-116.
34. Dangel, N.J., Knoll, A. and Puchta, H. (2014) MHF1 plays FANCM-dependentand -independent roles in DNA repair and homologous recombination in plants. Plant J., 78, 822-833
35. Leung, J.W.C., Wang, Y., Fong, K.W., Huen, M.S.Y., Li, L. and Chen, J. (2012) Fanconi anemia (FA) binding protein FAAP20 stabilizes FA complementation group A (FANCA) and participates in interstrand cross-link repair. Proc. Natl. Acad. Sci. U.S.A., 109, 4491-4496.
36. Ciccia, A., Ling, C., Coulthard, R., Yan, Z., Xue, Y., Meetei, A.R., Laghmani, E.H., Joenje, H., McDonald, N., de Winter, J.P. et al. (2007) Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol. Cell, 25, 331-343.
37. Ling, C., Ishiai, M., Ali, A.M., Medhurst, A.L., Neveling, K., Kalb, R., Yan, Z., Xue, Y., Oostra, A.B., Auerbach, A.D. et al. (2007) FAAP100 is essential for activation of the Fanconi anemia-associated DNA damage response pathway. EMBO J., 26, 2104-2114.
38. Collis, S.J., Barber, L.J., Ward, J.D., Martin, J.S. and Boulton, S.J. (2006) C. elegans FANCD2 responds to replication stress and functions in interstrand cross-link repair. DNA Repair (Amst)., 5, 1398-1406.
39. Lee, K.Y., Yang, I., Park, J.E., Baek, O.R., Chung, K.Y. and Koo, H.S. (2007) Developmental stage- and DNA damage-specific functions of C. elegans FANCD2. Biochem. Biophys. Res. Commun., 352, 479-485.
40. Fontebasso, Y., Etheridge, T.J., Oliver, A.W., Murray, J.M. and Carr, A.M. (2013) The conserved Fanconi anemia nuclease Fan1 and the SUMO E3 ligase Pli1 act in two novel Pso2-independent pathways of DNA interstrand crosslink repair in yeast. DNA Repair (Amst)., 12, 1011-1023.
41. Kratz, K., Schöpf, B., Kaden, S., Sendoel, A., Eberhard, R., Lademann, C., Cannavó, E., Sartori, A.A., Hengartner, M.O. and Jiricny, J. (2010) Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell, 142, 77-88.
42. Smogorzewska, A., Desetty, R., Saito, T.T., Schlabach, M., Lach, F.P., Sowa, M.E., Clark, A.B., Kunkel, T.A., Harper, J.W., Colaiácovo, M.P. et al. (2010) A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol. Cell, 39, 36-47.
43. MacKay, C., Déclais, A.-C., Lundin, C., Agostinho, A., Deans, A.J., MacArtney, T.J., Hofmann, K., Gartner, A., West, S.C., Helleday, T. et al. (2010) Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell, 142, 65-76.
44. Klovstad, M., Abdu, U. and Schüpbach, T. (2008) Drosophila brca2 is required for mitotic and meiotic DNA repair and efficient activation of the meiotic recombination checkpoint. PLoS Genet., 4, e31.
45. Martin, J.S., Winkelmann, N., Petalcorin, M.I.R., McIlwraith, M.J. and Boulton, S.J. (2005) RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair. Mol. Cell. Biol., 25, 3127-3139.
46. Knoll, A. and Puchta, H. (2011) The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. J. Exp. Bot., 62, 1565-1579.
47. Youds, J.L., Barber, L.J., Ward, J.D., Collis, S.J., O'Neil, N.J., Boulton, S.J. and Rose, A.M. (2008) DOG-1 is the Caenorhabditis elegans BRIP1/FANCJ homologue and functions in interstrand cross-link repair. Mol. Cell. Biol., 28, 1470-1479.
48. Bleuyard, J.-Y., Gallego, M.E., Savigny, F. and White, C.I. (2005) Differing requirements for the Arabidopsis Rad51 paralogs in meiosis and DNA repair. Plant J., 41, 533-545.
49. Abdu, U., González-Reyes, A., Ghabrial, A. and Schüpbach, T. (2003) The Drosophila spn-D gene encodes a RAD51C-like protein that is required exclusively during meiosis. Genetics, 165, 197-204.
50. Ward, J.D., Barber, L.J., Petalcorin, M.I., Yanowitz, J. and Boulton, S.J. (2007) Replication blocking lesions present a unique substrate for homologous recombination. EMBO J., 26, 3384-3396.
51. Kang, M.H. (2011) Cancel all Hollidays for SLX4 mutations: identification of a new Fanconi anemia subtype, FANCP. Clin. Genet., 80, 28-30.
52. Mullen, J.R., Kaliraman, V., Ibrahim, S.S. and Brill, S.J. (2001) Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics, 157, 103-118.
53. Coulon, S., Gaillard, P.-H.L., Chahwan, C., McDonald, W.H., Yates, J.R. and Russell, P. (2004) Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell, 15, 71-80.
54. Andersen, S.L., Bergstralh, D.T., Kohl, K.P., LaRocque, J.R., Moore, C.B. and Sekelsky, J.J. (2009) Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell, 35, 128-135.
55. Majumder, S., Kramer, B., Sekelsky, J.J., Carolina, N. and Hill, C. (2002) Drosophila MUS312 Interacts with the Short Article MEI-9 to Generate Meiotic Crossovers. Mol. Cell, 10, 1503-1509.
56. Saito, T.T., Youds, J.L., Boulton, S.J. and Colaiácovo, M.P. (2009) Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet., 5, e1000735.
57. Bogliolo, M., Schuster, B., Stoepker, C., Derkunt, B., Su, Y., Raams, A., Trujillo, J.P., Minguillón, J., Ramírez, M.J., Pujol, R. et al. (2013) Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause fanconi anemia. Am. J. Hum. Genet., 92, 800-806.
58. Dubest, S., Gallego, M.E. and White, C.I. (2002) Role of the AtRad1p endonuclease in homologous recombination in plants. EMBO Rep., 3, 1049-1054.
59. Schiestl, R.H. and Prakash, S. (1988) RAD1, an excision repair gene of Saccharomyces cerevisiae is also involved in recombination. Mol. Cell. Biol., 8, 3619-3626.
60. Basmacioglu, C.N., Subramani, S., Clegg, M., Nasim, A., Carr, A.M., Schmidt, H., Kirchhoff, S., Muriel, W.J., Sheldrick, K.S., Griffiths, D.J. et al. (1994) he radl6 gene of Schizosaccharomyces pombe: a homolog of the RADI gene of Saccharomyces cerevisiae. Mol. Cell. Biol., 14, 2029-2040.
61. Dèrozier, S., Samson, F., Tamby, J.-P., Guichard, C., Brunaud, V., Grevet, P., Gagnot, S., Label, P., Leplé, J.-C., Lecharny, A. et al. (2011) Exploration of plant genomes in the FLAGdb++ environment. Plant Methods, 7, 8.
62. Lamesch, P., Berardini, T.Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M. et al. (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res., 40, D1202-D1210.
63. Dangel, N.J., Knoll, A. and Puchta, H. (2014) MHF1 plays Fanconi anaemia complementation group M protein (FANCM)-dependent and FANCM-independent roles in DNA repair and homologous recombination in plants. Plant J., 78, 822-833.
64. Siaud, N., Dray, E., Gy, I., Gérard, E., Takvorian, N. and Doutriaux, M.-P. (2004) Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J., 23, 1392-1401.
65. Abe, K., Osakabe, K., Nakayama, S., Endo, M., Tagiri, A., Todoriki, S., Ichikawa, H. and Toki, S. (2005) Arabidopsis RAD51C gene is important for homologous recombination in meiosis and mitosis. Plant Physiol., 139, 896-908.
66. Li, W., Yang, X., Lin, Z., Timofejeva, L., Xiao, R., Makaroff, C.A. and Ma, H. (2005) The AtRAD51C gene is required for normal meiotic chromosome synapsis and double-stranded break repair in Arabidopsis. Plant Physiol., 138, 965-976.
67. Crismani, W., Portemer, V., Froger, N., Chelysheva, L., Horlow, C., Vrielynck, N. and Mercier, R. (2013) MCM8 is required for a pathway of meiotic double-strand break repair independent of DMC1 in Arabidopsis thaliana. PLoS Genet., 9, e1003165.
68. Bhattacharjee, S., Osman, F., Feeney, L., Lorenz, A., Bryer, C. and Whitby, M.C. (2013) MHF1-2/CENP-S-X performs distinct roles in centromere metabolism and genetic recombination. Open Biol., 3, 130102.
69. Tao, Y., Jin, C., Li, X., Qi, S., Chu, L., Niu, L., Yao, X. and Teng, M. (2012) The structure of the FANCM-MHF complex reveals physical features for functional assembly. Nat. Commun., 3, 782.
70. Yang, H., Zhang, T., Tao, Y., Wu, L., Li, H., Zhou, J., Zhong, C. and Ding, J. (2012) Saccharomyces cerevisiae MHF complex structurally resembles the histones (H3-H4)2 heterotetramer and functions as a heterotetramer. Structure, 20, 364-370.
71. Whitby, M.C. (2010) The FANCM family of DNA helicases/translocases. DNA Repair (Amst)., 9, 224-236.