Human PSF concentrates DNA and stimulates duplex capture in DMC1-mediated homologous pairing

Nucleic Acids Research

Volumn 40, Issue 7, 2012, Pages 3031-3041

  Morozumi, Yuichi ^a   Ino, Ryohei ^a   Takaku, Motoki ^a   Hosokawa, Mihoko ^b   Chuma, Shinichiro ^b,c   Kurumizaka, Hitoshi ^a  

^a WASEDA UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DOUBLE STRANDED DNA; POLYPYRIMIDINE TRACT BINDING PROTEIN ASSOCIATED SPLICING FACTOR; PROTEIN DMC1; RECOMBINASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASE PAIRING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SPECIFICITY; MEIOSIS; MITOTIC RECOMBINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SPERMATID; SPERMATOCYTE; SPERMATOGONIUM;

ANIMALS; CELL CYCLE PROTEINS; DNA; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HOMOLOGOUS RECOMBINATION; HUMANS; MALE; MICE; NUCLEAR PROTEINS; RAD51 RECOMBINASE; RNA-BINDING PROTEINS; SPERMATOZOA;

EID: 84860168135     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1229     Document Type: Article

References (60)

1. Petronczki, M., Siomos, M.F. and Nasmyth, K. (2003) Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell, 112, 423-440. (Pubitemid 36263077)
2. Neale, M.J. and Keeney, S. (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature, 442, 153-158. (Pubitemid 44086556)
3. Pittman, D.L., Cobb, J., Schimenti, K.J., Wilson, L.A., Cooper, D.M., Brignull, E., Handel, M.A. and Schimenti, J.C. (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell, 1, 697-705. (Pubitemid 128379247)
4. Yoshida, K., Kondoh, G., Matsuda, Y., Habu, T., Nishimune, Y. and Morita, T. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell, 1, 707-718. (Pubitemid 128379248)
5. Bannister, A.A., Pezza, R.J., Donaldson, J.R., de Rooij, D.G., Schimenti, K.J., Camerini-Otero, R.D. and Schimenti, J.C. (2007) A dominant, recombination-defective allele of Dmc1 causing male-specific sterility. PLoS Biol., 5, 1-10.
6. Bishop, D.K., Park, D., Xu, L. and Kleckner, N. (1992) DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell, 69, 439-456.
7. Cox, M.M., Goodman, M.F., Kreuzer, K.N., Sherratt, D.J., Sandler, S.J. and Marians, K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41. (Pubitemid 30143124)
8. Symington, L.S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev., 66, 630-670. (Pubitemid 35425112)
9. West, S.C. (2003) Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell. Biol., 4, 435-445. (Pubitemid 36648589)
10. San Filippo, J., Sung, P. and Klein, H. (2008) Mechanism of Eukaryotic Homologous Recombination. Annu. Rev. Biochem., 77, 229-257.
11. Li, Z., Golub, E.I., Gupta, R. and Radding, C.M. (1997) Recombination activities of HsDmc1 protein, the meiotic human homolog of RecA protein. Proc. Natl Acad. Sci. USA, 94, 11221-11226. (Pubitemid 27450979)
12. Hong, E.L., Shinohara, A. and Bishop, D.K. (2001) Saccharomyces cerevisiae Dmc1 protein promotes renaturation of single-strand DNA (ssDNA) and assimilation of ssDNA into homologous super-coiled duplex DNA. J. Biol. Chem., 276, 41906-41912.
13. Kinebuchi, T., Kagawa, W., Enomoto, R., Tanaka, K., Miyagawa, K., Shibata, T., Kurumizaka, H. and Yokoyama, S. (2004) Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1. Mol. Cell, 14, 363-374. (Pubitemid 38591407)
14. Sehorn, M.G., Sigurdsson, S., Bussen, W., Unger, V.M. and Sung, P. (2004) Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature, 429, 433-437. (Pubitemid 38715136)
15. Bugreev, D.V., Golub, E.I., Stasiak, A.Z., Stasiak, A. and Mazin, A.V. (2005) Activation of human meiosis-specific recombinase Dmc1 by Ca2+. J. Biol. Chem., 280, 26886-26895. (Pubitemid 41040723)
16. Sakane, I., Kamataki, C., Takizawa, Y., Nakashima, M., Toki, S., Ichikawa, H., Ikawa, S., Shibata, T. and Kurumizaka, H. (2008) Filament formation and robust strand exchange activities of the rice DMC1A and DMC1B proteins. Nucleic Acids Res., 36, 4266-4276.
17. Petukhova, G.V., Pezza, R.J., Vanevski, F., Ploquin, M., Masson, J.Y. and Camerini-Otero, R.D. (2005) The Hop2 and Mnd1 proteins act in concert with Rad51 and Dmc1 in meiotic recombination. Nat. Struct. Mol. Biol., 12, 449-453. (Pubitemid 43085906)
18. Enomoto, R., Kinebuchi, T., Sato, M., Yagi, H., Kurumizaka, H. and Yokoyama, S. (2006) Simulation of DNA strand exchange by the human TBPIP/Hop2-Mnd1 complex. J. Biol. Chem., 281, 5575-5581. (Pubitemid 43847654)
19. Pezza, R.J., Petukhova, G.V., Ghirlando, R. and Camerini-Otero, R.D. (2006) Molecular activities of meiosis-specific proteins Hop2, Mnd1, and the Hop2-Mnd1 complex. J. Biol. Chem., 281, 18426-18434. (Pubitemid 44035501)
20. Ploquin, M., Petukhova, G.V., Morneau, D., Déry, U., Bransi, A., Stasiak, A., Camerini-Otero, R.D. and Masson, J.Y. (2007) Stimulation of fission yeast and mouse Hop2-Mnd1 of the Dmc1 and Rad51 recombinases. Nucleic Acids Res., 35, 2719-2733. (Pubitemid 47073684)
21. Pezza, R.J., Voloshin, O.N., Vanevski, F. and Camerini-Otero, R.D. (2007) Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. Genes Dev., 21, 1758-1766. (Pubitemid 47076475)
22. Haruta, N., Kurokawa, Y., Murayama, Y., Akamatsu, Y., Unzai, S., Tsutsui, Y. and Iwasaki, H. (2006) The Swi5-Sfr1 complex stimulates Rhp51/Rad51-and Dmc1-mediated DNA strand exchange in vitro. Nat. Struct. Mol. Biol., 13, 823-30. (Pubitemid 44338777)
23. Sarai, N., Kagawa, W., Kinebuchi, T., Kagawa, A., Tanaka, K., Miyagawa, K., Ikawa, S., Shibata, T., Kurumizaka, H. and Yokoyama, S. (2006) Stimulation of Dmc1-mediated DNA strand exchange by the human Rad54B protein. Nucleic Acids Res., 34, 4429-4437. (Pubitemid 44567042)
24. Sarai, N., Kagawa, W., Fujikawa, N., Saito, K., Hikiba, J., Tanaka, K., Miyagawa, K., Kurumizaka, H. and Yokoyama, S. (2008) Biochemical analysis of the N-terminal domain of human RAD54B. Nucleic Acids Res., 36, 5441-5450.
25. Dray, E., Dunlop, M.H., Kauppi, L., San Filippo, J., Wiese, C., Tsai, M.S., Begovic, S., Schild, D., Jasin, M. and Keeney, S. (2011) Molecular basis for enhancement of the meiotic DMC1 recombinase by RAD51 associated protein 1 (RAD51AP1). Proc. Natl Acad. Sci. USA, 108, 3560-3565.
26. Chi, P., San Filippo, J., Sehorn, M.G., Petukhova, G.V. and Sung, P. (2007) Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes Dev., 21, 1747-1757. (Pubitemid 47076474)
27. Modesti, M., Budzowska, M., Baldeyron, C., Demmers, J.A., Ghirlando, R. and Kanaar, R. (2007) RAD51AP1 is a structure-specific DNA binding protein that stimulates joint molecule formation during RAD51-mediated homologous recombination. Mol. Cell, 28, 468-481. (Pubitemid 350030562)
28. Wiese, C., Dray, E., Groesser, T., San Filippo, J., Shi, I., Collins, D.W., Tsai, M.S., Williams, G.J., Rydberg, B. and Sung, P. (2007) Promotion of homologous recombination and genomic stability by RAD51AP1 via RAD51 recombinase enhancement. Mol. Cell, 28, 482-490. (Pubitemid 350030564)
29. Patton, J.G., Porro, E.B., Galceran, J., Tempst, P. and Nadal-Ginard, B. (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev., 7, 393-406. (Pubitemid 23139233)
30. Kaneko, S., Rozenblatt-Rosen, O., Meyerson, M. and Manley, J.L. (2007) The multifunctional protein p54nrb/PSF recruits the exonuclease XRN2 to facilitate pre-mRNA 30 processing and transcription termination. Genes Dev., 21, 1779-1789. (Pubitemid 47076477)
31. Buxadé, M., Morrice, N., Krebs, D.L. and Proud, C.G. (2008) The PSF.p54nrb complex is a novel Mnk substrate that binds the mRNA for tumor necrosis factor a. J. Biol. Chem., 283, 57-65.
32. Urban, R.J., Bodenburg, Y., Kurosky, A., Wood, T.G. and Gasic, S. (2000) Polypyrimidine tract-binding protein-associated splicing factor is a negative regulator of transcriptional activity of the porcine p450scc insulin-like growth factor response element. Mol. Endocrinol., 14, 774-782. (Pubitemid 32260491)
33. Urban, R.J., Bodenburg, Y.H. and Wood, T.G. (2002) NH2 terminus of PTB-associated splicing factor binds to the porcine P450scc IGF-I response element. Am. J. Physiol. Endocrinol. Metab., 283, E423-E427. (Pubitemid 35230478)
34. Urban, R.J. and Bodenburg, Y. (2002) PTB-associated splicing factor regulates growth factor-stimulated gene expression in mammalian cells. Am. J. Physiol. Endocrinol. Metab., 283, E794-E798.
35. Song, X., Sui, A. and Garen, A. (2004) Binding of mouse VL30 retrotransposon RNA to PSF protein induces genes repressed by PSF: effects on steroidogenesis and oncogenesis. Proc. Natl Acad. Sci. USA, 101, 621-626. (Pubitemid 38084686)
36. Song, X., Sun, Y. and Garen, A. (2005) Roles of PSF protein and VL30 RNA in reversible gene regulation. Proc. Natl Acad. Sci. USA, 102, 12189-12193. (Pubitemid 41291150)
37. Bladen, C.L., Udayakumar, D., Takeda, Y. and Dynan, W.S. (2005) Identification of the polypyrimidine tract binding proteinassociated splicing factor.p54(nrb) complex as a candidate DNA double-strand break rejoining factor. J. Biol. Chem., 280, 5205-5210. (Pubitemid 40279991)
38. Salton, M., Lerenthal, Y., Wang, S.Y., Chen, D.J. and Shiloh, Y. (2010) Involvement of matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle, 9, 1568-1576.
39. Ha, K., Takeda, Y. and Dynan, W.S. (2011) Sequences in PSF/SFPQ mediate radioresistance and recruitment of PSF/SFPQ-containing complexes to DNA damage sites in human cells. DNA Repair, 10, 252-259.
40. Morozumi, Y., Takizawa, Y., Takaku, M. and Kurumizaka, H. (2009) Human PSF binds to RAD51 and modulates its homologous-pairing and strand-exchange activities. Nucleic Acids Res., 37, 4296-4307.
41. Rajesh, C., Baker, D.K., Pierce, A.J. and Pittman, D.L. (2011) The splicing-factor related protein SFPQ/PSF interacts with RAD51D and is necessary for homology-directed repair and sister chromatid cohesion. Nucleic Acids Res., 39, 132-145.
42. Akhmedov, A.T. and Lopez, B.S. (2000) Human 100-kDa homologous DNA-pairing protein is the splicing factor PSF and promotes DNA strand invasion. Nucleic Acids Res., 28, 3022-3030. (Pubitemid 30624091)
43. Kuwahara, S., Ikei, A., Taguchi, Y., Tabuchi, Y., Fujimoto, N., Obinata, M., Uesugi, S. and Kurihara, Y. (2006) PSPC1, NONO, and SFPQ are expressed in mouse Sertoli cells and may function as coregulators of androgen receptor-mediated transcription. Biol. Reprod., 75, 352-359. (Pubitemid 44268069)
44. Scherthan, H., Jerratsch, M., Li, B., Smith, S., Hultén, M., Lock, T. and de Lange, T. (2000) Mammalian meiotic telomeres: protein composition and redistribution in relation to nuclear pores. Mol. Biol. Cell, 11, 4189-4203.
45. Chuma, S. and Nakatsuji, N. (2001) Autonomous transition into meiosis of mouse fetal germ cells in vitro and its inhibition by gp130-mediated signaling. Dev. Biol., 229, 468-479. (Pubitemid 32108706)
46. Matsuo, Y., Sakane, I., Takizawa, Y., Takahashi, M. and Kurumizaka, H. (2006) Roles of the human Rad51 L1 and L2 loops in DNA binding. FEBS J., 273, 3148-3159. (Pubitemid 43990920)
47. Ishida, T., Takizawa, Y., Sakane, I. and Kurumizaka, H. (2008) The Lys313 residue of the human Rad51 protein negatively regulates the strand-exchange activity. Genes Cells, 13, 91-103.
48. Kurumizaka, H., Ikawa, S., Nakada, M., Eda, K., Kagawa, W., Takata, M., Takeda, S., Yokoyama, S. and Shibata, T. (2001) Homologous-pairing activity of the human DNA-repair proteins Xrcc3.Rad51C. Proc. Natl Acad. Sci. USA, 98, 5538-5543. (Pubitemid 32435677)
49. Kagawa, W., Kurumizaka, H., Ikawa, S., Yokoyama, S. and Shibata, T. (2001) Homologous pairing promoted by the human Rad52 protein. J. Biol. Chem., 276, 35201-35208.
50. Lio, Y.C., Mazin, A.V., Kowalczykowski, S.C. and Chen, D.J. (2003) Complex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro. J. Biol. Chem, 278, 2469-2478. (Pubitemid 36801323)
51. Takizawa, Y., Kinebuchi, T., Kagawa, W., Yokoyama, S., Shibata, T. and Kurumizaka, H. (2004) Mutational analyses of the human Rad51-Tyr315 residue, a site for phosphorylation in leukaemia cells. Genes Cells, 9, 781-790. (Pubitemid 39199906)
52. Takaku, M., Machida, S., Hosoya, N., Nakayama, S., Takizawa, Y., Sakane, I., Shibata, T., Miyagawa, K. and Kurumizaka, H. (2009) Recombination activator function of the novel RAD51-and RAD51B-binding protein, human EVL. J. Biol. Chem., 284, 14326-14336.
53. Takaku, M., Tsujita, T., Horikoshi, N., Takizawa, Y., Qing, Y., Hirota, K., Ikura, M., Ikura, T., Takeda, S. and Kurumizaka, H. (2011) Purification of the human SMN-GEMIN2 complex and assessment of its stimulation of RAD51-mediated DNA recombination reactions. Biochemistry, 50, 6797-6805.
54. Hsieh, P., Camerini-Otero, C.S. and Camerini-Otero, R.D. (1992) The synapsis event in the homologous pairing of DNAs: RecA recognizes and pairs less than one helical repeat of DNA. Proc. Natl Acad. Sci. USA, 89, 6492-6496.
55. Chow, S.A. and Radding, C.M. (1985) Ionic inhibition of formation of RecA nucleoprotein networks blocks homologous pairing. Proc. Natl Acad. Sci. USA, 82, 5646-5650.
56. Tsang, S.S., Chow, S.A. and Radding, C.M. (1985) Networks of DNA and RecA protein are intermediates in homologous pairing. Biochemistry, 24, 3226-3232. (Pubitemid 15028725)
57. Pezza, R.J., Camerini-Otero, R.D. and Bianco, P.R. (2010) Hop2-Mnd1 condenses DNA to stimulate the synapsis phase of DNA strand exchange. Biophys. J., 99, 3763-3772.
58. Kovalenko, O.V., Golub, E.I., Bray-Ward, P., Ward, D.C. and Radding, C.M. (1997) A novel nucleic acid-binding protein that interacts with human rad51 recombinase. Nucleic Acids Res., 25, 4946-4953. (Pubitemid 28022255)
59. Shinohara, M., Shita-Yamaguchi, E., Buerstedde, J.M., Shinagawa, H., Ogawa, H. and Shinohara, A. (1997) Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics, 147, 1545-1556.
60. Tanaka, K., Hiramoto, T., Fukuda, T. and Miyagawa, K. (2000) A novel human rad54 homologue, Rad54B, associates with Rad51. J. Biol. Chem., 275, 26316-26321.