Structure of the hDmc1-ssDNA filament reveals the principles of its architecture

PLoS ONE

Volumn 5, Issue 1, 2010, Pages

  Okorokov, Andrei L ^a   Chaban, Yuriy L ^b   Bugreev, Dmitry V ^c,d   Hodgkinson, Julie ^b   Mazin, Alexander V ^c   Orlova, Elena V ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d INSTITUTE OF CHEMICAL BIOLOGY AND FUNDAMENTAL MEDICINE   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; CALCIUM; DMC1 PROTEIN; DOUBLE STRANDED DNA; MAGNESIUM; NUCLEOPROTEIN; PROTEIN SUBUNIT; RAD51 PROTEIN; RECA PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; DMC1 PROTEIN, HUMAN; DNA BINDING PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA HELIX; DNA STRUCTURE; DNA TEMPLATE; ELECTRON MICROSCOPY; HUMAN; MEIOSIS; PRESYNAPTIC POTENTIAL; PROMOTER REGION; AGAR GEL ELECTROPHORESIS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; NUCLEOTIDE SEQUENCE;

EUKARYOTA;

ADENOSINE TRIPHOSPHATASES; BASE SEQUENCE; BINDING SITES; CELL CYCLE PROTEINS; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ELECTROPHORESIS, AGAR GEL; HUMANS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR;

EID: 77649161198     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0008586     Document Type: Article

References (55)

1. Page SL, Hawley RS (2003) Chromosome choreography: the meiotic ballet. Science 301: 785-789.
2. Bishop DK (2006) Multiple mechanisms of meiotic recombination. Cell 127: 1095-1097.
3. Neale MJ, Keeney S (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442: 153-158.
4. Hoeijmakers JH (2001) Genome maintenance mechanisms for preventing cancer. Nature 411: 366-374. 5. West SC (2003) Molecular views of recombination proteins and their control. Nat Rev Mol Cell Biol 6: 435-445.
5. Wyman C, Kanaar R (2006) DNA double-strand break repair: all's well that ends well. Annu Rev Genet 40: 363-383.
6. Lynn A, Ashley T, Hassold T (2004) Variation in human meiotic recombination. Annu Rev Genomics Hum Genet 5: 317-349.
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.
8. Seitz EM, Haseltine CA, Kowalczykowski SC (2001) DNA recombination and repair in the archaea. Adv Appl Microbiol 50: 101-169.
9. Masson JY, West SC (2001) The Rad51 and Dmc1 recombinases: a nonidentical twin relationship. Trends Biochem Sci 26: 131-136.
10. Bishop DK, Park D, Xu L, 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.
11. Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, et al. (1998) Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol Cell 1: 697-705.
12. Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, et al. (1998) The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol Cel 5: 707-718.
13. Masson JY, Davies AA, Hajibagheri N, Van Dyck E, Benson FE, et al. (1999) The meiosis-specific recombinase hDmc1 forms ring structures and interacts with hRad51. EMBO J 18: 6552-6560.
14. Schwacha A, Kleckner N (1997) Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell 90: 1123-1135.
15. Hunter N, Kleckner N (2001) The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell 106: 59-70.
16. Bannister LA, Pezza RJ, Donaldson JR, de Rooij DG, Schimenti KJ, et al. (2007) A dominant, recombination-defective allele of Dmc1 causing male-specific sterility. PLoS Biol 5: e105.
17. Passy SI, Yu X, Li Z, Radding CM, Masson JY, et al. (1999) Human Dmc1 protein binds DNA as an octameric ring. Proc Natl Acad Sci U S A 96: 10684-10688.
18. Shin DS, Pellegrini L, Daniels DS, Yelent B, Craig L, et al. (2003) Full-length archaeal Rad51 structure and mutants: mechanisms for RAD51 assembly and control by BRCA2. EMBO J 22: 4566-4576.
19. Conway AB, Lynch TW, Zhang Y, Fortin GS, Fung CW, et al. (2004) Crystal structure of a Rad51 filament. Nat Struct Mol Biol 11: 791-796.
20. Wu Y, He Y, Moya IA, Qian X, Luo Y (2004) Crystal structure of archaeal recombinase RADA: a snapshot of its extended conformation. Mol Cell 15(3): 423-435.
21. Kinebuchi T, Kagawa W, Enomoto R, Tanaka K, Miyagawa K, et al. (2004) Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1. Mol Cell 14: 363-374.
22. Wu Y, Qian X, He Y, Moya IA, Luo Y (2005) Crystal structure of an ATPase-active form of Rad51 homolog from Methanococcus voltae. Insights into potassium dependence. J Biol Chem 280: 722-728.
23. Chen LT, Ko TP, Chang YC, Lin KA, Chang CS, et al. (2007a) Crystal structure of the left-handed archaeal RadA helical filament: identification of a functional motif for controlling quaternary structures and enzymatic functions of RecA family proteins. Nucleic Acids Res 35: 1787-1801.
24. Chen LT, Ko TP, Chang YW, Lin KA, Wang AH, et al. (2007b) Structural and functional analyses of five conserved positively charged residues in the L1 and N-terminal DNA binding motifs of archaeal RADA protein. PLoS ONE 2(9): e858.
25. Yu X, Jacobs SA, West SC, Ogawa T, Egelman EH (2001) Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc Natl Acad Sci U S A 98: 8419-8424.
26. Galkin VE, Wu Y, Zhang XP, Qian X, He Y, et al. (2006) The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Structure 4: 983-92.
27. Kinebuchi T, Kagawa W, Kurumizaka H, Yokoyama S (2005) Role of the N-terminal domain of the human DMC1 protein in octamer formation and DNA binding. J Biol Chem 280: 28382-28387.
28. Yang S, Yu X, Seitz EM, Kowalczykowski SC, Egelman EH (2001) Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J Mol Biol 314: 1077-1085.
29. Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P (2004) Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429: 433-437.
30. 2+. J Biol Chem 280: 26886-26895.
31. Lee MH, Chang YC, Hong EL, Grubb J, Chang CS, et al. (2005) Calcium ion promotes yeast Dmc1 activity via formation of long and fine helical filaments with single-stranded DNA. J Biol Chem 280: 40980-40984.
32. Chang YC, Lo YH, Lee MH, Leng CH, Hu SM, et al. (2005) Molecular visualization of the yeast Dmc1 protein ring and Dmc1-ssDNA nucleoprotein complex. Biochemistry 44: 6052-8.
33. Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG, et al. (2008) A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res 36(12): 4057-4066.
34. Dube P, Tavares P, Lurz R, van Heel M (1993) The portal protein of bacteriophage SPP1: a DNA pump with 13-fold symmetry. EMBO J 12: 1303-1309.
35. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24.
36. VanLoock MS, Yu X, Yang S, Lai AL, Low C, et al. (2003) ATP-mediated conformational changes in the RecA filament. Structure 11: 187-196.
37. Chen Z, Yang H, Pavletich NP (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453 (7194): 489-494.
38. Aihara H, Ito Y, Kurumizaka H, Yokoyama S, Shibata T (1999) The N-terminal domain of the human Rad51 protein binds DNA: structure and a DNA binding surface as revealed by NMR. J Mol Biol 290: 495-504.
39. Navaza J, Lepault J, Rey FA, Alvarez-Rúa C, Borge J (2002) On the fitting of model electron densities into EM reconstructions: a reciprocal-space formulation. Acta Crystallogr D Biol Crystallogr 58: 1820-1825.
40. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera - A Visualization System for Exploratory Research and Analysis. J Comput Chem 25: 1605-1612.
41. Story RM, Weber IT, Steitz TA (1992) The structure of the E. coli recA protein monomer and polymer. Nature 355: 318-325.
42. Xing X, Bell CE (2004) Crystal structures of Escherichia coli RecA in a compressed helical filament. J Mol Biol 342: 1471-1485.
43. Nishinaka T, Ito Y, Yokoyama S, Shibata T (1997) An extended DNA structure through deoxyribose-base stacking induced by RecA protein. Proc Natl Acad Sci U S A 94: 6623-6628.
44. Stasiak A, Di Capua E, Koller T (1981) Elongation of duplex DNA by recA protein. J Mol Biol 151: 557-564.
45. Benson FE, Stasiak A, West SC (1994) Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J 13 (23): 5764-5771.
46. Egelman EH (2001) Does a stretched DNA structure dictate the helical geometry of RecA-like filaments? J Mol Biol 309: 539-542.
47. Kurumizaka H, Aihara H, Ikawa S, Kashima T, Bazemore LR, et al. (1996) A possible role of the C-terminal domain of the RecA protein. A gateway model for double-stranded DNA binding. J Biol Chem 271: 33515-33524.
48. Liu Y, Eisenberg D (2002) 3D domain swapping: as domains continue to swap. Protein Sci 11(6): 1285-1299.
49. Gupta RC, Golub E, Bi B, Radding CM (2001) The synaptic activity of HsDmc1, a human recombination protein specific to meiosis. Proc Natl Acad Sci U S A 98(15): 8433-8439.
50. van Heel M, Gowen B, Matadeen R, Orlova EV, Finn R, et al. (2000) Single-particle electron cryo-microscopy: towards atomic resolution. Q Rev Biophys 33: 307-369.
51. White HE, Saibil HR, Ignatiou A, Orlova EV (2004) Recognition and separation of single particles with size variation by statistical analysis of their images. J Mol Biol 336: 453-460.
52. Frank J, Radermacher M, Penczek P, Zhu J, Li Y, et al. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116: 190-199.
53. Radermacher M (1988) Three-dimensional reconstruction of single particles from random and nonrandom tilt series. J Electron Microsc Tech 9: 359-394.
54. Saxton WO, Baumeister W (1986) Principles of organization in S layers. J Mol Biol 187: 251-253.
55. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Research 31: 3381-3385.