Binding and unwinding: SF3 viral helicases

Current Opinion in Structural Biology

Volumn 15, Issue 1 SPEC. ISS., 2005, Pages 77-85

  Hickman, Alison Burgess ^a   Dyda, Fred ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DOUBLE STRANDED DNA; ENZYME VARIANT; HELICASE; PEPTIDE; RECA PROTEIN; VIRUS ENZYME; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; CORRELATION ANALYSIS; CRYSTAL STRUCTURE; DNA DETERMINATION; DNA HELIX; DNA PROTEIN COMPLEX; DNA REPLICATION; DNA VIRUS; ENZYME ANALYSIS; ENZYME BINDING; ENZYME STRUCTURE; GENOME ANALYSIS; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN STRUCTURE; REVIEW; RNA ANALYSIS; RNA VIRUS; SIMIAN VIRUS 40; STRUCTURE ANALYSIS;

EID: 13844254123     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.12.001     Document Type: Review

References (51)

1. M.R. Singleton, and D.B. Wigley Modularity and specialization in superfamily 1 and 2 helicases J Bacteriol 184 2002 1819 1826
2. S.S. Patel, and K.M. Picha Structure and function of hexameric helicases Annu Rev Biochem 69 2000 651 697
3. N. Tuteja, and R. Tuteja Prokaryotic and eukaryotic DNA helicases Eur J Biochem 271 2004 1835 1848
4. R.M. Story, I.T. Weber, and T.A. Steitz The structure of the E. coli recA protein monomer and polymer Nature 355 1992 318 325
5. H.S. Subramanya, L.E. Bird, J.A. Brannigan, and D.B. Wigley Crystal structure of a DExx box DNA helicase Nature 384 1996 379 383
6. S.S. Velankar, P. Soultanas, M.S. Dillingham, H.S. Subramanya, and D.B. Wigley Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism Cell 97 1999 75 84
7. M.R. Sawaya, S. Guo, S. Tabor, C.C. Richardson, and T. Ellenberger Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7 Cell 99 1999 167 177
8. M.R. Singleton, M.R. Sawaya, T. Ellenberger, and D.B. Wigley Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides Cell 101 2000 589 600
9. J.M. Caruthers, and D.B. McKay Helicase structure and mechanism Curr Opin Struct Biol 12 2002 123 133
10. A.E. Gorbalenya, and E.V. Koonin Helicases: amino acid sequence comparisons and structure-function relationships Curr Opin Struct Biol 3 1993 419 429
11. A.E. Gorbalenya, E.V. Koonin, and Y.I. Wolf A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses FEBS Lett 262 1990 145 148
12. L.M. Iyer, D.D. Leipe, E.V. Koonin, and L. Aravind Evolutionary history and higher order classification of AAA+ ATPases J Struct Biol 146 2004 11 31 This paper reviews the 15 currently available structures of AAA+ proteins and provides a brief description of the 26 identified families of AAA+ ATPases.
13. E.V. Koonin A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication Nucleic Acids Res 21 1993 2541 2547
14. N. Tuteja, and R. Tuteja Unraveling DNA helicases Eur J Biochem 271 2004 1849 1863
15. D. Li, R. Zhao, W. Lilyestrom, D. Gai, R. Zhang, J.A. DeCaprio, E. Fanning, A. Jochimiak, G. Szakonyi, and X.S. Chen Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen Nature 423 2003 512 518 This paper reports the first structure of an SF3 helicase and demonstrates the structural basis of hexamerization. The protein forms a two-tiered assembly, with a positively charged hole in the center of the hexamer. Models incorporating an 'iris' motion are proposed for origin melting and DNA unwinding during replication.
16. J.A. James, C.R. Escalante, M. Yoon-Robarts, T.A. Edwards, R.M. Linden, and A.K. Aggarwal Crystal structure of the SF3 helicase from adeno-associated virus type 2 Structure 11 2003 1025 1035 This work reports the crystal structure of one of the four forms of Rep encoded by AAV and found in infected cells.
17. J.A. James, A.K. Aggarwal, R.M. Linden, and C.R. Escalante Structure of adeno-associated virus type 2 Rep40-ADP complex: insight into nucleotide recognition and catalysis by superfamily 3 helicases Proc Natl Acad Sci USA 101 2004 12455 12460
18. E.A. Abbate, J.M. Berger, and M.R. Botchan The X-ray structure of the papillomavirus helicase in complex with its molecular matchmaker E2 Genes Dev 18 2004 1981 1996 This paper reports the structure of a heterodimeric complex containing the E2 activation domain bound to the E1 helicase AAA+ domain. This complex represents a step along the pathway for the assembly of the hexameric helicase and demonstrates how E2 regulates the process by sterically preventing hexamerization.
19. J. Mendez, and B. Stillman Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins Bioessays 25 2003 1158 1167
20. Y. Ishimi A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex J Biol Chem 272 1997 24508 24513
21. K. Labib, and J.F. Diffley Is the MCM2-7 complex the eukaryotic DNA replication fork helicase? Curr Opin Genet Dev 11 2001 64 70
22. C.N. Cole, and S.D. Conzen Polyomaviridae: the viruses and their replication D.M. Knipe P.M. Howley Fundamental Virology edn 4 2001 Lippincott Williams & Wilkins Philadelphia 985 1018
23. M. Valle, C. Gruss, L. Halmer, J.M. Carazo, and L.E. Donate Large T-antigen double hexamers imaged at the simian virus 40 origin of replication Mol Cell Biol 20 2000 34 41
24. J.A. Borowiec, and J. Hurwitz Localized melting and structural changes in the SV40 origin of replication induced by T-antigen EMBO J 7 1988 3149 3158
25. P.M. Howley, and D.R. Lowy Papillomaviruses and their replication D.M. Knipe P.M. Howley Fundamental Virology edn 4 2001 Lippincott Williams & Wilkins Philadelphia 1019 1051
26. J.S. Liu, S.R. Kuo, A.M. Makhov, D.M. Cyr, J.D. Griffith, T.R. Broker, and L.T. Chow Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication J Biol Chem 273 1998 30704 30712
27. E.T. Fouts, X. Yu, E.H. Egelman, and M.R. Botchan Biochemical and electron microscopic image analysis of the hexameric E1 helicase J Biol Chem 274 1999 4447 4458
28. R.H. Smith, and R.M. Kotin Adeno-associated virus N.L. Craig R. Craigie M. Gellert A.M. Lambowitz Mobile DNA II 2002 ASM Press Washington DC 905 923
29. R.O. Snyder, D. Im, T. Ni, X. Xiao, R.J. Samulski, and N. Muzyczka Features of the adeno-associated virus origin involved in substrate recognition by the viral Rep protein J Virol 67 1993 6096 6104
30. P. Ward, M. Falkenberg, P. Elias, M. Weitzman, and R.M. Linden Rep-dependent initiation of adeno-associated virus type 2 DNA replication by a herpes simplex virus type 1 replication complex in a reconstituted system J Virol 75 2001 10250 10258
31. X. Zhou, I. Zolotukhin, D.S. Im, and N. Muzyczka Biochemical characterization of adeno-associated virus Rep68 DNA helicase and ATPase activities J Virol 73 1999 1580 1590
32. X. Luo, D.G. Sanford, P.A. Bullock, and W.W. Bachovchin Solution structure of the origin DNA-binding domain of SV40 T-antigen Nat Struct Biol 3 1996 1034 1039
33. E.J. Enemark, G. Chen, D.E. Vaughn, A. Stenlund, and L. Joshua-Tor Crystal structure of the DNA binding domain of the replication initiation protein E1 from papillomavirus Mol Cell 6 2000 149 158
34. A.B. Hickman, D.R. Ronning, R.M. Kotin, and F. Dyda Structural unity among viral origin binding proteins: crystal structure of the nuclease domain of adeno-associated virus Rep Mol Cell 10 2002 327 337
35. I.A. Mastrangelo, P.V. Hough, J.S. Wall, M. Dodson, F.B. Dean, and J. Hurwitz ATP-dependent assembly of double hexamers of SV40 T antigen at the viral origin of DNA replication Nature 338 1989 658 662
36. M.G. Gomez-Lorenzo, M. Valle, J. Frank, C. Gruss, C.O. Sorzano, X.S. Chen, L.E. Donate, and J.M. Carazo Large T antigen on the simian virus 40 origin of replication: a 3D snapshot prior to DNA replication EMBO J 22 2003 6205 6213 This three-dimensional cryo-EM study complements the crystallization work in [1] and provides experimental support for the models in [1]. Particularly tantalizing are strands of density, attributed to ssDNA, that protrude away from the interface between head-to-head hexamers.
37. B.Y. Lin, A.M. Makhov, J.D. Griffith, T.R. Broker, and L.T. Chow Chaperone proteins abrogate inhibition of the human papillomavirus (HPV) E1 replicative helicase by the HPV E2 protein Mol Cell Biol 22 2002 6592 6604
38. +: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes Genome Res 9 1999 27 43
39. M.J. Davey, D. Jeruzalmi, J. Kuriyan, and M. O'Donnell Motors and switches: AAA+ machines within the replisome Nat Rev Mol Cell Biol 3 2002 826 835
40. L. Holm, and C. Sander Dali/FSSP classification of three-dimensional protein folds Nucleic Acids Res 25 1997 231 234
41. R.H. Smith, and R.M. Kotin The Rep52 gene product of adeno-associated virus is a DNA helicase with 3′-to-5′ polarity J Virol 72 1998 4874 4881
42. G. Loeber, J.E. Stenger, S. Ray, R.E. Parsons, M.E. Anderson, and P. Tegtmeyer The zinc finger region of simian virus 40 large T antigen is needed for hexamer assembly and origin melting J Virol 65 1991 3167 3174
43. M. Yoon-Robarts, A.G. Blouin, S. Bleker, J.A. Kleinschmidt, A.K. Aggarwal, C.R. Escalante, and R.M. Linden Residues within the B′ motif are critical for DNA binding by the SF3 helicase Rep40 of adeno-associated virus type 2 J Biol Chem 279 2004 50472 50481
44. A.B. Hickman, D.R. Ronning, Z.N. Perez, R.M. Kotin, and F. Dyda The nuclease domain of adeno-associated virus Rep coordinates replication initiation using two distinct DNA recognition interfaces Mol Cell 13 2004 403 414
45. W.S. Joo, H.Y. Kim, J.D. Purviance, K.R. Sreekumar, and P.A. Bullock Assembly of T-antigen double hexamers on the simian virus 40 core origin requires only a subset of the available binding sites Mol Cell Biol 18 1998 2677 2687
46. K. Yamada, T. Miyata, D. Tsuchiya, T. Oyama, Y. Fujiwara, T. Ohnishi, H. Iwasaki, H. Shinagawa, M. Ariyoshi, K. Mayanagi, and K. Morikawa Crystal structure of the RuvA-RuvB complex: a structural basis for the Holliday junction migrating motor machinery Mol Cell 10 2002 671 681
47. J.A. King, R. Dubielzig, D. Grimm, and J.A. Kleinschmidt DNA helicase-mediated packaging of adeno-associated virus type 2 genomes into preformed capsids EMBO J 20 2001 3282 3291
48. R. Dubielzig, J.A. King, S. Weger, A. Kern, and J.A. Kleinschmidt Adeno-associated virus type 2 protein interactions: formation of pre-encapsidation complexes J Virol 73 1999 8989 8998
49. D. Gai, R. Zhao, D. Li, C.V. Finkielstein, and X.S. Chen Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen Cell 119 2004 47 60
50. A.R. Stewart, J.A. Lednicky, U.S. Benzick, M.J. Tevethia, and J.S. Butel Identification of a variable region at the carboxy terminus of SV40 large T-antigen Virology 221 1996 355 361
51. S. Titolo, K. Brault, J. Majewski, P.W. White, and J. Archambault Characterization of the minimal DNA binding domain of the human papillomavirus E1 helicase: fluorescence anisotropy studies and characterization of a dimerization-defective mutant protein J Virol 77 2003 5178 5191