DNA structure modulates the oligomerization properties of the AAV initiator protein Rep68

PLoS Pathogens

Volumn 5, Issue 7, 2009, Pages

  Mansilla Soto, Jorge ^a   Yoon Robarts, Miran ^a   Rice, William J ^b   Arya, Shailee ^a   Escalante, Carlos R ^a,c   Linden, R Michael ^a,d  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK STRUCTURAL BIOLOGY CENTER   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E1; HELICASE; HETERODUPLEX; NUCLEIC ACID BINDING PROTEIN; PROTEIN LTAG; PROTEIN REP68; SF3 ENZYME; UNCLASSIFIED DRUG; VIRUS DNA; DNA BINDING PROTEIN; E1 PROTEIN, BOVINE PAPILLOMAVIRUS; REP PROTEINS, ADENO ASSOCIATED VIRUS 2; REP PROTEINS, ADENO-ASSOCIATED VIRUS 2; SINGLE STRANDED DNA; VIRUS PROTEIN; VIRUS T ANTIGEN;

ADENO ASSOCIATED VIRUS; ARTICLE; COMPLEX FORMATION; CRYOBIOLOGY; DNA BINDING; DNA REPLICATION; DNA STRUCTURE; FEMALE; HUMAN; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE; CHEMISTRY; CONFORMATION; CRYOELECTRON MICROSCOPY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN MULTIMERIZATION;

ADENO-ASSOCIATED VIRUS; BOVINE PAPILLOMAVIRUS; PARVOVIRUS; SIMIAN VIRUS 40;

ANTIGENS, POLYOMAVIRUS TRANSFORMING; CRYOELECTRON MICROSCOPY; DEPENDOVIRUS; DNA, SINGLE-STRANDED; DNA, VIRAL; DNA-BINDING PROTEINS; NUCLEIC ACID CONFORMATION; PROTEIN MULTIMERIZATION; VIRAL PROTEINS;

EID: 70049085266     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000513     Document Type: Article

References (38)

1. Dutheil N, Linden RM (2006) Site-specific integration by adeno-associated virus. In: Kerr JRCS, Bloom ME, Linden RM, Parrish CR, eds. Parvoviruses. London: Edward Arnold Limited. pp 213-236.
2. Linden RM, Berns KI (2000) Molecular biology of adeno-associated viruses. Contrib Microbiol 4: 68-84.
3. Chejanovsky N, Carter BJ (1989) Mutagenesis of an AUG codon in the adeno-associated virus rep gene: effects on viral DNA replication. Virology 173: 120-128. (Pubitemid 19268255)
4. King JA, Dubielzig R, Grimm D, Kleinschmidt JA (2001) DNA helicase-mediated packaging of adeno-associated virus type 2 genomes into preformed capsids. Embo J 20: 3282-3291. (Pubitemid 32612015)
5. Hermonat PL, Labow MA, Wright R, Berns KI, Muzyczka N (1984) Genetics of adeno-associated virus: isolation and preliminary characterization of adeno-associated virus type 2 mutants. J Virol 51: 329-339. (Pubitemid 14091419)
6. Holscher C, Kleinschmidt JA, Burkle A (1995) High-level expression of adeno-associated virus (AAV) Rep78 or Rep68 protein is sufficient for infectious-particle formation by a rep-negative AAV mutant. J Virol 69: 6880-6885.
7. Tratschin JD, Miller IL, Carter BJ (1984) Genetic analysis of adeno-associated virus: properties of deletion mutants constructed in vitro and evidence for an adeno-associated virus replication function. J Virol 51: 611-619.
8. Surosky RT, Urabe M, Godwin SG, McQuiston SA, Kurtzman GJ, et al. (1997) Adeno-associated virus Rep proteins target DNA sequences to a unique locus in the human genome. J Virol 71: 7951-7959. (Pubitemid 27391747)
9. Walker SL, Wonderling RS, Owens RA (1997) Mutational analysis of the adeno-associated virus type 2 Rep68 protein helicase motifs. J Virol 71: 6996-7004.
10. Stenlund A (2003) Initiation of DNA replication: lessons from viral initiator proteins. Nat Rev Mol Cell Biol 4: 777-785.
11. Dignam SS, Correia JJ, Nada SE, Trempe JP, Dignam JD (2007) Activation of the ATPase activity of adeno-associated virus Rep68 and Rep78. Biochemistry 46: 6364-6374.
12. Li Z, Brister JR, Im DS, Muzyczka N (2003) Characterization of the adenoassociated virus Rep protein complex formed on the viral origin of DNA replication. Virology 313: 364-376. (Pubitemid 37040679)
13. Smith RH, Spano AJ, Kotin RM (1997) The Rep78 gene product of adeno-associated virus (AAV) self-associates to form a hexameric complex in the presence of AAV ori sequences. J Virol 71: 4461-4471.
14. James JA, Escalante CR, Yoon-Robarts M, Edwards TA, Linden RM, et al. (2003) Crystal structure of the SF3 helicase from adeno-associated virus type 2. Structure 11: 1025-1035. (Pubitemid 36966791)
15. James JA, Aggarwal AK, Linden RM, Escalante CR (2004) Structure of adeno-associated virus type 2 Rep40-ADP complex: insight into nucleotide recognition and catalysis by superfamily 3 helicases. Proc Natl Acad Sci U S A 101: 12455-12460.
16. Yoon-Robarts M, Blouin AG, Bleker S, Kleinschmidt JA, Aggarwal AK, et al. (2004) Residues within the B′ motif are critical for DNA binding by the superfamily 3 helicase Rep40 of adeno-associated virus type 2. J Biol Chem 279: 50472-50481. (Pubitemid 39577866)
17. Urabe M, Hasumi Y, Kume A, Surosky RT, Kurtzman GJ, et al. (1999) Charged-to-alanine scanning mutagenesis of the N-terminal half of adeno-associated virus type 2 Rep78 protein. J Virol 73: 2682-2693. (Pubitemid 29135653)
18. Hickman AB, Ronning DR, Perez ZN, Kotin RM, Dyda F (2004) The nuclease domain of adeno-associated virus rep coordinates replication initiation using two distinct DNA recognition interfaces. Mol Cell 13: 403-414.
19. Erzberger JP, Berger JM (2006) Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu Rev Biophys Biomol Struct 35: 93-114. (Pubitemid 43877371)
20. Valle M, Chen XS, Donate LE, Fanning E, Carazo JM (2006) Structural basis for the cooperative assembly of large T antigen on the origin of replication. J Mol Biol 357: 1295-1305. (Pubitemid 43357989)
21. Hickman AB, Ronning DR, Kotin RM, Dyda F (2002) Structural unity among viral origin binding proteins: crystal structure of the nuclease domain of adeno-associated virus Rep. Mol Cell 10: 327-337.
22. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
23. Ryan JH, Zolotukhin S, Muzyczka N (1996) Sequence requirements for binding of Rep68 to the adeno-associated virus terminal repeats. J Virol 70: 1542-1553. (Pubitemid 26062912)
24. Wu J, Davis MD, Owens RA (1999) Factors affecting the terminal resolution site endonuclease, helicase, and ATPase activities of adeno-associated virus type 2 Rep proteins. J Virol 73: 8235-8244. (Pubitemid 29441685)
25. Garcia De La Torre J, Huertas ML, Carrasco B (2000) Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys J 78: 719-730. (Pubitemid 30211830)
26. Sclafani RA, Fletcher RJ, Chen XS (2004) Two heads are better than one: regulation of DNA replication by hexameric helicases. Genes Dev 18: 2039-2045. (Pubitemid 39166621)
27. Brister JR, Muzyczka N (1999) Rep-mediated nicking of the adeno-associated virus origin requires two biochemical activities, DNA helicase activity and transesterification. J Virol 73: 9325-9336.
28. Ward P (2006) Replication of adeno-associated virus DNA. In: Kerr JRCS, Bloom ME, Linden RM, Parrish CR, eds. Parvoviruses. London: Edward Arnold Limited. pp 189-211.
29. Linden RM, Winocour E, Berns KI (1996) The recombination signals for adeno-associated virus site-specific integration. Proc Natl Acad Sci U S A 93: 7966-7972. (Pubitemid 26277148)
30. Lamartina S, Ciliberto G, Toniatti C (2000) Selective cleavage of AAVS1 substrates by the adeno-associated virus type 2 rep68 protein is dependent on topological and sequence constraints. J Virol 74: 8831-8842. (Pubitemid 30759581)
31. Weitzman MD, Kyostio SR, Kotin RM, Owens RA (1994) Adeno-associated virus (AAV) Rep proteins mediate complex formation between AAV DNA and its integration site in human DNA. Proc Natl Acad Sci U S A 91: 5808-5812.
32. Yoon M, Smith DH, Ward P, Medrano FJ, Aggarwal AK, et al. (2001) Aminoterminal domain exchange redirects origin-specific interactions of adeno-associated virus rep78 in vitro. J Virol 75: 3230-3239. (Pubitemid 32225886)
33. Escalante CR, Nistal-Villan E, Shen L, Garcia-Sastre A, Aggarwal AK (2007) Structure of IRF-3 bound to the PRDIII-I regulatory element of the human interferon-beta enhancer. Mol Cell 26: 703-716. (Pubitemid 46856241)
34. Schuck P (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys J 78: 1606-1619.
35. Cole JL (2004) Analysis of heterogeneous interactions. Meth Enzymol 384: 212-232.
36. 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. (Pubitemid 26093143)
37. Meinke G, Bullock PA, Bohm A (2006) Crystal structure of the simian virus 40 large T-antigen origin-binding domain. J Virol 80: 4304-4312.
38. Enemark EJ, Joshua-Tor L (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442: 270-275. (Pubitemid 44114897)