Oligomeric properties of adeno-associated virus Rep68 reflect its multifunctionality

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 1232-1241

  Zarate Perez, Francisco ^a   Mansilla Soto, Jorge ^b   Bardelli, Martino ^c   Burgner II, John W ^a   Villamil Jarauat, Maria ^a   Kekilli, Demet ^d   Samso, Monserrat ^a   Linden, R Michael ^c,e   Escalante, Carlos R ^a  

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

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c ST THOMAS HOSPITAL   (United Kingdom)

^d UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CYSTEINE; DIMER; HEPTAMER; MONOMER; OCTAMER; OLIGOMER; PROTEIN REP68; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENO ASSOCIATED VIRUS; ARTICLE; BIOLOGICAL MODEL; CELL STRAIN HEK293; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; ELECTRON MICROSCOPY; GEL PERMEATION CHROMATOGRAPHY; GENETIC TRANSFECTION; HELA CELL; HYDRODYNAMIC MODELING; IN VITRO STUDY; MOLECULAR WEIGHT; MULTIPLE RING STRUCTURE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SEDIMENTATION VELOCITY ULTRACENTRIFUGATION; ULTRACENTRIFUGATION; VIRUS REPLICATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DEPENDOVIRUS; DNA-BINDING PROTEINS; HYDRODYNAMICS; MICROSCOPY, ELECTRON; PROTEIN MULTIMERIZATION; ULTRACENTRIFUGATION; VIRAL PROTEINS;

ADENO-ASSOCIATED VIRUS;

EID: 84871971837     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02441-12     Document Type: Article

References (53)

1. Hickman AB, Dyda F. 2005. Binding and unwinding: SF3 viral helicases. Curr. Opin. Struct. Biol. 15:77-85.
2. Singleton MR, Dillingham MS, Wigley DB. 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76:23-50.
3. + proteins. Annu. Rev. Biophys. Biomol. Struct. 35: 93-114.
4. + superfamily ATPases: common structure-diverse function. Genes Cells 6:575-597.
5. James JA, Escalante CR, Yoon-Robarts M, Edwards TA, Linden RM, Aggarwal AK. 2003. Crystal structure of the SF3 helicase from adenoassociated virus type 2. Structure 11:1025-1035.
6. Owens RA, Weitzman MD, Kyostio SR, Carter BJ. 1993. Identification of a DNA-binding domain in the amino terminus of adeno-associated virus Rep proteins. J. Virol. 67:997-1005.
7. Yoon-Robarts M, Blouin AG, Bleker S, Kleinschmidt JA, Aggarwal AK, Escalante CR, Linden RM. 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.
8. Chiorini JA, Wiener SM, Owens RA, Kyostio SR, Kotin RM, Safer B. 1994. Sequence requirements for stable binding and function of Rep68 on the adeno-associated virus type 2 inverted terminal repeats. J. Virol. 68: 7448-7457.
9. Chiorini JA, Yang L, Safer B, Kotin RM. 1995. Determination of adenoassociated virus Rep68 and Rep78 binding sites by random sequence oligonucleotide selection. J. Virol. 69:7334-7338.
10. Im DS, Muzyczka N. 1990. The AAV origin binding protein Rep68 is an ATP-dependent site-specific endonuclease with DNA helicase activity. Cell 61:447-457.
11. Kyostio SR, Wonderling RS, Owens RA. 1995. Negative regulation of the adeno-associated virus (AAV) P5 promoter involves both the P5 rep binding site and the consensus ATP-binding motif of the AAV Rep68 protein. J. Virol. 69:6787-6796.
12. Iyer LM, Koonin EV, Leipe DD, Aravind L. 2005. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res. 33: 3875-3896.
13. Dean FB, Borowiec JA, Eki T, Hurwitz J. 1992. The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. J. Biol. Chem. 267:14129-14137.
14. Sedman J, Stenlund A. 1998. The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities. J. Virol. 72:6893-6897.
15. Wessel R, Schweizer J, Stahl H. 1992. Simian virus 40 T-antigen DNA helicase is a hexamer which forms a binary complex during bidirectional unwinding from the viral origin of DNA replication. J. Virol. 66:804-815.
16. Berns KI. 1990. Parvovirus replication. Microbiol. Rev. 54:316-329.
17. Zhou X, Zolotukhin I, Im DS, Muzyczka N. 1999. Biochemical characterization of adeno-associated virus rep68 DNA helicase and ATPase activities. J. Virol. 73:1580-1590.
18. Brister JR, Muzyczka N. 2000. Mechanism of Rep-mediated adenoassociated virus origin nicking. J. Virol. 74:7762-7771.
19. Mansilla-Soto J, Yoon-Robarts M, Rice WJ, Arya S, Escalante CR, Linden RM. 2009. DNA structure modulates the oligomerization prop- erties of the AAV initiator protein Rep68. PLoS Pathog. 5:e1000513. doi: 10.1371/journal.ppat.1000513.
20. Maggin JE, James JA, Chappie JS, Dyda F, Hickman AB. 2012. The amino acid linker between the endonuclease and helicase domains of adeno- associated virus type 5 Rep plays a critical role in DNA-dependent oligomerization. J. Virol. 86:3337-3346.
21. Zarate-Perez F, Bardelli M, Burgner JW, II, Villamil-Jarauta M, Das K, Kekilli D, Mansilla-Soto J, Linden RM, Escalante CR. 2012. The interdomain linker of AAV-2 Rep68 is an integral part of its oligomerization domain: role of a conserved SF3 helicase residue in oligomerization. PLoS Pathog. 8:e1002764. doi:10.1371/journal.ppat.1002764.
22. 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.
23. Packman LC, Perham RN. 1982. Quaternary structure of the pyruvate dehydrogenase multienzyme complex of Bacillus stearothermophilus studied by a new reversible cross-linking procedure with bis(imidoesters). Biochemistry 21:5171-5175.
24. Schuck P. 2003. On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320:104-124.
25. Vistica J, Dam J, Balbo A, Yikilmaz E, Mariuzza RA, Rouault TA, Schuck P. 2004. Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition. Anal. Biochem. 326:234-256.
26. Bjornson KP, Amaratunga M, Moore KJ, Lohman TM. 1994. Singleturnover kinetics of helicase-catalyzed DNA unwinding monitored continuously by fluorescence energy transfer. Biochemistry 33:14306-14316.
27. Baginski ES, Foa PP, Zak B. 1967. Microdetermination of inorganic phosphate, phospholipids, and total phosphate in biologic materials. Clin. Chem. 13:326-332.
28. Zeltner N, Kohlbrenner E, Clement N, Weber T, Linden RM. 2010. Near-perfect infectivity of wild-type AAV as benchmark for infectivity of recombinant AAV vectors. Gene Ther. 17:872-879.
29. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, Sali A. 2000. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29:291-325.
30. Kim DE, Chivian D, Baker D. 2004. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 32:W526-W531. doi:10.1093/nar/gkh468.
31. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501.
32. Brookes E, Demeler B, Rosano C, Rocco M. 2010. The implementation of SOMO (SOlution MOdeller) in the UltraScan analytical ultracentrifugation data analysis suite: enhanced capabilities allow the reliable hydrodynamic modeling of virtually any kind of biomacromolecule. Eur. Biophys. J. 39:423-435.
33. 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.
34. Schuck P. 2000. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling. Biophys. J. 78:1606-1619.
35. Mueller-Cajar O, Stotz M, Wendler P, Hartl FU, Bracher A, Hayer- Hartl M. 2011. Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase. Nature 479:194-199.
36. Garcia de la Torre J, Navarro S, Lopez Martinez MC, Diaz FG, Lopez Cascales JJ. 1994. HYDRO: a computer program for the prediction of hydrodynamic properties of macromolecules. Biophys. J. 67:530-531.
37. Rai N, Nollmann M, Spotorno B, Tassara G, Byron O, Rocco M. 2005. SOMO (SOlution MOdeler) differences between X-ray- and NMRderived bead models suggest a role for side chain flexibility in protein hydrodynamics. Structure 13:723-734.
38. 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.
39. Crampton DJ, Ohi M, Qimron U, Walz T, Richardson CC. 2006. Oligomeric states of bacteriophage T7 gene 4 primase/helicase. J. Mol. Biol. 360:667-677.
40. Costa A, Pape T, van Heel M, Brick P, Patwardhan A, Onesti S. 2006. Structural basis of the Methanothermobacter thermautotrophicus MCM helicase activity. Nucleic Acids Res. 34:5829-5838.
41. Pape T, Meka H, Chen S, Vicentini G, van Heel M, Onesti S. 2003. Hexameric ring structure of the full-length archaeal MCM protein complex. EMBO Rep. 4:1079-1083.
42. Yu X, VanLoock MS, Poplawski A, Kelman Z, Xiang T, Tye BK, Egelman EH. 2002. The Methanobacterium thermoautotrophicum MCM protein can form heptameric rings. EMBO Rep. 3:792-797.
43. Akoev V, Gogol EP, Barnett ME, Zolkiewski M. 2004. Nucleotideinduced switch in oligomerization of the AAA+ ATPase ClpB. Protein Sci. 13:567-574.
44. Nikulin A, Stolboushkina E, Perederina A, Vassilieva I, Blaesi U, Moll I, Kachalova G, Yokoyama S, Vassylyev D, Garber M, Nikonov S. 2005. Structure of Pseudomonas aeruginosa Hfq protein. Acta Crystallogr. D Biol. Crystallogr. 61:141-146.
45. Thompson MW, Miller J, Maurizi MR, Kempner E. 1998. Importance of heptameric ring integrity for activity of Escherichia coli ClpP. Eur. J. Biochem. 258:923-928.
46. Stasiak AZ, Larquet E, Stasiak A, Muller S, Engel A, Van Dyck E, West SC, Egelman EH. 2000. The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10:337-340.
47. Crampton DJ, Mukherjee S, Richardson CC. 2006. DNA-induced switch from independent to sequential dTTP hydrolysis in the bacteriophage T7 DNA helicase. Mol. Cell 21:165-174.
48. Farris KD, Fasina O, Sukhu L, Li L, Pintel DJ. 2010. Adeno-associated virus small rep proteins are modified with at least two types of polyubiquitination. J. Virol. 84:1206-1211.
49. Sukhu L, Pintel D. 2011. The large Rep protein of adeno-associated virus type 2 is polyubiquitinated. J. Gen. Virol. 92:2792-2796.
50. Weger S, Hammer E, Heilbronn R. 2004. SUMO-1 modification regulates the protein stability of the large regulatory protein Rep78 of adeno associated virus type 2 (AAV-2). Virology 330:284-294.
51. Collaco R, Prasad KM, Trempe JP. 1997. Phosphorylation of the adenoassociated virus replication proteins. Virology 232:332-336.
52. Narasimhan D, Collaco R, Kalman-Maltese V, Trempe JP. 2002. Hyperphosphorylation of the adeno-associated virus Rep78 protein inhibits terminal repeat binding and helicase activity. Biochim. Biophys. Acta 1576: 298-305.
53. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ. 2005. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 33:W363-W367. doi:10.1093/nar/gki481.