Conformational changes in adeno-associated virus type 1 induced by genome packaging

Journal of Molecular Biology

Volumn 409, Issue 3, 2011, Pages 427-438

  Gerlach, Britta ^a   Kleinschmidt, Jürgen A ^a   Böttcher, Bettina ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

AAV1; conformational changes; cryo electron microscopy; DNA packaging; icosahedral image reconstruction

Indexed keywords

CAPSID PROTEIN; PHOSPHOLIPASE;

ADENO ASSOCIATED VIRUS; ADENO ASSOCIATED VIRUS TYPE 1; ARTICLE; BETA SHEET; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; IMAGE RECONSTRUCTION; LIFE CYCLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; VIRUS CAPSID; VIRUS GENOME; VIRUS MORPHOLOGY;

ADENO-ASSOCIATED VIRUS; ADENO-ASSOCIATED VIRUS - 1; MIRIDAE;

EID: 79956061794     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.062     Document Type: Article

References (52)

1. Calcedo R., Vandenberghe L.H., Gao G., Lin J., and Wilson J.M. Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses J. Infect. Dis. 199 2009 381 390
2. Daya S., and Berns K.I. Gene therapy using adeno-associated virus vectors Clin. Microbiol. Rev. 21 2008 583 593
3. Gao G., Vandenberghe L.H., and Wilson J.M. New recombinant serotypes of AAV vectors Curr. Gene Ther. 5 2005 285 297 (Pubitemid 40895013)
4. Choi V.W., McCarty D.M., and Samulski R.J. AAV hybrid serotypes: improved vectors for gene delivery Curr. Gene Ther. 5 2005 299 310 (Pubitemid 40895014)
5. Gao G., Vandenberghe L.H., Alvira M.R., Lu Y., Calcedo R., Zhou X., and Wilson J.M. Clades of adeno-associated viruses are widely disseminated in human tissues J. Virol. 78 2004 6381 6388 (Pubitemid 38715936)
6. Summerford C., and Samulski R.J. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions J. Virol. 72 1998 1438 1445 (Pubitemid 28116931)
7. Handa A., Muramatsu S., Qiu J., Mizukami H., and Brown K.E. Adeno-associated virus (AAV)-3-based vectors transduce haematopoietic cells not susceptible to transduction with AAV-2-based vectors J. Gen. Virol. 81 2000 2077 2084 (Pubitemid 30599187)
8. Wu Z., Miller E., Agbandje-McKenna M., and Samulski R.J. Alpha2,3 and alpha2,6 N-linked sialic acids facilitate efficient binding and transduction by adeno-associated virus types 1 and 6 J. Virol. 80 2006 9093 9103 (Pubitemid 44359983)
9. Kaludov N., Brown K.E., Walters R.W., Zabner J., and Chiorini J.A. Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity J. Virol. 75 2001 6884 6893 (Pubitemid 32641575)
10. Walters R.W., Yi S.M., Keshavjee S., Brown K.E., Welsh M.J., Chiorini J.A., and Zabner J. Binding of adeno-associated virus type 5 to 2,3-linked sialic acid is required for gene transfer J. Biol. Chem. 276 2001 20610 20616
11. Salo R.J., and Mayor H.D. Structural polypeptides of parvoviruses Virology 78 1977 340 345 (Pubitemid 8110988)
12. Zadori Z., Szelei J., Lacoste M.C., Li Y., Gariepy S., and Raymond P. A viral phospholipase A2 is required for parvovirus infectivity Dev. Cell 1 2001 291 302 (Pubitemid 33653063)
13. Girod A., Wobus C.E., Zadori Z., Ried M., Leike K., and Tijssen P. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity J. Gen. Virol. 83 2002 973 978 (Pubitemid 34477268)
14. Sonntag F., Bleker S., Leuchs B., Fischer R., and Kleinschmidt J.A. Adeno-associated virus type 2 capsids with externalized VP1/VP2 trafficking domains are generated prior to passage through the cytoplasm and are maintained until uncoating occurs in the nucleus J. Virol. 80 2006 11040 11054 (Pubitemid 44706545)
15. Bleker S., Sonntag F., and Kleinschmidt J.A. Mutational analysis of narrow pores at the fivefold symmetry axes of adeno-associated virus type 2 capsids reveals a dual role in genome packaging and activation of phospholipase A2 activity J. Virol. 79 2005 2528 2540 (Pubitemid 40204607)
16. Kronenberg S., Bottcher B., von der Lieth C.W., Bleker S., and Kleinschmidt J.A. A conformational change in the adeno-associated virus type 2 capsid leads to the exposure of hidden VP1 N termini J. Virol. 79 2005 5296 5303 (Pubitemid 40548198)
17. Myers M.W., and Carter B.J. Assembly of adeno-associated virus Virology 102 1980 71 82
18. Ruffing M., Zentgraf H., and Kleinschmidt J.A. Assembly of viruslike particles by recombinant structural proteins of adeno-associated virus type 2 in insect cells J. Virol. 66 1992 6922 6930
19. Govindasamy L., Padron E., McKenna R., Muzyczka N., Kaludov N., Chiorini J.A., and Agbandje-McKenna M. Structurally mapping the diverse phenotype of adeno-associated virus serotype 4 J. Virol. 80 2006 11556 11570 (Pubitemid 44788870)
20. Nam H.J., Lane M.D., Padron E., Gurda B., McKenna R., and Kohlbrenner E. Structure of adeno-associated virus serotype 8, a gene therapy vector J. Virol. 81 2007 12260 12271 (Pubitemid 350085841)
21. Xie Q., Bu W., Bhatia S., Hare J., Somasundaram T., Azzi A., and Chapman M.S. The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy Proc. Natl Acad. Sci. USA 99 2002 10405 10410
22. Lerch T.F., Xie Q., and Chapman M.S. The structure of adeno-associated virus serotype 3B (AAV-3B): insights into receptor binding and immune evasion Virology 403 2010 26 36
23. Ng R., Govindasamy L., Gurda B.L., McKenna R., Kozyreva O.G., and Samulski R.J. Structural characterization of the dual glycan binding adeno-associated virus serotype 6 J. Virol. 84 2010 12945 12957
24. Kronenberg S., Kleinschmidt J.A., and Bottcher B. Electron cryo-microscopy and image reconstruction of adeno-associated virus type 2 empty capsids EMBO Rep. 2 2001 997 1002 (Pubitemid 33130605)
25. Levy H.C., Bowman V.D., Govindasamy L., McKenna R., Nash K., and Warrington K. Heparin binding induces conformational changes in adeno-associated virus serotype 2 J. Struct. Biol. 165 2009 146 156
26. O'Donnell J., Taylor K.A., and Chapman M.S. Adeno-associated virus-2 and its primary cellular receptor-cryo-EM structure of a heparin complex Virology 385 2009 434 443
27. Padron E., Bowman V., Kaludov N., Govindasamy L., Levy H., and Nick P. Structure of adeno-associated virus type 4 J. Virol. 79 2005 5047 5058 (Pubitemid 40464255)
28. Walters R.W., Agbandje-McKenna M., Bowman V.D., Moninger T.O., Olson N.H., and Seiler M. Structure of adeno-associated virus serotype 5 J. Virol. 78 2004 3361 3371 (Pubitemid 38568277)
29. Opie S.R., Warrington K.H. Jr, Agbandje-McKenna M., Zolotukhin S., and Muzyczka N. Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding J. Virol. 77 2003 6995 7006 (Pubitemid 36666892)
30. Kern A., Schmidt K., Leder C., Muller O.J., Wobus C.E., and Bettinger K. Identification of a heparin-binding motif on adeno-associated virus type 2 capsids J. Virol. 77 2003 11072 11081 (Pubitemid 37204297)
31. Agbandje-McKenna M., Llamas-Saiz A.L., Wang F., Tattersall P., and Rossmann M.G. Functional implications of the structure of the murine parvovirus, minute virus of mice Structure 6 1998 1369 1381 (Pubitemid 28541881)
32. Kaufmann B., Chipman P.R., Kostyuchenko V.A., Modrow S., and Rossmann M.G. Visualization of the externalized VP2 N termini of infectious human parvovirus B19 J. Virol. 82 2008 7306 7312 (Pubitemid 352031199)
33. Xie Q., and Chapman M.S. Canine parvovirus capsid structure, analyzed at 2.9 Å resolution J. Mol. Biol. 264 1996 497 520 (Pubitemid 27010741)
34. Kuck D., Kern A., and Kleinschmidt J.A. Development of AAV serotype-specific ELISAs using novel monoclonal antibodies J. Virol. Methods 140 2007 17 24 (Pubitemid 46185591)
35. Cotmore S.F., D'Abramo A.M., Ticknor C.M., and Tattersall P. Controlled conformational transitions in the MVM virion expose the VP1 N-terminus and viral genome without particle disassembly Virology 254 1999 169 181 (Pubitemid 29391724)
36. Harauz G., and Van Heel M. Exact filters for general geometry 3-dimensional reconstruction Optik 73 1986 146 156
37. Bottcher B., Wynne S.A., and Crowther R.A. Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy Nature 386 1997 88 91 (Pubitemid 27130926)
38. Finn R.D., Mistry J., Tate J., Coggill P., Heger A., and Pollington J.E. The Pfam protein families database Nucleic Acids Res. 38 2010 D211 D222
39. Ulyanov N.B., Bauer W.R., and James T.L. High-resolution NMR structure of an AT-rich DNA sequence J. Biomol. NMR 22 2002 265 280 (Pubitemid 34296109)
40. Kaludov N., Padron E., Govindasamy L., McKenna R., Chiorini J.A., and Agbandje-McKenna M. Production, purification and preliminary X-ray crystallographic studies of adeno-associated virus serotype 4 Virology 306 2003 1 6 (Pubitemid 36293389)
41. Lerch T.F., Xie Q., Ongley H.M., Hare J., and Chapman M.S. Twinned crystals of adeno-associated virus serotype 3b prove suitable for structural studies Acta Crystallogr. Sect. F 65 2009 177 183
42. Lane M.D., Nam H.J., Padron E., Gurda-Whitaker B., Kohlbrenner E., and Aslanidi G. Production, purification, crystallization and preliminary X-ray analysis of adeno-associated virus serotype 8 Acta Crystallogr. Sect. F 61 2005 558 561 (Pubitemid 44210843)
43. Kaufmann B., Simpson A.A., and Rossmann M.G. The structure of human parvovirus B19 Proc. Natl Acad. Sci. USA 101 2004 11628 11633 (Pubitemid 39095347)
44. Böttcher B., and Crowther R.A. Difference imaging reveals ordered regions of RNA in turnip yellow mosaic virus Structure 4 1996 387 394 (Pubitemid 126657533)
45. Ludtke S.J., Baldwin P.R., and Chiu W. EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97 (Pubitemid 30013436)
46. Crowther R.A., and Bottcher B. Electron cryomicroscopy of hepatitis B virus core shell D. Turk, L. Johnson, Methods in Macromolecular Crystallography 2001 IOS Press Amsterdam, The Netherlands 193 200
47. Crowther R.A., Kiselev N.A., Bottcher B., Berriman J.A., Borisova G.P., Ose V., and Pumpens P. Three-dimensional structure of hepatitis B virus core particles determined by Electron cryomicroscopy Cell 77 1994 943 950 (Pubitemid 24187691)
48. van Heel M., Harauz G., Orlova E.V., Schmidt R., and Schatz M. A new generation of the IMAGIC image processing system J. Struct. Biol. 116 1996 17 24 (Pubitemid 26093118)
49. Shaikh T.R., Gao H., Baxter W.T., Asturias F.J., Boisset N., Leith A., and Frank J. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs Nat. Protoc. 3 2008 1941 1974
50. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
51. Ross C.J., Twisk J., Bakker A.C., Miao F., Verbart D., and Rip J. Correction of feline lipoprotein lipase deficiency with adeno-associated virus serotype 1-mediated gene transfer of the lipoprotein lipase S447X beneficial mutation Hum. Gene. Ther. 17 2006 487 499 (Pubitemid 43794488)
52. Wobus C.E., Hugle-Dorr B., Girod A., Petersen G., Hallek M., and Kleinschmidt J.A. Monoclonal antibodies against the adeno-associated virus type 2 (AAV-2) capsid: epitope mapping and identification of capsid domains involved in AAV-2-cell interaction and neutralization of AAV-2 infection J. Virol. 74 2000 9281 9293