Adeno-associated virus capsid proteins may play a role in transcription and second-strand synthesis of recombinant genomes

Journal of Virology

Volumn 88, Issue 2, 2014, Pages 1071-1079

  Salganik, Maxim ^a,b   Aydemir, Fikret ^a   Nam, Hyun Joo ^a,c   McKenna, Robert ^a   Agbandje McKenna, Mavis ^a   Muzyczka, Nicholas ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c The University of Texas at Dallas   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; COMPLEMENTARY DNA; MESSENGER RNA; VIRUS DNA;

ADENO ASSOCIATED VIRUS; AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; DNA SECOND STRAND; DNA STRAND; DNA SYNTHESIS; GENOME ANALYSIS; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA SYNTHESIS; VIRAL GENE DELIVERY SYSTEM; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS GENOME; VIRUS MUTANT; VIRUS RECOMBINANT; VIRUS TRANSCRIPTION; VIRUS UNCOATING;

CAPSID PROTEINS; DEPENDOVIRUS; GENOME, VIRAL; HEK293 CELLS; HELA CELLS; HUMANS; MODELS, MOLECULAR; MUTATION; PARVOVIRIDAE INFECTIONS; RECOMBINATION, GENETIC; RNA, VIRAL; TRANSCRIPTION, GENETIC;

EID: 84891716579     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02093-13     Document Type: Article

References (35)

1. Bartlett JS, Wilcher R, Samulski RJ. 2000. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74:2777-2785. http://dx.doi.org/10.1128/JVI.74.6.2777-2785.2000.
2. Douar AM, Poulard K, Stockholm D, Danos O. 2001. Intracellular trafficking of adeno-associated virus vectors: routing to the late endosomal compartment and proteasome degradation. J. Virol. 75:1824-1833. http://dx.doi.org/10.1128/JVI.75.4.1824-1833.2001.
3. Hansen J, Qing K, Srivastava A. 2001. Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J. Virol. 75:4080-4090. http://dx.doi.org/10.1128/JVI.75.9.4080-4090.2001.
4. Sonntag F, Bleker S, Leuchs B, Fischer R, Kleinschmidt JA. 2006. 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. 80:11040-11054. http://dx.doi.org/10.1128/JVI.01056-06.
5. Girod A, Wobus CE, Zadori Z, Ried M, Leike K, Tijssen P, Kleinschmidt JA, Hallek M. 2002. The VP1 capsid protein of adeno-associated virus type 2 is carrying a phospholipase A2 domain required for virus infectivity. J. Gen. Virol. 83:973-978. http://vir.sgmjournals.org/content/83/5/973.long.
6. Grieger JC, Johnson JS, Gurda-Whitaker B, Agbandje-McKenna M, Samulski RJ. 2007. Surface-exposed adeno-associated virus Vp1-NLS capsid fusion protein rescues infectivity of noninfectious wild-type Vp2/Vp3 and Vp3-only capsids but not that of fivefold pore mutant virions. J. Virol. 81:7833-7843. http://dx.doi.org/10.1128/JVI.00580-07.
7. Grieger JC, Snowdy S, Samulski RJ. 2006. Separate basic region motifs within the adeno-associated virus capsid proteins are essential for infectivity and assembly. J. Virol. 80:5199-5210. http://dx.doi.org/10.1128/JVI.02723-05.
8. Popa-Wagner R, Porwal M, Kann M, Reuss M, Weimer M, Florin L, Kleinschmidt JA. 2012. Impact of VP1-specific protein sequence motifs on adeno-associated virus type 2 intracellular trafficking and nuclear entry. J. Virol. 86:9163-9174. http://dx.doi.org/10.1128/JVI.00282-12.
9. Akache B, Grimm D, Shen X, Fuess S, Yant SR, Glazer DS, Park J, Kay MA. 2007. A two-hybrid screen identifies cathepsins B and L as uncoating factors for adeno-associated virus 2 and 8. Mol. Ther. 15:330-339. http://dx.doi.org/10.1038/sj.mt.6300053.
10. Salganik M, Venkatakrishnan B, Bennett A, Lins B, Yarbrough J, Muzyczka N, Agbandje-McKenna M, McKenna R. 2012. Evidence for pH-dependent protease activity in the adeno-associated virus capsid. J. Virol. 86:11877-11885. http://dx.doi.org/10.1128/JVI.01717-12.
11. Nam HJ, Gurda BL, McKenna R, Potter M, Byrne B, Salganik M, Muzyczka N, Agbandje-McKenna M. 2011. Structural studies of adeno-associated virus serotype 8 capsid transitions associated with endosomal trafficking. J. Virol. 85:11791-11799. http://dx.doi.org/10.1128/JVI.05305-11.
12. Wu P, Xiao W, Conlon T, Hughes J, Agbandje-McKenna M, Ferkol T, Flotte T, Muzyczka N. 2000. Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J. Virol. 74:8635-8647. http://dx.doi.org/10.1128/JVI.74.18.8635-8647.2000.
13. Lochrie MA, Tatsuno GP, Christie B, McDonnell JW, Zhou S, Surosky R, Pierce GF, Colosi P. 2006. Mutations on the external surfaces of adeno-associated virus type 2 capsids that affect transduction and neutralization. J. Virol. 80:821-834. http://dx.doi.org/10.1128/JVI.80.2.821-834.2006.
14. Zhong L, Li B, Mah CS, Govindasamy L, Agbandje-McKenna M, Cooper M, Herzog RW, Zolotukhin I, Warrington KH, Jr, Weigel-Van Aken KA, Hobbs JA, Zolotukhin S, Muzyczka N, Srivastava A. 2008. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses. Proc. Natl. Acad. Sci. U. S. A. 105:7827-7832. http://dx.doi.org/10.1073/pnas.0802866105.
15. Zolotukhin S, Byrne BJ, Mason E, Zolotukhin I, Potter M, Chesnut K, Summerford C, Samulski RJ, Muzyczka N. 1999. Recombinant adenoassociated virus purification using novel methods improves infectious titer and yield. Gene Ther. 6:973-985. http://dx.doi.org/10.1038/sj.gt.3300938.
16. Zolotukhin S, Potter M, Zolotukhin I, Sakai Y, Loiler S, Fraites TJ, Jr, Chiodo VA, Phillipsberg T, Muzyczka N, Hauswirth WW, Flotte TR, Byrne BJ, Snyder RO. 2002. Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods (San Diego) 28:158-167. http://dx.doi.org/10.1016/S1046-2023(02)00220-7.
17. Wobus CE, Hugle-Dorr B, Girod A, Petersen G, Hallek M, Kleinschmidt JA. 2000. 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. 74:9281-9293. http://dx.doi.org/10.1128/JVI.74.19.9281-9293.2000.
18. Johnson JS, Samulski RJ. 2009. Enhancement of adeno-associated virus infection by mobilizing capsids into and out of the nucleolus. J. Virol. 83:2632-2644. http://dx.doi.org/10.1128/JVI.02309-08.
19. Wistuba A, Kern A, Weger S, Grimm D, Kleinschmidt JA. 1997. Subcellular compartmentalization of adeno-associated virus type 2 assembly. J. Virol. 71:1341-1352.
20. Ferrari FK, Samulski T, Shenk T, Samulski RJ. 1996. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 70:3227-3234.
21. Fisher KJ, Gao GP, Weitzman MD, DeMatteo R, Burda JF, Wilson JM. 1996. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J. Virol. 70:520-532.
22. Cathomen T, Stracker TH, Gilbert LB, Weitzman MD. 2001. A genetic screen identifies a cellular regulator of adeno-associated virus. Proc. Natl. Acad. Sci. U. S. A. 98:14991-14996. http://dx.doi.org/10.1073/pnas.261567198.
23. Qing K, Hansen J, Weigel-Kelley KA, Tan M, Zhou S, Srivastava A. 2001. Adeno-associated virus type 2-mediated gene transfer: role of cellular FKBP52 protein in transgene expression. J. Virol. 75:8968-8976. http://dx.doi.org/10.1128/JVI.75.19.8968-8976.2001.
24. Qing K, Khuntirat B, Mah C, Kube DM, Wang XS, Ponnazhagan S, Zhou S, Dwarki VJ, Yoder MC, Srivastava A. 1998. Adeno-associated virus type 2-mediated gene transfer: correlation of tyrosine phosphorylation of the cellular single-stranded D sequence-binding protein with transgene expression in human cells in vitro and murine tissues in vivo. J. Virol. 72:1593-1599.
25. Qing K, Li W, Zhong L, Tan M, Hansen J, Weigel-Kelley KA, Chen L, Yoder MC, Srivastava A. 2003. Adeno-associated virus type 2-mediated gene transfer: role of cellular T-cell protein tyrosine phosphatase in transgene expression in established cell lines in vitro and transgenic mice in vivo. J. Virol. 77:2741-2746. http://dx.doi.org/10.1128/JVI.77.4.2741-2746.2003.
26. Qing K, Wang XS, Kube DM, Ponnazhagan S, Bajpai A, Srivastava A. 1997. Role of tyrosine phosphorylation of a cellular protein in adenoassociated virus 2-mediated transgene expression. Proc. Natl. Acad. Sci. U. S. A. 94:10879-10884. http://dx.doi.org/10.1073/pnas.94.20.10879.
27. Zhong L, Li B, Jayandharan G, Mah CS, Govindasamy L, Agbandje-McKenna M, Herzog RW, Weigel-Van Aken KA, Hobbs JA, Zolotukhin S, Muzyczka N, Srivastava A. 2008. Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 381:194-202. http://dx.doi.org/10.1016/j.virol.2008.08.027.
28. Jayandharan GR, Zhong L, Li B, Kachniarz B, Srivastava A. 2008. Strategies for improving the transduction efficiency of single-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther. 15:1287-1293. http://dx.doi.org/10.1038/gt.2008.89.
29. Jayandharan GR, Zhong L, Sack BK, Rivers AE, Li M, Li B, Herzog RW, Srivastava A. 2010. Optimized adeno-associated virus (AAV)-protein phosphatase-5 helper viruses for efficient liver transduction by single-stranded AAV vectors: therapeutic expression of factor IX at reduced vector doses. Hum. Gene Ther. 21:271-283. http://dx.doi.org/10.1089/hum.2009.100.
30. McCraw DM, O'Donnell JK, Taylor KA, Stagg SM, Chapman MS. 2012. Structure of adeno-associated virus-2 in complex with neutralizing monoclonal antibody A20. Virology 431:40-49. http://dx.doi.org/10.1016/j.virol.2012.05.004.
31. Ihalainen TO, Niskanen EA, Jylhava J, Paloheimo O, Dross N, Smolander H, Langowski J, Timonen J, Vihinen-Ranta M. 2009. Parvovirus induced alterations in nuclear architecture and dynamics. PLoS One 4:e5948. http://dx.doi.org/10.1371/journal.pone.0005948.
32. Hansen J, Qing K, Srivastava A. 2001. Infection of purified nuclei by adeno-associated virus 2. Mol. Ther. 4:289-296. http://dx.doi.org/10.1006/mthe.2001.0457.
33. Xiao W, Warrington KH, Jr, Hearing P, Hughes J, Muzyczka N. 2002. Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J. Virol. 76:11505-11517. http://dx.doi.org/10.1128/JVI.76.22.11505-11517.2002.
34. Cohen S, Behzad AR, Carroll JB, Pante N. 2006. Parvoviral nuclear import: bypassing the host nuclear-transport machinery. J. Gen. Virol. 87:3209-3213. http://dx.doi.org/10.1099/vir.0.82232-0.
35. Cohen S, Pante N. 2005. Pushing the envelope: microinjection of minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope. J. Gen. Virol. 86:3243-3252. http://dx.doi.org/10.1099/vir.0.80967-0.