Role of cellular FKBP52 protein in intracellular trafficking of recombinant adeno-associated virus 2 vectors

Virology

Volumn 353, Issue 2, 2006, Pages 283-293

  Zhao, Weihong ^a,b,c   Zhong, Li ^a,b   Wu, Jianqing ^a,b,c   Chen, Linyuan ^a,b   Qing, Keyun ^d   Weigel Kelley, Kirsten A ^a,b   Larsen, Steven H ^e   Shou, Weinian ^e   Warrington Jr , Kenneth H ^a,b   Srivastava, Arun ^a,b  

^a UNIVERSITY OF FLORIDA   (United States)

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

^c NANJING MEDICAL UNIVERSITY   (China)

^d ELI LILLY AND COMPANY   (United States)

^e INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adeno associated virus type 2; FK506 binding protein; Gene expression; Gene transfer; Intracellular trafficking; Murine embryo fibroblasts; Viral vectors

Indexed keywords

CELL PROTEIN; CHAPERONE; FK 506 BINDING PROTEIN; FKBP52 PROTEIN; HYDROXYUREA; PARVOVIRUS VECTOR; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL NUCLEUS; CONTROLLED STUDY; DNA SYNTHESIS; EMBRYO; FIBROBLAST; GENE EXPRESSION; HETEROZYGOSITY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; TRANSGENE; VIRUS PARTICLE; VIRUS RECOMBINANT; WILD TYPE;

ANIMALS; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CELLS, CULTURED; DEPENDOVIRUS; DYNEIN ATPASE; FIBROBLASTS; GENE EXPRESSION; GENE THERAPY; GENETIC VECTORS; HETEROZYGOTE; MICE; MICE, KNOCKOUT; MOLECULAR CHAPERONES; MOLECULAR WEIGHT; TACROLIMUS; TRANSDUCTION, GENETIC;

ADENO-ASSOCIATED VIRUS - 2; MURINAE;

EID: 33748690311     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.04.042     Document Type: Article

References (55)

1. Bartlett J.S., Wilcher R., and Samulski R.J. Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J. Virol. 74 6 (2000) 2777-2785
2. Berns K.I., and Giraud C. Biology of adeno-associated virus. Curr. Top. Microbiol. Immunol. 218 (1996) 1-23
3. Conlon T.J., and Flotte T.R. Recombinant adeno-associated virus vectors for gene therapy. Expert Opin. Biol. Ther. 4 7 (2004) 1093-1101
4. Czar M.J., Owens-Grillo J.K., Dittmar K.D., Hutchison K.A., Zacharek A.M., Leach K.L., Deibel Jr. M.R., and Pratt W.B. Characterization of the protein-protein interactions determining the heat shock protein (hsp90.hsp70.hsp56) heterocomplex. J. Biol. Chem. 269 15 (1994) 11155-11161
5. Czar M.J., Owens-Grillo J.K., Yem A.W., Leach K.L., Deibel Jr. M.R., Welsh M.J., and Pratt W.B. The hsp56 immunophilin component of untransformed steroid receptor complexes is localized both to microtubules in the cytoplasm and to the same nonrandom regions within the nucleus as the steroid receptor. Mol. Endocrinol. 8 12 (1994) 1731-1741
6. Denny W.B., Prapapanich V., Smith D.F., and Scammell J.G. Structure-function analysis of squirrel monkey FK506-binding protein 51, a potent inhibitor of glucocorticoid receptor activity. Endocrinology 146 7 (2005) 3194-3201
7. Douar A.M., Poulard K., Stockholm D., and Danos O. Intracellular trafficking of adeno-associated virus vectors: routing to the late endosomal compartment and proteasome degradation. J. Virol. 75 4 (2001) 1824-1833
8. Duan D., Li Q., Kao A.W., Yue Y., Pessin J.E., and Engelhardt J.F. Dynamin is required for recombinant adeno-associated virus type 2 infection. J. Virol. 73 12 (1999) 10371-10376
9. Ferrari F.K., Samulski T., Shenk T., and Samulski R.J. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J. Virol. 70 5 (1996) 3227-3234
10. Fisher K.J., Gao G.P., Weitzman M.D., DeMatteo R., Burda J.F., and Wilson J.M. Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J. Virol. 70 1 (1996) 520-532
11. Galigniana M.D., Radanyi C., Renoir J.M., Housley P.R., and Pratt W.B. Evidence that the peptidylprolyl isomerase domain of the hsp90-binding immunophilin FKBP52 is involved in both dynein interaction and glucocorticoid receptor movement to the nucleus. J. Biol. Chem. 276 18 (2001) 14884-14889
12. Hansen J., Qing K., Kwon H.J., Mah C., and Srivastava A. Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J. Virol. 74 2 (2000) 992-996
13. Hansen J., Qing K., and Srivastava A. Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J. Virol. 75 9 (2001) 4080-4090
14. Hansen J., Qing K., and Srivastava A. Infection of purified nuclei by adeno-associated virus 2. Mol. Ther. 4 4 (2001) 289-296
15. Horak V., and Flechon J.E. Immunocytochemical characterisation of rabbit and mouse embryonic fibroblasts. Reprod., Nutr., Dev. 38 6 (1998) 683-695
16. Lux K., Goerlitz N., Schlemminger S., Perabo L., Goldnau D., Endell J., Leike K., Kofler D.M., Finke S., Hallek M., and Buning H. Green fluorescent protein-tagged adeno-associated virus particles allow the study of cytosolic and nuclear trafficking. J. Virol. 79 18 (2005) 11776-11787
17. Mah C., Qing K., Khuntirat B., Ponnazhagan S., Wang X.S., Kube D.M., Yoder M.C., and Srivastava A. Adeno-associated virus type 2-mediated gene transfer: role of epidermal growth factor receptor protein tyrosine kinase in transgene expression. J. Virol. 72 12 (1998) 9835-9843
18. Mallik R., and Gross S.P. Molecular motors: strategies to get along. Curr. Biol. 14 22 (2004) R971-R982
19. Marshall E. Gene therapy. Viral vectors still pack surprises. Science 294 5547 (2001) 1640
20. McCarty D.M., Monahan P.E., and Samulski R.J. Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis. Gene Ther. 8 16 (2001) 1248-1254
21. Mukherjee P., Guha S., and Bose S.R. Chemical transformation of Swiss mouse embryo fibroblasts in primary culture. Neoplasma 31 5 (1984) 557-564
22. Muller M.T. Binding of the herpes simplex virus immediate-early gene product ICP4 to its own transcription start site. J. Virol. 61 3 (1987) 858-865
23. Murray J.W., and Wolkoff A.W. Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv. Drug Delivery Rev. 55 11 (2003) 1385-1403
24. Muzyczka N. Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr. Top. Microbiol. Immunol. 158 (1992) 97-129
25. Perrot-Applanat M., Cibert C., Geraud G., Renoir J.M., and Baulieu E.E. The 59 kDa FK506-binding protein, a 90 kDa heat shock protein binding immunophilin (FKBP59-HBI), is associated with the nucleus, the cytoskeleton and mitotic apparatus. J. Cell Sci. 108 Pt. 5 (1995) 2037-2051
26. Pratt W.B. The hsp90-based chaperone system: involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med. 217 4 (1998) 420-434
27. Pratt W.B., and Toft D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 18 3 (1997) 306-360
28. Pratt W.B., Silverstein A.M., and Galigniana M.D. A model for the cytoplasmic trafficking of signalling proteins involving the hsp90-binding immunophilins and p50cdc37. Cell Signal 11 12 (1999) 839-851
29. Pratt W.B., Galigniana M.D., Harrell J.M., and DeFranco D.B. Role of hsp90 and the hsp90-binding immunophilins in signalling protein movement. Cell Signal 16 8 (2004) 857-872
30. Qing K., Wang X.S., Kube D.M., Ponnazhagan S., Bajpai A., and Srivastava A. Role of tyrosine phosphorylation of a cellular protein in adeno-associated virus 2-mediated transgene expression. Proc. Natl. Acad. Sci. U.S.A. 94 20 (1997) 10879-10884
31. Qing K., Khuntirat B., Mah C., Kube D.M., Wang X.S., Ponnazhagan S., Zhou S., Dwarki V.J., Yoder M.C., and Srivastava A. 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 2 (1998) 1593-1599
32. Qing K., Mah C., Hansen J., Zhou S., Dwarki V., and Srivastava A. Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat. Med. 5 1 (1999) 71-77
33. Qing K., Hansen J., Weigel-Kelley K.A., Tan M., Zhou S., and Srivastava A. Adeno-associated virus type 2-mediated gene transfer: role of cellular FKBP52 protein in transgene expression. J. Virol. 75 19 (2001) 8968-8976
34. Qing K., Li W., Zhong L., Tan M., Hansen J., Weigel-Kelley K.A., Chen L., Yoder M.C., and Srivastava A. 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 4 (2003) 2741-2746
35. Russell D.W., Alexander I.E., and Miller A.D. DNA synthesis and topoisomerase inhibitors increase transduction by adeno-associated virus vectors. Proc. Natl. Acad. Sci. U.S.A. 92 12 (1995) 5719-5723
36. Sanchez E.R., Faber L.E., Henzel W.J., and Pratt W.B. The 56-59-kilodalton protein identified in untransformed steroid receptor complexes is a unique protein that exists in cytosol in a complex with both the 70- and 90-kilodalton heat shock proteins. Biochemistry 29 21 (1990) 5145-5152
37. Sanlioglu S., Benson P.K., Yang J., Atkinson E.M., Reynolds T., and Engelhardt J.F. Endocytosis and nuclear trafficking of adeno-associated virus type 2 are controlled by rac1 and phosphatidylinositol-3 kinase activation. J. Virol. 74 19 (2000) 9184-9196
38. Schmitt J., Pohl J., and Stunnenberg H.G. Cloning and expression of a mouse cDNA encoding p59, an immunophilin that associates with the glucocorticoid receptor. Gene 132 2 (1993) 267-271
39. Seisenberger G., Ried M.U., Endress T., Buning H., Hallek M., and Brauchle C. Real-time single-molecule imaging of the infection pathway of an adeno-associated virus. Science 294 5548 (2001) 1929-1932
40. Seksek O., Biwersi J., and Verkman A.S. Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J. Cell Biol. 138 1 (1997) 131-142
41. Suikkanen S., Saajarvi K., Hirsimaki J., Valilehto O., Reunanen H., Vihinen-Ranta M., and Vuento M. Role of recycling endosomes and lysosomes in dynein-dependent entry of canine parvovirus. J. Virol. 76 9 (2002) 4401-4411
42. Summerford C., and Samulski R.J. Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J. Virol. 72 2 (1998) 1438-1445
43. Wang Z., Ma H.I., Li J., Sun L., Zhang J., and Xiao X. Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther. 10 26 (2003) 2105-2111
44. Warrington Jr. K.H., Gorbatyuk O.S., Harrison J.K., Opie S.R., Zolotukhin S., and Muzyczka N. Adeno-associated virus type 2 VP2 capsid protein is nonessential and can tolerate large peptide insertions at its N terminus. J. Virol. 78 12 (2004) 6595-6609
45. Welte M.A. Bidirectional transport along microtubules. Curr. Biol. 14 13 (2004) R525-R537
46. Wistuba A., Kern A., Weger S., Grimm D., and Kleinschmidt J.A. Subcellular compartmentalization of adeno-associated virus type 2 assembly. J. Virol. 71 2 (1997) 1341-1352
47. 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 19 (2000) 9281-9293
48. Wochnik G.M., Ruegg J., Abel G.A., Schmidt U., Holsboer F., and Rein T. FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J. Biol. Chem. 280 6 (2005) 4609-4616
49. Wu B., Li P., Liu Y., Lou Z., Ding Y., Shu C., Ye S., Bartlam M., Shen B., and Rao Z. 3D structure of human FK506-binding protein 52: implications for the assembly of the glucocorticoid receptor/Hsp90/immunophilin heterocomplex. Proc. Natl. Acad. Sci. U.S.A. 101 22 (2004) 8348-8353
50. Xiao W., Warrington Jr. K.H., Hearing P., Hughes J., and Muzyczka N. Adenovirus-facilitated nuclear translocation of adeno-associated virus type 2. J. Virol. 76 22 (2002) 11505-11517
51. Xu J., Ma C., Bass C., and Terwilliger E.F. A combination of mutations enhances the neurotropism of AAV-2. Virology 341 2 (2005) 203-214
52. Zhong L., Chen L., Li Y., Qing K., Weigel-Kelley K.A., Chan R.J., Yoder M.C., and Srivastava A. Self-complementary adeno-associated virus 2 (AAV)-T cell protein tyrosine phosphatase vectors as helper viruses to improve transduction efficiency of conventional single-stranded AAV vectors in vitro and in vivo. Mol. Ther. 10 5 (2004) 950-957
53. Zhong L., Li W., Yang Z., Chen L., Li Y., Qing K., Weigel-Kelley K.A., Yoder M.C., Shou W., and Srivastava A. Improved transduction of primary murine hepatocytes by recombinant adeno-associated virus 2 vectors in vivo. Gene Ther. 11 14 (2004) 1165-1169
54. Zhong L., Li W., Yang Z., Qing K., Tan M., Hansen J., Li Y., Chen L., Chan R.J., Bischof D., Maina N., Weigel-Kelley K.A., Zhao W., Larsen S.H., Yoder M.C., Shou W., and Srivastava A. Impaired nuclear transport and uncoating limit recombinant adeno-associated virus 2 vector-mediated transduction of primary murine hematopoietic cells. Hum. Gene Ther. 15 12 (2004) 1207-1218
55. Zhong L., Qing K., Si Y., Chen L., Tan M., and Srivastava A. Heat-shock treatment-mediated increase in transduction by recombinant adeno-associated virus 2 vectors is independent of the cellular heat-shock protein 90. J. Biol. Chem. 279 13 (2004) 12714-12723