A dual role of EGFR protein tyrosine kinase signaling in ubiquitination of AAV2 capsids and viral second-strand DNA synthesis

Molecular Therapy

Volumn 15, Issue 7, 2007, Pages 1323-1330

  Zhong, Li ^a,c   Zhao, Weihong ^a,b   Wu, Jianqing ^a,b   Li, Baozheng ^a   Zolotukhin, Sergei ^a   Govindasamy, Lakshmanan ^a   Agbandje McKenna, Mavis ^a   Srivastava, Arun ^a,c  

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

^b NANJING MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CAPSID PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE; FK 506 BINDING PROTEIN; PARVOVIRUS VECTOR; PROTEASOME; PROTEIN TYROSINE PHOSPHATASE; TYROSINE; TYRPHOSTIN; TYRPHOSTIN 23; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS DNA;

ADENO ASSOCIATED VIRUS; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DNA STRAND; DNA SYNTHESIS; ENZYME INHIBITION; HUMAN; HUMAN CELL; INTRACELLULAR TRANSPORT; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UBIQUITINATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

BIOLOGICAL TRANSPORT; CAPSID; CAPSID PROTEINS; CELL NUCLEUS; DEPENDOVIRUS; DNA, VIRAL; GENE EXPRESSION; GENETIC VECTORS; HELA CELLS; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSGENES; UBIQUITINATION;

ADENO-ASSOCIATED VIRUS - 2; MIRIDAE;

EID: 34250727017     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/sj.mt.6300170     Document Type: Article

References (50)

1. Bems, KI and Giraud, C (1996). Biology of adeno-associated virus. Curr Top Microbiol Immunol 218: 1-23.
2. Muzyczka, N (1992). Use of adeno-associated virus as a general transduction vector for mammalian cells. Curr Top Microbiol Immunol 158: 97-129.
3. Flotte, T, Carter, B, Conrad, C, Guggino, W, Reynolds T, Rosenstein, B et al. (1996). A phase I study of an adeno-associated virus-CFTR gene vector in adult CF patients with mild lung disease. Hum Gene Ther 7: 1145-1159.
4. Kay, MA, Manno, CS, Ragni, MV, Larson, PJ, Couto, LB, McClelland, A et al. (2000). Evidence for gene transfer and expression of factor IX in haermophilia B patients treated with an AAV vector. Nat Genet 24: 257-261.
5. Flotte, TR, Brantly, ML, Spencer, LT, Byrne, BJ, Spencer, CT, Baker, DJ, et al. (2004). Phase I trial of intramuscular injection of a recombinant adeno-associated virus alpha 1-antitrypsin (rAAV2-CB-hAAT) gene vector to AAT-deficient adults. Hum Gene Ther 15: 93-128.
6. Kaplitt, MG, Leone, P, Samulski, RJ, Xiao, X, Pfaff, DW, O'Malley, KL et al. (1994). Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 8: 148-154.
7. Xiao, X, Li, J and Samulski, RJ (1996). Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J. Virol 70: 8098-8108.
8. Yang, GS, Schmidt, M, Yan, Z, Lindbloom, JD, Harding, TC, Donahue, BA et al. (2002). Virus-mediated transduction of murine retina with adeno-associated virus: Effects of viral capsid and genome size. J Virol 76: 7651-7660.
9. Summerford, C and Samulski, RJ (1998). Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445.
10. Qing, K, Mah, C, Hansen, J, Zhou, S, Dwarki, V and Srivastava, A (1999). Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat Med 5: 71-77.
11. Summerford, C, Bartlett, JS and Samulski, RJ (1999). AlphaVbeta5 integrin: A co-receptor for adeno-associated virus type 2 infection. Nat Med 5: 78-82.
12. Kashiwakura, Y, Tamayose, K, Iwabuchi, K, Hirai, Y, Shimada, T, Matsumoto, K et al (2005). Hepatocyte growth factor receptor is a coreceptor for adeno-associated virus type 2 infection. J Virol 79: 609-614.
13. Akache, B, Grimm, D, Pandey, K, Yant, SR, Xu, H and Kay, MA (2006). The 37/67-kilodalton laminin receptor is a receptor for adeno-associated virus serotypes 8, 2, 3, and 9. J Virol 80: 9831-9836.
14. Hansen, J, Qing, K, Kwon, HJ, Mah, C and Srivastava, A (2000). Impaired intracellular trafficking of adeno-associated virus type 2 vectors limits efficient transduction of murine fibroblasts. J Virol 74 992-996.
15. Hansen, J, Qing, K and 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.
16. Douar, AM, Poulard, K, Stockholm, D and Danos, O (2001). Intracellular trafficking of adeno-associated virus vectors: Routing to the late endosomal compartment and proteasome degradation. J Virol 75 1824-1833.
17. Zhao, W, Zhong, L, Wu, J, Chen, L, Qing, K, Weigel-Kelley, KA et al. (2006). Role of cellular FKBP52 protein in intracellular trafficking of recombinant adeno-associated virus 2 vectors. Virology 353 283-293.
18. Thomas, CE, Storm, TA, Huang, Z and Kay, MA (2004). Rapid uncoating of vector genomes is the key to efficient liver transduction with pseudotyped adeno-associated virus vectors. J Virol 78: 3110-3122.
19. Zhong, L, Li, W, Yang, Z, Qing, K, Tan, M, Hansen, J et al. (2004). Impaired nuclear transport and uncoating limit recombinant adeno-associated virus 2 vector-mediated transduction of primary murine hematopoietic cells. Hum Gene Ther 15: 1207-1218.
20. Ferrari, FK, Samulski, T, Shenk, T and 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 and Wilson, JM (1996). Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis. J Virol 70: 520-532.
22. Qing, K, Wang, XS, Kube, DM, Ponnazhagan, S, Bajpai, A and Srivastava, A (1997). Role of tyrosine phosphorylation of a cellular protein in adeno-associated virus 2-mediated transgene expression. Proc Natl Acad Sci USA 94: 10879-10884.
23. Qing, K, Khuntirat, B, Mah, C, Kube, DM, Wang, XS, Ponnazhagan, S et al. (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.
24. Qing, K, Hansen, J, Weigel-Kelley, KA, Tan, M, Zhou, S and Srivastava, A (2001). Adeno-associated virus type 2-mediated gene transfer: Role of cellular FKBP52 protein in transgene expression. J Virol 75: 8968-8976.
25. Qing, K, Li, W, Zhong, L, Tan, M, Hansen, J, Weigel-Kelley, KA et al. (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.
26. Zhong, L, Qing, K, Si, Y, Chen, L, Tan, M and Srivastava, A (2004). 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: 12714-12723.
27. Zhong, L, Li, W, Yang, Z, Chen, L, Li, Y, Qing, K et al. (2004). Improved transduction of primary murine hepatocytes by recombinant adeno-associated virus 2 vectors in vivo. Gene Ther 11: 1165-1169.
28. Zhong, L, Chen, L, Li, Y, Qing, K, Weigel-Kelley, KA, Chan, RJ et al. (2004). 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: 950-957.
29. Tan, M, Qing, K, Zhou, S, Yoder, MC and Srivastava, A (2001). Adeno-associated virus 2-mediated transduction and erythroid lineage-restricted long-term expression of the human beta-globin gene in hematopoietic cells from homozygous beta-thalassemic mice. Mol Ther 3: 940-946.
30. Zhong, L, Li, W, Li, Y, Zhao, W, Wu, J, Li, B et al. (2006). Evaluation of primitive murine hematopoietic stem and progenitor cell transduction in vitro and in vivo by recombinant adeno-associated virus vector serotypes 1 through S. Hum Gene Ther 17: 321-333.
31. Duan, D, Yue, Y, Yan, Z, Yang, J and Engelhardt, JF (2000). Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 105: 1573-1587.
32. Ding, W, Zhang, LN, Yeaman, C and Engelhardt, JF (2006). rAAV2 traffics through both the late and the recycling endosomes in a dose-dependent fashion. Mol Ther 13: 671-682.
33. Haglund, K, Sigismund, S, Polo, S, Szymkiewicz, I, Di Fiore, PP and Dikic, I (2003). Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation. Nat Cell Biol 5: 461-466.
34. Yan, Z, Zak, R, Zhang, Y, Ding, W, Godwin S, Munson, K et al. (2004). Distinct classes of proteasome-modulating agents cooperatively augment recombinant adeno-associated virus type 2 and type 5-mediated transduction from the apical surfaces of human airway epithelia. J Virol 78: 2863-2874.
35. Jennings, K, Miyamae T, Traister, R, Marinov, A, Katakura, S, Sowders, D, et al. (2005). Proteasome inhibition enhances AAV-mediated transgene expression in human synoviocytes in vitro and in vivo. Mol Ther 11: 600-607.
36. Brown, K, Gerstberger, S, Carlson, L, Franzoso, G and Siebenlist, U (1995). Control-of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 267: 1485-1488.
37. Traenckner, EB, Pahl, HL, Henkel, T, Schmidt KN, Wilk, S and Baeuerle, PA (1995). Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J 14: 2876-2883.
38. Cenciarelli, C, Wilhelm, KG Jr, Guo, A and Weissman, AM (1996). T cell antigen receptor ubiquitination is a consequence of receptor-mediated tyrosine kinase activation. J Biol Chem 271: 8709-8713.
39. Paolini, R, Serra, A, Molfetta, R, Piccoli, M, Frati, L and Santoni, A (1999). Tyrosine kinase-dependent ubiquitination of CD16 zeta subunit in human NK cells following receptor engagement. Eur J Immunol 29 3179-3187.
40. Stem, KA, Visser Smit, GD, Place, TL, Winistorfer, S, Piper, RC and Lill, NL (2007). EGF receptor fate is controlled by Hrs tyrosine phosphorylation sites that regulate Hrs degradation. Mol Cell Biol 27: 888-898.
41. Penrose, KJ and McBride, AA (2000). Proteasome-mediated degradation of the papillomavirus E2-TA protein is regulated by phosphorylation and can modulate viral genome copy number. J Virol 74: 6031-6038.
42. Penrose, KJ, Garcia-Alai, M, de Prat-Gay, G and McBride, AA (2004). Casein kinase II phosphorylation-induced conformational switch triggers degradation of the papillomavirus E2 protein. J Biol Chem 279 22430-22439.
43. Mah, C, Qing, K, Khuntirat, B, Ponnazhagan, S, Wang, XS, Kube, DM et al. (1998). Adeno-associated virus type 2-mediated gene transfer: role of epidermal growth factor receptor protein tyrosine kinase in transgene expression. J Virol 72: 9835-9843.
44. McCarty, DM, Fu, H, Monahan, PE, Toulson, CE, Naik P and Samulski, RJ (2003). Adeno-associated virus terminal repeat (TR) mutant generates self-complementary vectors to overcome the rate-limiting step to transduction in vivo. Gene Ther 10: 2112-2118.
45. Wang, Z, Ma, HI, Li, J, Sun, L, Zhang, J and Xiao, X (2003). Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo. Gene Ther 10: 2105-2111.
46. Wu, J, Zhao, W, Zhong, L, Han, Z, Li, B, Ma, W et al. (2007). Self-complementary recombinant adeno-associated virus vectors: Packaging capacity and the role of Rep proteins in vector purity. Hum Gene Ther 18 171-182.
47. Pickart, CM (2001). Mechanisms underlying ubiquitination. Ann Rev Biochem 70: 503-533.
48. Yan, Z, Zak, R, Luxton, GW, Ritchie, TC, Bantel-Schaal, U and Engelhardt, JF (2002). Ubiquitination of both adeno-associated virus type 2 and 5 capsid proteins affects the transduction efficiency of recombinant vectors. J Virol 76: 2043-2053.
49. Auricchio, A, Hildinger, M, O'Connor, E, Gao, GP and Wilson, JM (2001). Isolation of highly infectious and pure adeno-associated virus type 2 vectors with a single-step gravity-flow column. Hum Gene Ther 12: 71-76.
50. 2+-calmodulin-dependent protein kinase II via MAP kinase signaling in cultured vascular smooth muscle cells. Anesthesiology 96: 148-154.