Enhanced baculovirus-mediated transduction of human cancer cells by tumor-homing peptides

Journal of Virology

Volumn 80, Issue 13, 2006, Pages 6603-6611

  Mäkelä, Anna R ^a   Matilainen, Heli ^a   White, Daniel J ^a   Ruoslahti, Erkki ^b   Oker Blom, Christian ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PROTEIN F3; PROTEIN LYP1; TUMOR PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS VECTOR;

ARTICLE; BACULOVIRUS; BREAST CANCER; CANCER CELL; GENE TRANSFER; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTERNALIZATION; LEPIDOPTERA; LIVER CELL CARCINOMA; PEPTIDE ANALYSIS; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN MODIFICATION; VIRAL GENE THERAPY; VIRUS ENVELOPE; VIRUS INHIBITION;

BACULOVIRIDAE; BREAST NEOPLASMS; CAPSID PROTEINS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; GENE THERAPY; GLYCOPROTEINS; HUMANS; NEOPLASM PROTEINS; PEPTIDE LIBRARY; PEPTIDES; PROTEIN BINDING; TRANSDUCTION, GENETIC; VESICULAR STOMATITIS-INDIANA VIRUS;

VESICULAR STOMATITIS VIRUS;

EID: 33745227413     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00528-06     Document Type: Article

References (63)

1. Airenne, K. J., M. O. Hiltunen, M. P. Turunen, A. M. Turunen, O. H. Laitinen, M. S. Kulomaa, and S. Yla-Herttuala. 2000. Baculovirus-mediated periadventitial gene transfer to rabbit carotid artery. Gene Ther. 7:1499-1504.
2. Akerman, M. E., W. C. Chan, P. Laakkonen, S. N. Bhatia, and E. Ruoslahti. 2002. Nanocrystal targeting in vivo. Proc. Natl. Acad. Sci. USA 99:12617-12621.
3. Arap, W., R. Pasqualini, and E. Ruoslahti. 1998. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 279:377-380.
4. Baker, A. H., A. Kritz, L. M. Work, and S. A. Nicklin. 2005. Cell-selective viral gene delivery vectors for the vasculature. Exp. Physiol. 90:27-31.
5. Barsoum, J., R. Brown, M. McKee, and F. M. Boyce. 1997. Efficient transduction of mammalian cells by a recombinant baculovirus having the vesicular stomatitis virus G glycoprotein. Hum. Gene Ther. 8:2011-2018.
6. Beck, C., H. Uramoto, J. Boren, and L. M. Akyurek. 2004. Tissue-specific targeting for cardiovascular gene transfer. Potential vectors and future challenges. Curr. Gene Ther. 4:457-467.
7. Boyce, F. M., and N. L. Bucher. 1996. Baculovirus-mediated gene transfer into mammalian cells. Proc. Natl. Acad. Sci. USA 93:2348-2352.
8. Chappie, S. D., and I. M. Jones. 2002. Non-polar distribution of green fluorescent protein on the surface of Autographe californica nucleopolyhedrovirus using a heterologous membrane anchor. J. Biotechnol. 95:269-275.
9. Christian, S., J. Pilch, M. E. Akerman, K. Porkka, P. Laakkonen, and E. Ruoslahti. 2003. Nucleolin expressed at the cell surface is a marker of endothelial cells in angiogenic blood vessels. J. Cell Biol. 163:871-878.
10. Clay, W. C., J. P. Condreay, L. B. Moore, S. L. Weaver, M. A. Watson, T. A. Kost, and J. J. Lorenz. 2003. Recombinant baculoviruses used to study estrogen receptor function in human osteosarcoma cells. ASSAY Drug Dev. Technol. 1:801-810.
11. Condreay, J. P., S. M. Witherspoon, W. C. Clay, and T. A. Kost. 1999. Transient and stable gene expression in mammalian cells transduced with a recombinant baculovirus vector. Proc. Natl. Acad. Sci. USA 96:127-132.
12. Deng, J. S., B. Ballou, and J. K. Hofmeister. 1996. Internalization of antinucleolin antibody into viable HEp-2 cells. Mol. Biol. Rep. 23:191-195.
13. Doms, R. W., D. S. Keller, A. Helenius, and W. E. Balch. 1987. Role for adenosine triphosphate in regulating the assembly and transport of vesicular stomatitis virus G protein trimers. J. Cell Biol. 105:1957-1969.
14. Doms, R. W., A. Ruusala, C. Machamer, J. Helenius, A. Helenius, and J. K. Rose. 1988. Differential effects of mutations in three domains on folding, quaternary structure, and intracellular transport of vesicular stomatitis virus G protein. J. Cell Biol. 107:89-99.
15. Duisit, G., S. Saleun, S. Douthe, J. Barsoum, G. Chadeuf, and P. Mouiller. 1999. Baculovirus vector requires electrostatic interactions including heparan sulfate for efficient gene transfer in mammalian cells. J. Gene Med. 1:93-102.
16. Facciabene, A., L. Aurisicchio, and N. La Monica. 2004. Baculovirus vectors elicit antigen-specific immune responses in mice. J. Virol. 78:8663-8672.
17. Gao, R., C. J. McCormick, M. J. Arthur, R. Ruddell, F. Oakley, D. E. Smart, F. R. Murphy, M. P. Harris, and D. A. Mann. 2002. High efficiency gene transfer into cultured primary rat and human hepatic stellate cells using baculovirus vectors. Liver 22:15-22.
18. Ghosh, S., M. K. Parvez, K. Banerjee, S. K. Sarin, and S. E. Hasnain. 2002. Baculovirus as mammalian cell expression vector for gene therapy: an emerging strategy. Mol. Ther. 6:5-11.
19. Ho, Y. C., H. C. Chen, K. C. Wang, and Y. C. Hu. 2004. Highly efficient baculovirus-mediated gene transfer into rat chondrocytes. Biotechnol. Bioeng. 88:643-651.
20. Ho, Y. C., Y. C. Chung, S. M. Hwang, K. C. Wang, and Y. C. Hu. 2005. Transgene expression and differentiation of baculovirus-transduced human mesenchymal stem cells. J. Gene Med. 7:860-868.
21. Hoare, J., S. Waddington, H. C. Thomas, C. Coutelle, and M. J. McGarvey. 2005. Complement inhibition rescued mice allowing observation of transgene expression following intraportal delivery of baculovirus in mice. J. Gene Med. 7:325-333.
22. Hoffman, J. A., E. Giraudo, M. Singh, L. Zhang, M. Inoue, K. Porkka, D. Hanahan, and E. Ruoslahti. 2003. Progressive vascular changes in a transgenic mouse model of squamous cell carcinoma. Cancer Cell 4:383-391.
23. Hofmann, C., A. Huser, W. Lehnert, and M. Strauss. 1999. Protection of baculovirus-vectors against complement-mediated inactivation by recombinant soluble complement receptor type 1. Biol. Chem. 380:393-395.
24. Hofmann, C., W. Lehnert, and M. Strauss. 1998. The baculovirus system for gene delivery into hepatocytes. Gene Ther. Mol. Biol. 1:231-239.
25. Hofmann, C., V. Sandig, G. Jennings, M. Rudolph, P. Schlag, and M. Strauss. 1995. Efficient gene transfer into human hepatocytes by baculovirus vectors. Proc. Natl. Acad. Sci. USA 92:10099-10103.
26. Huser, A., and C. Hofmann. 2003. Baculovirus vectors: novel mammalian cell gene-delivery vehicles and their applications. Am. J. Pharmacogenomics 3:53-63.
27. Huser, A., M. Rudolph, and C. Hofmann. 2001. Incorporation of decay-accelerating factor into the baculovirus envelope generates complement-resistant gene transfer vectors. Nat. Biotechnol. 19:451-455.
28. Ivaska, J., J. Kapyla, O. Pentikainen, A. M. Hoffren, J. Hermonen, P. Huttunen, M. S. Johnson, and J. Heino. 1999. A peptide inhibiting the collagen binding function of integrin alpha21 domain. J. Biol. Chem. 274:3513-3521.
29. Kaikkonen, M. U., J. K. Raty, K. J. Airenne, T. Wirth, T. Heikura, and S. Yla-Herttuala. 2006. Truncated vesicular stomatitis virus G protein improves baculovirus transduction efficiency in vitro and in vivo. Gene Ther. 13:304-312.
30. Keddie, B. A., G. W. Aponte, and L. E. Volkman. 1989. The pathway of infection of Autographe californica nuclear polyhedrosis virus in an insect host. Science 243:1728-1730.
31. Kitagawa, Y., H. Tani, C. K. Limn, T. M. Matsunaga, K. Moriishi, and Y. Matsuura. 2005. Ligand-directed gene targeting to mammalian cells by pseudotype baculoviruses. J. Virol. 79:3639-3652.
32. Kost, T. A., and J. P. Condreay. 2002. Recombinant baculoviruses as mammalian cell gene-delivery vectors. Trends Biotechnol. 20:173-180.
33. Kost, T. A., J. P. Condreay, and D. L. Jarvis. 2005. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat. Biotechnol. 23:567-575.
34. Kreis, T. E., and H. F. Lodish. 1986. Oligomerization is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell 46:929-937.
35. Kukkonen, S. P., K. J. Airenne, V. Marjomaki, O. H. Laitinen, P. Lehtolainen, P. Kankaanpaa, A. J. Mahonen, J. K. Raty, H. R. Nordlund, C. Oker-Blom, M. S. Kulomaa, and S. Yla-Herttuala. 2003. Baculovirus capsid display: a novel tool for transduction imaging. Mol. Ther. 8:853-862.
36. Laakkonen, P., M. E. Akerman, H. Biliran, M. Yang, F. Ferrer, T. Karpanen, R. M. Hoffman, and E. Ruoslahti. 2004. Antitumor activity of a homing peptide that targets tumor lymphatics and tumor cells. Proc. Natl. Acad. Sci. USA 101:9381-9386.
37. Laakkonen, P., K. Porkka, J. A. Hoffman, and E. Ruoslahti. 2002. A tumor-homing peptide with a targeting specificity related to lymphatic vessels. Nat. Med. 8:751-755.
38. Lehtolainen, P., K. Tyynela, J. Kannasto, K. J. Airenne, and S. Yla-Herttuala. 2002. Baculoviruses exhibit restricted cell type specificity in rat brain: a comparison of baculovirus- and adenovirus-mediated intracerebral gene transfer in vivo. Gene Ther. 9:1693-1699.
39. Li, Y., X. Wang, H. Guo, and S. Wang. 2004. Axonal transport of recombinant baculovirus vectors. Mol. Ther. 10:1121-1129.
40. Liang, C. Y., H. Z. Wang, T. X. Li, Z. H. Hu, and X. W. Chen. 2004. High efficiency gene transfer into mammalian kidney cells using baculovirus vectors. Arch. Virol. 149:51-60.
41. Matilainen, H., J. Rinne, L. Gilbert, V. Marjomaki, H. Reunanen, and C. Oker-Blom. 2005. Baculovirus entry into human hepatoma cells. J. Virol. 79:15452-15459.
42. Ojala, K., J. Koski, W. Ernst, R. Grabherr, I. Jones, and C. Oker-Blom. 2004. Improved display of synthetic 1gG-binding domains on the baculovirus surface. Technol. Cancer Res. Treat. 3:77-84.
43. Ojala, K., D. G. Mottershead, A. Suokko, and C. Oker-Blom. 2001. Specific binding of baculoviruses displaying gp64 fusion proteins to mammalian cells. Biochem. Biophys. Res. Commun. 284:777-784.
44. Oker-Blom, C., K. J. Airenne, and R. Grabherr. 2003. Baculovirus display strategies: emerging tools for eukaryotic libraries and gene delivery. Brief. Funct. Genomics Proteomics 2:244-253.
45. Park, S. W., H. K. Lee, T. G. Kim, S. K. Yoon, and S. Y. Paik. 2001. Hepatocyte-specific gene expression by baculovirus pseudotyped with vesicular stomatitis virus envelope glycoprotein. Biochem. Biophys. Res. Commun. 289:444-450.
46. Pasqualini, R., and E. Ruoslahti. 1996. Tissue targeting with phage peptide libraries. Mol. Psychiatry 1:423.
47. Pieroni, L., D. Maione, and N. La Monica. 2001. In vivo gene transfer in mouse skeletal muscle mediated by baculovirus vectors. Hum. Gene Ther. 12:871-881.
48. Porkka, K., P. Laakkonen, J. A. Hoffman, M. Bernasconi, and E. Ruoslahti. 2002. A fragment of the HMGN2 protein homes to the nuclei of tumor cells and tumor endothelial cells in vivo. Proc. Natl. Acad. Sci. USA 99:7444-7449.
49. Raty, J. K., K. J. Airenne, A. T. Marttila, V. Marjomaki, V. P. Hytonen, P. Lehtolainen, O. H. Laitinen, A. J. Mahonen, M. S. Kulomaa, and S. Yla-Herttuala. 2004. Enhanced gene delivery by avidin-displaying baculovirus. Mol. Ther. 9:282-291.
50. Robison, C. S., and M. A. Whitt. 2000. The membrane-proximal stem region of vesicular stomatitis virus G protein confers efficient virus assembly. J. Virol. 74:2239-2246.
51. Ruoslahti, E. 2002. Drug targeting to specific vascular sites. Drug Discov. Today 7:1138-1143.
52. Salminen, M., K. J. Airenne, R. Rinnankoski, J. Reimari, O. Valilehto, J. Rinne, S. Suikkanen, S. Kukkonen, S. Yla-Herttuala, M. S. Kulomaa, and M. Vihinen-Ranta. 2005. Improvement in nuclear entry and transgene expression of baculoviruses by disintegration of microtubules in human hepa-tocytes. J. Virol. 79:2720-2728.
53. Sandig, V., C. Hofmann, S. Steinert, G. Jennings, P. Schlag, and M. Strauss. 1996. Gene transfer into hepatocytes and human liver tissue by baculovirus vectors. Hum. Gene Ther. 7:1937-1945.
54. Snyder, E. L., and S. F. Dowdy. 2004. Cell penetrating peptides in drug delivery. Pharm. Res. 21:389-393.
55. Song, S. U., and F. M. Boyce. 2001. Combination treatment for osteosarcoma with baculoviral vector mediated gene therapy (p53) and chemotherapy (adriamycin). Exp. Mol. Med. 33:46-53.
56. Tani, H., C. K. Limn, C. C. Yap, M. Onishi, M. Nozaki, Y. Nishimune, N. Okahashi, Y. Kitagawa, R. Watanabe, R. Mochizuki, K. Moriishi, and Y. Matsuura. 2003. In vitro and in vivo gene delivery by recombinant baculoviruses. J. Virol. 77:9799-9808.
57. Tani, H., M. Nishijima, H. Ushijima, T. Miyamura, and Y. Matsuura. 2001. Characterization of cell-surface determinants important for baculovirus infection. Virology 279:343-353.
58. van Loo, N. D., E. Fortunati, E. Ehlert, M. Rabelink, F. Grosveld, and B. J. Scholte. 2001. Baculovirus infection of nondividing mammalian cells: mechanisms of entry and nuclear transport of capsids. J. Virol. 75:961-970.
59. Weisz, O. A., A. M. Swift, and C. E. Machamer. 1993. Oligomerization of a membrane protein correlates with its retention in the Golgi complex. J. Cell Biol. 122:1185-1196.
60. Whitt, M. A., and J. S. Manning. 1988. A phosphorylated 34-kDa protein and a subpopulation of polyhedrin are thiol linked to the carbohydrate layer surrounding a baculovirus occlusion body. Virology 163:33-42.
61. Wickham, T. J. 2000. Targeting adenovirus. Gene Ther. 7:110-114.
62. Wiethoff, C. M., and C. R. Middaugh. 2003. Barriers to nonviral gene delivery. J. Pharm. Sci. 92:203-217.
63. Zorko, M., and U. Langel. 2005. Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv. Drug Delivery Rev. 57:529-545.