Enhanced therapeutic efficacy of an adenovirus-PEI-bile-acid complex in tumors with low coxsackie and adenovirus receptor expression

Biomaterials

Volumn 35, Issue 21, 2014, Pages 5505-5516

  Lee, Cho Hee ^a   Kasala, Dayananda ^a   Na, Youjin ^a   Lee, Min Sang ^b   Kim, Sung Wan ^a,c   Jeong, Ji Hoon ^b   Yun, Chae Ok ^a  

^a Hanyang University   (South Korea)

^b Sungkyunkwan University   (South Korea)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

Cancer gene therapy; Coxsackie and adenovirus receptor; Deoxycholic acid; Oncolytic adenovirus; Poly(ethyleneimine)

Indexed keywords

BACTERIOPHAGES; BODY FLUIDS; CELL DEATH; DISEASES; EFFICIENCY; GENE THERAPY; GENE TRANSFER; MOLECULAR BIOLOGY; POLYETHYLENES;

CANCER GENE THERAPY; COXSACKIE AND ADENOVIRUS RECEPTOR; DEOXYCHOLIC ACID; ONCOLYTIC ADENOVIRUS; POLYETHYLENEIMINE;

TUMORS;

ANTINEOPLASTIC AGENT; BILE ACID; COXSACKIE VIRUS AND ADENOVIRUS RECEPTOR LIKE MEMBRANE PROTEIN; POLYETHYLENEIMINE;

ADENOVIRIDAE; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; DRUG SCREENING; FEMALE; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HEK293 CELL LINE; HUMAN; MCF 7 CELL LINE; METABOLISM; MOUSE; NICK END LABELING; NUDE MOUSE; ONCOLYTIC VIROTHERAPY; PHYSICAL CHEMISTRY; PROCEDURES; TRANSMISSION ELECTRON MICROSCOPY; TUMOR CELL LINE;

ADENOVIRIDAE; ANIMALS; ANTINEOPLASTIC AGENTS; BILE ACIDS AND SALTS; CELL LINE, TUMOR; COXSACKIE AND ADENOVIRUS RECEPTOR-LIKE MEMBRANE PROTEIN; FEMALE; GENETIC VECTORS; HEK293 CELLS; HUMANS; IN SITU NICK-END LABELING; MCF-7 CELLS; MICE; MICE, NUDE; MICROSCOPY, ELECTRON, TRANSMISSION; ONCOLYTIC VIROTHERAPY; PHYSICOCHEMICAL PHENOMENA; POLYETHYLENEIMINE; TRANSDUCTION, GENETIC; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899474705     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.03.060     Document Type: Article

References (49)

1. Jemal A., Bray F., Center M.M., Ferlay J., Ward E., Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61:69-90.
2. Davis J.J., Fang B. Oncolytic virotherapy for cancer treatment: challenges and solutions. JGene Med 2005, 7:1380-1389.
3. Yamamoto M., Curiel D.T. Current issues and future directions of oncolytic adenoviruses. Mol Ther 2010, 18:243-250.
4. Singh R., Kostarelos K. Designer adenoviruses for nanomedicine and nanodiagnostics. Trends Biotechnol 2009, 27:220-229.
5. Choi J.W., Lee J.S., Kim S.W., Yun C.O. Evolution of oncolytic adenovirus for cancer treatment. Adv Drug Deliv Rev 2012, 64:720-729.
6. Kaplan J.M. Adenovirus-based cancer gene therapy. Curr Gene Ther 2005, 5:595-605.
7. Choi J.W., Kang E., Kwon O.J., Yun T.J., Park H.K., Kim P.H., et al. Local sustained delivery of oncolytic adenovirus with injectable alginate gel for cancer virotherapy. Gene Ther 2013, 20:880-892.
8. Kim P.H., Sohn J.H., Choi J.W., Jung Y., Kim S.W., Haam S., et al. Active targeting and safety profile of PEG-modified adenovirus conjugated with herceptin. Biomaterials 2011, 32:2314-2326.
9. Kim J., Li Y., Kim S.W., Lee D.S., Yun C.O. Therapeutic efficacy of a systemically delivered oncolytic adenovirus - biodegradable polymer complex. Biomaterials 2013, 34:4622-4631.
10. Nigatu A.S., Vupputuri S., Flynn N., Neely B.J., Ramsey J.D. Evaluation of cell-penetrating peptide/adenovirus particles for transduction of CAR-negative cells. JPharm Sci 2013, 102:1981-1993.
11. Kanerva A., Hemminki A. Modified adenoviruses for cancer gene therapy. Int J Cancer 2004, 110:475-480.
12. Dmitriev I., Krasnykh V., Miller C.R., Wang M., Kashentseva E., Mikheeva G., et al. An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. JVirol 1998, 72:9706-9713.
13. Miller C.R., Buchsbaum D.J., Reynolds P.N., Douglas J.T., Gillespie G.Y., Mayo M.S., et al. Differential susceptibility of primary and established human glioma cells to adenovirus infection: targeting via the epidermal growth factor receptor achieves fiber receptor-independent gene transfer. Cancer Res 1998, 58:5738-5748.
14. Douglas J.T., Kim M., Sumerel L.A., Carey D.E., Curiel D.T. Efficient oncolysis by a replicating adenovirus (ad) invivo is critically dependent on tumor expression of primary ad receptors. Cancer Res 2001, 61:813-817.
15. Meunier-Durmort C., Grimal H., Sachs L.M., Demeneix B.A., Forest C. Adenovirus enhancement of polyethylenimine-mediated transfer of regulated genes in differentiated cells. Gene Ther 1997, 4:808-814.
16. Fernandez C.A., Rice K.G. Engineered nanoscaled polyplex gene delivery systems. Mol Pharmacol 2009, 6:1277-1289.
17. Wan Y., Han J., Fan G., Zhang Z., Gong T., Sun X. Enzyme-responsive liposomes modified adenoviral vectors for enhanced tumor cell transduction and reduced immunogenicity. Biomaterials 2013, 34:3020-3030.
18. Chillon M., Lee J.H., Fasbender A., Welsh M.J. Adenovirus complexed with polyethylene glycol and cationic lipid is shielded from neutralizing antibodies invitro. Gene Ther 1998, 5:995-1002.
19. Fasbender A., Zabner J., Chillon M., Moninger T.O., Puga A.P., Davidson B.L., et al. Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer invitro and invivo. JBiol Chem 1997, 272:6479-6489.
20. van der Poel H.G., Molenaar B., van Beusechem V.W., Haisma H.J., Rodriguez R., Curiel D.T., et al. Epidermal growth factor receptor targeting of replication competent adenovirus enhances cytotoxicity in bladder cancer. JUrol 2002, 168:266-272.
21. Park J., Kim W.J. Current status of gene delivery: spotlight on nanomaterial-polymer hybrids. JDrug Target 2012, 20:648-666.
22. Park T.G., Jeong J.H., Kim S.W. Current status of polymeric gene delivery systems. Adv Drug Deliv Rev 2006, 58:467-486.
23. Fischer D., Bieber T., Li Y., Elsasser H.P., Kissel T. Anovel non-viral vector for DNA delivery based on low molecular weight, branched polyethylenimine: effect of molecular weight on transfection efficiency and cytotoxicity. Pharm Res 1999, 16:1273-1279.
24. Kim W.J., Yockman J.W., Jeong J.H., Christensen L.V., Lee M., Kim Y.H., et al. Anti-angiogenic inhibition of tumor growth by systemic delivery of PEI-g-PEG-RGD/pCMV-sFlt-1 complexes in tumor-bearing mice. JControl Release 2006, 114:381-388.
25. Bajaj A., Kondaiah P., Bhattacharya S. Synthesis and gene transfection efficacies of PEI-cholesterol-based lipopolymers. Bioconjug Chem 2008, 19:1640-1651.
26. Hofmann A.F., Mysels K.J. Bile acid solubility and precipitation invitro and invivo: the role of conjugation, pH, and Ca2+ ions. JLipid Res 1992, 33:617-626.
27. Chae S.Y., Kim H.J., Lee M.S., Jang Y.L., Lee Y., Lee S.H., et al. Energy-independent intracellular gene delivery mediated by polymeric biomimetics of cell-penetrating peptides. Macromol Biosci 2011, 11:1169-1174.
28. Lee D., Kim D., Mok H., Jeong J.H., Choi D., Kim S.H. Bioreducible crosslinked polyelectrolyte complexes for MMP-2 siRNA delivery into human vascular smooth muscle cells. Pharm Res 2012, 29:2213-2224.
29. Kang Y.A., Shin H.C., Yoo J.Y., Kim J.H., Kim J.S., Yun C.O. Novel cancer antiangiotherapy using the VEGF promoter-targeted artificial zinc-finger protein and oncolytic adenovirus. Mol Ther 2008, 16:1033-1040.
30. Kim P.H., Kim T.I., Yockman J.W., Kim S.W., Yun C.O. The effect of surface modification of adenovirus with an arginine-grafted bioreducible polymer on transduction efficiency and immunogenicity in cancer gene therapy. Biomaterials 2010, 31:1865-1874.
31. Yun C.O., Kim E., Koo T., Kim H., Lee Y.S., Kim J.H. ADP-overexpressing adenovirus elicits enhanced cytopathic effect by induction of apoptosis. Cancer Gene Ther 2005, 12:61-71.
32. Karlin S., Brendel V. Charge configurations in viral proteins. Proc Natl Acad Sci U S A 1988, 85:9396-9400.
33. Kim P.H., Kim J., Kim T.I., Nam H.Y., Yockman J.W., Kim M., et al. Bioreducible polymer-conjugated oncolytic adenovirus for hepatoma-specific therapy via systemic administration. Biomaterials 2011, 32:9328-9342.
34. Meier O., Greber U.F. Adenovirus endocytosis. JGene Med 2003, 5:451-462.
35. Wang L.H., Rothberg K.G., Anderson R.G. Mis-assembly of clathrin lattices on endosomes reveals a regulatory switch for coated pit formation. JCell Biol 1993, 123:1107-1117.
36. Aoki T., Nomura R., Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 1999, 253:629-636.
37. Perumal O.P., Inapagolla R., Kannan S., Kannan R.M. The effect of surface functionality on cellular trafficking of dendrimers. Biomaterials 2008, 29:3469-3476.
38. Vercauteren D., Vandenbroucke R.E., Jones A.T., Rejman J., Demeester J., De Smedt S.C., et al. The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Mol Ther 2010, 18:561-569.
39. Alemany R., Balague C., Curiel D.T. Replicative adenoviruses for cancer therapy. Nat Biotechnol 2000, 18:723-727.
40. Kelly E., Russell S.J. History of oncolytic viruses: genesis to genetic engineering. Mol Ther 2007, 15:651-659.
41. Kim J., Kim J.H., Choi K.J., Kim P.H., Yun C.O. E1A- and E1B-Double mutant replicating adenovirus elicits enhanced oncolytic and antitumor effects. Hum Gene Ther 2007, 18:773-786.
42. Li Y., Pong R.C., Bergelson J.M., Hall M.C., Sagalowsky A.I., Tseng C.P., et al. Loss of adenoviral receptor expression in human bladder cancer cells: a potential impact on the efficacy of gene therapy. Cancer Res 1999, 59:325-330.
43. Kim J., Kim P.H., Kim S.W., Yun C.O. Enhancing the therapeutic efficacy of adenovirus in combination with biomaterials. Biomaterials 2012, 33:1838-1850.
44. Park Y., Kang E., Kwon O.J., Hwang T., Park H., Lee J.M., et al. Ionically crosslinked Ad/chitosan nanocomplexes processed by electrospinning for targeted cancer gene therapy. JControl Release 2010, 148:75-82.
45. Kwon O.J., Kang E., Kim S., Yun C.O. Viral genome DNA/lipoplexes elicit in situ oncolytic viral replication and potent antitumor efficacy via systemic delivery. JControl Release 2011, 155:317-325.
46. dos Santos T., Varela J., Lynch I., Salvati A., Dawson K.A. Effects of transport inhibitors on the cellular uptake of carboxylated polystyrene nanoparticles in different cell lines. PloS one 2011, 6:e24438.
47. Araki N., Johnson M.T., Swanson J.A. Arole for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. JCell Biol 1996, 135:1249-1260.
48. Hernandez-Alcoceba R. Recent advances in oncolytic virus design. Clin Transl Oncol 2011, 13:229-239.
49. Kwon O.J., Kang E., Choi J.W., Kim S.W., Yun C.O. Therapeutic targeting of chitosan-PEG-folate-complexed oncolytic adenovirus for active and systemic cancer gene therapy. JControl Release 2013, 169:257-265.