Dual tumor targeting with pH-sensitive and bioreducible polymer-complexed oncolytic adenovirus

Biomaterials

Volumn 41, Issue , 2015, Pages 53-68

  Moon, Chang Yoon ^a   Choi, Joung Woo ^a   Kasala, Dayananda ^a   Jung, Soo Jung ^a   Kim, Sung Wan ^a,b   Yun, Chae Ok ^a  

^a Hanyang University   (South Korea)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Bioreducible polymer; Cancer gene therapy; Oncolytic adenovirus; PH sensitive; Systemic administration; Tumor microenvironment

Indexed keywords

BIOCOMPATIBILITY; CYTOLOGY; DISEASES; GENE EXPRESSION; GENE THERAPY; PH SENSORS; POLYMERS; VIRUSES;

BIOREDUCIBLE POLYMER; CANCER GENE THERAPY; ONCOLYTIC ADENOVIRUS; PH SENSITIVE; SYSTEMIC ADMINISTRATION; TUMOR MICROENVIRONMENT;

TUMORS;

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; INTERLEUKIN 6; ONCOLYTIC ADENOVIRUS; POLYMER; SHORT HAIRPIN RNA; VASCULOTROPIN; ANGIOGENESIS INHIBITOR; BIOMATERIAL; ONCOLYTIC VIRUS; VASCULOTROPIN A;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BIOCOMPATIBILITY; BRAIN TUMOR CELL LINE; CANCER GENE THERAPY; COMPLEX FORMATION; CONTROLLED STUDY; ENCAPSULATION; ENDOCYTOSIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOGENICITY; LIVER TOXICITY; MCF 7 CELL LINE; MOUSE; NONHUMAN; PH; PINOCYTOSIS; VASCULARIZATION; ADENOVIRIDAE; ANIMAL; CELL DEATH; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG EFFECTS; ENDOSOME; GENETIC TRANSDUCTION; HEK293 CELL LINE; IMMUNE EVASION; LIVER; METABOLISM; PATHOLOGY; PHYSIOLOGY; SYNTHESIS; TUMOR CELL LINE;

ADENOVIRIDAE;

ADENOVIRIDAE; ANGIOGENESIS INHIBITORS; ANIMALS; BIOCOMPATIBLE MATERIALS; CELL DEATH; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; ENDOCYTOSIS; ENDOSOMES; HEK293 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNE EVASION; LIVER; MICE; ONCOLYTIC VIRUSES; POLYMERS; TRANSDUCTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84916918372     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.11.021     Document Type: Article

References (49)

1. Wold W.S., Toth K. Adenovirus vectors for gene therapy, vaccination and cancer gene therapy. Curr Gene Ther 2013, 13:421-433.
2. Choi I.K., Yun C.O. Recent developments in oncolytic adenovirus-based immunotherapeutic agents for use against metastatic cancers. Cancer Gene Ther 2013, 20:70-76.
3. 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.
4. Bachtarzi H., Stevenson M., Fisher K. Cancer gene therapy with targeted adenoviruses. Expert Opin Drug Deliv 2008, 5:1231-1240.
5. Yun C.O. Overcoming the extracellular matrix barrier to improve intratumoral spread and therapeutic potential of oncolytic virotherapy. Curr Opin Mol Ther 2008, 10:356-361.
6. Guo Z.S., Thorne S.H., Bartlett D.L. Oncolytic virotherapy: molecular targets in tumor-selective replication and carrier cell-mediated delivery of oncolytic viruses. Biochim Biophys Acta 2008, 1785:217-231.
7. Russell S.J., Peng K.W., Bell J.C. Oncolytic virotherapy. Nat Biotechnol 2012, 30:658-670.
8. Harrop R., John J., Carroll M.W. Recombinant viral vectors: cancer vaccines. Adv Drug Deliv Rev 2006, 58:931-947.
9. Reid T., Galanis E., Abbruzzese J., Sze D., Andrews J., Romel L., et al. Intra-arterial administration of a replication-selective adenovirus (dl1520) in patients with colorectal carcinoma metastatic to the liver: a phase I trial. Gene Ther 2001, 8:1618-1626.
10. Kwon O.J., Kim P.H., Huyn S., Wu L., Kim M., Yun C.O. Ahypoxia- and {alpha}-fetoprotein-dependent oncolytic adenovirus exhibits specific killing of hepatocellular carcinomas. Clin Cancer Res 2010, 16:6071-6082.
11. Yu W., Fang H. Clinical trials with oncolytic adenovirus in China. Curr Cancer Drug Target 2007, 7:141-148.
12. Cichon G., Schmidt H.H., Benhidjeb T., Loser P., Ziemer S., Haas R., et al. Intravenous administration of recombinant adenoviruses causes thrombocytopenia, anemia and erythroblastosis in rabbits. JGene Med 1999, 1:360-371.
13. Meier O., Greber U.F. Adenovirus endocytosis. JGene Med 2003, 5:451-462.
14. 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.
15. Wang C., Pham P.T. Polymers for viral gene delivery. Expert Opin Drug Deliv 2008, 5:385-401.
16. Kang E., Yun C.O. Current advances in adenovirus nanocomplexes: more specificity and less immunogenicity. BMB Rep 2010, 43:781-788.
17. Kasala D., Choi J.W., Kim S.W., Yun C.O. Utilizing adenovirus vectors for gene delivery in cancer. Expert Opin Drug Deliv 2014, 11:379-392.
18. Lee W.J., Kim Y.O., Choi I.K., Rah D.K., Yun C.O. Adenovirus-relaxin gene therapy for keloids: implication for reversing pathological fibrosis. Br J Dermatol 2011, 165:673-677.
19. 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.
20. Eto Y., Yoshioka Y., Mukai Y., Okada N., Nakagawa S. Development of PEGylated adenovirus vector with targeting ligand. Int J Pharm 2008, 354:3-8.
21. Han J., Zhao D., Zhong Z., Zhang Z., Gong T., Sun X. Combination of adenovirus and cross-linked low molecular weight PEI improves efficiency of gene transduction. Nanotechnology 2010, 21:105106.
22. Park J.W., Mok H., Park T.G. Physical adsorption of PEG grafted and blocked poly-L-lysine copolymers on adenovirus surface for enhanced gene transduction. JControl Release 2010, 142:238-244.
23. Fischer D., Li Y., Ahlemeyer B., Krieglstein J., Kissel T. Invitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. Biomaterials 2003, 24:1121-1131.
24. Lee E.S., Gao Z., Bae Y.H. Recent progress in tumor pH targeting nanotechnology. JControl Release 2008, 132:164-170.
25. 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.
26. Yoo J.Y., Kim J.H., Kwon Y.G., Kim E.C., Kim N.K., Choi H.J., et al. VEGF-specific short hairpin RNA-expressing oncolytic adenovirus elicits potent inhibition of angiogenesis and tumor growth. Mol Ther 2007, 15:295-302.
27. Ko J., Park K., Kim Y.S., Kim M.S., Han J.K., Kim K., et al. Tumoral acidic extracellular pH targeting of pH-responsive MPEG-poly(beta-amino ester) block copolymer micelles for cancer therapy. JControl Release 2007, 123:109-115.
28. Zhang C.Y., Yang Y.Q., Huang T.X., Zhao B., Guo X.D., Wang J.F., et al. Self-assembled pH-responsive MPEG-b-(PLA-co-PAE) block copolymer micelles for anticancer drug delivery. Biomaterials 2012, 33:6273-6283.
29. 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.
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. 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.
32. Aoki T., Nomura R., Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 1999, 253:629-636.
33. 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.
34. Meier O., Greber U.F. Adenovirus endocytosis. JGene Med 2004, 6(Suppl.1):S152-S163.
35. Xu Z., Tian J., Smith J.S., Byrnes A.P. Clearance of adenovirus by Kupffer cells is mediated by scavenger receptors, natural antibodies, and complement. JVirol 2008, 82:11705-11713.
36. Muruve D.A., Barnes M.J., Stillman I.E., Libermann T.A. Adenoviral gene therapy leads to rapid induction of multiple chemokines and acute neutrophil-dependent hepatic injury invivo. Hum Gene Ther 1999, 10:965-976.
37. Lieber A., He C.Y., Meuse L., Schowalter D., Kirillova I., Winther B., et al. The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. JVirol 1997, 71:8798-8807.
38. O'Riordan C.R., Lachapelle A., Delgado C., Parkes V., Wadsworth S.C., Smith A.E., et al. PEGylation of adenovirus with retention of infectivity and protection from neutralizing antibody invitro and invivo. Hum Gene Ther 1999, 10:1349-1358.
39. Fisher K.D., Green N.K., Hale A., Subr V., Ulbrich K., Seymour L.W. Passive tumour targeting of polymer-coated adenovirus for cancer gene therapy. JDrug Target 2007, 15:546-551.
40. Fisher K.D., Stallwood Y., Green N.K., Ulbrich K., Mautner V., Seymour L.W. Polymer-coated adenovirus permits efficient retargeting and evades neutralising antibodies. Gene Ther 2001, 8:341-348.
41. 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.
42. 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.
43. Yao X.L., Yoshioka Y., Ruan G.X., Chen Y.Z., Mizuguchi H., Mukai Y., et al. Optimization and internalization mechanisms of PEGylated adenovirus vector with targeting peptide for cancer gene therapy. Biomacromolecules 2012, 13:2402-2409.
44. Yao X., Yoshioka Y., Morishige T., Eto Y., Narimatsu S., Kawai Y., et al. Tumor vascular targeted delivery of polymer-conjugated adenovirus vector for cancer gene therapy. Mol Ther 2011, 19:1619-1625.
45. Kim J., Nam H.Y., Kim T.I., Kim P.H., Ryu J., Yun C.O., et al. Active targeting of RGD-conjugated bioreducible polymer for delivery of oncolytic adenovirus expressing shRNA against IL-8 mRNA. Biomaterials 2011, 32:5158-5166.
46. Morrison J., Briggs S.S., Green N.K., Thoma C., Fisher K.D., Kehoe S., et al. Cetuximab retargeting of adenovirus via the epidermal growth factor receptor for treatment of intraperitoneal ovarian cancer. Hum Gene Ther 2009, 20:239-251.
47. Zhang X., Lin Y., Gillies R.J. Tumor pH and its measurement. JNucl Med 2010, 51:1167-1170.
48. Lee C.H., Kasala D., Na Y., Lee M.S., Kim S.W., Jeong J.H., et al. Enhanced therapeutic efficacy of an adenovirus-PEI-bile-acid complex in tumors with low coxsackie and adenovirus receptor expression. Biomaterials 2014, 35:5505-5516.
49. Croyle M.A., Chirmule N., Zhang Y., Wilson J.M. "Stealth" adenoviruses blunt cell-mediated and humoral immune responses against the virus and allow for significant gene expression upon readministration in the lung. JVirol 2001, 75:4792-4801.