A heterotypic bystander effect for tumor cell killing after adeno-associated virus/phage-mediated, vascular-targeted suicide gene transfer

Molecular Cancer Therapeutics

Volumn 8, Issue 8, 2009, Pages 2383-2391

  Trepel, Martin ^a   Stoneham, Charlotte A ^b   Eleftherohorinou, Hariklia ^b   Mazarakis, Nicholas D ^b   Pasqualini, Renata ^c   Arap, Wadih ^c   Hajitou, Amin ^b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

18ALPHA GLYCYRRHETINIC ACID; CONNEXIN 26; CONNEXIN 43; GANCICLOVIR; PARVOVIRUS VECTOR; THYMIDINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BYSTANDER EFFECT; CANCER CELL CULTURE; CANCER GENE THERAPY; CANCER GRAFT; CANCER INHIBITION; CELL COMMUNICATION; CELL KILLING; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; GAP JUNCTION; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUDE MOUSE; PRIORITY JOURNAL; PROMOTER REGION; SUICIDE GENE; SUICIDE GENE THERAPY;

ANIMALS; BACTERIOPHAGES; BYSTANDER EFFECT; CELL LINE, TUMOR; DEPENDOVIRUS; ENDOTHELIAL CELLS; FEMALE; FIBROBLAST GROWTH FACTOR 4; GAP JUNCTIONS; GENE THERAPY; GENES, TRANSGENIC, SUICIDE; GENETIC VECTORS; GLYCYRRHETINIC ACID; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEOPLASMS; RATS; THYMIDINE KINASE;

EID: 68849090740     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0110     Document Type: Article

References (45)

1. Moolten FL, Wells JM. Curability of tumors bearing herpes thymidine kinase genes transferred by retroviral vectors. J Natl Cancer Inst 1990;82:297-300.
2. Culver KW, Ram Z, Wallbridge S, Ishii H, Oldfield EH, Blaese RM. In vivo gene therapy with retroviral vector-producer cells for treatment of experimental brain tumors. Science 1992;256:1550-2.
3. Cole C, Qiao J, Kottke T, et al. Tumor-targeted, systemic delivery of therapeutic viral vectors using hitchhiking on antigen-specific T cells. Nat Med 2005;11:1073-81.
4. Hamel W, Magnelli L, Chiarugi VP, Israel MA. Herpes simplex virus thymidine kinase/ganciclovir-mediated apoptotic death of bystander cells. Cancer Res 1996;56:2697-702.
5. Grignet-Debrus C, Cool V, Baudson N, Velu T, Calberg-Bacq CM. The role of cellular- and prodrug-associated factors in the bystander effect induced by the Varicella zoster and Herpes simplex viral thymidine kinases in suicide gene therapy. Cancer Gene Ther 2000;7:1456-68.
6. Ram Z, Culver KW, Oshiro EM, et al. Therapy of malignant brain tumors by intratumoral implantation of retroviral vector-producing cells. Nat Med 1997;3:1354-61.
7. Folkman J. Principles and practice of oncology. In: DeVita VT, Hellman S, Rosenberg SA editors. Cancer: 5th ed. Philadelphia: Lippincott; 1997. p. 3075-85.
8. St Croix B, Rago C, Velculescu V, et al. Genes expressed in human tumor endothelium. Science 2000;289:1197-202.
9. Hajitou A, Arap W, Pasqualini R. Vascular targeting: recent advances and therapeutic perspectives. Trends Cardiovasc Med 2006;16:80-8.
10. Reynolds PN, Zinn KR, Gavrilyuk VD, et al. A targetable injectable adenoviral vector for selective gene delivery to pulmonary endothelium in vivo. Mol Ther 2000;2:562-78.
11. Hart SL, Knight AM, Harbottle RP, et al. Cell binding and internalization by filamentous phage displaying a cyclic Arg-Gly-Asp-containing peptide. J Biol Chem 1994;269:12468-74.
12. Kassner PD, Burg MA, Baird A, Larocca D. Genetic selection of phage engineered for receptor-mediated gene transfer to mammalian cells. Biochem Biophys Res Commun 1999;264:921-8.
13. Larocca D, Kassner PD, Witte A, Ladner RC, Pierce GF, Baird A. Gene transfer to mammalian cells using genetically targeted filamentous bacteriophage. FASEB J 1999;13:727-34.
14. Nicklin S, Buening H, Dishart KL, et al. Efficient and selective AAV2-mediated gene transfer directed to human vascular endothelial cells. Mol Ther 2001;4:174-81.
15. Masood R, Gordon EM, Whitley MD, et al. Retroviral vectors bearing IgG-binding motifs for antibody-mediated targeting of vascular endothelial growth factor receptors. Int J Mol Med 2001;8:335-43.
16. Müller O, Kaul F, Weitzman MD, et al. Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat Biotechnol 2003;21:1040-6.
17. Lieber A. AAV display - homing in on the target. Nat Biotechnol 2003;21:1011-3.
18. White SJ, Nicklin SA, Büning H, et al. Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 2004;109:513-9.
19. Shinozaki K, Suominen E, Carrick F, et al. Efficient infection of tumor endothelial cells by a capsid-modified adenovirus. Gene Ther 2006;13:52-9.
20. Hajitou A, Trepel M, Lilley CE, et al. A hybrid vector for ligand-directed tumor targeting and molecular imaging. Cell 2006;125:385-98.
21. Hajitou A, Lev DC, Hannay JA, et al. A preclinical model for predicting drug response in soft-tissue sarcoma with targeted AAVP molecular imaging. Proc Natl Acad Sci U S A 2008;105:4471-6.
22. Tandle A, Hanna E, Lorang D, et al. Tumor vasculature-targeted delivery of tumor necrosis factor-α. Cancer 2009;115:128-39.
23. Arap W, Pasqualini R, Ruoslahti E. Cancer treatment by targeted drug delivery to tumor vasculature in a mouse model. Science 1998;279:377-80.
24. vβ3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 1994;79:1157-64.
25. Ellerby HM, Arap W, Ellerby LM, et al. Anti-cancer activity of targeted pro-apoptotic peptides. Nat Med 1999;5:1032-8.
26. Hood JD, Bednarski M, Frausto R, Guccione S, Reisfeld RA, Xiang R. Tumor regression by targeted gene delivery to the neovasculature. Science 2002;296:2404-7.
27. vβ3 integrin. Mol Cancer Res 2004;2:663-73.
28. Hajitou A, Rangel R, Trepel M, et al. Design and construction of targeted AAVP vectors for mammalian cell transduction. Nat Protoc 2007;2:523-31.
29. Hajitou A, Sounni NE, Devy L, et al. Down-regulation of vascular endothelial growth factor by tissue inhibitor of metalloproteinase-2: effect on in vivo mammary tumor growth and angiogenesis. Cancer Res 2001;61:3450-7.
30. Black ME, Kokoris MS, Sabo P. Herpes simplex virus-1 thymidine kinase mutants created by semi-random sequence mutagenesis improve prodrug-mediated tumor cell killing. Cancer Res 2001;61:3022-6.
31. 18F-FEAU. Nat Protoc 2007;2:416-23.
32. Mesnil M, Yamasaki H. Bystander effect in herpes simplex virus-thymidine kinase/ganciclovir cancer gene therapy: role of gap-junctional intercellular communication. Cancer Res 2002;60:3989-99.
33. Mesnil M, Piccoli C, Tiraby G, Willecke K, Yamasaki H. Bystander killing of cancer cells by herpes simplex virus thymidine kinase gene is mediated by connexins. Proc Natl Acad Sci U S A 1996;93:1831-5.
34. Mesnil M, Piccoli C, Yamasaki H. A tumor suppressor gene, Cx26, also mediates the bystander effect in HeLa cells. Cancer Res 1997;57:2929-32.
35. Freeman SM, Abboud CN, Whartenby KA, Abraham GN. The bystander effect: tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 1993;53:5274-84.
36. Ram Z, Walbridge S, Shawker T, Culver KW, Blaese M, Oldfield EH. The effect of thymidine kinase transduction and ganciclovir therapy on tumor vasculature and growth of 9L gliomas in rats. J Neurosurg 1994;81:256-60.
37. Dilber MS, Gahrton G. Suicide gene therapy: possible applications in haematopoietic disorders. J Intern Med 2001;249:359-67.
38. Azzam EI, Little JB. The radiation-induced bystander effect: evidence and significance. Hum Exp Toxicol 2004;23:61-5.
39. Kuriyama S, Kikukawa M, Masui K, et al. Cancer gene therapy with HSVtk/GCV system depends on T-cell-mediated immune responses and causes apoptotic death of tumor cells in vivo. Int J Cancer 1999;83:374-80.
40. Nicholas TW, Read SB, Burrows FJ, Kruse CA. Suicide gene therapy with Herpes simplex virus thymidine kinase and ganciclovir is enhanced with connexins to improve gap junctions and bystander effects. Histol Histopathol 2003;18:495-507.
41. Burrows FJ, Gore M, Smiley WR, et al. Purified herpes simplex virus thymidine kinase retroviral particles: III. Characterization of bystander killing mechanisms in transfected tumor cells. Cancer Gene Ther 2002;9:87-95.
42. Bai S, Du L, Liu W, Whittle IR, He L. Tentative novel mechanism of the bystander effect in glioma gene therapy with HSV-TK/GCV system. Biochem Biophys Res Commun 1999;259:455-9.
43. Ramesh R, Marrogi AJ, Munshi A, Abboud CN, Freeman SM. In vivo analysis of the bystander effect: a cytokine cascade. Exp Hematol 1996;24:829-38.
44. Barba D, Hardin J, Sadelain M, Gage FH. Development of anti-tumor immunity following thymidine kinase-mediated killing of experimental brain tumors. Proc Natl Acad Sci U S A 1994;91:4348-52.
45. Okada T, Shah M, Higginbotham JN, et al. AV.TK-mediated killing of subcutaneous tumors in situ results in effective immunization against established secondary intracranial tumor deposits. Gene Ther 2001;8:1315-22.