Vascular-targeted cancer gene therapy

Expert Opinion on Biological Therapy

Volumn 4, Issue 12, 2004, Pages 1911-1920

  Dougherty, Graeme J ^a,b   Davis, Peter D ^b   Dougherty, Shona T ^a  

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

^b Angiogene Pharmaceuticals Ltd   (United Kingdom)

Author keywords

Gene therapy; Tumour angiogenesis; Vascular targeting; Viral vector

Indexed keywords

ADAPTOR PROTEIN; ADENOVIRUS VECTOR; ALPHA5 INTEGRIN; ANGIOPOIETIN RECEPTOR; BETA1 INTEGRIN; BETA3 INTEGRIN; CADHERIN; CD51 ANTIGEN; COMBRETASTATIN A4; COMPLEMENTARY DNA; ENDOGLIN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; IMMUNOGLOBULIN F(AB) FRAGMENT; INTERCELLULAR ADHESION MOLECULE 2; MESSENGER RNA; N ACETYLCOLCHINOL PHOSPHATE; NERVE CELL ADHESION MOLECULE; OSTEOPONTIN; PARVOVIRUS VECTOR; PEPTIDE DERIVATIVE; RETROVIRUS VECTOR; SERINE 2 METHOXY 5 [2 (3,4,5 TRIMETHOXYPHENYL)VINYL]ANILIDE; TUBULIN; UNINDEXED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VERY LATE ACTIVATION ANTIGEN 1; VERY LATE ACTIVATION ANTIGEN 2; VITRONECTIN RECEPTOR;

ANTINEOPLASTIC ACTIVITY; ATAXIA; CANCER PAIN; CANCER THERAPY; CELL SPECIFICITY; CELL TYPE; CLINICAL TRIAL; DEPOLYMERIZATION; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; EXPERIMENTAL MODEL; GENE TARGETING; GENE TRANSFER; HEART DISEASE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NEUROLOGIC DISEASE; NONHUMAN; REVIEW; TARGET CELL; TECHNIQUE; TRANSCRIPTION REGULATION; TUMOR BLOOD FLOW; TUMOR CELL; TUMOR GROWTH; TUMOR VASCULARIZATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY;

ENDOTHELIUM, VASCULAR; GENE TARGETING; GENE THERAPY; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC;

ADENOVIRIDAE; ANIMALIA; PARVOVIRUS; UNIDENTIFIED RETROVIRUS;

EID: 10344230402     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.4.12.1911     Document Type: Review

References (93)

1. ROCHLITZ CF: Gene therapy of cancer. Swiss Med. Wkly (2001) 131:4-9.
2. SMILEY WR, LAUBERT B, HOWARD BD et al.: Establishment of parameters for optimal transduction efficiency and antitumor effects with purified high-titer HSV-TK retroviral vector in established solid tumors. Hum. Gene Ther. (1997) 8:965-977.
3. RAINOV NG, KRAMM CM: Vector delivery methods and targeting strategies for gene therapy of brain tumors. Curr. Gene Ther. (2001) 1:367-383.
4. BILBAO R, BUSTOS M, ALZUGUREN P et al.: A blood-tumor barrier limits gene transfer to experimental liver cancer: the effect of vasoactive compounds. Gene Ther. (2000) 7:1824-1832.
5. JAIN RK: Vascular and interstitial barriers to delivery of therapeutic agents in tumors. Cancer Metastasis Rev. (1990) 9:253-266.
6. FOLKMAN J: Tumor angiogenesis. Adv. Cancer Res. (1985) 43:175-203.
7. FOLKMAN J: Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. (2002) 29:15-18.
8. DENEKAMP J: Vascular attack as a therapeutic strategy for cancer. Cancer Metastasis Rev. (1990) 9:267-282. A first-rate review by an early proponent and passionate advocate of the approach, describing the rationale and merits of targeting tumour vasculature.
9. RANIERI G, GASPARINI G: Angiogenesis and angiogenesis inhibitors: a new potential anticancer therapeutic strategy. Curr. Drug Targets Immune Endocr. Metabol. Disord. (2001) 1:241-253.
10. NICHOLSON B, SCHAEFER G, THEODORESCU D: Angiogenesis in prostate cancer: biology and therapeutic opportunities. Cancer Metastasis Rev. (2001) 20:297-319.
11. SIM BK, MACDONALD NJ, GUBISH ER: Angiostatin and endostatin: endogenous inhibitors of tumor growth. Cancer Metastasis Rev. (2000) 19:181-190.
12. KERBEL RS: Antiangiogenic drugs and current strategies for the treatment of lung cancer. Semin. Oncol. (2004) 31:54-60.
13. DENEKAMP J, DASU A, WAITES A: Vasculature and microenvironmental gradients: the missing links in novel approaches to cancer therapy. Adv. Enzyme Regul. (1998) 38:281-299.
14. CHAPLIN DJ, HILL SA: Selective induction of tumor ischemia: development of vascular targeting agents for cancer therapy. Curr. Opin. Investig. Drugs (2002) 3:1381-1384.
15. DAVIS PD, DOUGHERTY GJ, BLAKEY DC et al.: ZD6126: a novel vascular-targeting agent that causes selective destruction of tumor vasculature. Cancer Res. (2002) 62:7247-7253.
16. THORPE PE, CHAPLIN DJ, BLAKEY DC: The first international conference on vascular targeting: meeting overview. Cancer Res. (2003) 63:1144-1147.
17. SIEMANN DW, CHAPLIN DJ, HORSMAN MR: Vascular-targeting therapies for treatment of malignant disease. Cancer (2004) 100:2491-2499. Timely review focusing on small molecule vascular-targeting agents, describing recent progress and clinical experience.
18. THORPE PE: Vascular targeting agents as cancer therapeutics. Clin. Cancer Res. (2004) 10:415-427.
19. SMITH L, BYERS JF: Gene therapy in the post-Gelsinger era. JONAS Healthc. Law Ethics Regul. (2002) 4:104-110.
20. RUBANYI GM: The future of human gene therapy. Mol. Aspects Med. (2001) 22:113-142.
21. WILLIAMS DA, BAUM C: Medicine. Gene therapy-new challenges ahead. Science (2003) 302:400-401.
22. KAISER J: Gene therapy. Seeking the cause of induced leukemias in X-SCID trial. Science (2003) 299:495.
23. KOHN DB, SADELAIN M, GLORIOSO JC: Occurrence of leukaemia following gene therapy of X-linked SCID. Nat. Rev. Cancer (2003) 3:477-488.
24. MCCORMACK MP, FORSTER A, DRYNAN L, PANNELL R, RABBITTS TH: The LMO2 T-cell oncogene is activated via chromosomal translocations or retroviral insertion during gene therapy but has no mandatory role in normal T-cell development. Mol. Cell Biol. (2003) 23:9003-9013.
25. FOX JL: US authorities uphold suspension of SCID gene therapy. Nat. Biotechnol. (2003) 21:217.
26. CHAPLIN DJ, DOUGHERTY GJ: Tumour vasculature as a target for cancer therapy. Br. J. Cancer (1999) 80(Suppl. 1):57-64.
27. YANG ZY, DUCKERS HJ, SULLIVAN NJ, SANCHEZ A, NABEL EG, NABEL GJ: Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat. Med. (2000) 6:886-889.
28. DROPULIC B, MASTERS CL: Entry of neurotropic arboviruses into the central nervous system: an in vitro study using mouse brain endothelium. J. Inject. Dis. (1990) 161:685-691.
29. GERNA G, BALDANTI F, REVELLO MG: Pathogenesis of human cytomegalovirus infection and cellular targets. Hum. Immunol. (2004) 65:381-386.
30. AGNELLO V, ABEL G: Localization of hepatitis C virus in cutaneous vasculitic lesions in patients with type II cryoglobulinemia. Arthritis Rheum. (1997) 40:2007-2015.
31. CHI D, HENRY J, KELLEY J, THORPE R, SMITH JK, KRISHNASWAMY G: The effects of HIV infection on endothelial function. Endothelium (2000) 7:223-242.
32. TOMKO RP, XU R, PHILIPSON L: HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA (1997) 94:3352-3356.
33. BERGELSON JM, CUNNINGHAM JA, DROGUETT G et al.: Isolation of a common receptor for Coxsackie B viruses and adenoviruses 2 and 5. Science (1997) 275:1320-1323. Identification and initial characterisation of CAR, the broadly distributed cell surface molecule that functions as a receptor for adenoviral vectors.
34. WICKHAM TJ, MATHIAS P, CHERESH DA, NEMEROW GR: Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell (1993) 73:309-319. Description of the two-step model in which initegrins play an essential role in the uptake of adenoviral particles after initial binding to CAR.
35. GREBER UF, WILLETTS M, WEBSTER P, HELENIUS A: Stepwise dismantling of adenovirus 2 during entry into cells. Cell (1993) 75:477-486.
36. WANG K, HUANG S, KAPOOR-MUNSHI A, NEMEROW G: Adenovirus internalization and infection require dynamin. J. Virol. (1998) 72:3455-3458.
37. BERGELSON JM: Receptors mediating adenovirus attachment and internalization. Biochem. Pharmocol. (1999) 57:975-979.
38. MICHAEL SI, HONG JS, CURIEL DT, ENGLER JA: Addition of a short peptide ligand to the adenovirus fiber protein. Gene Ther. (1995) 2:660-668.
39. PEARSON AS, KOCH PE, ATKINSON N et al.: Factors limiting adenovirus-mediated gene transfer into human lung and pancreatic cancer cell lines. Clin. Cancer Res. (1999) 5:4208-4213.
40. BILBAO G, GOMEZ-NAVARRO J, CURIEL DT: Targeted adenoviral vectors for cancer gene therapy. Adv. Exp. Med. Biol. (1998) 451:365-374. Curiel and colleagues have played a leading role in the development of targetable adenoviral vectors, and this review details both their experience and the challenges associated with this approach.
41. KRASNYKH V, DMITRIEV I, NAVARRO JG et al.: Advanced generation adenoviral vectors possess augmented gene transfer efficiency based upon coxsackie adenovirus receptor-independent cellular entry capacity. Cancer Res. (2000) 60:6784-6787.
42. WICKHAM TJ, LEE GM, TITUS JA et al.: Targeted adenovirus-mediated gene delivery to T cells via CD3. J. Virol (1997) 71:7663-7669. Formal demonstration that a single cell surface protein (in this case CD3) can substitute for both CAR and integrins to permit the infection of target cells by genetically engineered adenoviral vectors.
43. ADAMS MD, KERLAVAGE AR, FLEISCHMANN RD et al.: Initial assessment of human gene diversity and expression patterns based upon 83 million nucleotides of cDNA sequence. Nature (1995) 377:3-174.
44. DENEKAMP J: Review article: angiogenesis, neovascular proliferation and vascular pathophysiology as targets for cancer therapy. Br. J. Radiol. (1993) 66:181-196.
45. ZHANG HT, GORN M, SMITH K, GRAHAM AP, LAU KK, BICKNELL R: Transcriptional profiling of human microvascular endothelial cells in the proliferative and quiescent state using cDNA arrays. Angiogenesis (1999) 3:211-219.
46. SENGER DR, CLAFFEY KP, BENES JE, PERRUZZI CA, SERGIOU AP, DETMAR M: Angiogenesis promoted by vascular endothelial growth factor: regulation through alpha1beta1 and alpha2beta1 integrins. Proc. Natl. Acad. Sci. USA (1997) 94:13612-13617.
47. FABBRI M, CASTELLANI P, GOTWALS PJ, KOTELIANSKI V, ZARDI L, ZOCCHI MR: A functional monoclonal antibody recognizing the human alpha 1-integrin I-domain. Tissue Antigens (1996) 48:47-51.
48. ENENSTEIN J, KRAMER RH: Confocal microscopic analysis of integral expression on the microvasculature and its sprouts in the neonatal foreskin. J. Invest. Dermatol. (1994) 103:381-386.
49. DEFILIPPI P, VAN HINSBERGH V, BERTOLOTTO A, ROSSINO P, SILENGO L, TARONE G: Differential distribution and modulation of expression of alpha 1/beta 1 integrin on human endothelial cells. J. Cell Biol. (1991) 114:855-863.
50. BROOKS PC, MONTGOMERY AM, ROSENFELD M et al.: Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell (1994) 79:1157-1164.
51. BROOKS PC, STROMBLAD S, KLEMKE R, VISSCHER D, SARKAR FH, CHERESH DA: Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. J. Clin. Invest. (1995) 96:1815-1822.
52. KOZIAN DH, AUGUSTIN HG: Rapid identification of differentially expressed endothelial cell genes by RNA display. Biochem. Biophys. Res. Commun. (1995) 209:1068-1075.
53. PROLS F, LOSER B, MARX M: Differential expression of osteopontin, PC4, and CEC5, a novel mRNA species, during in vitro angiogenesis. Exp. Cell Res. (1998) 239:1-10.
54. KRASNYKH V, DMITRIEV I, MIKHEEVA G, MILLER CR, BELOUSOVA N, CURIEL DT: Characterization of an adenovirus vector containing a heterologous peptide epitope in the HI loop of the fiber knob. J. Virol. (1998) 72:1844-1852.
55. NICKLIN SA, WHITE SJ, NICOL CG, VON SEGGERN DJ, BAKER AH: In vitro and in vivo characterisation of endothelial cell selective adenoviral vectors. J. Gene Med. (2004) 6:300-308. One of several recent papers in which phage display techniques were used to isolate defined peptides that were then incorporated into the adenoviral fibre protein in order to produce vectors that preferentially target endothelial cells.
56. MULLER OJ, KAUL F, WEITZMAN MD et al.: Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat. Biotechnol (2003) 21:1040-1046.
57. WHITE SJ, NICKLIN SA, BUNING H et al.: Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation (2004) 109:513-519.
58. LIU L, ANDERSON WF, BEART RW, GORDON EM, HALL FL: Incorporation of tumor vasculature targeting motifs into moloney murine leukemia virus env escort proteins enhances retrovirus binding and transduction of human endothelial cells. J. Virol. (2000) 74:5320-5328.
59. 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) 8:335-343.
60. DOUGHERTY GJ, PETERS CE, DOUGHERTY ST, MCBRIDE WH, CHAPLIN DJ: Development of targetable retroviral vectors. Transfus. Sci. (1996) 17:121-128.
61. GRAULICH W, NETTELBECK DM, FISCHER D, KISSEL T, MULLER R: Cell type specificity of the human endoglin promoter. Gene (1999) 227:55-62.
62. NICKLIN SA, REYNOLDS PN, BROSNAN MJ et al.: Analysis of cell-specific promoters for viral gene therapy targeted at the vascular endothelium. Hypertension (2001) 38:65-70.
63. REYNOLDS PN, NICKLIN SA, KALIBEROVA L et al.: Combined transductional and transcriptional targeting improves the specificity of transgene expression in vivo. Nat. Biotechnol. (2001) 19:838-842.
64. KORHÔNEN J, LAHTINEN I, HALMEKYTO M et al.: Endothelial-specific gene expression directed by the the gene promoter in vivo. Blood (1995) 86:1828-1835.
65. DE PALMA M, VENNERI MA, NALDINI L: In vivo targeting of tumor endothelial cells by systemic delivery of lentiviral vectors. Hum. Gene Ther. (2003) 14:1193-1206.
66. COWAN PJ, SHINKEL TA, WITORT EJ, BARLOW H, PEARSE MJ, D'APICE AJ: Targeting gene expression to endothelial cells in transgenic mice using the human intercellular adhesion molecule 2 promoter. Transplantation (1996) 62:155-160.
67. VELASCO B, RAMIREZ JR, RELLOSO M et al.: Vascular gene transfer driven by endoglin and ICAM-2 endothelial-specific promoters. Gene Ther. (2001) 8:897-904.
68. RICHARDSON TB, KASPERS J, PORTER CD: Retroviral hybrid LTR vector strategy: functional analysis of LTR elements and generation of endothelial cell specificity. Gene Ther. (2004) 11:775-783.
69. DANCER A, JULIEN S, BOUILLOT S, POINTU H, VERNET M, HUBER P: Expression of thymidine kinase driven by an endothelial-specific promoter inhibits tumor growth of Lewis lung carcinoma cells in transgenic mice. Gene Ther. (2003) 10:1170-1178.
70. JAGER U, ZHAO Y, PORTER CD: Endothelial cell-specific transcriptional targeting from a hybrid long terminal repeat retrovirus vector containing human preproendothelin-1 promoter sequences. J. Virol. (1999) 73:9702-9709.
71. MAVRIA G, JAGER U, PORTER CD: Generation of a high titre retroviral vector for endothelial cell-specific gene expression in vivo. Gene Ther. (2000) 7:368-376.
72. VARDA-BLOOM N, SHAISH A, GONEN A. et al.: Tissue-specific gene therapy directed to tumor angiogenesis. Gene Ther. (2001) 8:819-827.
73. CHO J, LIM W, JANG S, LEE Y: Development of an efficient endothelial cell specific vector using promoter and 5' untranslated sequences from the human preproendothelin-1 gene. Exp. Mol. Med. (2003) 35:269-274.
74. GREENBERGER S, SHAISH A, VARDA-BLOOM N et al.: Transcription-controlled gene therapy against tumor angiogenesis. J. Clin. Invest. (2004) 113:1017-1024.
75. SAVONTAUS MJ, SAUTER BV, HUANG TG, WOO SL: Transcriptional targeting of conditionally replicating adenovirus to dividing endothelial cells. Gene Ther. (2002) 9:972-979.
76. DAI C, MCANINCH RE, SUTTON RE: Identification of synthetic endothelial cell-specific promoters by use of a high-throughput screen. J. Virol. (2004) 78:6209-6221. A promising study describing a novel technique that can be used to derive synthetic promoter elements that exhibit high activity and specificity for particular cell types.
77. EDELMAN GM, MEECH R, OWENS GC, JONES FS: Synthetic promoter elements obtained by nucleotide sequence variation and selection for activity. Proc. Natl. Acad. Sci. USA (2000) 97:3038-3043. Isolation of synthetic muscle-specific promoter elements that exhibit activity greater than that of commonly used naturally occurring sequences.
78. LI X, EASTMAN EM, SCHWARTZ RJ, DRAGHIA-AKLI R: Synthetic muscle promoters: activities exceeding naturally occurring regulatory sequences. Nat. Biotechnol. (1999) 17:241-245.
79. WORTHINGTON J, ROBSON T, MURRAY M, O'ROURKE M, KEILTY G, HIRST DG: Modification of vascular tone using iNOS under the control of a radiation-inducible promoter. Gene Ther. (2000) 7:1126-1131.
80. GRECO O, MARPLES B, DACHS GU, WILLIAMS KJ, PATTERSON AV, SCOTT SD: Novel chimeric gene promoters responsive to hypoxia and ionizing radiation. Gene Ther. (2002) 9:1403-1411.
81. KUFE D, WEICHSELBAUM R: Radiation therapy, activation for gene transcription and the development of genetic radiotherapy-therapeutic strategies in oncology. Cancer Biol. Ther. (2003) 2:326-329.
82. CARPENITO C, DAVIS PD, DOUGHERTY ST, DOUGHERTY GJ: Exploiting the differential production of angiogenic factors within the tumor microenvironment in the design of a novel vascular-targeted gene therapy-based approach to the treatment of cancer. Int. J. Radiat. Oncol. Biol. Phys. (2002) 54:1473-1478. Description of a novel, functional targeting strategy that exploits the differential production of VEGF within the tumour microenvironment in order to selectively kill tumour-associated vascular endothelial cells.
83. ACKER T, PLATE KH: Hypoxia and hypoxia inducible factors (HIF) as important regulators of tumor physiology. Cancer Treat. Res. (2004) 117:219-248.
84. CROSS MJ, DIXELIUS J, MATSUMOTO T, CLAESSON-WELSH L: VEGF-receptor signal transduction. Trends Biochem. Sci. (2003) 28:488-494.
85. HAYES GM, CARPENITO C, DAVIS PD, DOUGHERTY ST, DIRKS JF, DOUGHERTY GJ: Alternative splicing as a novel of means of regulating the expression of therapeutic genes. Cancer Gene Ther. (2002) 9:133-141. Demonstration of the use of differential alternative splicing as a means of targeting gene expression to particular cell types.
86. GRIFFIOEN AW, COENEN MJ, DAMEN CA et al.: CD44 is involved in tumor angiogenesis; an activation antigen on human endothelial cells. Blood (1997) 90:1150-1159.
87. RAFII S: Circulating endothelial precursors: mystery, reality, and promise. J. Clin. Invest. (2000) 105:17-19.
88. REYES M, DUDEK A, JAHAGIRDAR B, KOODIE L, MARKER PH, VERFAILLIE CM: Origin of endothelial progenitors in human postnatal bone marrow. J. Clin. Invest. (2002) 109:337-346.
89. RAFII S, LYDEN D: Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. (2003) 9:702-712.
90. LIN Y, WEISDORF DJ, SOLOVEY A, HEBBEL RP: Origins of circulating endothelial cells and endothelial outgrowth from blood. J. Clin. Invest. (2000) 105:71-77.
91. LYDEN D, HATTORI K, DIAS S et al.: Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat. Med (2001) 7:1194-1201.
92. DAVIDOFF AM, NG CY, BROWN P et al.: Bone marrow-derived cells contribute to tumor neovasculature and, when modified to express an angiogenesis inhibitor, can restrict tumor growth in mice. Clin. Cancer Res. (2001) 7:2870-2879. Important study demonstrating that bone marrow-derived endothelial cell precursors can be used as vehicles to deliver therapeutic genes to tumour vasculature.
93. DE PALMA M, VENNERI MA, ROCA C, NALDINI L: Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat. Med. (2003) 9:789-795.