Transcriptional targeting of tumor endothelial cells for gene therapy

Advanced Drug Delivery Reviews

Volumn 61, Issue 7-8, 2009, Pages 542-553

  Dong, Zhihong ^a   Nör, Jacques E ^a,b,c  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b University of Michigan   (United States)

^c UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

Author keywords

Angiogenesis; Cancer; Promoter; Review; Tumor microenvironment

Indexed keywords

ANGIOGENESIS; CANCER; CANCER GENE THERAPY; CLINICAL TRIAL; GENE THERAPY; PATHOBIOLOGY; PROMOTER; THERAPEUTIC GENES; THERAPEUTIC STRATEGY; TUMOR MICROENVIRONMENT;

BLOOD VESSEL PROSTHESES; BLOOD VESSELS; CELL MEMBRANES; GENES; GENETIC ENGINEERING; ONCOLOGY; SELF ASSEMBLY; TUMORS;

ENDOTHELIAL CELLS;

ADENOVIRUS VECTOR; GANCICLOVIR; LENTIVIRUS VECTOR; PARVOVIRUS VECTOR; RETROVIRUS VECTOR;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; CANCER GENE THERAPY; CANCER INHIBITION; ENDOTHELIUM CELL; GENE EXPRESSION; GENE IDENTIFICATION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; LONG TERMINAL REPEAT; METASTASIS; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; TUMOR GROWTH;

ANIMALS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE THERAPY; GENES, TRANSGENIC, SUICIDE; HUMANS; NEOPLASMS; TRANSCRIPTION, GENETIC;

EID: 65749104010     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.addr.2009.02.006     Document Type: Review

References (167)

1. Folkman J. Toward an understanding of angiogenesis: search and discovery. Perspect. Biol. Med. 29 (1985) 10-36
2. Kerbel R.S. Inhibition of tumor angiogenesis as a strategy to circumvent acquired resistance to anti-cancer therapeutic agents. Bioessays 13 (1991) 31-36
3. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1 (1995) 27-31
4. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438 (2005) 932-936
5. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285 (1971) 1182-1186
6. Folkman J. Anti-angiogenesis: new concept for therapy of solid tumors. Ann. Surg. 175 (1972) 409-416
7. Folkman J. What is the evidence that tumors are angiogenesis dependent?. J. Natl. Cancer Inst. 82 (1990) 4-6
8. Grunstein J., Roberts W.G., Mathieu-Costello O., Hanahan D., and Johnson R.S. Tumor-derived expression of vascular endothelial growth factor is a critical factor in tumor expansion and vascular function. Cancer Res. 59 (1999) 1592-1598
9. Ferrara N., Gerber H.P., and LeCouter J. The biology of VEGF and its receptors. Nat. Med. 9 (2003) 669-676
10. Ingber D., Fujita T., Kishimoto S., Sudo K., Kanamaru T., Brem H., and Folkman J. Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature 348 (1990) 555-557
11. Kim K.J., Li B., Winer J., Armanini M., Gillett N., Phillips H.S., and Ferrara N. Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo. Nature 362 (1993) 841-844
12. O'Reilly M.S., Holmgren L., Shing Y., Chen C., Rosenthal R.A., Moses M., Lane W.S., Cao Y., Sage E.H., and Folkman J. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79 (1994) 315-328
13. Brekken R.A., Overholser J.P., Stastny V.A., Waltenberger J., Minna J.D., and Thorpe P.E. Selective inhibition of vascular endothelial growth factor (VEGF) receptor 2 (KDR/Flk-1) activity by a monoclonal anti-VEGF antibody blocks tumor growth in mice. Cancer Res. 60 (2000) 5117-5124
14. Ishida T., Kundu R.K., Yang E., Hirata K., Ho Y.D., and Quertermous T. Targeted disruption of endothelial cell-selective adhesion molecule inhibits angiogenic processes in vitro and in vivo. J. Biol. Chem. 278 (2003) 34598-34604
15. Folkman J. Is angiogenesis an organizing principle in biology and medicine?. J. Pediatr. Surg. 42 (2007) 1-11
16. Folkman J. What is the role of endothelial cells in angiogenesis?. Lab. Invest. 51 (1984) 601-604
17. Fukumura D., and Jain R.K. Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc. Res. 74 (2007) 72-84
18. St Croix B., Rago C., Velculescu V., Traverso G., Romans K.E., Montgomery E., Lal A., Riggins G.J., Lengauer C., Vogelstein B., and Kinzler K.W. Genes expressed in human tumor endothelium. Science 289 (2000) 1197-1202
19. Christian S., Ahorn H., Novatchkova M., Garin-Chesa P., Park J.E., Weber G., Eisenhaber F., Rettig W.J., and Lenter M.C. Molecular cloning and characterization of EndoGlyx-1, an EMILIN-like multisubunit glycoprotein of vascular endothelium. J. Biol. Chem. 276 (2001) 48588-48595
20. Buckanovich R.J., Sasaroli D., O'Brien-Jenkins A., Botbyl J., Hammond R., Katsaros D., Sandaltzopoulos R., Liotta L.A., Gimotty P.A., and Coukos G. Tumor vascular proteins as biomarkers in ovarian cancer. J. Clin. Oncol. 25 (2007) 852-861
21. Seaman S., Stevens J., Yang M.Y., Logsdon D., Graff-Cherry C., and St Croix B. Genes that distinguish physiological and pathological angiogenesis. Cancer Cell 11 (2007) 539-554
22. Ghilardi C., Chiorino G., Dossi R., Nagy Z., Giavazzi R., and Bani M. Identification of novel vascular markers through gene expression profiling of tumor-derived endothelium. BMC Genomics 9 (2008) 201-219
23. Ferrara N., Hillan K.J., Gerber H.P., and Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 3 (2004) 391-400
24. Wu Y., Li Z.Y., Zhao X., Kan B., and Wei Y.Q. Inhibition of ovarian tumor growth by gene therapy with recombinant soluble vascular endothelial growth factor receptor 2. Hum. Gene Ther. 17 (2006) 941-948
25. Kuhnert F., Tam B.Y., Sennino B., Gray J.T., Yuan J., Jocson A., Nayak N.R., Mulligan R.C., McDonald D.M., and Kuo C.J. Soluble receptor-mediated selective inhibition of VEGFR and PDGFRbeta signaling during physiologic and tumor angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 10185-10190
26. Bandyopadhyay A., Lopez-Casillas F., Malik S.N., Montiel J.L., Mendoza V., Yang J., and Sun L.Z. Antitumor activity of a recombinant soluble betaglycan in human breast cancer xenograft. Cancer Res. 62 (2002) 4690-4695
27. Silva R., D'Amico G., Hodivala-Dilke K.M., and Reynolds L.E. Integrins: the keys to unlocking angiogenesis. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1703-1713
28. Avraamides C.J., Garmy-Susini B., and Varner J.A. Integrins in angiogenesis and lymphangiogenesis. Nat. Rev., Cancer 8 (2008) 604-617
29. Delbaldo C., Raymond E., Vera K., Hammershaimb L., Kaucic K., Lozahic S., Marty M., and Faivre S. Phase I and pharmacokinetic study of etaracizumab (Abegrin), a humanized monoclonal antibody against alphavbeta3 integrin receptor, in patients with advanced solid tumors. Invest. New Drugs 26 (2008) 35-43
30. Beekman K.W., Colevas A.D., Cooney K., Dipaola R., Dunn R.L., Gross M., Keller E.T., Pienta K.J., Ryan C.J., Smith D., and Hussain M. Phase II evaluations of cilengitide in asymptomatic patients with androgen-independent prostate cancer: scientific rationale and study design. Clin. Genitourin. Cancer 4 (2006) 299-302
31. St George J.A. Gene therapy progress and prospects: adenoviral vectors. Gene Ther. 10 (2003) 1135-1141
32. Verma I.M., and Weitzman M.D. Gene therapy: twenty-first century medicine. Annu. Rev. Biochem. 74 (2005) 711-738
33. Barker S.D., Dmitriev I.P., Nettelbeck D.M., Liu B., Rivera A.A., Alvarez R.D., Curiel D.T., and Hemminki A. Combined transcriptional and transductional targeting improves the specificity and efficacy of adenoviral gene delivery to ovarian carcinoma. Gene Ther. 10 (2003) 1198-1204
34. Orphanides G., and Reinberg D. A unified theory of gene expression. Cell 108 (2002) 439-451
35. Nettelbeck D.M., Jerome V., and Muller R. Gene therapy: designer promoters for tumour targeting. Trends Genet. 16 (2000) 174-181
36. Papadakis E.D., Nicklin S.A., Baker A.H., and White S.J. Promoters and control elements: designing expression cassettes for gene therapy. Curr. Gene Ther. 4 (2004) 89-113
37. Morishita K., Johnson D.E., and Williams L.T. A novel promoter for vascular endothelial growth factor receptor (flt-1) that confers endothelial-specific gene expression. J. Biol. Chem. 270 (1995) 27948-27953
38. Patterson C., Perrella M.A., Hsieh C.M., Yoshizumi M., Lee M.E., and Haber E. Cloning and functional analysis of the promoter for KDR/flk-1, a receptor for vascular endothelial growth factor. J. Biol. Chem. 270 (1995) 23111-23118
39. Mancuso D.J., Tuley E.A., Westfield L.A., Worrall N.K., Shelton-Inloes B.B., Sorace J.M., Alevy Y.G., and Sadler J.E. Structure of the gene for human von Willebrand factor. J. Biol. Chem. 264 (1989) 19514-19527
40. Korhonen J., Lahtinen I., Halmekyto M., Alhonen L., Janne J., Dumont D., and Alitalo K. Endothelial-specific gene expression directed by the tie gene promoter in vivo. Blood 86 (1995) 1828-1835
41. Schlaeger T.M., Qin Y., Fujiwara Y., Magram J., and Sato T.N. Vascular endothelial cell lineage-specific promoter in transgenic mice. Development 121 (1995) 1089-1098
42. Breier G., Breviario F., Caveda L., Berthier R., Schnurch H., Gotsch U., Vestweber D., Risau W., and Dejana E. Molecular cloning and expression of murine vascular endothelial-cadherin in early stage development of cardiovascular system. Blood 87 (1996) 630-641
43. Cowan P.J., Tsang D., Pedic C.M., Abbott L.R., Shinkel T.A., d'Apice A.J., and Pearse M.J. The human ICAM-2 promoter is endothelial cell-specific in vitro and in vivo and contains critical Sp1 and GATA binding sites. J. Biol. Chem. 273 (1998) 11737-11744
44. Collins T., Williams A., Johnston G.I., Kim J., Eddy R., Shows T., Gimbrone Jr. M.A., and Bevilacqua M.P. Structure and chromosomal location of the gene for endothelial-leukocyte adhesion molecule 1. J. Biol. Chem. 266 (1991) 2466-2473
45. Marsden P.A., Heng H.H., Scherer S.W., Stewart R.J., Hall A.V., Shi X.M., Tsui L.C., and Schappert K.T. Structure and chromosomal localization of the human constitutive endothelial nitric oxide synthase gene. J. Biol. Chem. 268 (1993) 17478-17488
46. Bloch K.D., Friedrich S.P., Lee M.E., Eddy R.L., Shows T.B., and Quertermous T. Structural organization and chromosomal assignment of the gene encoding endothelin. J. Biol. Chem. 264 (1989) 10851-10857
47. Shibuya M., Yamaguchi S., Yamane A., Ikeda T., Tojo A., Matsushime H., and Sato M. Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5 (1990) 519-524
48. de Vries C., Escobedo J.A., Ueno H., Houck K., Ferrara N., and Williams L.T. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255 (1992) 989-991
49. Terman B.I., Dougher-Vermazen M., Carrion M.E., Dimitrov D., Armellino D.C., Gospodarowicz D., and Bohlen P. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem. Biophys. Res. Commun. 187 (1992) 1579-1586
50. Millauer B., Wizigmann-Voos S., Schnurch H., Martinez R., Moller N.P., Risau W., and Ullrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72 (1993) 835-846
51. Quinn T.P., Peters K.G., De Vries C., Ferrara N., and Williams L.T. Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 7533-7537
52. Ikeda T., Wakiya K., and Shibuya M. Characterization of the promoter region for flt-1 tyrosine kinase gene, a receptor for vascular endothelial growth factor. Growth Factors 13 (1996) 151-162
53. Nicklin S.A., Reynolds P.N., Brosnan M.J., White S.J., Curiel D.T., Dominiczak A.F., and Baker A.H. Analysis of cell-specific promoters for viral gene therapy targeted at the vascular endothelium. Hypertension 38 (2001) 65-70
54. Reynolds P.N., Nicklin S.A., Kaliberova L., Boatman B.G., Grizzle W.E., Balyasnikova I.V., Baker A.H., Danilov S.M., and Curiel D.T. Combined transductional and transcriptional targeting improves the specificity of transgene expression in vivo. Nat. Biotechnol. 19 (2001) 838-842
55. Minami T., Donovan D.J., Tsai J.C., Rosenberg R.D., and Aird W.C. Differential regulation of the von Willebrand factor and Flt-1 promoters in the endothelium of hypoxanthine phosphoribosyltransferase-targeted mice. Blood 100 (2002) 4019-4025
56. Bellamy W.T. Expression of vascular endothelial growth factor and its receptors in multiple myeloma and other hematopoietic malignancies. Semin. Oncol. 28 (2001) 551-559
57. Bellamy W.T., Richter L., Sirjani D., Roxas C., Glinsmann-Gibson B., Frutiger Y., Grogan T.M., and List A.F. Vascular endothelial cell growth factor is an autocrine promoter of abnormal localized immature myeloid precursors and leukemia progenitor formation in myelodysplastic syndromes. Blood 97 (2001) 1427-1434
58. von Marschall Z., Cramer T., Hocker M., Burde R., Plath T., Schirner M., Heidenreich R., Breier G., Riecken E.O., Wiedenmann B., and Rosewicz S. De novo expression of vascular endothelial growth factor in human pancreatic cancer: evidence for an autocrine mitogenic loop. Gastroenterology 119 (2000) 1358-1372
59. von Marschall Z., Cramer T., Hocker M., Finkenzeller G., Wiedenmann B., and Rosewicz S. Dual mechanism of vascular endothelial growth factor upregulation by hypoxia in human hepatocellular carcinoma. Gut 48 (2001) 87-96
60. Bauerschmitz G.J., Nettelbeck D.M., Kanerva A., Baker A.H., Hemminki A., Reynolds P.N., and Curiel D.T. The flt-1 promoter for transcriptional targeting of teratocarcinoma. Cancer Res. 62 (2002) 1271-1274
61. Wu Y., and Patterson C. The human KDR/flk-1 gene contains a functional initiator element that is bound and transactivated by TFII-I. J. Biol. Chem. 274 (1999) 3207-3214
62. Elvert G., Kappel A., Heidenreich R., Englmeier U., Lanz S., Acker T., Rauter M., Plate K., Sieweke M., Breier G., and Flamme I. Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha ) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1). J. Biol. Chem. 278 (2003) 7520-7530
63. Plate K.H., Breier G., Weich H.A., and Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359 (1992) 845-848
64. Brown L.F., Berse B., Jackman R.W., Tognazzi K., Manseau E.J., Dvorak H.F., and Senger D.R. Increased expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in kidney and bladder carcinomas. Am. J. Pathol. 143 (1993) 1255-1262
65. Brown L.F., Berse B., Jackman R.W., Tognazzi K., Manseau E.J., Senger D.R., and Dvorak H.F. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in adenocarcinomas of the gastrointestinal tract. Cancer Res. 53 (1993) 4727-4735
66. Takahashi Y., Kitadai Y., Bucana C.D., Cleary K.R., and Ellis L.M. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res. 55 (1995) 3964-3968
67. Millauer B., Shawver L.K., Plate K.H., Risau W., and Ullrich A. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 367 (1994) 576-579
68. Millauer B., Longhi M.P., Plate K.H., Shawver L.K., Risau W., Ullrich A., and Strawn L.M. Dominant-negative inhibition of Flk-1 suppresses the growth of many tumor types in vivo. Cancer Res. 56 (1996) 1615-1620
69. Dias S., Hattori K., Heissig B., Zhu Z., Wu Y., Witte L., Hicklin D.J., Tateno M., Bohlen P., Moore M.A., and Rafii S. Inhibition of both paracrine and autocrine VEGF/VEGFR-2 signaling pathways is essential to induce long-term remission of xenotransplanted human leukemias. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 10857-10862
70. Ryden L., Linderholm B., Nielsen N.H., Emdin S., Jonsson P.E., and Landberg G. Tumor specific VEGF-A and VEGFR2/KDR protein are co-expressed in breast cancer. Breast Cancer Res. Treat. 82 (2003) 147-154
71. Straume O., and Akslen L.A. Increased expression of VEGF-receptors (FLT-1, KDR, NRP-1) and thrombospondin-1 is associated with glomeruloid microvascular proliferation, an aggressive angiogenic phenotype, in malignant melanoma. Angiogenesis 6 (2003) 295-301
72. Kyzas P.A., Stefanou D., Batistatou A., and Agnantis N.J. Potential autocrine function of vascular endothelial growth factor in head and neck cancer via vascular endothelial growth factor receptor-2. Mod. Pathol. 18 (2005) 485-494
73. Heidenreich R., Kappel A., and Breier G. Tumor endothelium-specific transgene expression directed by vascular endothelial growth factor receptor-2 (Flk-1) promoter/enhancer sequences. Cancer Res. 60 (2000) 6142-6147
74. Song W., Sun Q., Dong Z., Spencer D.M., Nunez G., and Nor J.E. Antiangiogenic gene therapy: disruption of neovascular networks mediated by inducible caspase-9 delivered with a transcriptionally targeted adenoviral vector. Gene Ther. 12 (2005) 320-329
75. Partanen J., Armstrong E., Makela T.P., Korhonen J., Sandberg M., Renkonen R., Knuutila S., Huebner K., and Alitalo K. A novel endothelial cell surface receptor tyrosine kinase with extracellular epidermal growth factor homology domains. Mol. Cell. Biol. 12 (1992) 1698-1707
76. Runting A.S., Stacker S.A., and Wilks A.F. Tie2, a putative protein tyrosine kinase from a new class of cell surface receptor. Growth Factors 9 (1993) 99-105
77. Dumont D.J., Yamaguchi T.P., Conlon R.A., Rossant J., and Breitman M.L. Tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene 7 (1992) 1471-1480
78. Korhonen J., Partanen J., Armstrong E., Vaahtokari A., Elenius K., Jalkanen M., and Alitalo K. Enhanced expression of the tie receptor tyrosine kinase in endothelial cells during neovascularization. Blood 80 (1992) 2548-2555
79. Iwama A., Hamaguchi I., Hashiyama M., Murayama Y., Yasunaga K., and Suda T. Molecular cloning and characterization of mouse TIE and TEK receptor tyrosine kinase genes and their expression in hematopoietic stem cells. Biochem. Biophys. Res. Commun. 195 (1993) 301-309
80. Ziegler S.F., Bird T.A., Schneringer J.A., Schooley K.A., and Baum P.R. Molecular cloning and characterization of a novel receptor protein tyrosine kinase from human placenta. Oncogene 8 (1993) 663-670
81. Korhonen J., Polvi A., Partanen J., and Alitalo K. The mouse tie receptor tyrosine kinase gene: expression during embryonic angiogenesis. Oncogene 9 (1994) 395-403
82. Dumont D.J., Fong G.H., Puri M.C., Gradwohl G., Alitalo K., and Breitman M.L. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev. Dyn. 203 (1995) 80-92
83. Hatva E., Kaipainen A., Mentula P., Jaaskelainen J., Paetau A., Haltia M., and Alitalo K. Expression of endothelial cell-specific receptor tyrosine kinases and growth factors in human brain tumors. Am. J. Pathol. 146 (1995) 368-378
84. Kaipainen A., Vlaykova T., Hatva E., Bohling T., Jekunen A., Pyrhonen S., and Alitalo K. Enhanced expression of the tie receptor tyrosine kinase mesenger RNA in the vascular endothelium of metastatic melanomas. Cancer Res. 54 (1994) 6571-6577
85. Sato T.N., Tozawa Y., Deutsch U., Wolburg-Buchholz K., Fujiwara Y., Gendron-Maguire M., Gridley T., Wolburg H., Risau W., and Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376 (1995) 70-74
86. Puri M.C., Rossant J., Alitalo K., Bernstein A., and Partanen J. The receptor tyrosine kinase TIE is required for integrity and survival of vascular endothelial cells. EMBO J. 14 (1995) 5884-5891
87. Martin V., Liu D., Fueyo J., and Gomez-Manzano C. Tie2: a journey from normal angiogenesis to cancer and beyond. Histol. Histopathol. 23 (2008) 773-780
88. Iljin K., Dube A., Kontusaari S., Korhonen J., Lahtinen I., Oettgen P., and Alitalo K. Role of ets factors in the activity and endothelial cell specificity of the mouse Tie gene promoter. FASEB J. 13 (1999) 377-386
89. Schlaeger T.M., Bartunkova S., Lawitts J.A., Teichmann G., Risau W., Deutsch U., and Sato T.N. Uniform vascular-endothelial-cell-specific gene expression in both embryonic and adult transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 3058-3063
90. De Palma M., Venneri M.A., Roca C., and Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat. Med. 9 (2003) 789-795
91. Suzuki S., Sano K., and Tanihara H. Diversity of the cadherin family: evidence for eight new cadherins in nervous tissue. Cell Regul. 2 (1991) 261-270
92. Gory S., Vernet M., Laurent M., Dejana E., Dalmon J., and Huber P. The vascular endothelial-cadherin promoter directs endothelial-specific expression in transgenic mice. Blood 93 (1999) 184-192
93. Dancer A., Julien S., Bouillot S., Pointu H., Vernet M., and 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. 10 (2003) 1170-1178
94. Staunton D.E., Dustin M.L., and Springer T.A. Functional cloning of ICAM-2, a cell adhesion ligand for LFA-1 homologous to ICAM-1. Nature 339 (1989) 61-64
95. Cowan P.J., Shinkel T.A., Witort E.J., Barlow H., Pearse M.J., and d'Apice A.J. Targeting gene expression to endothelial cells in transgenic mice using the human intercellular adhesion molecule 2 promoter. Transplantation 62 (1996) 155-160
96. Richardson T.B., Kaspers J., and Porter C.D. Retroviral hybrid LTR vector strategy: functional analysis of LTR elements and generation of endothelial cell specificity. Gene Ther. 11 (2004) 775-783
97. De Palma M., Venneri M.A., and Naldini L. In vivo targeting of tumor endothelial cells by systemic delivery of lentiviral vectors. Hum. Gene Ther. 14 (2003) 1193-1206
98. Bevilacqua M.P. Endothelial-leukocyte adhesion molecules. Annu. Rev. Immunol. 11 (1993) 767-804
99. Kraling B.M., Razon M.J., Boon L.M., Zurakowski D., Seachord C., Darveau R.P., Mulliken J.B., Corless C.L., and Bischoff J. E-selectin is present in proliferating endothelial cells in human hemangiomas. Am. J. Pathol. 148 (1996) 1181-1191
100. Bandyopadhyay S., Ashraf M.Z., Daher P., Howe P.H., and DiCorleto P.E. HOXA9 participates in the transcriptional activation of E-selectin in endothelial cells. Mol. Cell. Biol. 27 (2007) 4207-4216
101. Jaggar R.T., Chan H.Y., Harris A.L., and Bicknell R. Endothelial cell-specific expression of tumor necrosis factor-alpha from the KDR or E-selectin promoters following retroviral delivery. Hum. Gene Ther. 8 (1997) 2239-2247
102. Walton T., Wang J.L., Ribas A., Barsky S.H., Economou J., and Nguyen M. Endothelium-specific expression of an E-selectin promoter recombinant adenoviral vector. Anticancer Res. 18 (1998) 1357-1360
103. Huang P.L., Huang Z., Mashimo H., Bloch K.D., Moskowitz M.A., Bevan J.A., and Fishman M.C. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377 (1995) 239-242
104. Rudic R.D., Shesely E.G., Maeda N., Smithies O., Segal S.S., and Sessa W.C. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J. Clin. Invest. 101 (1998) 731-736
105. Freedman J.E., Sauter R., Battinelli E.M., Ault K., Knowles C., Huang P.L., and Loscalzo J. Deficient platelet-derived nitric oxide and enhanced hemostasis in mice lacking the NOSIII gene. Circ. Res. 84 (1999) 1416-1421
106. Lee P.C., Salyapongse A.N., Bragdon G.A., Shears 2nd L.L., Watkins S.C., Edington H.D., and Billiar T.R. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol. 277 (1999) H1600-8
107. Aicher A., Heeschen C., Mildner-Rihm C., Urbich C., Ihling C., Technau-Ihling K., Zeiher A.M., and Dimmeler S. Essential role of endothelial nitric oxide synthase for mobilization of stem and progenitor cells. Nat. Med. 9 (2003) 1370-1376
108. Fish J.E., and Marsden P.A. Endothelial nitric oxide synthase: insight into cell-specific gene regulation in the vascular endothelium. Cell. Mol. Life Sci. 63 (2006) 144-162
109. Chen A.F., Jiang S.W., Crotty T.B., Tsutsui M., Smith L.A., O'Brien T., and Katusic Z.S. Effects of in vivo adventitial expression of recombinant endothelial nitric oxide synthase gene in cerebral arteries. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 12568-12573
110. Deng W., Bivalacqua T.J., Chattergoon N.N., Hyman A.L., Jeter Jr. J.R., and Kadowitz P.J. Adenoviral gene transfer of eNOS: high-level expression in ex vivo expanded marrow stromal cells. Am. J. Physiol. Cell Physiol. 285 (2003) C1322-C1329
111. Smith Jr. R.S., Agata J., Xia C.F., Chao L., and Chao J. Human endothelial nitric oxide synthase gene delivery protects against cardiac remodeling and reduces oxidative stress after myocardial infarction. Life Sci. 76 (2005) 2457-2471
112. Guillot P.V., Guan J., Liu L., Kuivenhoven J.A., Rosenberg R.D., Sessa W.C., and Aird W.C. A vascular bed-specific pathway. J. Clin. Invest. 103 (1999) 799-805
113. Sadler J.E. von Willebrand factor. J. Biol. Chem. 266 (1991) 22777-22780
114. Aird W.C., Jahroudi N., Weiler-Guettler H., Rayburn H.B., and Rosenberg R.D. Human von Willebrand factor gene sequences target expression to a subpopulation of endothelial cells in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 4567-4571
115. Aird W.C., Edelberg J.M., Weiler-Guettler H., Simmons W.W., Smith T.W., and Rosenberg R.D. Vascular bed-specific expression of an endothelial cell gene is programmed by the tissue microenvironment. J. Cell Biol. 138 (1997) 1117-1124
116. Ozaki K., Yoshida T., Ide H., Saito I., Ikeda Y., Sugimura T., and Terada M. Use of von Willebrand factor promoter to transduce suicidal gene to human endothelial cells, HUVEC. Hum. Gene Ther. 7 (1996) 1483-1490
117. Yang D.I., Chen S., Ezekiel U.R., Xu J., Wu Y., and Hsu C.Y. Antisense RNA to inducible nitric oxide synthase reduces cytokine-mediated brain endothelial cell death. Ann. N. Y. Acad. Sci. 1042 (2005) 439-447
118. Yanagisawa M., Kurihara H., Kimura S., Tomobe Y., Kobayashi M., Mitsui Y., Yazaki Y., Goto K., and Masaki T. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature 332 (1988) 411-415
119. Miyauchi T., and Masaki T. Pathophysiology of endothelin in the cardiovascular system. Annu. Rev. Physiol. 61 (1999) 391-415
120. Lee M.E., Bloch K.D., Clifford J.A., and Quertermous T. Functional analysis of the endothelin-1 gene promoter. Evidence for an endothelial cell-specific cis-acting sequence. J. Biol. Chem. 265 (1990) 10446-10450
121. Harats D., Kurihara H., Belloni P., Oakley H., Ziober A., Ackley D., Cain G., Kurihara Y., Lawn R., and Sigal E. Targeting gene expression to the vascular wall in transgenic mice using the murine preproendothelin-1 promoter. J. Clin. Invest. 95 (1995) 1335-1344
122. Varda-Bloom N., Shaish A., Gonen A., Levanon K., Greenbereger S., Ferber S., Levkovitz H., Castel D., Goldberg I., Afek A., Kopolovitc Y., and Harats D. Tissue-specific gene therapy directed to tumor angiogenesis. Gene Ther. 8 (2001) 819-827
123. Harats D., Ben-Shushan D., Cohen H., Gonen A., Barshack I., Goldberg I., Greenberger S., Hodish I., Harari A., Varda-Bloom N., Levanon K., Grossman E., Chaitidis P., Kuhn H., and Shaish A. Inhibition of carcinogenesis in transgenic mouse models over-expressing 15-lipoxygenase in the vascular wall under the control of murine preproendothelin-1 promoter. Cancer Lett. 229 (2005) 127-134
124. Mavria G., Harrington K.J., Marshall C.J., and Porter C.D. In vivo efficacy of HSV-TK transcriptionally targeted to the tumour vasculature is augmented by combination with cytotoxic chemotherapy. J. Gene Med. 7 (2005) 263-275
125. Hermens W.T., and Verhaagen J. Viral vectors, tools for gene transfer in the nervous system. Prog. Neurobiol. 55 (1998) 399-432
126. Brandwijk R.J., Griffioen A.W., and Thijssen V.L. Targeted gene-delivery strategies for angiostatic cancer treatment. Trends Mol. Med. 13 (2007) 200-209
127. Vile R.G., Tuszynski A., and Castleden S. Retroviral vectors. From laboratory tools to molecular medicine. Mol. Biotechnol. 5 (1996) 139-158
128. Mavria G., and Porter C.D. Reduced growth in response to ganciclovir treatment of subcutaneous xenografts expressing HSV-tk in the vascular compartment. Gene Ther. 8 (2001) 913-920
129. Jager U., Zhao Y., and Porter C.D. Endothelial cell-specific transcriptional targeting from a hybrid long terminal repeat retrovirus vector containing human prepro-endothelin-1 promoter sequences. J. Virol. 73 (1999) 9702-9709
130. Mavria G., Jager U., and Porter C.D. Generation of a high titre retroviral vector for endothelial cell-specific gene expression in vivo. Gene Ther. 7 (2000) 368-376
131. Trono D. Lentiviral vectors: turning a deadly foe into a therapeutic agent. Gene Ther. 7 (2000) 20-23
132. Lotti F., Menguzzato E., Rossi C., Naldini L., Ailles L., Mavilio F., and Ferrari G. Transcriptional targeting of lentiviral vectors by long terminal repeat enhancer replacement. J. Virol. 76 (2002) 3996-4007
133. Shichinohe T., Bochner B.H., Mizutani K., Nishida M., Hegerich-Gilliam S., Naldini L., and Kasahara N. Development of lentiviral vectors for antiangiogenic gene delivery. Cancer Gene Ther. 8 (2001) 879-889
134. Pariente N., Mao S.H., Morizono K., and Chen I.S. Efficient targeted transduction of primary human endothelial cells with dual-targeted lentiviral vectors. J. Gene Med. 10 (2008) 242-248
135. Ali M., Lemoine N.R., and Ring C.J. The use of DNA viruses as vectors for gene therapy. Gene Ther. 1 (1994) 367-384
136. Savontaus M.J., Sauter B.V., Huang T.G., and Woo S.L. Transcriptional targeting of conditionally replicating adenovirus to dividing endothelial cells. Gene Ther. 9 (2002) 972-979
137. Stackhouse M.A., Buchsbaum D.J., Kancharla S.R., Grizzle W.E., Grimes C., Laffoon K., Pederson L.C., and Curiel D.T. Specific membrane receptor gene expression targeted with radiolabeled peptide employing the erbB-2 and DF3 promoter elements in adenoviral vectors. Cancer Gene Ther. 6 (1999) 209-219
138. Mahasreshti P.J., Navarro J.G., Kataram M., Wang M.H., Carey D., Siegal G.P., Barnes M.N., Nettelbeck D.M., Alvarez R.D., Hemminki A., and Curiel D.T. Adenovirus-mediated soluble FLT-1 gene therapy for ovarian carcinoma. Clin. Cancer Res. 7 (2001) 2057-2066
139. Everts M., Kim-Park S.A., Preuss M.A., Passineau M.J., Glasgow J.N., Pereboev A.V., Mahasreshti P.J., Grizzle W.E., Reynolds P.N., and Curiel D.T. Selective induction of tumor-associated antigens in murine pulmonary vasculature using double-targeted adenoviral vectors. Gene Ther. 12 (2005) 1042-1048
140. Izumi M., Kawakami Y., Glasgow J.N., Belousova N., Everts M., Kim-Park S., Yamamoto S., Wang M., Le L.P., Reynolds P.N., and Curiel D.T. In vivo analysis of a genetically modified adenoviral vector targeted to human CD40 using a novel transient transgenic model. J. Gene Med. 7 (2005) 1517-1525
141. Work L.M., Ritchie N., Nicklin S.A., Reynolds P.N., and Baker A.H. Dual targeting of gene delivery by genetic modification of adenovirus serotype 5 fibers and cell-selective transcriptional control. Gene Ther. 11 (2004) 1296-1300
142. Kaliberov S.A., Kaliberova L.N., and Buchsbaum D.J. Combined ionizing radiation and sKDR gene delivery for treatment of prostate carcinomas. Gene Ther. 12 (2005) 407-417
143. Tenenbaum L., Lehtonen E., and Monahan P.E. Evaluation of risks related to the use of adeno-associated virus-based vectors. Curr. Gene Ther. 3 (2003) 545-565
144. Zacchigna S., Zentilin L., Morini M., Dell'Eva R., Noonan D.M., Albini A., and Giacca M. AAV-mediated gene transfer of tissue inhibitor of metalloproteinases-1 inhibits vascular tumor growth and angiogenesis in vivo. Cancer Gene Ther. 11 (2004) 73-80
145. White S.J., Nicklin S.A., Buning H., Brosnan M.J., Leike K., Papadakis E.D., Hallek M., and Baker A.H. Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109 (2004) 513-519
146. Davidoff A.M., Nathwani A.C., Spurbeck W.W., Ng C.Y., Zhou J., and Vanin E.F. rAAV-mediated long-term liver-generated expression of an angiogenesis inhibitor can restrict renal tumor growth in mice. Cancer Res. 62 (2002) 3077-3083
147. Streck C.J., Zhou J., Ng C.Y., Zhang Y., Nathwani A.C., and Davidoff A.M. Longterm recombinant adeno-associated, virus-mediated, liver-generated expression of an angiogenesis inhibitor improves survival in mice with disseminated neuroblastoma. J. Am. Coll. Surg. 199 (2004) 78-86
148. Denby L., Nicklin S.A., and Baker A.H. Adeno-associated virus (AAV)-7 and -8 poorly transduce vascular endothelial cells and are sensitive to proteasomal degradation. Gene Ther. 12 (2005) 1534-1538
149. Niidome T., and Huang L. Gene therapy progress and prospects: nonviral vectors. Gene Ther. 9 (2002) 1647-1652
150. Ragusa A., Garcia I., and Penades S. Nanoparticles as nonviral gene delivery vectors. IEEE Trans. Nanobioscience 6 (2007) 319-330
151. MacCorkle R.A., Freeman K.W., and Spencer D.M. Synthetic activation of caspases: artificial death switches. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 3655-3660
152. Nor J.E., Hu Y., Song W., Spencer D.M., and Nunez G. Ablation of microvessels in vivo upon dimerization of iCaspase-9. Gene Ther. 9 (2002) 444-451
153. Song W., Dong Z., Jin T., Mantellini M.G., Nunez G., and Nor J.E. Cancer gene therapy with iCaspase-9 transcriptionally targeted to tumor endothelial cells. Cancer Gene Ther. 15 (2008) 667-675
154. Nawa A., Ishida D., and ChenHong L. New paradigm of herpes simplex virus type 1 thymidine kinase (HSV-TK)/ganciclovir (GCV). Nippon Rinsho. 64 Suppl 3 (2006) 345-349
155. Pramudji C., Shimura S., Ebara S., Yang G., Wang J., Ren C., Yuan Y., Tahir S.A., Timme T.L., and Thompson T.C. In situ prostate cancer gene therapy using a novel adenoviral vector regulated by the caveolin-1 promoter. Clin. Cancer Res. 7 (2001) 4272-4279
156. Li B.J., Zhang C., Yi Y.X., Hao Y., Liu X.P., and Ou Q.J. Vascular damage and anti-angiogenic effects of tumor vessel-targeted adenovirus-mediated herpes simplex virus thymidine kinase gene. World J. Gastroenterol. 13 (2007) 4006-4010
157. Smythe W.R. Prodrug/drug sensitivity gene therapy: current status. Curr. Oncol. Rep. 2 (2000) 17-22
158. LeBlanc H.N., and Ashkenazi A. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ. 10 (2003) 66-75
159. Huang Y., and Sheikh M.S. TRAIL death receptors and cancer therapeutics. Toxicol. Appl. Pharmacol. 224 (2007) 284-289
160. Kaliberov S.A., Kaliberova L.N., Stockard C.R., Grizzle W.E., and Buchsbaum D.J. Adenovirus-mediated FLT1-targeted proapoptotic gene therapy of human prostate cancer. Mol. Ther. 10 (2004) 1059-1070
161. Cavazzana-Calvo M., Hacein-Bey S., de Saint Basile G., Gross F., Yvon E., Nusbaum P., Selz F., Hue C., Certain S., Casanova J.L., Bousso P., Deist F.L., and Fischer A. Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. Science 288 (2000) 669-672
162. Hacein-Bey-Abina S., von Kalle C., Schmidt M., Le Deist F., Wulffraat N., McIntyre E., Radford I., Villeval J.L., Fraser C.C., Cavazzana-Calvo M., and Fischer A. A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. N. Engl. J. Med. 348 (2003) 255-256
163. Zurita A.J., Arap W., and Pasqualini R. Mapping tumor vascular diversity by screening phage display libraries. J. Control. Release 91 (2003) 183-186
164. Luz-Madrigal A., Clapp C., Aranda J., and Vaca L. In vivo transcriptional targeting into the retinal vasculature using recombinant baculovirus carrying the human flt-1 promoter. Virol. J. 4 (2007) 88-100
165. Evans V., Hatzopoulos A., Aird W.C., Rayburn H.B., Rosenberg R.D., and Kuivenhoven J.A. Targeting the Hprt locus in mice reveals differential regulation of Tie2 gene expression in the endothelium. Physiol. Genomics 2 (2000) 67-75
166. Kisseleva T., Song L., Vorontchikhina M., Feirt N., Kitajewski J., and Schindler C. NF-kappaB regulation of endothelial cell function during LPS-induced toxemia and cancer. J. Clin. Invest. 116 (2006) 2955-2963
167. Maxwell I.H., Kaletta C., Naujoks K., and Maxwell F. Targeting diphtheria toxin A-chain transcription to activated endothelial cells using an E-selectin promoter. Angiogenesis 6 (2003) 31-38