A targetable, injectable adenoviral vector for selective gene delivery to pulmonary endothelium in vivo

Molecular Therapy

Volumn 2, Issue 6, 2000, Pages 562-578

  Reynolds, Paul N ^a   Zinn, Kurt R ^e   Gavrilyuk, Vitaliy D ^d   Balyasnikova, Irina V ^d   Rogers, Buck E ^b   Buchsbaum, Donald J ^b   Wang, Ming H ^a   Miletich, David J ^d   Grizzle, William E ^c   Douglas, Joanne T ^a   Danilov, Sergei M ^d   Curiel, David T ^a  

^a University of Alabama at Birmingham   (United States)

^b The University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Adenovirus; Angiotensin converting enzyme; Gene therapy; Lung; Noninvasive imaging; Targeting; Tropism; Vascular

Indexed keywords

ADENOVIRIDAE;

DIPEPTIDYL CARBOXYPEPTIDASE; PRIMER DNA;

ADENOVIRUS; ANIMAL; ARTICLE; CELL STRAIN 3T3; CHO CELL; ELECTRON MICROSCOPY; ENDOTHELIUM; ENZYMOLOGY; GENE VECTOR; GENETICS; HAMSTER; IMMUNOHISTOCHEMISTRY; LUNG; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; RAT; ULTRASTRUCTURE;

3T3 CELLS; ADENOVIRIDAE; ANIMALS; BASE SEQUENCE; CHO CELLS; CRICETINAE; DNA PRIMERS; ENDOTHELIUM; GENETIC VECTORS; IMMUNOHISTOCHEMISTRY; LUNG; MICE; MICROSCOPY, ELECTRON; PEPTIDYL-DIPEPTIDASE A; RATS;

EID: 0034577049     PISSN: 15250016     EISSN: None     Source Type: Journal    
DOI: 10.1006/mthe.2000.0205     Document Type: Article

References (69)

1. Brody, S. L., and Crystal, R. G. (1994). Adenovirus-mediated in vivo gene transfer. Ann. N.Y. Acad. Sci. 716: 90-101.
2. Caldwell, P. R., Seegal, B. C., Hsu, K. C., Das, M., and Soffer, R. L. (1976). Angiotensin-converting enzyme: Vascular endothelial localization. Science 191: 1050-1051.
3. Schuster, D. P., Crouch, E. C., Parks, W. C., Johnson, T., and Botney, M. D. (1996). Angiotensin converting enzyme expression in primary pulmonary hypertension. Am. J. Respir. Crit. Care Med. 154: 1087-1091.
4. Franke, F. E., Metzger, R., Bohle, R. M., Kerkman, L., Alhence-Gelas, F., and Danilov, S. M. (1997). CD143 Workshop: Angiotensin-I-converting enzyme (CD143) on endothelial cells in normal and in pathological conditions. In Leukocyte Typing VI (T. Kishimoto et al., Eds.), pp. 749-751. Garland Publishing, New York.
5. Morrell, N. W., Atochina, E. N., Morris, K. G., Danilov, S. M., and Stenmark, K. R. (1995). Angiotensin converting enzyme expression is increased in small pulmonary arteries of rats with hypoxia-induced pulmonary hypertension [published erratum appears in J. Clin. Invest. 97(1): 271]. J. Clin. Invest. 96: 1823-1833.
6. Fishel, R. S., et al. (1995). Fibroblast growth factor stimulates angiotensin converting enzyme expression in vascular smooth muscle cells. Possible mediator of the response to vascular injury. J. Clin. Invest. 95: 377-387.
7. Moraes, D., and Loscalzo, J. (1997). Pulmonary hypertension: Newer concepts in diagnosis and management. Clin. Cardiol. 20: 676-682.
8. Deng, Z., et al. (2000). Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am. J. Hum. Genet. 67: 737-744.
9. Bergelson, J. M., et al. (1997). Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5. Science 275: 1320-1323.
10. Tomko, R. P., Xu, R., and Philipson, L. (1997). HCAR and MCAR: The human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses. Proc. Natl. Acad. Sci. USA 94: 3352-3356.
11. Hong, S. S., Karayan, L., Tournier, J., Curiel, D. T., and Boulanger, P. A. (1997). Adenovirus type 5 fiber knob binds to MHC Class I alpha-2 domain at the surface of human epithelial and B lymphoblastoid cells. EMBO J. 16: 2294-2306.
12. Davison, E., Kirby, I., Elliott, T., and Santis, G. (1999). The human HLA-A*0201 allele, expressed in hamster cells, is not a high-affinity receptor for adenovirus type 5 fiber. J. Virol. 73: 4513-4517.
13. Wickham, T. J., Mathias, P., Cheresh, D. A., and Nemerow, G. R. (1993). Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 73: 309-319.
14. Bai, M., Harfe, B., and Freimuth, P. (1993). Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J. Virol. 67: 5198-5205.
15. Miller, C. R., et al. (1998). 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. 58: 5738-5748.
16. Dmitriev, I., et al. (1998). An adenovirus vector with genetically modified fibers demonstrates expanded tropism via utilization of a coxsackievirus and adenovirus receptor-independent cell entry mechanism. J. Virol. 72: 9706-9713.
17. Blackwell, J. L., et al. (1999). Retargeting to EGFR enhances adenovirus infection efficiency of squamous cell carcinoma. Arch. Otolaryngol. Head Neck Surg. 125: 856-863.
18. Kasono, K., et al. (1999). Selective gene delivery to head and neck cancer cells via an integrin targeted adenoviral vector. Clin. Cancer Res. 5: 2571-2579.
19. Zabner, J., Freimuth, P., Puga, A., Fabrega, A., and Welsh, M. J. (1997). Lack of high affinity fiber receptor activity explains the resistance of ciliated airway epithelia to adenovirus infection. J. Clin. Invest. 100: 1144-1149.
20. Walters, R. W., Grunst, T., Bergelson, J. M., Finberg, R. W., Welsh, M. J., and Zabner, J. (1999). Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia. J. Biol. Chem. 274: 10219-10226.
21. Kaner, R. J., et al. (1999). Modification of the genetic program of human alveolar macrophages by adenovirus vectors in vitro is feasible but inefficient, limited in part by the low level of expression of the coxsackie/adenovirus receptor. Am. J. Respir. Cell Mol. Biol. 20: 361-370.
22. Yee, D., et al. (1996). Adenovirus-mediated gene transfer of herpes simplex virus thymidine kinase in an ascites model of human breast cancer. Hum. Gene Ther. 7: 1251-1257.
23. van der Eb, M. M., et al. (1998). Severe hepatic dysfunction after adenovirus-mediated transfer of the herpes simplex virus thymidine kinase gene and ganciclovir administration. Gene Ther. 5: 451-458.
24. Herz, J., and Gerard, R. D. (1993). Adenovirus-mediated transfer of low density lipoprotein receptor gene acutely accelerates cholesterol clearance in normal mice. Proc. Natl. Acad. Sci. USA 90: 2812-2816.
25. Graham, F., and Prevec, L. (1991). Manipulation of adenovirus vectors. In Methods in Molecular Biology. Vol. 7 - Gene Transfer and Expression Techniques (E. J. Murray and J. M. Walker, Eds.), pp. 109-129. Humana Press, Clifton, NJ.
26. Rosenfeld, M. E., et al. (1996). Adenoviral-mediated delivery of herpes simplex virus thymidine kinase results in tumor reduction and prolonged survival in a SCID mouse model of human ovarian carcinoma. J. Mol. Med. 74: 455-462.
27. Rogers, B. E., et al. (1999). In vivo localization of [(111)In]-DTPA-D-Phe1-octreotide to human ovarian tumor xenografts induced to express the somatostatin receptor subtype 2 using an adenoviral vector. Clin. Cancer Res. 5: 383-393.
28. Raben, D., et al. (1996). Enhancement of radiolabeled antibody binding and tumor localization through adenoviral transduction of the human carcinoembryonic antigen qene. Gene Ther. 3: 567-580.
29. Pederson, L. C., et al. (1997). Molecular chemotherapy combined with radiation therapy enhances killing of cholangiocarcinoma cells in vitro and in vivo. Cancer Res. 57: 4325-4332.
30. Balyasnikova, I. V., Gavrilyuk, V. D., McDonald, T., Berkowitz, R., Miletich, D. J., and Danilov, S. M. (1999). Antibody mediated lung endothelium targeting: 1. In vitro model using a cell line expressing angiotensin converting enzyme. Tumor Targeting 4: 70-83.
31. Douglas, J. T., Rogers, B. E., Rosenfeld, M. E., Michael, S. I., Feng, M., and Curiel, D. T. (1996). Targeted gene delivery by tropism-modified adenoviral vectors. Nat. Biotech. 14: 1574-1578.
32. Wickham, T. J., et al. (1996). Targeted adenovirus gene transfer to endothelial and smooth muscle cells by using bispecific antibodies. J. Virol. 70: 6831-6838.
33. Krasnykh, V. N., Mikheeva, G. V., Douglas, J. T., and Curiel, D. T. (1996). Generation of recombinant adenovirus vectors with modified fibers for altering viral tropism. J. Virol. 70: 6839-6846.
34. Hiemisch, H., et al. (1993). Purification of radiolabeled monoclonal antibodies to angiotensin-converting enzyme significantly improves specificity and efficacy of its targeting into the lung. Nucl. Med. Biol. 20: 435-441.
35. Muzykantov, V. R., et al. (1996). Endothelial cells internalize monoclonal antibody to angiotensin-converting enzyme. Am. J. Physiol. 270: L704-L713.
36. Grizzle, W. E., Myers, R. B., Manne, U., Stockard, C. R., Harkins, L. E., and Srivastava, S. (1998). Factors affecting immunohistochemical evaluation of biomarker expression in neoplasia. In John Walkerís Methods in Molecular Medicine - Tumor Marker Protocols (M. Hanausek and Z. Walaszek, Eds.), pp. 161-179. Humana Press, Totowa, NJ.
37. Grizzle, W. E., Myers, R. B., Manne, U., and Srivastava, S. (1998). Immunohistochemical evaluation of biomarkers in prostatic and colorectal neoplasia. In John Walkerís Methods in Molecular Medicine - Tumor Marker Protocols (M. Hanausek and Z. Walaszek Eds.), pp. 143-160. Humana Press, Totowa, NJ.
38. Kuroki, M., Greiner, J. W., Simpson, J. F., Primus, F. J., Guadagni, F., and Schlom, J. (1989). Serologic mapping and biochemical characterization of the carcinoembryonic antigen epitopes using fourteen distinct monoclonal antibodies. Int. J. Cancer 44: 208-218.
39. Miller, S. A., Dykes, D. D., and Polesky, H. F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 16: 1215.
40. Muzykantov, V. R., Atochina, E. N., Ischiropoulos, H., Danilov, S. M., and Fisher, A. B. (1996). Immunotargeting of antioxidant enzyme to the pulmonary endothelium. Proc. Natl. Acad. Sci. USA 93: 5213-5218.
41. Atochina, E. N., Balyasnikova, I. V., Danilov, S. M., Granger, D. N., Fisher, A. B., and Muzykantov, V. R. (1998). Immunotargeting of catalase to ACE or ICAM-1 protects perfused rat lungs against oxidative stress. Am. J. Physiol. 275: L806-L817.
42. Muzykantov, V. R., Martynov, A. V., Puchnina, E. A., and Danilov, S. M. (1989). In vivo administration of glucose oxidase conjugated with monoclonal antibodies to angiotensin-converting enzyme. The tissue distribution, blood clearance, and targeting into rat lungs. Am. Rev. Respir. Dis. 139: 1464-1473.
43. Danilov, S. M., et al. (1991). Lung is the target organ for a monoclonal antibody to angiotensin-converting enzyme. Lab. Invest. 64: 118-124.
44. Wickham, T. J., Carrion, M. E., and Kovesdi, I. (1995). Targeting of adenovirus penton base to new receptors through replacement of its RGD motif with other receptor-specific peptide motifs. Gene Ther. 2: 750-756.
45. Wickham, T. J., Roelvink, P. W., Brough, D. E., and Kovesdi, I. (1996). Adenovirus targeted to heparan-containing receptors increases its gene delivery efficiency to multiple cell types. Nat. Biotech. 14: 1570-1573.
46. Goldman, C. K., et al. (1997). Targeted gene delivery to Kaposi's sarcoma cells via the fibroblast growth factor receptor. Cancer Res. 57: 1447-1451.
47. Rogers, B. E., et al. (1997). Enhanced in vivo gene delivery utilizing tropism-modified adenovirus vectors. Tumor Targeting 3: 25-31.
48. Wickham, T. J., et al. (1997). Increased in vitro and in vivo gene transfer by adenovirus vectors containing chimeric fiber proteins. J. Virol. 71: 8221-8229.
49. Wickham, T. J., et al. (1997). Targeted adenovirus-mediated gene delivery to T cells via CD3. J. Virol. 71: 7663-7669.
50. Watkins, S. J., Mesyanzhinov, V. V., Kurochkina, L. P., and Hawkins, R. E. (1997). The adenobody approach to viral targeting - Specific and enhanced adenoviral gene delivery. Gene Ther. 4: 1004-1012.
51. Rancourt, C., et al. (1998). FGF2-enhancement of adenovirus-mediated delivery of the herpes simplex virus thymidine kinase gene results in augmented therapeutic benefit in a murine model of ovarian cancer. Clin. Cancer Res. 4: 2455-2461.
52. Reynolds, P. N., et al. (1998). Targeting adenoviral infection with basic fibroblast growth factor enhances gene delivery to vascular endothelial and smooth muscle cells. Tumor Targeting 3: 156-168.
53. Krasnykh, V., Dmitriev, I., Mikheeva, G., Miller, C. R., Belousova, N., and Curiel, D. T. (1998). Characterization of an adenovirus vector containing a heterologous peptide epitope in the HI loop of the fiber knob. J. Virol. 72: 1844-1852.
54. Tillman, B. W., et al. (1999). Maturation of dendritic cells accompanies high efficiency gene transfer by a CD40-targeted adenoviral vector. J. Immunol. 162: 6378-6383.
55. Couffinhal, T., Kearney, M., Sullivan, A., Silver, M., Tsurumi, Y., and Isner, J. M. (1997). Histochemical staining following LacZ gene transfer underestimates transfection efficiency. Hum. Gene Ther. 8: 929-934.
56. Page, C., Rose, M., Yacoub, M., and Pigott, R. (1992). Antigenic heterogeneity of vascular endothelium. Am. J. Pathol. 141: 673-683.
57. Pearson, D. A., et al. (1996). Somatostatin receptor-binding peptides labeled with technetium-99m: Chemistry and initial biological studies. J. Med. Chem. 39: 1361-1371.
58. Vallabhajosula, S., et al. (1996). Preclinical evaluation of technetium-99m-labeled somatostatin receptor-binding peptides. J. Nucl. Med. 37: 1016-1022.
59. Virgolini, I., et al. (1998). Somatostatin receptor subtype specificity and in vivo binding of a novel tumor tracer, 99mTc-P829. Cancer Res. 58: 1850-1859.
60. Blum, J. E., Handmaker, H., and Rinne, N. A. (1999). The utility of a somatostatin-type receptor binding peptide radiopharmaceutical (P829) in the evaluation of solitary pulmonary nodules. Chest 115: 224-232.
61. Worgall, S., Wolff, G., Falckpedersen, E., and Crystal, R. G. (1997). Innate immune mechanisms dominate elimination of adenoviral vectors following in vivo administration. Hum. Gene Ther. 8: 37-44.
62. Wolff, G., Worgall, S., Vanrooijen, N., Song, W. R., Harvey, B. G., and Crystal, R. G. (1997). Enhancement of in vivo adenovirus-mediated gene transfer and expression by prior depletion of tissue macrophages in the target organ. J. Virol. 71: 624-629.
63. Lieber, A., et al. (1997). The role of Kupffer cell activation and viral gene expression in early liver toxicity after infusion of recombinant adenovirus vectors. J. Virol. 71: 8798-8807.
64. Douglas, J. T., et al. (1999). A system for the propagation of adenoviral vectors with genetically modified receptor specificities. Nat. Biotech. 17: 470-475.
65. Roelvink, P. W., Mi Lee, G., Einfeld, D. A., Kovesdi, I., and Wickham, T. J. (1999). Identification of a conserved receptor-binding site on the fiber proteins of CAR-recognizing adenoviridae. Science 286: 1568-1571.
66. Danilov, S., et al. (1994). Interaction of mAb to angiotensin-converting enzyme (ACE) with antigen in vitro and in vivo: Antibody targeting to the lung induces ACE antigenic modulation. Int. Immunol. 6: 1153-1160.
67. Meyrick, B. O., and Perkett, E. A. (1989). The sequence of cellular and hemodynamic changes of chronic pulmonary hypertension induced by hypoxia and other stimuli. Am. Rev. Respir. Dis. 140: 1486-1489.
68. Gu, D. L., et al. (1999). Fibroblast growth factor 2 retargeted adenovirus has redirected cellular tropism: Evidence for reduced toxicity and enhanced antitumor activity in mice. Cancer Res. 59: 2608-2614.
69. Reynolds, P. N., Dmitriev, I., and Curiel, D. T. (1999). Insertion of an RGD motif into the HI loop of adenovirus alters the transgene expression profile of the systemically administered vector. Gene Ther. 6: 1336-1339.