Circumvention of anti-adenovirus neutralizing immunity by administration of an adenoviral vector of an alternate serotype

Human Gene Therapy

Volumn 8, Issue 1, 1997, Pages 99-109

  Mack, Charles A ^a   Song, Wen Ru ^a   Carpenter, Heather ^a   Wickham, Tom J ^b   Kovesdi, Imre ^b   Harvey, Ben Gary ^a   Magovern, Christopher J ^a   Isom, O Wayne ^a   Rosengart, Todd ^a   Falck Pedersen, Eric ^c   Hackett, Neil R ^a   Crystal, Ronald G ^a   Mastrangeli, Andrea ^a  

^a WEILL CORNELL MEDICAL CENTER   (United States)

^b GENVEC INC   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCURONIDASE; NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EXPRESSION VECTOR; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG LAVAGE; MALE; MOUSE; NONHUMAN; RAT; SEROTYPE; SERUM; TRANSGENE; VIRUS IMMUNITY; VIRUS NEUTRALIZATION;

EID: 16944367354     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.1997.8.1-99     Document Type: Article

References (59)

1. ADAM, É., NASZ, I., and LENGYEL, A. (1995). Antigenic homogeneity among the adenovirus hexon types of subgenus C. Arch. Virol. 140, 1297-1301.
2. BAI, M., CAMPISI, L., and FREIMUTH, P. (1994). Vitronectin receptor antibodies inhibit infection of HeLa and A549 cells by adenovirus type 12 but not by adenovirus type 2. J. Virol. 68, 5925-5932.
3. BARR, D., TUBB, J., FERGUSON, D., SCARIA, A., LIEBER, A., WILSON, C., PERKINS, J., and KAY, M.A. (1995). Strain related variations in adenovirally mediated transgene expression from mouse hepatocytes in vivo: Comparisons between immunocompetent and immunodeficient inbred strains. Gene Ther. 2, 151-155.
4. BRADFORD, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
5. CRYSTAL, R.G., McELVANEY, N.G., ROSENFELD, M.A., CHU, C.S., MASTRANGELI, A., HAY, J.G., BRODY, S.L., JAFFE, H.A., EISSA, N.T., and DANEL, C. (1994). Administration of an adenovirus containing the human CFTR cDNA to the respiratory tract of individuals with cystic fibrosis. Nature Genet. 8, 42-51.
6. DAI, Y., SCHWARZ, E.M., GU, D., ZHANG, W.-W., SARVETNICK, M., and VERMA, I.M. (1995). Cellular and humoral immune responses to adenoviral vectors containing factor IX gene: Tolerization of factor IX and vector antigens allows for long-term expression. Proc. Natl. Acad. Sci. USA 92, 1401-1405.
7. DE MATTEO, R.P., RAPER, S.E., AHN, M., FISHER, K.J., BURKE, C., RADU, A., WIDERA, G., CLAYTOR, B.R., BARKER, C.F., and MARKMANN, J.F. (1995). Gene transfer to the thymus. A means of abrogating the immune response to recombinant adenovirus. Ann. Surg. 222, 229-239.
8. DONG, J.Y., WANG, D.H., VANGINKEL, F.W., PASCUAL, D.W., and FRIZZELL, R.A. (1996). Systematic analysis of repeated gene delivery into animal lungs with a recombinant adenovirus vector. Hum. Gene Ther. 7, 319-331.
9. ENGELHARDT, J.F., SIMON, R.H., YANG, Y., ZEPEDA, M., WEBER-PENDLETON, S., DORANZ, B., GROSSMAN, M., and WILSON, J.M. (1993). Adenovirus-mediated transfer of the CFTR gene to lung of nonhuman primates: Biological efficacy study. Hum. Gene Ther. 4, 759-769.
10. FLOMENBERG, P., PIASKOWSKI, V., TRUITT, R.L., and CASPER, J.T. (1995). Characterization of human proliferative T cell responses to adenovirus. J Infect Dis 171, 1090-1096.
11. GALL, J., KASS-EISLER, A., LEINWAND, L., and FALCK-PEDERSEN, E. (1996). Adenovirus type 5 and 7 capsid chimera: Fiber replacement alters receptor tropism without affecting primary immune neutralizing epitopes. J. Virol. 70, 2116-2123.
12. GILGENKRANTZ, H., DUBOC, D., JUILLARD, V., COUTON, D., PAVIRANI, A., GUILLET, J.G., BRIAND, P., and KAHN, A. (1995). Transient expression of genes transferred in vivo into heart using first-generation adenoviral vectors: Role of the immune response. Hum. Gene Ther. 6, 1265-1274.
13. 5 integrin is necessary for efficient adenovirus-mediated gene transfer in the human airway. J. Virol. 69, 5951-5958.
14. GREBER, U.F., WILLETTS, M., WEBSTER, P., and HELENIUS, A. (1993). Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75, 477-486.
15. HAY, J.G., McELVANEY, N.G., HERENA, J., and CRYSTAL, R.G. (1995). Modification of nasal epithelial potential differences of individuals with cystic fibrosis consequent to local administration of a normal CFTR cDNA adenovirus gene transfer vector. Hum. Gene Ther. 6, 1487-1496.
16. HERSH, J., CRYSTAL, R.G., and BEWIG, B. (1995). Modulation of gene expression after replication-deficient, recombinant adenovirus-mediated gene transfer by the product of a second adenovirus vector. Gene Ther. 2, 124-131.
17. HIERHOLZER, J.C. (1992). Adenoviruses in the immunocompromised host. Clin. Microbiol. Rev. 5, 262-274.
18. KAIER, B., and WIGAND, R. (1986). Antigenic homogeneity of adenovirus types 1, 2, 5, and 6. J. Med. Virol. 18, 283-287.
19. KAPLAN, J.M., STGEORGE, J.A., PENNINGTON, S.E., KEYES, L.D., JOHNSON, R.P., WADSWORTH, S.C., and SMITH, A.E. (1996). Humoral and cellular immune responses of nonhuman primates to long-term repeated lung exposure to Ad2/CFTR. Gene Ther. 3, 117-127.
20. KASS-EISLER, A., FALCK-PEDERSEN, E., ALVIRA, M., RIVERA, J., BUTTRICK, P.M., WITTENBERG, B.A., CIPRIANI, L., and LEINWAND, L.A. (1993). Quantitative determination of adenovirus-mediated gene delivery to rat cardiac myocytes in vitro and in vivo. Proc. Natl. Acad. Sci. USA 90, 11498-11502.
21. KASS-EISLER, A., FALCK-PEDERSEN, E., ELFENBEIN, D.H., ALVIRA, M., BUTTRICK, P.M., and LEINWAND, L.A. (1994). The impact of developmental stage, route of administration and the immune system on adenovirus-mediated gene transfer. Gene Ther. 1, 395-402.
22. KASS-EISLER, A., LEINWAND, L., GALL, J., BLOOM, B., and FALCK-PEDERSEN, E. (1996). Circumventing the immune response to adenovirus-mediated gene therapy. Gene Ther. 3, 154-162.
23. KAY, M.A., GRAHAM, F., LELAND, F., and WOO, S.L.C. (1995a). Therapeutic serum concentrations of human alpha-1-antitrypsin after adenoviral-mediated gene transfer into mouse hepatocytes. Hepatology 21, 815-819.
24. KAY, M.A., HOLTERMAN, A.X., MEUSE, L., GOWN, A., OCH, H.D., LINSLEY, P.S., and WILSON, C.B. (1995b). Long-term hepatic adenovirus-mediated gene expression in mice following ctla4ig administration. Nature Genet. 11, 191-197.
25. KJELLEN, L., and PEREIRA, H.G. (1968). Role of adenovirus antigens in the induction of virus neutralizing antibody. J. Gen. Virol. 2, 177-185.
26. KNOWLES, M.R., HOHNEKER, K.W., ZHOU, Z.Q., OLSEN, J.C., NOAH, T.L., HU, P.C., LEIGH, M.W., ENGELHARDT, J.F., EDWARDS, L.J., JONES, K.R., GROSSMAN, M., WILSON, J.M., JOHNSON, L.G., and BOUCHER, R.C. (1995). A controlled study of adenoviral-vector-mediated gene transfer in the nasal epithelium of patients with cystic fibrosis. N. Engl. J. Med. 333, 823-831.
27. KOLLS, J.K., LEI, D.H., ODOM, G., NELSON, S., SUMMER, W.R., GERBER, M.A., and SHELLITO, J.E. (1996). Use of transient CD4 lymphocyte depletion to prolong transgene expression of E1-deleted adenoviral vectors. Hum. Gene Ther. 7, 489-497.
28. KOZARSKY, K.F., JOOSS, K., DONAHEE, M., STRAUSS, J.F., III, and WILSON, J.M. (1996). Effective treatment of familial hypercholesterolaemia in the mouse model using adenovirus-mediated transfer of the VLDL receptor gene. Nature Genet. 13, 54-62.
29. MASTRANGELI, A., HARVEY, B.G., YAO, J., WOLFF, G., KOVESDI, I., CRYSTAL, R.G., and FALCK-PEDERSEN, E. (1996). "Sero-switch" adenovirus-mediated in vivo gene transfer: Circumvention of anti-adenovirus humoral immune defenses against repeat adenovirus vector administration by changing the adenovirus serotype. Hum. Gene Ther. 7, 79-87.
30. McCRAY, P.B., JR., ARMSTRONG, K., ZABNER, J., MILLER, D.W., KORETZKY, G.A., COUTURE, L., ROBILLARD, J.E., SMITH, A.E., and WELSH, M.J. (1995). Adenoviral-mediated gene transfer to fetal pulmonary epithelia in vitro and in vivo, J. Clin. Invest. 95, 2620-2632.
31. PFIZENMAIER, K., PAN, S.H., and KNOWLES, B.B. (1980). Preferential h-2 association in cytotoxic t cell responses to sv40 tumor-associated specific antigens. J. Immunol. 124, 1888-1891.
32. ROSENFELD, M.A., SIEGFRIED, W., YOSHIMURA, K., YONEYAMA, K., FUKAYAMA, M., STIER, L.E., PAAKKO, P.K., GILARDI, P., STRATFORD-PERRICAUDET, L.D., PERRICAUDET, M., et al. (1991). Adenovirus-mediated transfer of a recombinant alpha 1-antitrypsin gene to the lung epithelium in vivo. Science 252, 431-434.
33. ROSENFELD, M.A., YOSHIMURA, K., TRAPNELL, B.C., YONEYAMA, K., ROSENTHAL, E.R., DALEMANS, W., FUKAYAMA, M., BARGON, J., STIER, L.E., STRATFORD-PERRICAUDET, L., PERRICAUDET, M., GUGGINO, W.B., PAVIRANI, A., LECOCQ, J.-P., and CRYSTAL, R.G. (1992). In vivo transfer of the human cystic fibrosis transmembrane conductance regulator gene to the airway epithelium. Cell 68, 143-155.
34. SCHNURR, D., and DONDERO, M.E. (1993). Two new candidate adenovirus serotypes. Intervirology 36, 79-83.
35. SETOGUCHI, Y., JAFFE, H.A., CHU, C.S., and CRYSTAL, R.G. (1994). Intraperitoneal in vivo gene therapy to deliver alpha 1-antitrypsin to the systemic circulation. Am. J. Respir. Cell Mol. Biol. 10, 369-377.
36. SHENK, T. (1996). Adenoviridae: The viruses and their replication. In Fields Virology. B.N. Fields, D.M. Knipe, and P.M. Howley, eds. (Lippincott-Raven, Philadelphia) pp. 2111.
37. SMITH, T.A.G., WHITE, B.D., GARDNER, J.M., KALEKO, M., and McCLELLAND, A. (1996). Transient immunosuppression permits successful repetitive intravenous administration of an adenovirus vector. Gene Ther. 3, 496-502.
38. SMYTHE, W.R., KAISER, L.R., HWANG, H.C., AMIN, K.M., PILEWSKI, J.M., ECK, S.J., WILSON, J.M., and ALBELDA, S.M. (1994). Successful adenovirus-mediated gene transfer in an in vivo model of human malignant mesothelioma. Ann. Thorac. Surg. 57, 1395-1401.
39. SONG, W., COLLISSON, E.W., BILLINGSLEY, P.M., and BROWN, W.C. (1992). Induction of feline immunodeficiency virus-specific cytolytic T-cell responses from experimentally infected cats. J. Virol. 66, 5409-5417.
40. STRAUS, S.E. (1984). Adenovirus infections in humans. In The Adenoviruses. H.S. Ginsberg, eds. (Plenum Press, New York) pp. 451-496.
41. TRIPATHY, S.K., BLACK, H.B., GOLDWASSER, E., and LEIDEN, J.M. (1996). Immune responses to transgene-encoded proteins limit the stability of gene expression after injection of replication-defective adenovirus vectors. Nature Med. 2, 545-550.
42. VAN GINKEL, F.W., LIU, C., SIMECKA, J.W., DONG, J., GREENWAY, T., FRIZZELL, R.A., KIYONO, H., MCGHEE, J.R., and PASCUAL, D.W. (1995). Intratracheal gene delivery with adenoviral vector induces elevated systemic IgG and mucosal IgA antibodies to adenovirus and β-galactosidase. Hum. Gene Ther. 6, 895-903.
43. WALTER, J., YOU, Q.M., HAGSTROM, J.N., SANDS, M., and HIGH, K.A. (1996). Successful expression of human factor IX following repeat administration of an adenoviral vector in mice. Proc. Natl. Acad. Sci. USA 93, 3056-3061.
44. 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.
45. WILSON, J.M., ENGELHARDT, J.F., GROSSMAN, M., SIMON, R.H., and YANG, Y. (1994). Gene therapy of cystic fibrosis lung disease using E1 deleted adenoviruses: A phase I trial. Hum. Gene Ther. 5, 501-519.
46. WOHLFART, C. (1988). Neutralization of adenoviruses: kinetics, sotichiometry, and mechanisms. J. Virol. 62, 2321-2328.
47. WOHLFART, C.E., SVENSSON, U.K., and EVERITT, E. (1985). Interaction between HeLa cells and adenovirus type 2 virions neutralized by different antisera. J. Virol. 56, 896-903.
48. YANG, Y., NUNES, F.A., BERENCSI, K., FURTH, E.E., GONCZOL, E., and WILSON, J.M. (1994a). Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc. Natl. Acad. Sci. USA 91, 4407-4411.
49. YANG, Y., NUNES, F.A., BERENCSI, K., GONCZOL, E., ENGELHARDT, J.F., and WILSON, J.M. (1994b). Inactivation of E2a in recombinant adenoviruses improves the prospect for gene therapy in cystic fibrosis. Nature Genet. 7, 362-369.
50. YANG, Y., LI, Q., ERTL, H.C.J., and WILSON, J.M. (1995a). Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J. Virol. 69, 2004-2015.
51. YANG, Y.P., TRINCHIERI, G., and WILSON, J.M. (1995b). Recombinant IL-12 prevents formation of blocking IgA antibodies to recombinant adenovirus and allows repeated gene therapy to mouse lung. Nature Med. 1, 890-893.
52. YANG, Y., GREENOUGH, K., and WILSON, J.M. (1996a). Transient immune blockade prevents formation of neutralizing antibody to recombinant adenovirus and allows repeated gene transfer to mouse liver. Gene Ther. 3, 412-420.
53. YANG, Y., JOOSS, K.U., SU, Q., ERTL, H.C.J., and WILSON, J.M. (1996b). Immune responses to viral antigens versus transgene product in the elimination of recombinant adenovirus-infected hepatocytes in vivo. Gene Ther. 3, 137-144.
54. YEI, S., MITTEREDER, N., TANG, K., O'SULLIVAN, C., and TRAPNELL, B.C. (1994). Adenovirus-mediated gene transfer to cystic fibrosis: quantitative evaluation of repeated in vivo vector administration to the lung. Gene Ther. 1, 192-200.
55. ZABNER, J., COUTURE, L.A., GREGORY, R.J., GRAHAM, S.M., SMITH, A.E., and WELSH, M.J. (1993). Adenovirus-mediated gene transfer transiently corrects the chloride transport defect in nasal epithelia of patients with cystic fibrosis. Cell 75, 207-216.
56. ZABNER, J., PETERSEN, D.M., PUGA, A.P., GRAHAM, S.M., COUTURE, L.A., KEYES, L.D., LUKASON, M.J., ST GEORGE, J.A., GREGORY, R.J., SMITH, A.E., and WELSH, M.J. (1994). Safety and efficacy of repetitive adenovirus-mediated transfer of CFTR cDNA to airway epithelia of primates and cotton rats. Nature Genet. 6, 75-83.
57. ZABNER, J., RAMSEY, B.W., MEEKER, D.P., AITKEN, M.L., BALFOUR, R.P., GIBSON, R.L., LAUNSPACH, J., MOSCICKI, R.A., RICHARDS, S.M., STANDAERT, T.A., WILLIAMS-WARREN, J., WADSWORTH, S.C., SMITH, A.E., and WELSH, M.J. (1996). Repeat administration of an adenovirus vector encoding cystic fibrosis transmembrane conductance regulator to the nasal epithelium of patients with cystic fibrosis. J. Clin. Invest. 97, 1504-1511.
58. ZHANG, W.W., FANG, X., MAZUR, W., FRENCH, B.A., GEORGES, R.N., and ROTH, J.A. (1994). High-efficiency gene transfer and high-level expression of wild-type p53 in human lung cancer cells mediated by recombinant adenovirus. Cancer Gene Trier. 1, 5-13.
59. ZSENGELLER, Z.K., WERT, S.E., HULL, W.M., HU, X., YEI, S., TRAPNELL, B.C., and WHITSETT, J.A. (1995). Persistence of replication-deficient adenovirus-mediated gene transfer in lungs of immune-deficient (nu/nu) mice. Hum. Gene Ther. 6, 457-467.