Recombinant, replication-defective adenovirus gene transfer vectors induce cell cycle dysregulation and inappropriate expression of cyclin proteins

Journal of Virology

Volumn 72, Issue 12, 1998, Pages 9491-9502

  Wersto, Robert P ^a   Rosenthal, Eugene R ^a   Seth, Prem K ^b   Eissa, N Tony ^a   Donahue, Robert E ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYCLIN A; CYCLIN B; CYCLIN D1; CYCLIN DEPENDENT KINASE; CYCLINE; GENE PRODUCT; VIRUS VECTOR;

ADENOVIRUS; ANEUPLOIDY; ANIMAL CELL; ARTICLE; BRONCHUS MUCOSA; CELL CYCLE; CELL CYCLE G2 PHASE; CELL STRAIN 3T3; CONTROLLED STUDY; DEFECTIVE VIRUS; EPITHELIUM CELL; GENE TRANSFER; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OPEN READING FRAME; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRACHEA MUCOSA; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS REPLICATION;

EID: 0031775398     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.12.9491-9502.1998     Document Type: Article

References (87)

1. Akhter, S. A., C. A. Skaer, A. P. Kypson, P. H. McDonald, K. C. Peppel, D. D. Glower, R. J. Lefkowitz, and W. J. Koch. 1997. Restoration of beta-adrenergic signaling in failing cardiac ventricular myocytes via adenoviral-mediated gene transfer. Proc. Natl. Acad. Sci. USA 94:12100-12015.
2. Armentano, D., C. C. Sookdeo, K. M. Hehir, R. J. Gregory, J. A. St. George, G. A. Prince, S. C. Wadsworth, and A. E. Smith. 1995. Characterization of an adenovirus gene transfer vector containing an E4 deletion. Hum. Gene Ther. 6:1343-1353.
3. 3[H]-thymidine. Cell Prolif. 29:89-100.
4. Boucher, R. C. 1996. Current status of CF gene therapy. Trends Genet. 12: 81-84.
5. Brand, K., and M. Strauss. 1998. Presented at the 1st Annual Meeting of the American Society for Gene Therapy, May 28-31, Seattle, Wash.
6. Buchwald, M., R. Sood, and W. Auerbach. 1991. Expression of CFTR in cultured human intestinal epithelial cells, p. 241-252. In L.-C. Tsui, G. Romeo, R. Gieger, and S. Gorini (ed.), The identification of the CF (cystic fibrosis) gene: recent progress and new research strategies. Plenum Press, New York.
7. Bui, K. C., F. Wu, S. Buckley, L. Wu, R. Williams, D. Carbonaro-Hall, F. L. Hall, and D. Warburton. 1993. Cyclin A expression in normal and transformed alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 9:115-125.
8. Center for Biologies Evaluation and Research. 1996. Points to consider in human somatic cell therapy and gene therapy. Center for Biologies Evaluation and Research, Food and Drug Administration, Rockville, Md.
9. Chacho, M. S., E. Eppich, R. P. Wersto, and L. G. Koss. 1990. Influence of human papillomavirus on DNA ploidy determination in genital condylomas. Cancer 65:2291-2294.
10. Chang, M. W., E. Barr, J. Seltzer, Y.-Q. Jiang, G. J. Nabel, E. G. Nabel, M. S. Paracek, and J. M. Leiden. 1995. Cytostatic gene therapy for vascular proliferative disorders with a constitutively active form of the retinoblastoma gene product. Science 267:518-522.
11. KIP1. J. Clin. Investig. 97:1983-1988.
12. Coleman, T. R., and W. G. Dunphy. 1994. Cdc2 regulatory factors. Curr. Opin. Cell Biol. 6:877-882.
13. kip1 induces cell cycle arrest and loss of cyclin-cdk activity in human breast cancer cells. Oncogene 14:2283-2289.
14. Darzynkiewcz, Z., S. Bruno, G. Del Bino, W. Gorczyca, M. A. Hotz, P. Lassota, and F. Tragnos. 1992. Features of apoptotic cells measured by flow cytometry. Cytometry 13:795-808.
15. Darzynkiewcz, Z., J. Gong, G. Juan, B. Ardelt, and F. Tragnos. 1996. Cytometry of cyclin proteins. Cytometry 25:1-13.
16. Ding, M., Y. Feng, and D. D. Vandre. 1997. Partial characterization of the MPM-2 phosphoepitope. Exp. Cell Res. 231:3-13.
17. Douglas, J. T., and D. T. Curiel. 1997. Targeted adenoviral vectors for cancer gene therapy. Int. J. Oncol. 11:341-348. (Review.)
18. Dupuit, F., J.-M. Zahm, D. Pierrot, S. Brezillon, N. Bonnet, J.-L. Imler, A. Pavirini, and E. Puchelle. 1995. Regenerating cells in human airway epithelium represent preferential targets for recombinant adenovirus. Hum. Gene Ther. 6:1185-1193.
19. - adenovirus vectors for gene therapy for the respiratory manifestations of cystic fibrosis. Hum. Gene Ther. 5:1105-1114.
20. Engelhardt, J. F., Y. Yang, L. D. Stratford-Perricaudet, E. D. Allen, K. Kozarsky, M. Perricaudet, J. R. Yankaskas, and J. M. Wilson. 1993. Direct gene transfer of human CFTR into bronchial human epithelia of xenografts with E1-deleted adenoviruses. Nat. Genet. 4:27-33.
21. Felgner, P. L. 1996. Improvements in catonic liposomes for in vivo gene transfer. Hum. Gene Ther. 7:1791-1793.
22. Gahery-Segard, H., V. Molinier-Frenkel, C. L. Boulare, P. Saulnier, P. Opolon, R. Lengagne, E. Gautier, A. L. Cesne, L. Zitvogel, A. Venet, C. Schatz, M. Courtney, T. L. Chevalier, T. Tursz, J. G. Guillet, and F. Farace. 1997. Phase I trial of recombinant adenovirus gene transfer in lung cancer: longitudinal study of immune responses to transgene and viral proteins. J. Clin. Investig. 100:2218-2226.
23. Glotzer, M., A. W. Murray, and M. W. Kirschner. 1991. Cyclin is degraded by the ubiquitin pathway. Nature 349:132-138.
24. Grand, R. J. A., A. P. Ibrahim, A. M. R. Taylor, A. E. Milner, C. D. Gregory, P. H. Gallimore, and A. S. Turnell. 1998. Human cells arrest in S phase in response to adenovirus 12 E1A. Virology 244:330-342.
25. Griscelli, F., H. Li, A. Bennaceur-Griscelli, J. Soria, P. Opolon, C. Soria, M. Perricaudet, P. Yeh, and H. Lu. 1998. Angiostatin gene transfer: inhibition of tumor growth in vivo by blockage of endothelial cell proliferation associated with a mitosis arrest. Proc. Natl. Acad. Sci. USA 95:6367-6372.
26. Grubb, B. R., R. J. Pickles, H. Ye, J. R. Yankaskas, R. N. Vick, J. F. Engelhardt, J. M. Wilson, L. G. Johnson, and R. C. Boucher. 1994. Inefficient gene transfer by adenovirus vector to cystic fibrosis airway epithelia of mice and humans. Nature 371:802-806.
27. Gruenert, D. C., C. B. Basbaum, M. J. Welsh, M. Li, W. E. Finkbeiner, and J. A. Nadel. 1988. Characterization of human tracheal epithelial cells transformed by an origin-defective simian virus 40. Proc. Natl. Acad. Sci. USA 85: 5951-5955.
28. Halbert, D. N., J. R. Cutt, and T. Shenk. 1985. Adenovirus early region 4 encodes functions required for efficient DNA replication, late gene expression, and host cell shutoff. J. Virol. 56:250-257.
29. Hassid, S., M. P. Degaute, S. Dawance, K. Rombaut, N. Nagy, G. Choufani, C. Decaestecker, A. Danguy, I. Salmon, and R. Kiss. 1997. Determination of proliferative activity in nasal polyps. J. Clin. Pathol. 50:923-928.
30. cdc2 activity. J. Virol. 69:6705-6711.
31. Hinds, P. W., S. F. Dowdy, E. N. Eaton, A. Arnold, and R. A. Weinberg. 1994. Function of a human cyclin gene as an oncogene. Proc. Natl. Acad. Sci. USA 91:709-713.
32. Horwitz, M. S. 1990. Adenoviridae and their replication, p. 1679-1721. In B. N. Fields, and D. M. Knipe (ed.), Virology. Raven Press, New York, N.Y.
33. Jault, F. M., J.-M. Jault, F. Ruchti, E. A. Fortunato, C. Clark, J. Corbeil, D. D. Richman, and D. H. Spector. 1995. Cytomegalovirus infection induces high levels of cyclins, phosphorylated Rb, and p53, leading to cell cycle arrest. J. Virol. 69:6697-6704.
34. Jones, N., and T. Shenk. 1979. Isolation of adenovirus type 5 host range deletion mutants defective for transformation of rat embryo cells. Cell 17: 683-689.
35. Jooss, K., Y. Yang, and J. M. Wilson. 1996. Cyclophosphamide diminishes inflammation and prolongs transgene expression following delivery of adenoviral vectors to mouse lung and liver. Hum. Gene Ther. 7:1555-1566.
36. Joshi, U. S., Y. Q. Chen, G. P. Kalemkerian, M. R. Adil, M. Kraut, and F. H. Sarkar. 1998. Inhibition of tumor cell growth by p21WAF1 adenoviral gene transfer in lung cancer. Cancer Gene Ther. 5:183-191.
37. Kaczmarek, L., B. Ferguson, M. Rosenberg, and R. Baserga. 1986. Induction of cellular DNA synthesis by purified adenovirus E1a proteins. Virology 152: 1-10.
38. Kaplan, J. M., J. A. St. George, S. E. Pennington, L. D. Keyes, R. P. Johnson, S. C. Wadsworth, and A. E. Smith. 1996. Humoral and cellular immune responses of non-human primates to long-term repeated lung exposure to Ad2/CFTR-2. Gene Ther. 3:117-127.
39. Kaplan, J. M., and A. E. Smith. 1997. Transient immunosuppression with deoxyspergualin improves longevity of transgene expression and ability of readminister adenoviral vector to the mouse lung. Hum. Gene Ther. 8:1095-1104.
40. Kay, M. A., D. Liu, and P. M. Hoogerbrugge. 1977. Gene therapy. Proc. Natl. Acad. Sci. USA 94:12744-12746.
41. Knowles, M. R., K. W. Hohneker, Z. Zhou, J. C. Olsen, T. L. Noah, P. C. Hu, M. W. Leigh, J. F. Englehardt, L. J. Edwards, K. R. Jones, M. Grossman, J. M. Wilson, L. G. Johnson, and R. C. Boucher. 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.
42. Kozarsky, K., and J. M. Wilson. 1993. Gene therapy: adenovirus vectors. Curr. Opin. Genet. Dev. 3:499-503.
43. Lavoie, J. N., M. Nguyen, R. C. Marcellus, P. E. Branton, and G. C. Shore. 1998. E4orf4, a novel adenovirus death factor that induces p53-independent apoptosis by a pathway that is not inhibited by zVAD-fmk. J. Cell Biol. 140: 637-645.
44. Leigh, M. W., J. Kylander, J. R. Yankaskas, and R. C. Boucher. 1995. Cell proliferation in bronchial epithelium and submucosal glands of cystic fibrosis patients. Am. J. Respir. Cell Mol. Biol. 12:695-612.
45. Leppard, K. N. 1997. E4 gene function in adenovirus, adenovirus vector and adeno-associated virus infections. J. Gen. Virol. 78:2131-2138.
46. Li, X., and Z. Darzynkiewicz. 1995. Labeling DNA strand breaks with BrdUTP. Detection of apoptosis and cell proliferation. Cell Prolif. 28:572-579.
47. Mariassy, A. T. 1992. Epithelial cells of trachea and bronchi, p. 63-73. In R. A. Parent (ed.), Comparative biology of the normal lung. CRC Press, Boca Raton, Fla.
48. Marino, C. R., L. M. Matovcik, F. S. Gorrelick, and J. A. Cohn. 1991. Localization of the cystic fibrosis transmembrane conductance regulator in pancreas. J. Clin. Investig. 88:712-716.
49. Mittereder, N., K. L. March, and B. C. Trapnell. 1996. Evaluation of the concentration and bioactivity of adenovirus vectors for gene therapy. J. Virol. 70:7498-7509.
50. Moore, M., N. Horikoshi, and T. Shenk. 1996. Oncogenic potential of the adenovirus E4orf6 protein. Proc. Natl. Acad. Sci. USA 93:11295-11301.
51. Morgan, R. A., and W. F. Anderson. 1993. Human gene therapy. Annu. Rev. Biochem. 62:191-217.
52. Nordstrom, T., H. A. Nevanlinna, and L. C. Andersson. 1992. Mitosis-arresting effect of the calcium channel inhibitor SK&F 96365 on human leukemia cells. Exp. Cell Res. 202:487-494.
53. Ohwada, A., E. A. Hirschowitz, and R. G. Crystal. 1996. Regional delivery of an adenovirus vector containing the Escherichia coli cytosine deaminase gene to provide local activation of 5-fluorocytosine to suppress the growth of colon carcinoma metastatic to liver. Hum. Gene Ther. 7:1567-1576.
54. Overton, W. R. 1995. False DNA aneuploidy possibly caused by viral DNA. Cytometry 22:158.
55. Pickles, R. J., P. M. Barker, H. Ye, and R. C. Boucher. 1996. Efficient adenovirus-mediated gene transfer to basal but not columnar cells of cartilaginous airway epithelia. Hum. Gene Ther. 7:921-931.
56. Pollack, A. 1990. Flow cytometric cell-kinetic analysis by simultaneously staining nuclei with propidium iodide and fluorescein isothiocyanate. Methods Cell Biol. 33:315-323.
57. cdc2-cyclin B. J. Virol. 69:6859-6984.
58. Rogel, M. E., L. I. Wu, and M. Emerman. 1995. The human immunodeficiency virus type 1 vpr gene prevents cell proliferation during chronic infection. J. Virol. 69:882-888.
59. Ross, G., R. Erickson, D. Knorr, A. G. Motulsky, R. Parkman, J. Samulski, S. E. Strauss, and B. R. Smith. 1996. Gene therapy in the United States: a five-year status report. Hum. Gene Ther. 7:1781-1790.
60. Rousset, M. 1986. The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation. Biochemie 68: 1035-1040.
61. Salvant, B. S., E. A. Fortunato, and D. H. Spector. 1998. Cell cycle dysregulation by human cytomegalovirus: influence of the cell cycle phase at the time of infection and effects on cyclin transcription. J. Virol. 72:3729-3741.
62. INK4/CDKN2 and p53 genes cooperate to induce apoptotic tumor cell death. Nat. Med. 3:313-319.
63. Schauer, I. E., S. Siriwardana, T. A. Langan, and R. A. Sclafani. 1994. Cyclin D1 overexpression vs. retinoblastoma inactivation: implications for growth control evasion in non-small cell and small cell lung cancer. Proc. Natl. Acad. Sci. USA 91:7827-7831.
64. Schiavi, S. C., N. Abdelkader, S. Reber, S. Pennington, R. Narayana, J. M. McPherson, A. E. Smith, H. Hoppe IV, and S. H. Cheng. 1996. Biosynthetic and growth abnormalities are associated with high-level expression of CFTR in heterologous cells. Am. J. Physiol. 27:C341-C351.
65. Schoumacher, R. A., J. Ram, M. C. Iannuzzi, N. A. Bradbury, R. W. Wallace, C. Tom Hon, D. R. Kelly, S. M. Schmid, F. B. Gelder, T. A. Rado, and R. A. Frizzell. 1990. A cystic fibrosis pancreatic adenocarcinoma cell line. Proc. Natl. Acad. Sci. USA 87:4012-4016.
66. Schutte, B., M. M. J. Reynders, C. L. M. V. J. van Assche, P. S. G. J. Hupperets, F. T. Bosman, and C. H. Blijham. 1987. An improved method for the immunocytochemical detection of bromodeoxyuridine labeled nuclei using flow cytometry. Cytometry 8:372-376.
67. Seth, P. K., D. Fitzgerald, H. Ginsberg, M. Willingham, and I. Pastan. 1984. Evidence that the penton base of adenovirus is involved in potentiation of toxicity of Pseudomonas exotoxin conjugated to epidermal growth factor. Mol. Cell. Biol. 4:1528-1533.
68. Seth, P. K., M. Rosenfeld, J. Higginhothom, and R. G. Crystal. 1994. Mechanism of enhancement of DNA expression consequent to cointernalization of a replication-deficient adenovirus and unmodified plasmid DNA. J. Virol. 68:933-940.
69. Shenk, T., N. Jones, W. Colby, and D. Fowlkes. 1980. Functional analysis of adenovirus-5 host-range deletion mutants defective for transformation of rat embryo cells. Cold Spring Harbor Symp. Quant. Biol. 44:367-375.
70. 1 cyclins. Cell 73:1059-1065.
71. Shtrichman, R., and T. Kleinberger. 1988. Adenovirus type 5 E4 open reading frame protein induces apoptosis in transformed cells. J. Virol. 72: 2975-2982.
72. Teramotto, S., L. G. Johnson, W. Huang, M. W. Leigh, and R. C. Boucher. 1995. Effect of adenoviral vector infection on cell proliferation in cultured primary human airway epithelial cells. Hum. Gene Ther. 6:1045-1053.
73. Trusal, L. R., A. Anthony, and J. J. Docherty. 1975. Differential Feulgen-deoxyribonucleic acid hydrolysis patterns of herpes simplex virus type 1 and type 2 infected cells. J. Histochem. Cytochem. 23:283-288.
74. Wang, J., X. Chenivesse, B. Henglein, and C. Brechot. 1990. Hepatitis B virus integration in a cyclin A gene in a hepatocellular carcinoma. Nature 343: 555-557.
75. Wang, L., M. Zoppe, T. M. Hackeng, J. H. Griffin, K. F. Lee, and I. M. Verma. 1997. A factor IX-deficient mouse model for hemophilia B gene therapy. Proc. Natl. Acad. Sci. USA 94:11563-11566.
76. Wang, Q., and M. H. Finer. 1996. Second-generation adenovirus vectors. Nat. Med. 2:714-716.
77. Weiss, R. S., S. S. Lee, V. B. Prasad, and R. T. Javier. 1997. Human adenovirus early region 4 open reading frame 1 genes encode growth-transforming proteins that may be distantly related to dUTP pyrophosphatase enzymes. J. Virol. 71:1857-1870.
78. Wersto, R. P., R. L. Liblit, and L. G. Koss. 1991. Flow cytometric DNA analysis of human solid tumors: a review of the interpretation of DNA histograms. Hum. Pathol. 22:1085-1098.
79. Wersto, R. P., E. R. Rosenthal, R. G. Crystal, and K. R. Spring. 1996. Uptake of fluorescent dyes associated with functional expression of the cystic fibrosis transmembrane conductance regulator in epithelial cells. Proc. Natl. Acad. Sci. USA 93:1167-1172.
80. Wersto, R. P., and P. K. Seth. Unpublished data.
81. Wersto, R. P., and M. A. Stetler-Stevenson. 1995. Debris compensation of DNA histograms and its effect on S-phase analysis. Cytometry 20:43-52.
82. White, E. 1995. Regulation of p53-dependent apoptosis by E1A and E1B. Curr. Top. Microbiol. Immunol. 199:34-58.
83. Yang, Y., F. A. Nunes, K. Bercencsi, E. Gonczol, J. F. Engelhardt, and J. M. Wilson. 1994. Inactivation of E2a in recombinant adenoviruses improves the prospect for gene therapy in cystic fibrosis. Nat. Genet. 7:362-369.
84. Yang, Y., Q. Li, H. C. Ertl, and J. M. Wilson. 1995. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant adenoviruses. J. Virol. 69:2004-2015.
85. Zabner, J., D. M. Peterson, A. P. Puga, S. M. Graham, L. A. Couture, L. D. Keyes, M. J. Lukason, J. A. St. George, R. J. Gregory, A. E. Smith, and M. J. Welsh. 1994. Safety and efficacy of repetitive adenovirus-mediated transfer of CFTR cDNA to airway epithelia of primates and cotton rats. Nat. Genet. 6:75-83.
86. Zabner, J., B. W. Ramsey, D. P. Meeker, M. L. Aitken, R. P. Balfour, R. L. Gibson, J. Launspach, R. A. Moscicki, S. M. Richards, T. A. Standaert, J. Williams-Warren, S. C. Wadsworth, A. E. Smith, and M. J. Welsh. 1996. Repeat administration of an adenovirus vector encoding cystic fibrosis transmembrane conductance regulator to the nasal epithelium of patients with cystic fibrosis. J. Clin. Investig. 97:1504-1511.
87. Zeitlin, P. L., L. Lu, J. Rhim, G. Cutting, G. Stetten, K. A. Kiefer, R. Craig, and W. B. Guggino. 1991. A cystic fibrosis bronchial epithelial cell line: immortalization by adeno12-SV40 infection. Am. J. Respir. Cell Mol. Biol. 4: 313-319.