Epigenetic mechanisms in human adenovirus type 12 oncogenesis

Seminars in Cancer Biology

Volumn 19, Issue 3, 2009, Pages 136-143

  Doerfler, Walter ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Abortive infection and oncogenesis; Adenovirus DNA integration a general phenomenon; Alterations of methylation patterns upon foreign DNA insertion; De novo DNA methylation; Human adenovirus type 12; Integration of Ad12 DNA; Transgression of species barriers; Viral oncogenesis

Indexed keywords

VIRUS DNA;

ADENOVIRUS 12; CARCINOGENESIS; CARCINOGENICITY; CELL INTERACTION; CHROMOSOME INSERTION; DNA INTEGRATION; DNA METHYLATION; EPIGENETICS; FOOD INTAKE; GENE INSERTION; GENE LOCUS; GENE SILENCING; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; NONHUMAN; REVIEW; SYRIAN HAMSTER; TUMOR CELL; VIRUS GENOME; VIRUS INFECTION;

ADENOVIRUSES, HUMAN; ANIMALS; CELL TRANSFORMATION, VIRAL; CRICETINAE; DNA METHYLATION; DNA, VIRAL; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, VIRAL; GENE SILENCING; HUMANS; MICE; NEOPLASMS; VIRUS INTEGRATION;

EID: 63449105889     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2009.02.009     Document Type: Review

References (86)

1. Trentin J.J., Yabe Y., and Taylor G. The quest for human cancer viruses. Science (1962) 835-841
2. Hohlweg U., Hösel M., Dorn A., Webb D., Hilger-Eversheim K., Remus R., et al. Intraperitoneal dissemination of Ad12-induced undifferentiated neuroectodermal hamster tumors: de novo methylation and transcription patterns of integrated viral and of cellular genes. Virus Res (2003) 45-56
3. Berget S.M., Moore C., and Sharp P.A. Spliced segments at the 5′terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci USA (1977) 3171-3175
4. Chow L.T., Gelinas R.E., Broker T.R., and Roberts R.J. An amazing sequence arrangement at the 5′ ends of adenovirus 2 messenger RNA. Cell (1977) 1-8
5. Jones N., and Shenk T. An adenovirus type 5 early gene function regulates expression of other early viral genes. Proc Natl Acad Sci USA 76 (1979) 3665-3669
6. Nevins J.R. Mechanism of activation of early viral transcription by the adenovirus E1A gene product. Cell (1981) 213-220
7. Nagata K., Guggenheimer R.A., and Hurwitz J. Adenovirus DNA replication in vitro: synthesis of full-length DNA with purified proteins. Proc Natl Acad Sci USA (1983) 4266-4270
8. Doerfler W. DNA methylation and gene activity. Ann Rev Biochem (1983) 93-124
9. Hösel M., Webb D., Schröer J., and Doerfler W. The abortive infection of Syrian hamster cells with human adenovirus type 12. Curr Top Microbiol Immunol (2003) 415-440
10. Doerfler W. Human adenovirus type 12: crossing species barriers to immortalize the viral genome. Methods Mol Med (2007) 197-211
11. Sutter D., and Doerfler W. Methylation of integrated adenovirus type 12 DNA sequences in transformed cells is inversely correlated with viral gene expression. Proc Natl Acad Sci USA (1980) 253-256
12. Vardimon L., Neumann R., Kuhlmann I., Sutter D., and Doerfler W. DNA methylation and viral gene expression in adenovirus-transformed and -infected cells. Nucl Acids Res (1980) 2461-2473
13. Doerfler W. Foreign DNA in mammalian systems (2000), Wiley-VCH, Weinheim, New York, Chichester, Brisbane, Singapore, Toronto
14. Doerfler W. In pursuit of the first recognized epigenetic signal: DNA methylation. Epigenetics (2008) 125-133
15. Hahn B.H., Shaw G.M., De Cock K.M., and Sharp P.M. AIDS as a zoonosis: scientific and public health implications. Science (2000) 607-614
16. Holmes K.V. SARS coronavirus: a new challenge for prevention and therapy. J Clin Invest (2003) 1605-1609
17. Tumpey T.M., Basler C.F., Aguilar P.V., Zheng H., Solórzano A., Swayne D.E., et al. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science (2005) 77-80
18. Kuhlmann I., and Doerfler W. Shifts in the extent and patterns of DNA methylation upon explantation and subcultivation of adenovirus type 12-induced hamster tumor cells. Virology (1982) 169-180
19. Kuhlmann I., Achten S., Rudolph R., and Doerfler W. Tumor induction by human adenovirus type 12 in hamsters: loss of the viral genome from adenovirus type 12-induced tumor cells is compatible with tumor formation. EMBO J (1982) 79-86
20. Doerfler W. Nonproductive infection of baby hamster kidney cells (BHK21) with adenovirus type 12. Virology (1969) 587-606
21. Hösel M., Webb D., Schröer J., Schmitz B., and Doerfler W. The overexpression of the adenovirus type 12 pTP or E1A gene facilitates Ad12 DNA replication in non-permissive BHK21 hamster cells. J Virol (2001) 16041-16053
22. Hochstein N., Webb D., Hösel M., Seidel W., Auerochs S., and Doerfler W. Human CAR gene expression in non-permissive hamster cells boosts entry of type 12 adenovirions and nuclear import of viral DNA. J Virol (2008) 4159-4163
23. Ortin J., and Doerfler W. Transcription of the genome of adenovirus type 12. I. Viral mRNA in abortively infected and transformed cells. J Virol (1975) 27-35
24. Hösel M., Schröer J., Webb D., Jaroschevskaja E., and Doerfler W. Cellular and early viral factors in the interaction of adenovirus type 12 with hamster cells: the abortive response. Virus Res (2001) 1-16
25. Strohl W.A. The response of BHK21 cells to infection with type 12 adenovirus. II. Relationship of virus-stimulated DNA synthesis to other viral functions. Virology (1969) 653-665
26. Visser L., van Maarschalkerweerd M.W., Rozijn T.H., Wassenaar A.D., Reemst A.M., and Sussenbach J.S. Viral DNA sequences in adenovirus-transformed cells. Cold Spr Harbor Symp Quant Biol (1980) 541-550
27. Klimkait T., and Doerfler W. Adenovirus types 2 and 5 functions elicit replication and late expression of adenovirus type 12 DNA in hamster cells. J Virol (1985) 466-474
28. Klimkait T., and Doerfler W. E1B functions of type C adenoviruses play a role in the complementation of blocked adenovirus type 12 DNA replication and late gene transcription in hamster cells. Virology (1987) 109-120
29. Schiedner G., Schmitz B., and Doerfler W. Late transcripts of adenovirus type 12 DNA are not translated in hamster cells expressing the E1 region of adenovirus type 5. J Virol (1994) 5476-5482
30. Doerfler W. The fate of the DNA of adenovirus type 12 in baby hamster kidney cells. Proc Natl Acad Sci USA (1968) 636-643
31. Doerfler W. Integration of the deoxyribonucleic acid of adenovirus type 12 into the deoxyribonucleic acid of baby hamster kidney cells. J Virol (1970) 652-666
32. Ortin J., Scheidtmann K.H., Greenberg R., Westphal M., and Doerfler W. Transcription of the genome of adenovirus type 12. III. Maps of stable RNA from productively infected human cells and abortively infected and transformed hamster cells. J Virol (1976) 355-372
33. Groneberg J., Sutter D., Soboll H., and Doerfler W. Morphological revertants of adenovirus type 12-transformed hamster cells. J Gen Virol (1978) 635-645
34. Sutter D., Westphal M., and Doerfler W. Patterns of integration of viral DNA sequences in the genomes of adenovirus type 12-transformed hamster cells. Cell (1978) 569-585
35. Stabel S., Doerfler W., and Friis R.R. Integration sites of adenovirus type 12 DNA in transformed hamster cells and hamster tumor cells. J Virol (1980) 22-40
36. Deuring R., Winterhoff U., Tamanoi F., Stabel S., and Doerfler W. Site of linkage between adenovirus type 12 and cell DNAs in hamster tumour line CLAC3. Nature (1981) 81-84
37. Deuring R., Klotz G., and Doerfler W. An unusual symmetric recombinant between adenovirus type 12 DNA and human cell DNA. Proc Natl Acad Sci USA (1981) 3142-3146
38. Stabel S., and Doerfler W. Nucleotide sequence at the site of junction between adenovirus type 12 DNA and repetitive hamster cell DNA in transformed cell line CLAC1. Nucl Acids Res (1982) 8007-8023
39. Doerfler W., Gahlmann R., Stabel S., Deuring R., Lichtenberg U., Schulz M., et al. On the mechanism of recombination between adenoviral and cellular DNAs: the structure of junction sites. Curr Top Microbiol Immunol (1983) 193-228
40. Gahlmann R., and Doerfler W. Integration of viral DNA into the genome of the adenovirus type 2-transformed hamster cell line HE5 without loss or alteration of cellular nucleotides. Nucl Acids Res (1983) 7347-7361
41. Gahlmann R., Schulz M., and Doerfler W. Low molecular weight RNAs with homologies to cellular DNA at sites of adenovirus DNA insertion in hamster or mouse cells. EMBO J (1984) 3263-3269
42. Schulz M., Freisem-Rabien U., Jessberger R., and Doerfler W. Transcriptional activities of mammalian genomes at sites of recombination with foreign DNA. J Virol (1987) 344-353
43. Jessberger R., Heuss D., and Doerfler W. Recombination in hamster cell nuclear extracts between adenovirus type 12 DNA and two hamster preinsertion sequences. EMBO J (1989) 869-878
44. Tatzelt J., Scholz B., Fechteler K., Jessberger R., and Doerfler W. Recombination between adenovirus type 12 DNA and a hamster preinsertion sequence in a cell-free system. Patch homologies and fractionation of nuclear extracts. J Mol Biol (1992) 117-126
45. Tatzelt J., Fechteler K., Langenbach P., and Doerfler W. Fractionated nuclear extracts from hamster cells catalyze cell-free recombination at selective sequences between adenovirus DNA and a hamster preinsertion site. Proc Natl Acad Sci USA (1993) 7356-7360
46. Heller H., Kämmer C., Wilgenbus P., and Doerfler W. Chromosomal insertion of foreign (adenovirus type 12, plasmid, or bacteriophage lambda) DNA is associated with enhanced methylation of cellular DNA segments. Proc Natl Acad Sci USA (1995) 5515-5519
47. Knoblauch M., Schröer J., Schmitz B., and Doerfler W. The structure of adenovirus type 12 DNA integration sites in the hamster cell genome. J Virol (1996) 3788-3796
48. Schröer J., Hölker I., and Doerfler W. Adenovirus type 12 DNA firmly associates with mammalian chromosomes early after virus infection or after DNA transfer by the addition of DNA to the cell culture medium. J Virol (1997) 7923-7932
49. Hilger-Eversheim K., and Doerfler W. Clonal origin of adenovirus type 12-induced hamster tumors: nonspecific chromosomal integration sites of viral DNA. Cancer Res (1997) 3001-3009
50. Remus R., Kämmer C., Heller H., Schmitz B., Schell G., and Doerfler W. Insertion of foreign DNA into an established mammalian genome can alter the methylation of cellular DNA sequences. J Virol (1999) 1010-1022
51. Müller K., Heller H., and Doerfler W. Foreign DNA integration. Genome-wide perturbations of methylation and transcription in the recipient genomes. J Biol Chem (2001) 14271-14278
52. Hochstein N., Muiznieks I., Mangel L., Brondke H., and Doerfler W. The epigenetic status of an adenovirus transgenome upon long-term cultivation in hamster cells. J Virol (2007) 5349-5361
53. Günthert U., Schweiger M., Stupp M., and Doerfler W. DNA methylation in adenovirus, adenovirus-transformed cells, and host cells. Proc Natl Acad Sci USA (1976) 3923-3927
54. Kämmer C., and Doerfler W. Genomic sequencing reveals absence of DNA methylation in the major late promoter of adenovirus type 2 DNA in the virion and in productively infected cells. FEBS Lett (1995) 301-305
55. Doerfler W. Patterns of DNA methylation - evolutionary vestiges of foreign DNA inactivation as a host defense mechanism: A proposal. Biol Chem Hoppe-Seyler (1991) 557-564
56. Schubbert R., Renz D., Schmitz B., and Doerfler W. Foreign (M13) DNA ingested by mice reaches peripheral leukocytes, spleen and liver via the intestinal wall mucosa and can be covalently linked to mouse DNA. Proc Natl Acad Sci USA (1997) 961-966
57. Wronka G., Fechteler K., Schmitz B., and Doerfler W. Integrative recombination between adenovirus type 12 DNA and mammalian DNA in a cell-free system: joining by short sequence homologies. Virus Res (2002) 225-242
58. Schick J., Baczko K., Fanning E., Groneberg J., Burger H., and Doerfler W. Intracellular forms of adenovirus DNA: Integrated form of adenovirus DNA appears early in productive infection. Proc Natl Acad Sci USA (1976) 1043-1047
59. Deuring R., and Doerfler W. Proof of recombination between viral and cellular genomes in human KB cells productively infected by adenovirus type 12: structure of the junction site in a symmetric recombinant (SYREC). Gene (1983) 283-289
60. Burger H., and Doerfler W. Intracellular forms of adenovirus DNA. III. Integration of the DNA of adenovirus type 2 into host DNA in productively infected cells. J Virol (1974) 975-992
61. Kochanek S., Clemens P.R., Mitani K., Chen H.H., Chan S., and Caskey C.T. A new adenoviral vector: replacement of all viral coding sequences with 28 kb of DNA independently expressing both full-length dystrophin and beta-galactosidase. Proc Natl Acad Sci USA (1996) 5731-5736
62. Stephen S.L., Sivanandam V.G., and Kochanek S. Homologous and heterologous recombination between adenovirus vector DNA and chromosomal DNA. J Gene Med (2008) 1176-1189
63. Eick D., and Doerfler W. Integrated adenovirus type 12 DNA in the transformed hamster cell line T637: sequence arrangements at the termini of viral DNA and mode of amplification. J Virol (1982) 317-321
64. Pfeffer A., Schubbert R., Orend G., Hilger-Eversheim K., and Doerfler W. Integrated viral genomes can be lost from adenovirus type 12-induced hamster tumor cells in a clone-specific, multistep process with retention of the oncogenic phenotype. Virus Res (1999) 113-127
65. Wold W.S., Mackey J.K., Rigden P., and Green M. Analysis of human cancer DNA's for DNA sequence of human adenovirus serotypes 3, 7, 11, 14, 16, and 21 in group B1. Cancer Res (1979) 3479-3484
66. Wold W.S., and Green M. Historic milestones in cancer virology. Semin Oncol (1979) 461-478
67. Mende Y., Schneider P.M., Baldus S.E., and Doerfler W. PCR-screening of human esophageal and bronchial cancers reveals absence of adenoviral DNA sequences. Virus Res (2004) 81-85
68. Naumann A, Hochstein N, Fanning E, Doerfler W. A distinct DNA methylation boundary in the 5′-upstream sequence of the FMR1 promoter binds nuclear proteins and is lost in fragile X syndrome, submitted for publication, 2009.
69. Hertz J., Schell G., and Doerfler W. Factors affecting de novo methylation of foreign DNA in mouse embryonic stem cells. J Biol Chem (1999) 24232-24240
70. Vardimon L., Kressmann A., Cedar H., Maechler M., and Doerfler W. Expression of a cloned adenovirus gene is inhibited by in vitro methylation. Proc Natl Acad Sci USA (1982) 1073-1077
71. Kruczek I., and Doerfler W. The unmethylated state of the promoter/leader and 5′-regions of integrated adenovirus genes correlates with gene expression. EMBO J (1982) 409-414
72. Kruczek I., and Doerfler W. Expression of the chloramphenicol acetyltransferase gene in mammalian cells under the control of adenovirus type 12 promoters: effect of promoter methylation on gene expression. Proc Natl Acad Sci USA (1983) 7586-7590
73. Langner K.D., Vardimon L., Renz D., and Doerfler W. DNA methylation of three 5′C-C-G-G3′ sites in the promoter and 5′ region inactivates the E2a gene of adenovirus type 2. Proc Natl Acad Sci USA (1984) 2950-2954
74. Langner K.D., Weyer U., and Doerfler W. Trans effect of the E1 region of adenoviruses on the expression of a prokaryotic gene in mammalian cells: resistance to 5′-CCGG-3′ methylation. Proc Natl Acad Sci USA (1986) 1598-1602
75. Weisshaar B., Langner K.D., Jüttermann R., Müller U., Zock C., Klimkait T., et al. Reactivation of the methylation-inactivated late E2A promoter of adenovirus type 2 by E1A (13S) functions. J Mol Biol (1988) 255-270
76. Willis D.B., and Granoff A. Frog virus 3 DNA is heavily methylated at CpG sequences. Virology (1980) 250-257
77. Munnes M., Schetter C., Hölker I., and Doerfler W. A fully 5′-CG-3′ but not a 5′-CCGG-3′ methylated late frog virus 3 promoter retains activity. J Virol (1995) 2240-2247
78. Munnes M., and Doerfler W. DNA methylation in mammalian genomes: promoter activity and genetic imprinting. In: Dulbecco R. (Ed). Encyclopedia of human biology vol. 3 (1997), Academic Press, San Diego, New York, Boston, London, Sydney, Tokyo, Toronto 435-446
79. Lichtenberg U., Zock C., and Doerfler W. Insertion of adenovirus type 12 DNA in the vicinity of an intracisternal A particle genome in Syrian hamster tumor cells. J Virol (1987) 2719-2726
80. Lichtenberg U., Zock C., and Doerfler W. Integration of foreign DNA into mammalian genome can be associated with hypomethylation at site of insertion. Virus Res (1988) 335-342
81. Jähner D., and Jaenisch R. Retrovirus-induced de novo methylation of flanking host sequences correlates with gene inactivity. Nature (1985) 594-597
82. Meyer zu Altenschildesche G., Heller H., Wilgenbus P., Tjia S.T., and Doerfler W. Chromosomal distribution of the hamster intracisternal A-particle (IAP) retrotransposons. Chromosoma (1996) 341-344
83. Ushijima T., Morimura K., Hosoya Y., Okonogi H., Tatematsu M., Sugimura T., et al. Establishment of methylation-sensitive-representational difference analysis and isolation of hypo- and hypermethylated genomic fragments in mouse liver tumors. Proc Natl Acad Sci USA (1997) 2284-2289
84. Hohlweg U., and Doerfler W. On the fate of plant or other foreign genes upon the uptake in food or after intramuscular injection in mice. Mol Genet Genomics (2001) 225-233
85. Doerfler W. In: Cohn W.E., and Moldave K. (Eds). Adenoviral DNA integration and changes in DNA methylation patterns: a different view of insertional mutagenesis. Progr Nucleic Acid Res Mol Biol vol. 46 (1993) 1-36
86. Doerfler W., Hohlweg U., Müller K., Remus R., Heller H., and Hertz J. Foreign DNA integration - perturbations of the genome - oncogenesis. Ann N Y Acad Sci 945 (2001) 276-288