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Science 14 September 1962:
Vol. 137. no. 3533, pp. 835 - 841
DOI: 10.1126/science.137.3533.835
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Articles

The Quest for Human Cancer Viruses

A new approach to an old problem reveals cancer induction in hamsters by human adenovirus

John J. Trentin 1, Yoshiro Yabe 1, and Grant Taylor 1

1 The division of experimental biology of Baylor University College of Medicine and with the section of experimental pediatrics, University of Texas M. D. Anderson Hospital and Tumor Institute, Houston

A new approach to the important but difficult task of revealing possible human tumor viruses has been presented in this article. By systematic testing of already known human viruses for oncogenic properties, it was found that in hamsters injected intrapulmonarily with tissue culture fluid of human type 12 adenovirus within 24 hours after birth there was a very high incidence of malignant tumors at the site of injection in from 1 to 3 months. The tumorinducing activity was not lost by filtration through Selas 02 filters or by tissue culture passages in HeLa cells. Tumors thus induced grew in, and killed, a high percentage of the unconditioned young adult hamsters into which they were transplanted. No such tumors occurred in hamsters injected with control tissue culture fluid or with culture fluids of the other viruses tested, or in control breeder hamsters. The possibility that contamination with polyoma virus and simian virus 40 might be responsible for the tumors induced was specifically excluded by a variety of tests. The possible involvement of still other, as yet unknown, contaminant viruses was excluded by a positive association of the tumor-inducing ability with the adenovirus content. Of eight human sera tested, only those four which neutralized the adenovirus-type cytopathic effect also neutralized the tumor-inducing effect. Of 700 human sera tested, 26 percent contained CPE-neutralizing antibodies for type 12 adenovirus at titers of 1:4 and higher (23).


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The History of Tumor Virology.
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Cancer Res. 68, 7693-7706
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Human CAR Gene Expression in Nonpermissive Hamster Cells Boosts Entry of Type 12 Adenovirions and Nuclear Import of Viral DNA.
N. Hochstein, D. Webb, M. Hosel, W. Seidel, S. Auerochs, and W. Doerfler (2008)
J. Virol. 82, 4159-4163
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Investigation of Adenovirus Occurrence in Pediatric Tumor Entities.
K. Kosulin, C. Haberler, J. A. Hainfellner, G. Amann, S. Lang, and T. Lion (2007)
J. Virol. 81, 7629-7635
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Identification of Specific Cellular Genes Up-Regulated Late in Adenovirus Type 12 Infection.
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J. Virol. 79, 2404-2412
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Hypoxia and defective apoptosis drive genomic instability and tumorigenesis.
D. A. Nelson, T.-T. Tan, A. B. Rabson, D. Anderson, K. Degenhardt, and E. White (2004)
Genes & Dev. 18, 2095-2107
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Mechanisms by which DNA tumor virus oncoproteins target the Rb family of pocket proteins.
A.-M. Helt and D. A. Galloway (2003)
Carcinogenesis 24, 159-169
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Comparative Sequence Analysis of the Largest E1A Proteins of Human and Simian Adenoviruses.
N. Avvakumov, R. Wheeler, J. C. D'Halluin, and J. S. Mymryk (2002)
J. Virol. 76, 7968-7975
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Overexpression of the Adenovirus Type 12 (Ad12) pTP or E1A Gene Facilitates Ad12 DNA Replication in Nonpermissive BHK21 Hamster Cells.
M. Hosel, D. Webb, J. Schroer, B. Schmitz, and W. Doerfler (2001)
J. Virol. 75, 10041-10053
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Early Region 1 Transforming Functions Are Dispensable for Mammary Tumorigenesis by Human Adenovirus Type 9.
D. L. Thomas, S. Shin, B. H. Jiang, H. Vogel, M. A. Ross, M. Kaplitt, T. E. Shenk, and R. T. Javier (1999)
J. Virol. 73, 3071-3079
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Mechanism of E1A-Induced Transforming Growth Factor-beta (TGF-beta ) Resistance in Mouse Keratinocytes Involves Repression of TGF-beta Type II Receptor Transcription.
D. H. Kim, J. H. Chang, K. H. Lee, H.-Y. Lee, and S.-J. Kim (1997)
J. Biol. Chem. 272, 688-694
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Requirement for the adenovirus type 9 E4 region in production of mammary tumors.
R Javier, K Raska Jr, and T Shenk (1992)
Science 257, 1267-1271
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Differential NK cell and macrophage killing of hamster cells infected with nononcogenic or oncogenic adenovirus.
J. Cook and A. Lewis Jr (1984)
Science 224, 612-615
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Cell Transformation: A Study of Regulation with Types 5 and 12 Adenovirus Temperature-sensitive Mutants.
H. S. Ginsberg, M. J. Ensinger, R. S. Kauffman, A. J. Mayer, and U. Lundholm (1974)
Cold Spring Harb Symp Quant Biol 39, 419-426
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Early Events in Adenovirus-infected Cells.
W. C. Russell (1974)
Cold Spring Harb Symp Quant Biol 39, 551-557
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Recent Studies on the Characteristics of Adenovirus-infected and -transformed Cells.
J. K. McDougall, A. R. Dunn, and P. H. Gallimore (1974)
Cold Spring Harb Symp Quant Biol 39, 591-600
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Recent Advances in Oncology.
D. L. MORTON, C. M. HASKELL, Y. H. PILCH, F. C. SPARKS, and W. D. WINTERS (1972)
Ann Intern Med 77, 431-454
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Transcription of Adenovirus Genes in Productively Infected and in Transformed Cells.
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Cold Spring Harb Symp Quant Biol 35, 803-818
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Neoplastic Transformation in vitro of Hamster Lens Epithelium by Simian Virus 40.
D. M. Albert, A. S. Rabson, P. A. Grimes, and L. von Sallmann (1969)
Science 164, 1077-1078
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Adenovirus Tumorigenesis: Role of the Viral Genome in Determining Tumor Morphology.
W. A. Strohl, A. S. Rabson, and H. Rouse (1967)
Science 156, 1631-1633
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I. V. Sultanian and G. Freeman (1966)
Science 154, 665-667
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Viruses as Carcinogenic Agents.
B. M. Levy (1966)
Journal of Dental Research 45, 528-534
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Possible Implications of Virus-Induced Chromosomal Aberrations.
B. Hampar (1966)
Journal of Dental Research 45, 561-567
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A. B. SABIN (1966)
Arch Pediatr Adolesc Med 111, 1-10
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Oncogenicity of the Simian Adenoviruses.
R. N. Hull, I. S. Johnson, C. G. Culbertson, C. B. Reimer, and H. F. Wright (1965)
Science 150, 1044-1046
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Cyclic Structure of Adenovirus DNA.
K. O. Smith (1965)
Science 148, 100-102
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Papillomas of the Larynx.
A. M. DEKELBOUM (1965)
Arch Otolaryngol Head Neck Surg 81, 390-397
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Treatment of Epidemic Keratoconjunctivitis With Idoxuridine (IUDR).
S. D. HECHT, L. HANNA, T. W. SERY, and E. JAWETZ (1965)
Arch Ophthalmol 73, 49-54
   Abstract »    PDF »
Adenovirus-like Particles from Cancers Induced by Adenovirus-12 but Free of Infectious Virus.
K. O. Smith and J. L. Melnick (1964)
Science 145, 1190-1192
   Abstract »    PDF »
Adenovirus Type 12 Infection: Clinical and Laboratory Studies.
H. G. Cramblett and E. W. Edmond (1964)
JAMA 188, 1086-1088
   Abstract »    PDF »
Oncogenic Effect of Human Adenovirus Type 12, in Mice.
Y. Yabe, L. Samper, E. Bryan, G. Taylor, and J. J. Trentin (1964)
Science 143, 46-47
   Abstract »    PDF »
Inhibition by 5-Iododeoxyuridine of the Oncogenic Effects of Adenovirus Type 12 in Hamsters.
R. J. Huebner, W. T. Lane, A. D. Welch, P. Calabresi, R. W. McCollum, and W. H. Prusoff (1963)
Science 142, 488-490
   Abstract »    PDF »
Thoughts on Cancer Research, 1963.
A. GELLHORN (1963)
Ann Intern Med 59, 251-257
   Abstract »    PDF »


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