The history of tumor virology.

In the century since its inception, the field of tumor virology has provided groundbreaking insights into the causes of human cancer. Peyton Rous founded this scientific field in 1911 by discovering an avian virus that induced tumors in chickens; however, it took 40 years for the scientific community to comprehend the effect of this seminal finding. Later identification of mammalian tumor viruses in the 1930s by Richard Shope and John Bittner, and in the 1950s by Ludwik Gross, sparked the first intense interest in tumor virology by suggesting the possibility of a similar causal role for viruses in human cancers. This change in attitude opened the door in the 1960s and 1970s for the discovery of the first human tumor viruses--EBV, hepatitis B virus, and the papillomaviruses. Such knowledge proved instrumental to the development of the first cancer vaccines against cancers having an infectious etiology. Tumor virologists additionally recognized that viruses could serve as powerful discovery tools, leading to revolutionary breakthroughs in the 1970s and 1980s that included the concept of the oncogene, the identification of the p53 tumor suppressor, and the function of the retinoblastoma tumor suppressor. The subsequent availability of more advanced molecular technologies paved the way in the 1980s and 1990s for the identification of additional human tumor viruses--human T-cell leukemia virus type 1, hepatitis C virus, and Kaposi's sarcoma virus. In fact, current estimates suggest that viruses are involved in 15% to 20% of human cancers worldwide. Thus, viruses not only have been shown to represent etiologic agents for many human cancers but have also served as tools to reveal mechanisms that are involved in all human malignancies. This rich history promises that tumor virology will continue to contribute to our understanding of cancer and to the development of new therapeutic and preventive measures for this disease in the 21st century.

[1]  H. Hausen,et al.  Attempts to detect virus‐specific DNA in human tumors. I. Nucleic acid hybridizations with complementary RNA of human wart virus , 1974, International journal of cancer.

[2]  Seng-Lai Tan Hepatitis C Viruses , 2006 .

[3]  Selected concepts of cancer as a disease: from the Greeks to 1900. , 1985, Oncology nursing forum.

[4]  D. Baltimore Viral RNA-dependent DNA Polymerase: RNA-dependent DNA Polymerase in Virions of RNA Tumour Viruses , 1970, Nature.

[5]  R. Schlegel,et al.  HPV-1 L1 protein expressed in cos cells displays conformational epitopes found on intact virions. , 1992, Virology.

[6]  H. Alter,et al.  A "NEW" ANTIGEN IN LEUKEMIA SERA. , 1965, JAMA.

[7]  H. Towler,et al.  Adult T-cell leukemia : antigen in an ATL cell line and detection of antibodies to the antigen in human sera , 2022 .

[8]  M. Hilleman Critical overview and outlook: pathogenesis, prevention, and treatment of hepatitis and hepatocarcinoma caused by hepatitis B virus. , 2003, Vaccine.

[9]  M. Barbacid,et al.  Induction of mammary carcinomas in rats by nitroso-methylurea involves malignant activation of H-ras-1 locus by single point mutations , 1983, Nature.

[10]  R. Purcell,et al.  Detection of antibody to hepatitis C virus in prospectively followed transfusion recipients with acute and chronic non-A, non-B hepatitis. , 1989, The New England journal of medicine.

[11]  C. Prives,et al.  p53: more research and more questions , 2006, Cell Death and Differentiation.

[12]  Stephen H. Friend,et al.  A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma , 1986, Nature.

[13]  P. Moore,et al.  Clonal Integration of a Polyomavirus in Human Merkel Cell Carcinoma , 2008, Science.

[14]  J. M. Price,et al.  A urinary bladder tumor induced by a bovine cutaneous papilloma agent. , 1959, Cancer research.

[15]  Y. Nakamura,et al.  Allelotype of colorectal carcinomas. , 1989, Science.

[16]  D. Hungerford,et al.  A serum antigen (Australia antigen) in Down's syndrome, leukemia, and hepatitis. , 1967, Annals of internal medicine.

[17]  L. Donehower,et al.  Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours , 1992, Nature.

[18]  H. Varmus,et al.  DNA related to the transforming gene(s) of avian sarcoma viruses is present in normal avian DNA , 1976, Nature.

[19]  P. Rous METASTASIS AND TUMOR IMMUNITY: OBSERVATIONS WITH A TRANSMISSIBLE AVIAN NEOPLASM , 1910 .

[20]  A M Prince,et al.  An antigen detected in the blood during the incubation period of serum hepatitis. , 1968, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Trentin,et al.  The Quest for Human Cancer Viruses , 1962, Science.

[22]  D. Ganem,et al.  KSHV infection and the pathogenesis of Kaposi's sarcoma. , 2006, Annual review of pathology.

[23]  L. Gross "Spontaneous" leukemia developing in C3H mice following inoculation in infancy, with AK-leukemic extracts, or AK-embrvos. , 1951, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[24]  D. Burkitt A Children's Cancer Dependent on Climatic Factors , 1962, Nature.

[25]  C. Rice,et al.  The Hepatitis C Viruses , 2000, Current Topics in Microbiology and Immunology.

[26]  J. Brugge,et al.  Role of simian virus 40 gene A function in maintenance of transformation , 1975, Journal of virology.

[27]  E. Cesarman,et al.  Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. , 1994, Science.

[28]  A. Knudson Mutation and cancer: statistical study of retinoblastoma. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Levine,et al.  Characterization of a 54K Dalton cellular SV40 tumor antigen present in SV40-transformed cells and uninfected embryonal carcinoma cells , 1979, Cell.

[30]  H. Temin,et al.  Characteristics of an assay for Rous sarcoma virus and Rous sarcoma cells in tissue culture. , 1958, Virology.

[31]  M. Hilleman,et al.  The Vacuolating Virus, S.V.40 , 1960, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[32]  Charlotte Friend,et al.  CELL-FREE TRANSMISSION IN ADULT SWISS MICE OF A DISEASE HAVING THE CHARACTER OF A LEUKEMIA , 1957, The Journal of experimental medicine.

[33]  L. Dow,et al.  Polarity regulators and the control of epithelial architecture, cell migration, and tumorigenesis. , 2007, International review of cytology.

[34]  P. Tegtmeyer Function of simian virus 40 gene A in transforming infection , 1975, Journal of virology.

[35]  H J Alter,et al.  An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. , 1990, Science.

[36]  K. Khalili,et al.  Polyomaviruses and human cancer: molecular mechanisms underlying patterns of tumorigenesis. , 2004, Virology.

[37]  H. zur Hausen,et al.  Condylomata acuminata and human genital cancer. , 1976, Cancer research.

[38]  M. R. Hllleman,et al.  Recovery of New Agent from Patients with Acute Respiratory Illness , 1954, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[39]  M. Hilleman,et al.  Development of Tumors in Hamsters Inoculated in the Neonatal Period with Vacuolating Virus, SV40 ∗ , 1962, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[40]  R. Martin,et al.  Simian virus 40 functions required for the establishment and maintenance of malignant transformation , 1975, Journal of virology.

[41]  J. Butel,et al.  Cell transformation by viruses , 1971, In Vitro.

[42]  W. Blattner,et al.  Germ-line transmission of a mutated p53 gene in a cancer-prone family with Li–Fraumeni syndrome , 1990, Nature.

[43]  J. Nevins,et al.  Identification of a cellular transcription factor involved in E1A trans-activation , 1986, Cell.

[44]  H. Hausen,et al.  A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. , 1984, The EMBO journal.

[45]  D. Bilder Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. , 2004, Genes & development.

[46]  D. Lowy,et al.  Prevention of cancer through immunization: Prospects and challenges for the 21st century , 2007, European journal of immunology.

[47]  John D. Minna,et al.  Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma , 1980, Proceedings of the National Academy of Sciences.

[48]  J. Yodoi,et al.  Adult T-cell leukemia: clinical and hematologic features of 16 cases. , 1977, Blood.

[49]  J. Moloney Biological studies on a lymphoid-leukemia virus extracted from sarcoma 37. I. Origin and introductory investigations. , 1960, Journal of the National Cancer Institute.

[50]  Kuan-Teh Jeang,et al.  Human T-cell leukaemia virus type 1 (HTLV-1) infectivity and cellular transformation , 2007, Nature Reviews Cancer.

[51]  M. Wigler,et al.  Cloning the differences between two complex genomes , 1993, Science.

[52]  P. Vogt MILESTONES IN BIOLOGICAL RESEARCH Peyton Rous: Homage and Appraisal , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[53]  D. Lane,et al.  T antigen is bound to a host protein in SY40-transformed cells , 1979, Nature.

[54]  Garrison Fh,et al.  [History of cancer]. , 1926, Il Policlinico. Sezione pratica.

[55]  Deanna Cross,et al.  Gene therapy for cancer treatment: past, present and future. , 2006, Clinical medicine & research.

[56]  H. Temin THE EFFECTS OF ACTINOMYCIN D ON GROWTH OF ROUS SARCOMA VIRUS IN VITRO. , 1963, Virology.

[57]  Margaret E McLaughlin-Drubin,et al.  Viruses associated with human cancer. , 2008, Biochimica et biophysica acta.

[58]  J. Hesser,et al.  The relation of infection with the hepatitis B agent to primary hepatic carcinoma. , 1975, The American journal of pathology.

[59]  D. Lowy,et al.  Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Alemany Cancer selective adenoviruses. , 2007, Molecular aspects of medicine.

[61]  S. Jablonska,et al.  Epidermodysplasia verruciformis as a model in studies on the role of papovaviruses in oncogenesis. , 1972, Cancer research.

[62]  K. Helin,et al.  The role of p53 and pRB in apoptosis and cancer. , 2002, Current opinion in genetics & development.

[63]  P. Vogt,et al.  Differences between the Ribonucleic Acids of Transforming and Nontransforming Avian Tumor Viruses* , 1970, Proceedings of the National Academy of Sciences.

[64]  P. Tiollais,et al.  Hepatitis B virus. , 1991, Scientific American.

[65]  M. Houghton,et al.  Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. , 1989, Science.

[66]  P. Rous,et al.  A TRANSMISSIBLE AVIAN NEOPLASM. (SARCOMA OF THE COMMON FOWL.) , 1910, The Journal of experimental medicine.

[67]  E. Keogh Ectodermal Lesions Produced by the Virus of Rous Sarcoma. , 1938 .

[68]  V. Ellermann,et al.  Experimentelle Leukämie bei Hühnern. II , 1909, Zeitschrift für Hygiene und Infektionskrankheiten.

[69]  G. T. Diamandopoulos Cancer: an historical perspective. , 1996, Anticancer Research.

[70]  J J Bittner,et al.  SOME POSSIBLE EFFECTS OF NURSING ON THE MAMMARY GLAND TUMOR INCIDENCE IN MICE. , 1936, Science.

[71]  Blossom Damania,et al.  Infectious agents and cancer: criteria for a causal relation. , 2004, Seminars in cancer biology.

[72]  W. Henle,et al.  Immunofluorescence in Cells Derived from Burkitt's Lymphoma , 1966, Journal of bacteriology.

[73]  Jules L. Dienstag,et al.  An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis , 1989 .

[74]  L. Gissmann,et al.  A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[75]  R. Weinberg,et al.  The retinoblastoma protein and cell cycle control , 1995, Cell.

[76]  Lu-Yu Hwang,et al.  HEPATOCELLULAR CARCINOMA AND HEPATITIS B VIRUS A Prospective Study of 22 707 Men in Taiwan , 1981, The Lancet.

[77]  L. Gross “Spontaneous” Leukemia Developing in G3H Mice Following Inoculation, In Infancy, with AK-Emkemic.∗ , 1951 .

[78]  M. Epstein,et al.  MORPHOLOGICAL AND BIOLOGICAL STUDIES ON A VIRUS IN CULTURED LYMPHOBLASTS FROM BURKITT'S LYMPHOMA , 1965, The Journal of experimental medicine.

[79]  M. Lai,et al.  Universal hepatitis B vaccination in Taiwan and the incidence of hepatocellular carcinoma in children. Taiwan Childhood Hepatoma Study Group. , 1997, The New England journal of medicine.

[80]  C. Der,et al.  Transforming genes of human bladder and lung carcinoma cell lines are homologous to the ras genes of Harvey and Kirsten sarcoma viruses. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[81]  J. Butel,et al.  Viral carcinogenesis: revelation of molecular mechanisms and etiology of human disease. , 2000, Carcinogenesis.

[82]  M. Hilleman,et al.  Vaccine against human hepatitis B. , 1976, JAMA.

[83]  J. Nemunaitis,et al.  A prospective phase II trial of ONYX-015 adenovirus and chemotherapy in recurrent squamous cell carcinoma of the head and neck (the baylor experience) , 2000, Annals of Surgical Oncology.

[84]  L. Strong,et al.  Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. , 1990, Science.

[85]  Stephen H. Friend,et al.  Association between an oncogene and an anti-oncogene: the adenovirus E1A proteins bind to the retinoblastoma gene product , 1988, Nature.

[86]  R. Garcea,et al.  Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles , 1993, Journal of virology.

[87]  R. Weinberg,et al.  Human EJ bladder carcinoma oncogene is homologue of Harvey sarcoma virus ras gene , 1982, Nature.

[88]  Chun-Jen Liu,et al.  Viral hepatocarcinogenesis: from infection to cancer , 2008, Liver international : official journal of the International Association for the Study of the Liver.

[89]  I. Tannock,et al.  A controlled trial of intratumoral ONYX-015, a selectively-replicating adenovirus, in combination with cisplatin and 5-fluorouracil in patients with recurrent head and neck cancer , 2000, Nature Medicine.

[90]  A. Graffi CHLOROLEUKEMIA OF MICE , 1957, Annals of the New York Academy of Sciences.

[91]  R. Huebner,et al.  Oncogenes of RNA tumor viruses as determinants of cancer. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[92]  S. Mizutani,et al.  RNA-dependent DNA polymerase in virions of Rous sarcoma virus. , 1970, Nature.

[93]  R. Shope,et al.  INFECTIOUS PAPILLOMATOSIS OF RABBITS : WITH A NOTE ON THE HISTOPATHOLOGY , 1933 .

[94]  Wen-Hwa Lee,et al.  SV40 large tumor antigen forms a specific complex with the product of the retinoblastoma susceptibility gene , 1988, Cell.

[95]  H. Hausen Papillomaviruses and cancer: from basic studies to clinical application , 2002, Nature Reviews Cancer.

[96]  G. Martin,et al.  The road to Src , 2004, Oncogene.

[97]  P. Rous,et al.  THE PROGRESSION TO CARCINOMA OF VIRUS-INDUCED RABBIT PAPILLOMAS (SHOPE) , 1935, The Journal of experimental medicine.

[98]  P. Rous,et al.  A SARCOMA OF THE FOWL TRANSMISSIBLE BY AN AGENT SEPARABLE FROM THE TUMOR CELLS , 1911, Journal of Experimental Medicine.

[99]  R. Dulbecco Cell transformation by viruses. , 1969, Science.

[100]  C. Kardinal,et al.  A conceptual history of cancer. , 1979, Seminars in oncology.

[101]  I. Frazer,et al.  Expression of vaccinia recombinant HPV 16 L1 and L2 ORF proteins in epithelial cells is sufficient for assembly of HPV virion-like particles. , 1991, Virology.

[102]  R. Weinberg,et al.  The Biology of Cancer , 2006 .

[103]  M A Epstein,et al.  Historical background. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[104]  H. Temin THE PARTICIPATION OF DNA IN ROUS SARCOMA VIRUS PRODUCTION. , 1964, Virology.

[105]  W. Lee,et al.  Human retinoblastoma susceptibility gene: cloning, identification, and sequence , 1987, Science.

[106]  Harald zur Hausen,et al.  Papillomavirus infections — a major cause of human cancers , 1996 .

[107]  R. Huebner,et al.  Isolation of a Cytopathogenic Agent from Human Adenoids Undergoing Spontaneous Degeneration in Tissue Culture , 1953, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[108]  M. Houghton,et al.  PREVALENCE OF ANTIBODIES TO HEPATITIS C VIRUS IN ITALIAN PATIENTS WITH HEPATOCELLULAR CARCINOMA , 1989, The Lancet.

[109]  John B Liao,et al.  Viruses and Human Cancer , 2006, The Yale journal of biology and medicine.

[110]  G. E. Grubbs,et al.  Identification of the oncogenic substance in rhesus monkey kidney cell culture as simian virus 40. , 1962, Virology.

[111]  D. Lowy,et al.  Prospects for cervical cancer prevention by human papillomavirus vaccination. , 2006, Cancer research.

[112]  L. Gross A Filterable Agent, Recovered from Ak Leukemic Extracts, Causing Salivary Gland Carcinomas in C3H Mice.∗ , 1953, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[113]  A. Levine,et al.  The p53 proto-oncogene can act as a suppressor of transformation , 1989, Cell.