The origin, dynamics, and molecular evolution of transmissible cancers

Three transmissible cancers are known to have emerged naturally in the wild: canine transmissible venereal tumor (CTVT); Tasmanian devil facial tumor disease (DFTD); and a recently discovered leukemia-like cancer in soft-shell clams (Mya arenaria). These cancers have all acquired the ability to pass between individuals. DFTD emerged approximately 20 years ago and has decimated the Tasmanian devil population. CTVT arose over 10,000 years ago in an ancient breed of dog. The clam cancer is believed to have evolved at least 40 years ago. In this manuscript, we review CTVT and DFTD, the two transmissible mammalian cancers, and provide an overview of the leukemia-like cancer of clams. We showcase how genetics and genomics have enhanced our understanding of the unique biology, origins, and evolutionary histories of these rare cancers.

[1]  S. Goff,et al.  Horizontal Transmission of Clonal Cancer Cells Causes Leukemia in Soft-Shell Clams , 2015, Cell.

[2]  H. Siddle,et al.  Immunology of naturally transmissible tumours , 2014, Immunology.

[3]  S. Goff,et al.  Activation of transcription and retrotransposition of a novel retroelement, Steamer, in neoplastic hemocytes of the mollusk Mya arenaria , 2014, Proceedings of the National Academy of Sciences.

[4]  E. Murchison,et al.  The changing global distribution and prevalence of canine transmissible venereal tumour , 2014, BMC Veterinary Research.

[5]  L. Floeter-Winter,et al.  Leishmania sp. Amastigotes Identification in Canine Transmissible Venereal Tumor , 2014 .

[6]  S. Bettiol,et al.  Mouse Model of Devil Facial Tumour Disease Establishes That an Effective Immune Response Can be Generated Against the Cancer Cells , 2014, Front. Immunol..

[7]  C. Hanemann,et al.  Schwannomas and Their Pathogenesis , 2014, Brain pathology.

[8]  E. Hosseini,et al.  Retraction Note to: Canine transmissible venereal tumor and seminoma: a cytohistopathology and chemotherapy study of tumors in the growth phase and during regression after chemotherapy , 2014, Tumor Biology.

[9]  Peter J. Campbell,et al.  Transmissible Dog Cancer Genome Reveals the Origin and History of an Ancient Cell Lineage , 2014, Science.

[10]  Menna E. Jones,et al.  Anthropogenic selection enhances cancer evolution in Tasmanian devil tumours , 2013, Evolutionary applications.

[11]  H. Siddle,et al.  A tale of two tumours: Comparison of the immune escape strategies of contagious cancers☆ , 2013, Molecular immunology.

[12]  Menna E. Jones,et al.  Reversible epigenetic down-regulation of MHC molecules by devil facial tumour disease illustrates immune escape by a contagious cancer , 2013, Proceedings of the National Academy of Sciences.

[13]  M. Tsai,et al.  Gene-expression profiling to identify genes related to spontaneous tumor regression in a canine cancer model. , 2013, Veterinary immunology and immunopathology.

[14]  A. Papenfuss,et al.  Evolution of a contagious cancer: epigenetic variation in Devil Facial Tumour Disease , 2013, Proceedings of the Royal Society B: Biological Sciences.

[15]  P. Jallepalli,et al.  Chromothripsis: chromosomes in crisis. , 2012, Developmental cell.

[16]  Peter J. Campbell,et al.  Evolution of the cancer genome , 2012, Nature Reviews Genetics.

[17]  Stephen P. Jackson,et al.  Chromothripsis and cancer: causes and consequences of chromosome shattering , 2012, Nature Reviews Cancer.

[18]  K. Polyak,et al.  Intra-tumour heterogeneity: a looking glass for cancer? , 2012, Nature Reviews Cancer.

[19]  Menna E. Jones,et al.  Low MHC class II diversity in the Tasmanian devil (Sarcophilus harrisii) , 2012, Immunogenetics.

[20]  K. Belov,et al.  Evolution in a transmissible cancer: a study of the chromosomal changes in devil facial tumor (DFT) as it spreads through the wild Tasmanian devil population. , 2012, Cancer genetics.

[21]  Carolyn Tregidgo,et al.  Genome Sequencing and Analysis of the Tasmanian Devil and Its Transmissible Cancer , 2012, Cell.

[22]  C. Amemiya,et al.  Genomic Restructuring in the Tasmanian Devil Facial Tumour: Chromosome Painting and Gene Mapping Provide Clues to Evolution of a Transmissible Tumour , 2012, PLoS genetics.

[23]  T. Davoli,et al.  The causes and consequences of polyploidy in normal development and cancer. , 2011, Annual review of cell and developmental biology.

[24]  K. Belov,et al.  Allorecognition in the Tasmanian Devil (Sarcophilus harrisii), an Endangered Marsupial Species with Limited Genetic Diversity , 2011, PloS one.

[25]  John Trowsdale,et al.  The MHC, disease and selection. , 2011, Immunology letters.

[26]  Tom H. Pringle,et al.  Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil) , 2011, Proceedings of the National Academy of Sciences.

[27]  J. S. Welsh Contagious Cancer , 2011, The oncologist.

[28]  Mingming Jia,et al.  COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer , 2010, Nucleic Acids Res..

[29]  Menna E. Jones,et al.  MHC gene copy number variation in Tasmanian devils: implications for the spread of a contagious cancer , 2010, Proceedings of the Royal Society B: Biological Sciences.

[30]  Menna E. Jones,et al.  Evaluation of Selective Culling of Infected Individuals to Control Tasmanian Devil Facial Tumor Disease , 2010, Conservation biology : the journal of the Society for Conservation Biology.

[31]  A. C. Alessi,et al.  Reactivity of p53 protein in canine transmissible venereal tumor , 2010 .

[32]  Manolis Kellis,et al.  The Tasmanian Devil Transcriptome Reveals Schwann Cell Origins of a Clonally Transmissible Cancer , 2009, Science.

[33]  Shelly Lachish,et al.  Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction. , 2009, Ecology.

[34]  A. Burt,et al.  Extensive conservation of genomic imbalances in canine transmissible venereal tumors (CTVT) detected by microarray-based CGH analysis , 2009, Chromosome Research.

[35]  A. Burt,et al.  Origins and Evolution of a Transmissible Cancer , 2009, Evolution; international journal of organic evolution.

[36]  A. Kreiss,et al.  The humoral immune response of the Tasmanian devil (Sarcophilus harrisii) against horse red blood cells. , 2009, Veterinary immunology and immunopathology.

[37]  H. McCallum,et al.  Tasmanian devil facial tumour disease: lessons for conservation biology. , 2008, Trends in ecology & evolution.

[38]  K. Liao,et al.  Interactions of host IL-6 and IFN-γ and cancer-derived TGF-β1 on MHC molecule expression during tumor spontaneous regression , 2008, Cancer Immunology, Immunotherapy.

[39]  R. Fajardo,et al.  The T963C mutation of TP53 gene does not participate in the clonal origin of canine TVT , 2008, Veterinary Research Communications.

[40]  S. Otto,et al.  The Evolutionary Consequences of Polyploidy , 2007, Cell.

[41]  Katherine Belov,et al.  Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial , 2007, Proceedings of the National Academy of Sciences.

[42]  Clare E. Hawkins,et al.  Distribution and Impacts of Tasmanian Devil Facial Tumor Disease , 2007, EcoHealth.

[43]  Shelly Lachish,et al.  The impact of disease on the survival and population growth rate of the Tasmanian devil. , 2007, The Journal of animal ecology.

[44]  H. Muller,et al.  The Immune Response of the Tasmanian Devil (Sarcophilus harrisii) and Devil Facial Tumour Disease , 2007, EcoHealth.

[45]  L. Zitvogel,et al.  Selective Resistance of Tetraploid Cancer Cells against DNA Damage‐Induced Apoptosis , 2006, Annals of the New York Academy of Sciences.

[46]  R. Sharpe,et al.  The Pathology of Devil Facial Tumor Disease (DFTD) in Tasmanian Devils (Sarcophilus harrisii) , 2006, Veterinary pathology.

[47]  A. O'hara,et al.  The Immunohistochemical Characterization of Devil Facial Tumor Disease (DFTD) in the Tasmanian Devil (Sarcophilus harrisii) , 2006, Veterinary pathology.

[48]  Robin A. Weiss,et al.  Clonal Origin and Evolution of a Transmissible Cancer , 2006, Cell.

[49]  Clare E. Hawkins,et al.  Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii , 2006 .

[50]  A. Pearse,et al.  Allograft theory: Transmission of devil facial-tumour disease , 2006, Nature.

[51]  I. Cangul,et al.  A Clinico-pathological study on the effect of vincristine on transmissible venereal tumour in dogs. , 2005, Journal of veterinary medicine. A, Physiology, pathology, clinical medicine.

[52]  Menna E. Jones,et al.  Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore , 2004, Molecular ecology.

[53]  K. Liao,et al.  Tumor-Infiltrating Lymphocyte Secretion of IL-6 Antagonizes Tumor-Derived TGF-β1 and Restores the Lymphokine-Activated Killing Activity1 , 2004, The Journal of Immunology.

[54]  M. Gramiccia,et al.  Canine Transmissible Venereal Tumour Parasitized by Leishmania infantum , 2003, Veterinary Research Communications.

[55]  S. Mukaratirwa,et al.  Canine transmissible venereal tumour: Cytogenetic origin, immunophenotype, and immunobiology. A review , 2003, The Veterinary quarterly.

[56]  Chul-Joong Kim,et al.  Sequence analysis of canine LINE-1 elements and p53 gene in canine transmissible venereal tumor. , 2002, Journal of veterinary science.

[57]  F. Abramo,et al.  Primary cutaneous extragenital canine transmissible venereal tumour with Leishmania-laden neoplastic cells: a further suggestion of histiocytic origin? , 2002, Veterinary dermatology.

[58]  W. Marks,et al.  Transplant tumor registry: donor related malignancies , 2002, Transplantation.

[59]  K. Liao,et al.  Effect of tumor infiltrating lymphocytes on the expression of MHC molecules in canine transmissible venereal tumor cells. , 2002, Veterinary immunology and immunopathology.

[60]  T. Sun,et al.  Heat shock proteins in canine transmissible venereal tumor. , 2001, Veterinary immunology and immunopathology.

[61]  A. Das,et al.  Review of Canine Transmissible Venereal Sarcoma , 2000, Veterinary Research Communications.

[62]  S. Griffey,et al.  Canine transmissible venereal tumour: a morphological and immunohistochemical study of 11 tumours in growth phase and during regression after chemotherapy. , 2000, Journal of comparative pathology.

[63]  M. Day,et al.  Immunohistochemical study of the local inflammatory infiltrate in spontaneous canine transmissible venereal tumour at different stages of growth. , 1998, Veterinary immunology and immunopathology.

[64]  D. Rigal,et al.  Immunophenotype of the canine transmissible venereal tumour. , 1997, Veterinary immunology and immunopathology.

[65]  A. Méndez,et al.  Immunohistochemical Characterization of Canine Transmissible Venereal Tumor , 1996, Veterinary pathology.

[66]  C. Janeway Immunobiology: The Immune System in Health and Disease , 1996 .

[67]  J. Ting,et al.  Regulation of MHC gene expression. , 1993, Current opinion in immunology.

[68]  J. Agger,et al.  Risk factors associated with canine transmissible venereal tumour in Tanzania , 1992 .

[69]  J. Pound,et al.  Modulation of MHC antigen expression by viruses and oncogenes , 1991, Immunology Today.

[70]  F. Cleton Evolution of Cancer , 1991, British Journal of Cancer.

[71]  M. Yoshida,et al.  Chromosome analysis of canine transmissible sarcoma cells. , 1989, Zentralblatt fur Veterinarmedizin. Reihe A.

[72]  J. Chandler,et al.  Growth stage dependent expression of MHC antigens on the canine transmissible venereal sarcoma. , 1987, British Journal of Cancer.

[73]  J. B. Cohen,et al.  "Retroposon" insertion into the cellular oncogene c-myc in canine transmissible venereal tumor. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[74]  A. L. Idowu,et al.  A retrospective evaluation of four surgical methods of treating canine transmissible venereal tumour , 1984 .

[75]  A. Shalev,et al.  Lack of beta 2-microglobulin on the surface of canine transmissible venereal tumor cells. , 1984, Journal of the National Cancer Institute.

[76]  D. L. Hill,et al.  Canine Transmissible Venereal Sarcoma: Tumor Cell and Infiltrating Leukocyte Ultrastructure at Different Growth Stages , 1984, Veterinary pathology.

[77]  D. Thrall,et al.  ORTHOVOLTAGE RADIOTHERAPY OF CANINE TRANSMISSIBLE VENEREAL TUMORS , 1982 .

[78]  E. Macewen,et al.  Chemotherapeutic management of transmissible venereal tumors in 30 dogs. , 1980, Journal of the American Veterinary Medical Association.

[79]  Cockrill Jm,et al.  Transmission of transmissible venereal tumor of the dog to the coyote. , 1979 .

[80]  T. Cavalier-smith,et al.  Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. , 1978, Journal of cell science.

[81]  Ndiritu Cg,et al.  Extragenitally located transmissible venereal tumor in dogs. , 1977 .

[82]  S. Saila,et al.  PREVALENCE OF NEOPLASIA IN 10 NEW ENGLAND POPULATIONS OF THE SOFT‐SHELL CLAM (MYA ARENARIA) * , 1977, Annals of the New York Academy of Sciences.

[83]  P P Yevich,et al.  NEOPLASIA IN SOFT‐SHELL CLAMS (MY A ARENARIA) COLLECTED FROM OIL‐IMPACTED SITES , 1977, Annals of the New York Academy of Sciences.

[84]  T. J. Yang,et al.  Canine transmissible venereal sarcoma: transplantation studies in neonatal and adult dogs. , 1973, Journal of the National Cancer Institute.

[85]  M. Oshimura,et al.  Chromosomal banding patterns in primary and transplanted venereal tumors of the dog. , 1973, Journal of the National Cancer Institute.

[86]  D. Cohen,et al.  The biological behaviour of the transmissible venereal tumour in immunosuppressed dogs. , 1973, European journal of cancer.

[87]  D. Cohen Detection of humoral antibody to the transmissible venereal tumour of the dog , 1972, International journal of cancer.

[88]  G Barski,et al.  Cytogenetic study of Sticker venereal sarcoma in European dogs. , 1966, Journal of the National Cancer Institute.

[89]  D. A. Higgins Observations on the canine transmissible venereal tumour as seen in the Bahamas , 1966, Veterinary Record.

[90]  H. Cooper,et al.  Mosquito Transmission of a Reticulum Cell Sarcoma of Hamsters , 1965, Science.

[91]  H. Cooper,et al.  CHROMOSOME STUDIES OF A CONTAGIOUS RETICULUM CELL SARCOMA OF THE SYRIAN HAMSTER. , 1964, Journal of the National Cancer Institute.

[92]  S. Makino SOME EPIDEMIOLOGIC ASPECTS OF VENEREAL TUMORS OF DOGS AS REVEALED BY CHROMOSOME AND DNA STUDIES , 1963, Annals of the New York Academy of Sciences.

[93]  W. Banfield,et al.  A Contagious Tumor of the Hamster , 1961 .

[94]  A G KARLSON,et al.  THE TRANSMISSIBLE VENEREAL TUMOR OF DOGS: OBSERVATIONS ON FORTY GENERATIONS OF EXPERIMENTAL TRANSFERS , 1952, Annals of the New York Academy of Sciences.

[95]  R. Ashbel Spontaneous Transmissible Tumours in the Syrian Hamster , 1945, Nature.

[96]  Dr. med. Anton Sticker Transplantables Rundzellensarkom des Hundes , 1906, Zeitschrift für Krebsforschung.

[97]  Menna E. Jones,et al.  Biting injuries and transmission of Tasmanian devil facial tumour disease. , 2013, The Journal of animal ecology.

[98]  磯田 健志 Immunologically silent cancer clone transmission from mother to offspring , 2012 .

[99]  S. Plotkin Neurofibromatosis Type 2 , 2009 .

[100]  J. Bergfeld,et al.  Assessment of cellular immune responses of healthy and diseased Tasmanian devils (Sarcophilus harrisii). , 2008, Developmental and comparative immunology.

[101]  M. Martins,et al.  The Canine Transmissible Venereal Tumor : Etiology , Pathology , Diagnosis and Treatment , 2005 .

[102]  F. Garrido,et al.  Immunoselection by T lymphocytes generates repeated MHC class I‐deficient metastatic tumor variants , 2001, International Journal of Cancer.

[103]  水野 信哉,et al.  Role of lymphocytes in dogs experimentally re-challenged with canine transmissible sarcoma. , 1989 .

[104]  D. Cohen The canine transmissible venereal tumor: a unique result of tumor progression. , 1985, Advances in cancer research.

[105]  J. Beasley,et al.  Transmission of transmissible venereal tumor of the dog to the coyote. , 1979, American journal of veterinary research.

[106]  D. Cohen The transmissible venereal tumor of the dog--a naturally occurring allograft? A review. , 1978, Israel journal of medical sciences.

[107]  G A White,et al.  Transmissible venereal tumor in a dog. , 1976, Veterinary medicine, small animal clinician : VM, SAC.

[108]  R. Epstein,et al.  Histocompatibility typing and course of canine venereal tumors transplanted into unmodified random dogs. , 1974, Cancer research.

[109]  B. Bennett TRANSPLANTATION IMMUNOGENETICS OF THE CANINE TRANSMISSIBLE VENEREAL TUMOR. , 1974 .

[110]  H. Wade An experimental investigation of infective sarcoma of the dog, with a consideration of its relationship to cancer , 1908 .