Translation of new cancer treatments from pet dogs to humans

Naturally occurring cancers in pet dogs and humans share many features, including histological appearance, tumour genetics, molecular targets, biological behaviour and response to conventional therapies. Studying dogs with cancer is likely to provide a valuable perspective that is distinct from that generated by the study of human or rodent cancers alone. The value of this opportunity has been increasingly recognized in the field of cancer research for the identification of cancer-associated genes, the study of environmental risk factors, understanding tumour biology and progression, and, perhaps most importantly, the evaluation and development of novel cancer therapeutics.

[1]  M. Maeda,et al.  Overexpression of the p53 gene product in canine mammary tumors. , 2001, Oncology reports.

[2]  M. Mehren Beyond imatinib: second generation c-KIT inhibitors for the management of gastrointestinal stromal tumors. , 2006 .

[3]  K. Harvey,et al.  The Salvador–Warts–Hippo pathway — an emerging tumour-suppressor network , 2007, Nature Reviews Cancer.

[4]  R. Dubielzig,et al.  Liposome-encapsulated muramyl tripeptide phosphatidylethanolamine adjuvant immunotherapy for splenic hemangiosarcoma in the dog: a randomized multi-institutional clinical trial. , 1995, Clinical cancer research : an official journal of the American Association for Cancer Research.

[5]  T. Potter,et al.  Expression of bacterial superantigen genes in mice induces localized mononuclear cell inflammatory responses. , 1997, The Journal of clinical investigation.

[6]  G. Dakubo,et al.  Clinical implications and utility of field cancerization , 2007, Cancer Cell International.

[7]  M. Kris,et al.  Phase I Study of Inhaled Doxorubicin for Patients with Metastatic Tumors to the Lungs , 2007, Clinical Cancer Research.

[8]  P. Olson Using the canine genome to cure cancer and other diseases. , 2007, Theriogenology.

[9]  K. Hahn,et al.  Ferret oncology: diseases, diagnostics, and therapeutics. , 2004, The veterinary clinics of North America. Exotic animal practice.

[10]  A. Avery,et al.  Determining the significance of persistent lymphocytosis. , 2007, The Veterinary clinics of North America. Small animal practice.

[11]  B. Powers,et al.  Comparative aspects of osteosarcoma. Dog versus man. , 1991, Clinical orthopaedics and related research.

[12]  M. Henriksson,et al.  The Myc oncoprotein as a therapeutic target for human cancer. , 2006, Seminars in cancer biology.

[13]  E. Benjamini,et al.  Chemoimmunotherapy for canine lymphosarcoma , 1977, Cancer.

[14]  L. Glickman,et al.  Comparative longevity of pet dogs and humans: implications for gerontology research. , 1997, The journals of gerontology. Series A, Biological sciences and medical sciences.

[15]  H J Muller,et al.  ARTIFICIAL TRANSMUTATION OF THE GENE. , 1927, Science.

[16]  H. Joensuu,et al.  Bcl-2 protein expression and long-term survival in breast cancer. , 1994, The American journal of pathology.

[17]  A. Hart,et al.  Canine mammary cancer. II. Therapy and causes of death. , 1979, The Journal of small animal practice.

[18]  S. Galli,et al.  Spontaneous canine mast cell tumors express tandem duplications in the proto-oncogene c-kit. , 1999, Experimental hematology.

[19]  J. Modiano,et al.  The molecular basis of canine melanoma: pathogenesis and trends in diagnosis and therapy. , 1999, Journal of veterinary internal medicine.

[20]  H. Horvitz,et al.  Genetic control of programmed cell death in the nematode C. elegans , 1986, Cell.

[21]  E. Macewen,et al.  Spontaneously Occurring Tumors of Companion Animals as Models for Human Cancer , 2000, Cancer investigation.

[22]  R. Matus,et al.  Canine oral melanoma: comparison of surgery versus surgery plus Corynebacterium parvum. , 1986, Cancer investigation.

[23]  William A. Lee,et al.  GS-9219—A Novel Acyclic Nucleotide Analogue with Potent Antineoplastic Activity in Dogs with Spontaneous Non–Hodgkin's Lymphoma , 2008, Clinical Cancer Research.

[24]  R. Storb,et al.  Marrow Engraftment by Allogeneic Leukocytes in Lethally Irradiated Dogs , 1967 .

[25]  Eric T. Rosenthal,et al.  Cyclin: A protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division , 1983, Cell.

[26]  S. George,et al.  Intra‐arterial cisplatin with or without radiation in limb‐sparing for canine osteosarcoma , 1993, Cancer.

[27]  G. Ogilvie,et al.  Evaluation of single-agent chemotherapy for treatment of clinically evident osteosarcoma metastases in dogs: 45 cases (1987-1991). , 1993, Journal of the American Veterinary Medical Association.

[28]  E. Benjamini,et al.  TUMOR VACCINES FOR IMMUNOTHERAPY OF CANINE LYMPHOSARCOMA * , 1976, Annals of the New York Academy of Sciences.

[29]  P. Steerenberg,et al.  Equine sarcoid: BCG immunotherapy compared to cryosurgery in a prospective randomised clinical trial , 2004, Cancer Immunology, Immunotherapy.

[30]  S. Fosmire,et al.  Expression and Significance of p53, Rb, p21/waf-1, p16/ink-4a, and PTEN Tumor Suppressors in Canine Melanoma , 2002, Veterinary pathology.

[31]  H. Pehamberger,et al.  Comparative histopathology of grey-horse-melanoma and human malignant melanoma. , 2004, Pigment cell research.

[32]  C. London,et al.  Treatment of canine mast cell tumors with CCNU (lomustine). , 1999, Journal of veterinary internal medicine.

[33]  N. Shenoy,et al.  Phase I dose-escalating study of SU11654, a small molecule receptor tyrosine kinase inhibitor, in dogs with spontaneous malignancies. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[34]  T. Potter,et al.  In vivo tumor transfection with superantigen plus cytokine genes induces tumor regression and prolongs survival in dogs with malignant melanoma. , 1998, The Journal of clinical investigation.

[35]  P. Anderson,et al.  Aerosolized Granulocyte Macrophage Colony-Stimulating Factor (GM-CSF) Therapy in Metastatic Cancer , 2003, American journal of clinical oncology.

[36]  James A. Cuff,et al.  Genome sequence, comparative analysis and haplotype structure of the domestic dog , 2005, Nature.

[37]  R. Hicks,et al.  Multicenter phase II clinical study of iodine-131-rituximab radioimmunotherapy in relapsed or refractory indolent non-Hodgkin's lymphoma. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[38]  B. Fuchs,et al.  Comparative biology of human and canine osteosarcoma. , 2007, Anticancer research.

[39]  J. Sloan,et al.  Aerosol granulocyte macrophage-colony stimulating factor: a low toxicity, lung-specific biological therapy in patients with lung metastases. , 1999, Clinical cancer research : an official journal of the American Association for Cancer Research.

[40]  P. Anderson,et al.  Nebulized Interleukin 2 Liposomes: Aerosol Characteristics and Biodistribution , 1997, The Journal of pharmacy and pharmacology.

[41]  E. Kleinerman,et al.  Efficacy of Liposomal Muramyl Tripeptide (CGP 19835A) in the Treatment of Relapsed Osteosarcoma , 1995, American journal of clinical oncology.

[42]  Robert A. Weinberg,et al.  Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes , 1983, Nature.

[43]  E. Kleinerman Biologic therapy for osteosarcoma using liposome-encapsulated muramyl tripeptide. , 1995, Hematology/oncology clinics of North America.

[44]  L. Ferrer,et al.  Canine mast cell tumors express stem cell factor receptor. , 2000, The American Journal of dermatopathology.

[45]  M. Sznol,et al.  Systemic Administration of an Attenuated, Tumor-Targeting Salmonella typhimurium to Dogs with Spontaneous Neoplasia: Phase I Evaluation , 2005, Clinical Cancer Research.

[46]  G. Ogilvie,et al.  Acute and short-term toxicoses associated with the administration of doxorubicin to dogs with malignant tumors. , 1989, Journal of the American Veterinary Medical Association.

[47]  J. Wolchok,et al.  Development of a xenogeneic DNA vaccine program for canine malignant melanoma at the Animal Medical Center. , 2006, Vaccine.

[48]  A. Gudkov,et al.  Paradoxical role of apoptosis in tumor progression , 2003, Journal of cellular biochemistry.

[49]  Spatial accuracy of fractionated IMRT delivery studies in canine paraspinal irradiation. , 2003, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[50]  A. Hershey,et al.  Aberrant p53 Expression in Feline Vaccine-associated Sarcomas and Correlation with Prognosis , 2005, Veterinary pathology.

[51]  S. Dow,et al.  Genetic immunotherapy for cancer. , 1997, Seminars in veterinary medicine and surgery.

[52]  J. Fraumeni,et al.  Epidemiological features of canine renal neoplasms. , 1977, Cancer research.

[53]  A. Hershey,et al.  Inhalation chemotherapy for macroscopic primary or metastatic lung tumors: proof of principle using dogs with spontaneously occurring tumors as a model. , 1999, Clinical cancer research : an official journal of the American Association for Cancer Research.

[54]  M. Dewhirst Animal modeling and thermal dose. , 1989, Radiologic clinics of North America.

[55]  F. Galibert,et al.  Chromosome aberrations in canine multicentric lymphomas detected with comparative genomic hybridisation and a panel of single locus probes , 2003, British Journal of Cancer.

[56]  E. Kleinerman,et al.  Osteosarcoma: a randomized, prospective trial of the addition of ifosfamide and/or muramyl tripeptide to cisplatin, doxorubicin, and high-dose methotrexate. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[57]  I. Narama,et al.  Mast Cell Tumors of the Gastrointestinal Tract in 39 Dogs , 2002, Veterinary pathology.

[58]  D. J. Waters,et al.  Cancer clues from pet dogs. , 2006, Scientific American.

[59]  A. Porrello,et al.  Oncology of companion animals as a model for humans. an overview of tumor histotypes. , 2006, Journal of experimental & clinical cancer research : CR.

[60]  V. Yuzbasiyan-Gurkan,et al.  Mutations in the Juxtamembrane Domain of c-KIT Are Associated with Higher Grade Mast Cell Tumors in Dogs , 2002, Veterinary pathology.

[61]  I. Kola,et al.  Can the pharmaceutical industry reduce attrition rates? , 2004, Nature Reviews Drug Discovery.

[62]  S. Cory,et al.  The Bcl-2 apoptotic switch in cancer development and therapy , 2007, Oncogene.

[63]  B. Edgar,et al.  From Cell Structure to Transcription: Hippo Forges a New Path , 2006, Cell.

[64]  R. Storb,et al.  Canine models of bone marrow transplantation. , 1990, Laboratory animal science.

[65]  S. Hewitt,et al.  A randomized controlled trial of octreotide pamoate long-acting release and carboplatin versus carboplatin alone in dogs with naturally occurring osteosarcoma: evaluation of insulin-like growth factor suppression and chemotherapy. , 2002, Clinical cancer research : an official journal of the American Association for Cancer Research.

[66]  M. Höglund Bladder cancer, a two phased disease? , 2007, Seminars in cancer biology.

[67]  N. Pryer,et al.  Proof of target for SU11654: inhibition of KIT phosphorylation in canine mast cell tumors. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[68]  P. Anderson,et al.  Aerosol therapy for malignancy involving the lungs. , 2003, Current cancer drug targets.

[69]  P. Anderson,et al.  Interleukin‐2 liposome inhalation therapy is safe and effective for dogs with spontaneous pulmonary metastases , 1997, Cancer.

[70]  S. Mukaratirwa Prognostic and predictive markers in canine tumours: Rationale and relevance. A review , 2005, The Veterinary quarterly.

[71]  A. Avery,et al.  Diagnosis of mediastinal masses in dogs by flow cytometry. , 2006, Journal of veterinary internal medicine.

[72]  J. Wolchok,et al.  Vaccination with human tyrosinase DNA induces antibody responses in dogs with advanced melanoma. , 2006, Cancer immunity.

[73]  F. Haviv,et al.  Preclinical Evaluation of Antiangiogenic Thrombospondin-1 Peptide Mimetics, ABT-526 and ABT-510, in Companion Dogs with Naturally Occurring Cancers , 2006, Clinical Cancer Research.

[74]  B. Edgar,et al.  Filling out the Hippo pathway , 2007, Nature Reviews Molecular Cell Biology.

[75]  R. Dummer,et al.  Intratumoral injection of DNA encoding human interleukin 12 into patients with metastatic melanoma: clinical efficacy. , 2005, Human gene therapy.

[76]  H. Hydén,et al.  A receptor for phosphatidylserine-specific clearance of apoptotic cells , 2000, Nature.

[77]  E. Kirkness,et al.  A mutation in the canine BHD gene is associated with hereditary multifocal renal cystadenocarcinoma and nodular dermatofibrosis in the German Shepherd dog. , 2003, Human molecular genetics.

[78]  D. Thamm,et al.  Does L-asparaginase influence efficacy or toxicity when added to a standard CHOP protocol for dogs with lymphoma? , 2005, Journal of veterinary internal medicine.

[79]  L. Nasir,et al.  Bovine papillomaviral gene expression in equine sarcoid tumours. , 1999, Virus research.

[80]  A. Nardin,et al.  Liposomal muramyl tripeptide phosphatidylethanolamine: Targeting and activating macrophages for adjuvant treatment of osteosarcoma. , 2006, Current cancer drug targets.

[81]  J. Wolchok,et al.  Long-term survival of dogs with advanced malignant melanoma after DNA vaccination with xenogeneic human tyrosinase: a phase I trial. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[82]  A. Hart,et al.  Canine mammary cancer. II. Therapy and causes of death. , 1979, The Journal of small animal practice.

[83]  E. Keller,et al.  Current studies of liposome muramyl tripeptide (CGP 19835A lipid) therapy for metastasis in spontaneous tumors: a progress review. , 1994, Journal of drug targeting.

[84]  D. Wartenberg,et al.  Environmental causes for sinonasal cancers in pet dogs, and their usefulness as sentinels of indoor cancer risk. , 1998, Journal of toxicology and environmental health. Part A.

[85]  Genomics. A dog's breakfast? , 2003, Science.

[86]  R. Storb,et al.  Lymphocyte reactivity to autochthonous tumor cells in dogs with spontaneous malignancies. , 1974, Cellular immunology.

[87]  G. Mack Cancer researchers usher in dog days of medicine , 2005, Nature Medicine.

[88]  Ewan Birney,et al.  Estimating the neutral rate of nucleotide substitution using introns. , 2006, Molecular biology and evolution.

[89]  P. Schwarz,et al.  Limb-sparing treatment for osteosarcoma in dogs. , 1989, Journal of the American Veterinary Medical Association.

[90]  R. Birge,et al.  The Presumptive Phosphatidylserine Receptor Is Dispensable for Innate Anti-inflammatory Recognition and Clearance of Apoptotic Cells* , 2006, Journal of Biological Chemistry.

[91]  B. Craig,et al.  Effects of the cyclooxygenase inhibitor, piroxicam, on tumor response, apoptosis, and angiogenesis in a canine model of human invasive urinary bladder cancer. , 2002, Cancer research.

[92]  D. Knapp,et al.  Amputation and carboplatin for treatment of dogs with osteosarcoma: 48 cases (1991 to 1993). , 1996, Journal of veterinary internal medicine.

[93]  Knapp Dw,et al.  Naturally occurring cancer in pet dogs: important models for developing improved cancer therapy for humans. , 1997 .

[94]  J. Manola,et al.  Blood-Based Biomarkers of SU11248 Activity and Clinical Outcome in Patients with Metastatic Imatinib-Resistant Gastrointestinal Stromal Tumor , 2007, Clinical Cancer Research.

[95]  R. Storb,et al.  Treatment of canine malignancies by 1200 R total body irradiation and autologous marrow grafts. , 1975, Experimental hematology.

[96]  P. Morley,et al.  Utility of polymerase chain reaction for analysis of antigen receptor rearrangement in staging and predicting prognosis in dogs with lymphoma. , 2006, Journal of veterinary internal medicine.

[97]  C. Khanna,et al.  Spontaneous and genetically engineered animal models; use in preclinical cancer drug development. , 2004, European journal of cancer.

[98]  Hazim Jaradat,et al.  The utility of megavoltage computed tomography images from a helical tomotherapy system for setup verification purposes. , 2004, International journal of radiation oncology, biology, physics.

[99]  D. Thamm,et al.  Evaluation of a 6-month chemotherapy protocol with no maintenance therapy for dogs with lymphoma. , 2002, Journal of veterinary internal medicine.

[100]  D. J. Waters High-Grade Prostatic Intraepithelial Neoplasia in Dogs , 1999, European Urology.

[101]  A. Hasegawa,et al.  Aberrations of the p53 tumor suppressor gene in various tumors in dogs. , 2001, American journal of veterinary research.

[102]  C. Khanna,et al.  Targeting the lung: preclinical and comparative evaluation of anticancer aerosols in dogs with naturally occurring cancers. , 2003, Current cancer drug targets.

[103]  J. Henkin,et al.  Cooperative Activity of Cytotoxic Chemotherapy with Antiangiogenic Thrombospondin-I Peptides, ABT-526 in Pet Dogs with Relapsed Lymphoma , 2006, Clinical Cancer Research.

[104]  Alexander Kamb,et al.  Why is cancer drug discovery so difficult? , 2007, Nature Reviews Drug Discovery.

[105]  A Dog's Breakfast? , 2003, Science.

[106]  J. Fowler,et al.  Image guidance for precise conformal radiotherapy. , 2003, International journal of radiation oncology, biology, physics.

[107]  Francis Galibert,et al.  Construction of a 2-Mb resolution BAC microarray for CGH analysis of canine tumors. , 2005, Genome research.

[108]  K. Lindblad-Toh,et al.  The dog as a cancer model , 2006, Nature Biotechnology.

[109]  Y. Ishigatsubo,et al.  Phase II study of CHOP-GR therapy for advanced-stage follicular lymphoma , 2006, Leukemia & lymphoma.

[110]  F. Kabbinavar,et al.  A phase I and pharmacokinetic study of sunitinib administered daily for 2 weeks, followed by a 1-week off period , 2008, Cancer Chemotherapy and Pharmacology.

[111]  J E Moulder,et al.  The role of photodynamic therapy in posterior fossa brain tumors. A preclinical study in a canine glioma model. , 1993, Journal of neurosurgery.

[112]  Paul R. Avery,et al.  Distinct B-cell and T-cell lymphoproliferative disease prevalence among dog breeds indicates heritable risk. , 2005, Cancer research.

[113]  M. Heinrich,et al.  Gastrointestinal stromal tumour , 2007, The Lancet.

[114]  K. Lindblad-Toh,et al.  The dog and its genome , 2006 .

[115]  L. Hartwell,et al.  Cell cycle control and cancer. , 1994, Science.

[116]  R. Dubielzig,et al.  Adjuvant therapy for melanoma in dogs: results of randomized clinical trials using surgery, liposome-encapsulated muramyl tripeptide, and granulocyte macrophage colony-stimulating factor. , 1999, Clinical cancer research : an official journal of the American Association for Cancer Research.

[117]  S. Galli,et al.  Expression of stem cell factor receptor (c-kit) by the malignant mast cells from spontaneous canine mast cell tumours. , 1996, Journal of comparative pathology.

[118]  R. Dubielzig,et al.  Adjuvant therapy for osteosarcoma in dogs: results of randomized clinical trials using combined liposome-encapsulated muramyl tripeptide and cisplatin. , 1995, Clinical cancer research : an official journal of the American Association for Cancer Research.

[119]  P. Anderson Liposomal muramyl tripeptide phosphatidyl ethanolamine: ifosfamide-containing chemotherapy in osteosarcoma. , 2006, Future oncology.

[120]  D. Knapp,et al.  Canine transitional cell carcinoma. , 2003, Journal of veterinary internal medicine.

[121]  J. Webster,et al.  The Use of KIT and Tryptase Expression Patterns as Prognostic Tools for Canine Cutaneous Mast Cell Tumors , 2004, Veterinary pathology.

[122]  P. Anderson,et al.  Aerosol delivery of interleukin 2 liposomes is nontoxic and biologically effective: canine studies. , 1996, Clinical cancer research : an official journal of the American Association for Cancer Research.

[123]  C. Fletcher,et al.  The role of KIT in the management of patients with gastrointestinal stromal tumors. , 2007, Human pathology.