Skip to main content
Erschienen in: Cancer and Metastasis Reviews 1/2021

28.10.2020 | Non-Thematics Review

Beyond tradition and convention: benefits of non-traditional model organisms in cancer research

verfasst von: Rebecca M. Harman, Sanjna P. Das, Arianna P. Bartlett, Gat Rauner, Leanne R. Donahue, Gerlinde R. Van de Walle

Erschienen in: Cancer and Metastasis Reviews | Ausgabe 1/2021

Einloggen, um Zugang zu erhalten

Abstract

Traditional laboratory model organisms are indispensable for cancer research and have provided insight into numerous mechanisms that contribute to cancer development and progression in humans. However, these models do have some limitations, most notably related to successful drug translation, because traditional model organisms are often short-lived, small-bodied, genetically homogeneous, often immunocompromised, are not exposed to natural environments shared with humans, and usually do not develop cancer spontaneously. We propose that assimilating information from a variety of long-lived, large, genetically diverse, and immunocompetent species that live in natural environments and do develop cancer spontaneously (or do not develop cancer at all) will lead to a more comprehensive understanding of human cancers. These non-traditional model organisms can also serve as sentinels for environmental risk factors that contribute to human cancers. Ultimately, expanding the range of animal models that can be used to study cancer will lead to improved insights into cancer development, progression and metastasis, tumor microenvironment, as well as improved therapies and diagnostics, and will consequently reduce the negative impacts of the wide variety of cancers afflicting humans overall.
Literatur
14.
Zurück zum Zitat Zhang, B., Shimada, Y., Kuroyanagi, J., Nishimura, Y., Umemoto, N., Nomoto, T., et al. (2014). Zebrafish xenotransplantation model for cancer stem-like cell study and high-throughput screening of inhibitors. Tumour Biology: The Journal of the International Society for Oncodevelopmental Biology and Medicine, 35(12), 11861–11869. https://doi.org/10.1007/s13277-014-2417-8.CrossRef Zhang, B., Shimada, Y., Kuroyanagi, J., Nishimura, Y., Umemoto, N., Nomoto, T., et al. (2014). Zebrafish xenotransplantation model for cancer stem-like cell study and high-throughput screening of inhibitors. Tumour Biology: The Journal of the International Society for Oncodevelopmental Biology and Medicine, 35(12), 11861–11869. https://​doi.​org/​10.​1007/​s13277-014-2417-8.CrossRef
29.
Zurück zum Zitat Harman, R. M., Curtis, T. M., Argyle, D. J., Coonrod, S. A., & Van de Walle, G. R. (2016). A comparative study on the in vitro effects of the DNA methyltransferase inhibitor 5-Azacytidine (5-AzaC) in breast/mammary cancer of different mammalian species. Journal of Mammary Gland Biology and Neoplasia, 1–6. Harman, R. M., Curtis, T. M., Argyle, D. J., Coonrod, S. A., & Van de Walle, G. R. (2016). A comparative study on the in vitro effects of the DNA methyltransferase inhibitor 5-Azacytidine (5-AzaC) in breast/mammary cancer of different mammalian species. Journal of Mammary Gland Biology and Neoplasia, 1–6.
42.
49.
Zurück zum Zitat Luu, A., Macdonald, R., Oblak, M., Brisson, B., & Viloria-Petit, A. (2018). Optimization of an explant culture model to characterize cancer-associated exosomes in canine osteosarcoma. Luu, A., Macdonald, R., Oblak, M., Brisson, B., & Viloria-Petit, A. (2018). Optimization of an explant culture model to characterize cancer-associated exosomes in canine osteosarcoma.
53.
Zurück zum Zitat Cocola, C., Molgora, S., Piscitelli, E., Veronesi, M. C., Greco, M., Bragato, C., et al. (2017). FGF2 and EGF are required for self-renewal and organoid formation of canine normal and tumor breast stem cells. Journal of Cellular Biochemistry, 118(3), 570–584. https://doi.org/10.1002/jcb.25737.CrossRefPubMed Cocola, C., Molgora, S., Piscitelli, E., Veronesi, M. C., Greco, M., Bragato, C., et al. (2017). FGF2 and EGF are required for self-renewal and organoid formation of canine normal and tumor breast stem cells. Journal of Cellular Biochemistry, 118(3), 570–584. https://​doi.​org/​10.​1002/​jcb.​25737.CrossRefPubMed
68.
Zurück zum Zitat Sieren, J. C., Meyerholz, D. K., Wang, X.-J., Davis, B. T., Newell Jr., J. D., Hammond, E., et al. (February 9). Development and translational imaging of a TP53 porcine tumorigenesis model. The Journal of Clinical Investigation, 124(9), 4052–4066. https://doi.org/10.1172/JCI75447. Sieren, J. C., Meyerholz, D. K., Wang, X.-J., Davis, B. T., Newell Jr., J. D., Hammond, E., et al. (February 9). Development and translational imaging of a TP53 porcine tumorigenesis model. The Journal of Clinical Investigation, 124(9), 4052–4066. https://​doi.​org/​10.​1172/​JCI75447.
84.
Zurück zum Zitat Russell, W. M. S., & Burch, R. L. (1959). The principles of humane experimental technique. London: Methuen & Co. Ltd.. Russell, W. M. S., & Burch, R. L. (1959). The principles of humane experimental technique. London: Methuen & Co. Ltd..
90.
Zurück zum Zitat Mak, I. W., Evaniew, N., & Ghert, M. (2014). Lost in translation: Animal models and clinical trials in cancer treatment. American Journal of Translational Research, 6(2), 114–118.PubMedPubMedCentral Mak, I. W., Evaniew, N., & Ghert, M. (2014). Lost in translation: Animal models and clinical trials in cancer treatment. American Journal of Translational Research, 6(2), 114–118.PubMedPubMedCentral
105.
Zurück zum Zitat Casal, M., & Haskins, M. (2006). Large animal models and gene therapy. European Journal of Human Genetics, 14(3), 266–272.CrossRef Casal, M., & Haskins, M. (2006). Large animal models and gene therapy. European Journal of Human Genetics, 14(3), 266–272.CrossRef
108.
Zurück zum Zitat Rusk, A., McKeegan, E., Haviv, F., Majest, S., Henkin, J., & Khanna, C. (2006). Preclinical evaluation of antiangiogenic thrombospondin-1 peptide mimetics, ABT-526 and ABT-510, in companion dogs with naturally occurring cancers. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 12(24), 7444–7455. https://doi.org/10.1158/1078-0432.CCR-06-0109.CrossRef Rusk, A., McKeegan, E., Haviv, F., Majest, S., Henkin, J., & Khanna, C. (2006). Preclinical evaluation of antiangiogenic thrombospondin-1 peptide mimetics, ABT-526 and ABT-510, in companion dogs with naturally occurring cancers. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 12(24), 7444–7455. https://​doi.​org/​10.​1158/​1078-0432.​CCR-06-0109.CrossRef
109.
Zurück zum Zitat Pryer, N. K., Lee, L. B., Zadovaskaya, R., Yu, X., Sukbuntherng, J., Cherrington, J. M., & London, C. A. (2003). Proof of target for SU11654: Inhibition of KIT phosphorylation in canine mast cell tumors. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 9(15), 5729–5734. Pryer, N. K., Lee, L. B., Zadovaskaya, R., Yu, X., Sukbuntherng, J., Cherrington, J. M., & London, C. A. (2003). Proof of target for SU11654: Inhibition of KIT phosphorylation in canine mast cell tumors. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 9(15), 5729–5734.
110.
Zurück zum Zitat London, C. A., Hannah, A. L., Zadovoskaya, R., Chien, M. B., Kollias-Baker, C., Rosenberg, M., et al. (2003). Phase I dose-escalating study of SU11654, a small molecule receptor tyrosine kinase inhibitor, in dogs with spontaneous malignancies. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 9(7), 2755–2768. London, C. A., Hannah, A. L., Zadovoskaya, R., Chien, M. B., Kollias-Baker, C., Rosenberg, M., et al. (2003). Phase I dose-escalating study of SU11654, a small molecule receptor tyrosine kinase inhibitor, in dogs with spontaneous malignancies. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research, 9(7), 2755–2768.
112.
113.
117.
Zurück zum Zitat Tabone, M. D., Kalifa, C., Rodary, C., Raquin, M., Valteau-Couanet, D., & Lemerle, J. (1994). Osteosarcoma recurrences in pediatric patients previously treated with intensive chemotherapy. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology, 12(12), 2614–2620. https://doi.org/10.1200/JCO.1994.12.12.2614.CrossRef Tabone, M. D., Kalifa, C., Rodary, C., Raquin, M., Valteau-Couanet, D., & Lemerle, J. (1994). Osteosarcoma recurrences in pediatric patients previously treated with intensive chemotherapy. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology, 12(12), 2614–2620. https://​doi.​org/​10.​1200/​JCO.​1994.​12.​12.​2614.CrossRef
120.
Zurück zum Zitat Krol, A. D. G., le Cessie, S., Snijder, S., Kluin-Nelemans, J. C., Kluin, P. M., & Noordijk, E. M. (2003). Primary extranodal non-Hodgkin’s lymphoma (NHL): The impact of alternative definitions tested in the comprehensive Cancer Centre west population-based NHL registry. Annals of Oncology: Official Journal of the European Society for Medical Oncology, 14(1), 131–139. https://doi.org/10.1093/annonc/mdg004.CrossRef Krol, A. D. G., le Cessie, S., Snijder, S., Kluin-Nelemans, J. C., Kluin, P. M., & Noordijk, E. M. (2003). Primary extranodal non-Hodgkin’s lymphoma (NHL): The impact of alternative definitions tested in the comprehensive Cancer Centre west population-based NHL registry. Annals of Oncology: Official Journal of the European Society for Medical Oncology, 14(1), 131–139. https://​doi.​org/​10.​1093/​annonc/​mdg004.CrossRef
121.
Zurück zum Zitat Seo, K.-W., Choi, U.-S., Lee, J.-B., Kim, M.-I., Oh, Y.-I., Chung, J.-Y., et al. (2011). Central nervous system relapses in 3 dogs with B-cell lymphoma. The Canadian Veterinary Journal = La Revue Veterinaire Canadienne, 52(7), 778–783.PubMedPubMedCentral Seo, K.-W., Choi, U.-S., Lee, J.-B., Kim, M.-I., Oh, Y.-I., Chung, J.-Y., et al. (2011). Central nervous system relapses in 3 dogs with B-cell lymphoma. The Canadian Veterinary Journal = La Revue Veterinaire Canadienne, 52(7), 778–783.PubMedPubMedCentral
123.
Zurück zum Zitat Queiroga, F. L., Raposo, T., Carvalho, M. I., Prada, J., & Pires, I. (2011). Canine mammary tumours as a model to study human breast cancer: Most recent findings. In Vivo (Athens, Greece), 25(3), 455–465. Queiroga, F. L., Raposo, T., Carvalho, M. I., Prada, J., & Pires, I. (2011). Canine mammary tumours as a model to study human breast cancer: Most recent findings. In Vivo (Athens, Greece), 25(3), 455–465.
126.
Zurück zum Zitat Chocteau, F., Boulay, M.-M., Besnard, F., Valeau, G., Loussouarn, D., & Nguyen, F. (2019). Proposal for a histological staging system of mammary carcinomas in dogs and cats. Part 2: Feline mammary carcinomas. Frontiers in veterinary science, 6, 387. https://doi.org/10.3389/fvets.2019.00387. Chocteau, F., Boulay, M.-M., Besnard, F., Valeau, G., Loussouarn, D., & Nguyen, F. (2019). Proposal for a histological staging system of mammary carcinomas in dogs and cats. Part 2: Feline mammary carcinomas. Frontiers in veterinary science, 6, 387. https://​doi.​org/​10.​3389/​fvets.​2019.​00387.
127.
Zurück zum Zitat Moe, L. (2001). Population-based incidence of mammary tumours in some dog breeds. Journal of Reproduction and Fertility. Supplement, 57, 439–443.PubMed Moe, L. (2001). Population-based incidence of mammary tumours in some dog breeds. Journal of Reproduction and Fertility. Supplement, 57, 439–443.PubMed
129.
Zurück zum Zitat Gundim, L. F., de Araújo, C. P., Blanca, W. T., Guimarães, E. C., & Medeiros, A. A. (2016). Clinical staging in bitches with mammary tumors: Influence of type and histological grade. Canadian Journal of Veterinary Research = Revue Canadienne De Recherche Veterinaire, 80(4), 318–322.PubMedPubMedCentral Gundim, L. F., de Araújo, C. P., Blanca, W. T., Guimarães, E. C., & Medeiros, A. A. (2016). Clinical staging in bitches with mammary tumors: Influence of type and histological grade. Canadian Journal of Veterinary Research = Revue Canadienne De Recherche Veterinaire, 80(4), 318–322.PubMedPubMedCentral
130.
133.
Zurück zum Zitat Hayes, H. M., & Fraumeni, J. F. (1977). Epidemiological features of canine renal neoplasms. Cancer Research, 37(8 Pt 1), 2553–2556.PubMed Hayes, H. M., & Fraumeni, J. F. (1977). Epidemiological features of canine renal neoplasms. Cancer Research, 37(8 Pt 1), 2553–2556.PubMed
134.
Zurück zum Zitat Withrow, S. J., Vail, D. M., & Page, R. L. (Eds.). (2013). Withrow & MacEwen’s small animal clinical oncology (5th ed.). St. Louis, Missouri: Elsevier. Withrow, S. J., Vail, D. M., & Page, R. L. (Eds.). (2013). Withrow & MacEwen’s small animal clinical oncology (5th ed.). St. Louis, Missouri: Elsevier.
136.
Zurück zum Zitat De Maria, R., Olivero, M., Iussich, S., Nakaichi, M., Murata, T., Biolatti, B., & Di Renzo, M. F. (2005). Spontaneous feline mammary carcinoma is a model of HER2 overexpressing poor prognosis human breast cancer. Cancer Research, 65(3), 907–912.PubMed De Maria, R., Olivero, M., Iussich, S., Nakaichi, M., Murata, T., Biolatti, B., & Di Renzo, M. F. (2005). Spontaneous feline mammary carcinoma is a model of HER2 overexpressing poor prognosis human breast cancer. Cancer Research, 65(3), 907–912.PubMed
141.
Zurück zum Zitat Murakami, Y., Tateyama, S., Rungsipipat, A., Uchida, K., & Yamaguchi, R. (2000). Immunohistochemical analysis of Cyclin a, Cyclin D1 and P53 in mammary tumors, squamous cell carcinomas and basal cell tumors of dogs and cats. Journal of Veterinary Medical Science, 62(7), 743–750. https://doi.org/10.1292/jvms.62.743.CrossRef Murakami, Y., Tateyama, S., Rungsipipat, A., Uchida, K., & Yamaguchi, R. (2000). Immunohistochemical analysis of Cyclin a, Cyclin D1 and P53 in mammary tumors, squamous cell carcinomas and basal cell tumors of dogs and cats. Journal of Veterinary Medical Science, 62(7), 743–750. https://​doi.​org/​10.​1292/​jvms.​62.​743.CrossRef
159.
161.
Zurück zum Zitat Perk, K., & Hod, I. (1982). Sheep lung carcinoma: An endemic analogue of a sporadic human neoplasm. Journal of the National Cancer Institute, 69(4), 747–749.PubMed Perk, K., & Hod, I. (1982). Sheep lung carcinoma: An endemic analogue of a sporadic human neoplasm. Journal of the National Cancer Institute, 69(4), 747–749.PubMed
166.
Zurück zum Zitat Coricovac, D., Dehelean, C., Moaca, E.-A., Pinzaru, I., Bratu, T., Navolan, D., & Boruga, O. (2018). Cutaneous melanoma-a long road from experimental models to clinical outcome: A review. International Journal of Molecular Sciences, 19(6). https://doi.org/10.3390/ijms19061566. Coricovac, D., Dehelean, C., Moaca, E.-A., Pinzaru, I., Bratu, T., Navolan, D., & Boruga, O. (2018). Cutaneous melanoma-a long road from experimental models to clinical outcome: A review. International Journal of Molecular Sciences, 19(6). https://​doi.​org/​10.​3390/​ijms19061566.
170.
Zurück zum Zitat Rosengren Pielberg, G., Golovko, A., Sundström, E., Curik, I., Lennartsson, J., Seltenhammer, M. H., et al. (2008). A cis-acting regulatory mutation causes premature hair graying and susceptibility to melanoma in the horse. Nature Genetics, 40(8), 1004–1009. https://doi.org/10.1038/ng.185.CrossRefPubMed Rosengren Pielberg, G., Golovko, A., Sundström, E., Curik, I., Lennartsson, J., Seltenhammer, M. H., et al. (2008). A cis-acting regulatory mutation causes premature hair graying and susceptibility to melanoma in the horse. Nature Genetics, 40(8), 1004–1009. https://​doi.​org/​10.​1038/​ng.​185.CrossRefPubMed
184.
Zurück zum Zitat Rodríguez-Burford, C., Barnes, M. N., Berry, W., Partridge, E. E., & Grizzle, W. E. (2001). Immunohistochemical expression of molecular markers in an avian model: A potential model for preclinical evaluation of agents for ovarian cancer chemoprevention. Gynecologic Oncology, 81(3), 373–379. https://doi.org/10.1006/gyno.2001.6191.CrossRefPubMed Rodríguez-Burford, C., Barnes, M. N., Berry, W., Partridge, E. E., & Grizzle, W. E. (2001). Immunohistochemical expression of molecular markers in an avian model: A potential model for preclinical evaluation of agents for ovarian cancer chemoprevention. Gynecologic Oncology, 81(3), 373–379. https://​doi.​org/​10.​1006/​gyno.​2001.​6191.CrossRefPubMed
185.
187.
196.
Zurück zum Zitat Jaakkola, M., & Jakkola, J. (2002). Effects of environmental tobacco smoke on the respiratory health of adults. Scandinavian Journal of Work, Environment & Health, 28, 52–70. Jaakkola, M., & Jakkola, J. (2002). Effects of environmental tobacco smoke on the respiratory health of adults. Scandinavian Journal of Work, Environment & Health, 28, 52–70.
199.
Zurück zum Zitat Zierenberg-Ripoll, A., Pollard, R. E., Stewart, S. L., Allstadt, S. D., Barrett, L. E., Gillem, J. M., & Skorupski, K. A. (2018). Association between environmental factors including second-hand smoke and primary lung cancer in dogs: Tobacco smoke and lung cancer. Journal of Small Animal Practice, 59(6), 343–349. https://doi.org/10.1111/jsap.1277.8.CrossRef Zierenberg-Ripoll, A., Pollard, R. E., Stewart, S. L., Allstadt, S. D., Barrett, L. E., Gillem, J. M., & Skorupski, K. A. (2018). Association between environmental factors including second-hand smoke and primary lung cancer in dogs: Tobacco smoke and lung cancer. Journal of Small Animal Practice, 59(6), 343–349. https://​doi.​org/​10.​1111/​jsap.​1277.​8.CrossRef
201.
Zurück zum Zitat Ogilvie, G., Haschek, W., Withrow, S. J., Richardson, R., Harvey, H., Henderson, R., & Fowler, J. (1989). Classification of primary lung tumors in dogs: 210 cases (1975-1985). Journal of the Veterinary Medical Association, 195, 106–108. Ogilvie, G., Haschek, W., Withrow, S. J., Richardson, R., Harvey, H., Henderson, R., & Fowler, J. (1989). Classification of primary lung tumors in dogs: 210 cases (1975-1985). Journal of the Veterinary Medical Association, 195, 106–108.
204.
Zurück zum Zitat Garbe, P. (1988). The companion animal as a sentinal for environmentally related human diseases. Acta Veterinaria Scandinavica. Supplementum, 84, 290–292.PubMed Garbe, P. (1988). The companion animal as a sentinal for environmentally related human diseases. Acta Veterinaria Scandinavica. Supplementum, 84, 290–292.PubMed
212.
Zurück zum Zitat Lesage, V., & Kingsley, M. (1998). Updated status of the St. Lawrence River population of the Beluga Delphinapterus leucas. Canadian Field-Naturalist, 112, 98–113. Lesage, V., & Kingsley, M. (1998). Updated status of the St. Lawrence River population of the Beluga Delphinapterus leucas. Canadian Field-Naturalist, 112, 98–113.
222.
Zurück zum Zitat Kshitiz, Afzal, J., Maziarz, J. D., Hamidzadeh, A., Liang, C., Erkenbrack, E. M., … Wagner, G. P. (2019). Evolution of placental invasion and cancer metastasis are causally linked. Nature Ecology & Evolution, 3(12), 1743–1753. https://doi.org/10.1038/s41559-019-1046-4. Kshitiz, Afzal, J., Maziarz, J. D., Hamidzadeh, A., Liang, C., Erkenbrack, E. M., … Wagner, G. P. (2019). Evolution of placental invasion and cancer metastasis are causally linked. Nature Ecology & Evolution, 3(12), 1743–1753. https://​doi.​org/​10.​1038/​s41559-019-1046-4.
224.
Zurück zum Zitat Carvalho, M. I., Silva-Carvalho, R., Pires, I., Prada, J., Bianchini, R., Jensen-Jarolim, E., & Queiroga, F. L. (2016). A comparative approach of tumor-associated inflammation in mammary Cancer between humans and dogs. BioMed Research International, 2016, 1–12. https://doi.org/10.1155/2016/4917387.CrossRef Carvalho, M. I., Silva-Carvalho, R., Pires, I., Prada, J., Bianchini, R., Jensen-Jarolim, E., & Queiroga, F. L. (2016). A comparative approach of tumor-associated inflammation in mammary Cancer between humans and dogs. BioMed Research International, 2016, 1–12. https://​doi.​org/​10.​1155/​2016/​4917387.CrossRef
229.
231.
Zurück zum Zitat Zhao, Y., Tyshkovskiy, A., Muñoz-Espín, D., Tian, X., Serrano, M., de Magalhaes, J. P., et al. (2018). Naked mole rats can undergo developmental, oncogene-induced and DNA damage-induced cellular senescence. Proceedings of the National Academy of Sciences, 115(8), 1801–1806. https://doi.org/10.1073/pnas.1721160115.CrossRef Zhao, Y., Tyshkovskiy, A., Muñoz-Espín, D., Tian, X., Serrano, M., de Magalhaes, J. P., et al. (2018). Naked mole rats can undergo developmental, oncogene-induced and DNA damage-induced cellular senescence. Proceedings of the National Academy of Sciences, 115(8), 1801–1806. https://​doi.​org/​10.​1073/​pnas.​1721160115.CrossRef
239.
Zurück zum Zitat Nasser, N. J., Avivi, A., Shafat, I., Edovitsky, E., Zcharia, E., Ilan, N., et al. (2009). Alternatively spliced Spalax heparanase inhibits extracellular matrix degradation, tumor growth, and metastasis. Proceedings of the National Academy of Sciences, 106(7), 2253–2258. https://doi.org/10.1073/pnas.0812846106.CrossRef Nasser, N. J., Avivi, A., Shafat, I., Edovitsky, E., Zcharia, E., Ilan, N., et al. (2009). Alternatively spliced Spalax heparanase inhibits extracellular matrix degradation, tumor growth, and metastasis. Proceedings of the National Academy of Sciences, 106(7), 2253–2258. https://​doi.​org/​10.​1073/​pnas.​0812846106.CrossRef
241.
Zurück zum Zitat Sulak, M., Fong, L., Mika, K., Chigurupati, S., Yon, L., Mongan, N. P., … Lynch, V. J. (2016). TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants. eLife, 5, e11994. https://doi.org/10.7554/eLife.11994. Sulak, M., Fong, L., Mika, K., Chigurupati, S., Yon, L., Mongan, N. P., … Lynch, V. J. (2016). TP53 copy number expansion is associated with the evolution of increased body size and an enhanced DNA damage response in elephants. eLife, 5, e11994. https://​doi.​org/​10.​7554/​eLife.​11994.
248.
249.
Zurück zum Zitat Werner, H., Lapkina-Gendler, L., Achlaug, L., Nagaraj, K., Somri, L., Yaron-Saminsky, D., et al. (2019). Genome-wide profiling of laron syndrome patients identifies novel cancer protection pathways. Cells, 8(6). https://doi.org/10.3390/cells8060596. Werner, H., Lapkina-Gendler, L., Achlaug, L., Nagaraj, K., Somri, L., Yaron-Saminsky, D., et al. (2019). Genome-wide profiling of laron syndrome patients identifies novel cancer protection pathways. Cells, 8(6). https://​doi.​org/​10.​3390/​cells8060596.
256.
Zurück zum Zitat Caulin, A. F., Graham, T. A., Wang, L.-S., & Maley, C. C. (2015). Solutions to Peto’s paradox revealed by mathematical modelling and cross-species cancer gene analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1673), 20140222.CrossRef Caulin, A. F., Graham, T. A., Wang, L.-S., & Maley, C. C. (2015). Solutions to Peto’s paradox revealed by mathematical modelling and cross-species cancer gene analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1673), 20140222.CrossRef
Metadaten
Titel
Beyond tradition and convention: benefits of non-traditional model organisms in cancer research
verfasst von
Rebecca M. Harman
Sanjna P. Das
Arianna P. Bartlett
Gat Rauner
Leanne R. Donahue
Gerlinde R. Van de Walle
Publikationsdatum
28.10.2020
Verlag
Springer US
Erschienen in
Cancer and Metastasis Reviews / Ausgabe 1/2021
Print ISSN: 0167-7659
Elektronische ISSN: 1573-7233
DOI
https://doi.org/10.1007/s10555-020-09930-6

Weitere Artikel der Ausgabe 1/2021

Cancer and Metastasis Reviews 1/2021 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.