Avian Models for Human Carcinogenesis-Recent Findings from Molecular and Clinical Research
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy, práce podpořená grantem
Grantová podpora
NC7082
National Institute of Food and Agriculture
PubMed
39513904
PubMed Central
PMC11544849
DOI
10.3390/cells13211797
PII: cells13211797
Knihovny.cz E-zdroje
- Klíčová slova
- carcinogenesis, chorioallantoic membrane, hen model, oncoviruses, ovarian cancer,
- MeSH
- karcinogeneze * patologie genetika MeSH
- kur domácí MeSH
- kuřecí embryo MeSH
- lidé MeSH
- modely nemocí na zvířatech * MeSH
- nádory patologie genetika MeSH
- ptáci MeSH
- zvířata MeSH
- Check Tag
- kuřecí embryo MeSH
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
Birds, especially the chick and hen, have been important biomedical research models for centuries due to the accessibility of the avian embryo and the early discovery of avian viruses. Comprehension of avian tumor virology was a milestone in basic cancer research, as was that of non-viral genesis, as it enabled the discovery of oncogenes. Furthermore, studies on avian viruses provided initial insights into Kaposi's sarcoma and EBV-induced diseases. However, the role of birds in human carcinogenesis extends beyond the realm of virology research. Utilization of CAM, the chorioallantoic membrane, an easily accessible extraembryonic tissue with rich vasculature, has enabled studies on tumor-induced angiogenesis and metastasis and the efficient screening of potential anti-cancer compounds. Also, the chick embryo alone is an effective preclinical in vivo patient-derived xenograft model, which is important for the development of personalized therapies. Furthermore, adult birds may also closely resemble human oncogenesis, as evidenced by the laying hen, which is the only animal model of a spontaneous form of ovarian cancer. Avian models may create an interesting alternative compared with mammalian models, enabling the creation of a relatively cost-effective and easy-to-maintain platform to address key questions in cancer biology.
Department of Toxicology Poznan University of Medical Sciences 60 631 Poznan Poland
Flyblast BV 2020 Antwerp Belgium
Physiology Graduate Faculty North Carolina State University Raleigh NC 27695 USA
Prestage Department of Poultry Science North Carolina State University Raleigh NC 27695 USA
Veterinary Clinic of the Nicolaus Copernicus University in Torun 87 100 Torun Poland
Zobrazit více v PubMed
Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A., Bray F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA. Cancer J. Clin. 2021;71:209–249. doi: 10.3322/caac.21660. PubMed DOI
McLaughlin-Drubin M.E., Munger K. Viruses Associated with Human Cancer. Biochim. Biophys. Acta. 2008;1782:127–150. doi: 10.1016/j.bbadis.2007.12.005. PubMed DOI PMC
Justice J., Beemon K.L. Avian Retroviral Replication. Curr. Opin. Virol. 2013;3:664–669. doi: 10.1016/j.coviro.2013.08.008. PubMed DOI PMC
Fadly A.M. Avian retroviruses. Vet. Clin. N. Am. Food Anim. Pract. 1997;13:71–85. doi: 10.1016/S0749-0720(15)30365-0. PubMed DOI
Fandiño S., Gomez-Lucia E., Benítez L., Doménech A. Avian Leukosis: Will We Be Able to Get Rid of It? Animals. 2023;13:2358. doi: 10.3390/ani13142358. PubMed DOI PMC
Thomas J.M., Allison A.B., Holmes E.C., Phillips J.E., Bunting E.M., Yabsley M.J., Brown J.D. Molecular Surveillance for Lymphoproliferative Disease Virus in Wild Turkeys (Meleagris gallopavo) from the Eastern United States. PLoS ONE. 2015;10:e0122644. doi: 10.1371/journal.pone.0122644. PubMed DOI PMC
Adcock K.G., Berghaus R.D., Goodwin C.C., Ruder M.G., Yabsley M.J., Mead D.G., Nemeth N.M. Lymphoproliferative Disease Virus and Reticuloendotheliosis Virus Detection and Disease in Wild Turkeys (Meleagris gallopavo) J. Wildl. Dis. 2024;60:139–150. doi: 10.7589/JWD-D-23-00012. PubMed DOI
Caleiro G.S., Nunes C.F., Urbano P.R., Kirchgatter K., de Araujo J., Durigon E.L., Thomazelli L.M., Stewart B.M., Edwards D.C., Romano C.M. Detection of Reticuloendotheliosis Virus in Muscovy Ducks, Wild Turkeys, and Chickens in Brazil. J. Wildl. Dis. 2020;56:631–635. doi: 10.7589/2019-04-088. PubMed DOI
Freick M., Schreiter R., Weber J., Vahlenkamp T.W., Heenemann K. Avian Leukosis Virus (ALV) Is Highly Prevalent in Fancy-Chicken Flocks in Saxony. Arch. Virol. 2022;167:1169–1174. doi: 10.1007/s00705-022-05404-y. PubMed DOI PMC
Beemon K.L. Encyclopedia of Virology. 4th ed. Vol. 2. Academic Press; Cambridge, MA, USA: 2021. Avian Leukosis and Sarcoma Viruses (Retroviridae) pp. 122–126.
Mosad S.M., El-Tholoth M., El-Kenawy A.A., Abdel-Hafez L.J.M., El-Gohary F.A., El-Sharkawy H., Elsayed M.M., Saleh A.A., Elmahallawy E.K. Molecular Detection of Reticuloendotheliosis Virus 5′ Long Terminal Repeat Integration in the Genome of Avipoxvirus Field Strains from Different Avian Species in Egypt. Biology. 2020;9:257. doi: 10.3390/biology9090257. PubMed DOI PMC
Malhotra S., Winans S., Lam G., Justice J., Morgan R., Beemon K. Selection for Avian Leukosis Virus Integration Sites Determines the Clonal Progression of B-Cell Lymphomas. PLoS Pathog. 2017;13:e1006708. doi: 10.1371/journal.ppat.1006708. PubMed DOI PMC
Maclachlan N., Dubovi E.J., Barthold S.W., Swayne D., Winton J.R. Fenner’s Veterinary Virology. 5th ed. Academic Press; Cambridge, MA, USA: 2016. 581p
Cloft S.E., Kinstler S.R., Reno K.E., Sellers H.S., Franca M., Ecco R., Lee M.D., Maurer J.J., Wong E.A. Runting Stunting Syndrome in Broiler Chickens Is Associated with Altered Intestinal Stem Cell Morphology and Gene Expression. Avian Dis. 2022;66:85–94. doi: 10.1637/21-00109. PubMed DOI
Robinson F.R., Twiehaus M.J. Isolation of the Avian Reticuloendothelial Virus (Strain T) Avian Dis. 1974;18:278–288. doi: 10.2307/1589142. PubMed DOI
He S., Zhou M., Zheng H., Wang Y., Wu S., Gao Y., Chen J. Resveratrol Inhibits the Progression of Premature Senescence Partially by Regulating V-Rel Avian Reticuloendotheliosis Viral Oncogene Homolog A (RELA) and Sirtuin 1 (SIRT1) Ren. Fail. 2022;44:171–183. doi: 10.1080/0886022X.2022.2029488. PubMed DOI PMC
Mason A.S., Miedzinska K., Kebede A., Bamidele O., Al-Jumaili A.S., Dessie T., Hanotte O., Smith J. Diversity of Endogenous Avian Leukosis Virus Subgroup E (ALVE) Insertions in Indigenous Chickens. Genet. Sel. Evol. 2020;52:29. doi: 10.1186/s12711-020-00548-4. PubMed DOI PMC
Borodin A.M., Emanuilova Z.V., Smolov S.V., Ogneva O.A., Konovalova N.V., Terentyeva E.V., Serova N.Y., Efimov D.N., Fisinin V.I., Greenberg A.J., et al. Eradication of avian leukosis virus subgroups J and K in broiler cross chickens by selection against infected birds using multilocus PCR. PLoS ONE. 2022;17:e0269525. doi: 10.1371/journal.pone.0269525. PubMed DOI PMC
Li Q., Wang P., Li M., Lin L., Shi M., Li H., Deng Q., Teng H., Mo M., Wei T., et al. Recombinant subgroup B avian leukosis virus combined with the subgroup J env gene significantly increases its pathogenicity. Vet. Microbiol. 2020;250:108862. doi: 10.1016/j.vetmic.2020.108862. PubMed DOI
Nair V., Fadly A.M. Leukosis/Sarcoma Group. In: Swayne D.E., Glisson J.R., McDougald L.R., Nolan L.K., Suarez D.L., Nair V., editors. Diseases of Poultry. 13th ed. Wiley-Blackwell; Ames, IA, USA: 2013. pp. 553–592.
Přikryl D., Plachý J., Kučerová D., Koslová A., Reinišová M., Šenigl F., Hejnar J. The Novel Avian Leukosis Virus Subgroup K Shares Its Cellular Receptor with Subgroup A. J. Virol. 2019;93:e00580-19. doi: 10.1128/JVI.00580-19. PubMed DOI PMC
Khordadmehr M., Firouzamandi M., zehtab najafi M., Shahbazi R. Naturally Occurring Co-Infection of Avian Leukosis Virus (Subgroups A-E) and Reticuloendotheliosis Virus in Green Peafowls (Pavo Muticus) Rev. Bras. Ciênc. Avícola. 2017;19:609–614. doi: 10.1590/1806-9061-2017-0506. DOI
Zheng L.-P., Teng M., Li G.-X., Zhang W.-K., Wang W.-D., Liu J.-L., Li L.-Y., Yao Y., Nair V., Luo J. Current Epidemiology and Co-Infections of Avian Immunosuppressive and Neoplastic Diseases in Chicken Flocks in Central China. Viruses. 2022;14:2599. doi: 10.3390/v14122599. PubMed DOI PMC
Li L., Zhuang P., Cheng Z., Yang J., Bi J., Wang G. Avian Leukosis Virus Subgroup J and Reticuloendotheliosis Virus Coinfection Induced TRIM62 Regulation of the Actin Cytoskeleton. J. Vet. Sci. 2020;21:e49. doi: 10.4142/jvs.2020.21.e49. PubMed DOI PMC
Dibsy R., Bremaud E., Mak J., Favard C., Muriaux D. HIV-1 Diverts Cortical Actin for Particle Assembly and Release. Nat. Commun. 2023;14:6945. doi: 10.1038/s41467-023-41940-0. PubMed DOI PMC
Cui X., Zhang X., Xue J., Yao Y., Zhou D., Cheng Z. TMT-Based Proteomic Analysis Reveals Integrins Involved in the Synergistic Infection of Reticuloendotheliosis Virus and Avian Leukosis Virus Subgroup J. BMC Vet. Res. 2022;18:131. doi: 10.1186/s12917-022-03207-6. PubMed DOI PMC
Zhou D., Xue J., He S., Du X., Zhou J., Li C., Huang L., Nair V., Yao Y., Cheng Z. Reticuloendotheliosis Virus and Avian Leukosis Virus Subgroup J Synergistically Increase the Accumulation of Exosomal miRNAs. Retrovirology. 2018;15:45. doi: 10.1186/s12977-018-0427-0. PubMed DOI PMC
Lee J., Lee J., Choi C., Kim J.H. Blockade of Integrin A3 Attenuates Human Pancreatic Cancer via Inhibition of EGFR Signalling. Sci. Rep. 2019;9:2793. doi: 10.1038/s41598-019-39628-x. PubMed DOI PMC
Leonard M.K., Novak M., Snyder D., Snow G., Pamidimukkala N., McCorkle J.R., Yang X.H., Kaetzel D.M. The Metastasis Suppressor NME1 Inhibits Melanoma Cell Motility via Direct Transcriptional Induction of the Integrin Beta-3 Gene. Exp. Cell Res. 2019;374:85. doi: 10.1016/j.yexcr.2018.11.010. PubMed DOI PMC
An J.S., Moon J.H., Kim C., No J.K., Eun Y.G., Chang Lim Y. Integrin Alpha 6 as a Stemness Driver Is a Novel Promising Target for HPV (+) Head and Neck Squamous Cell Carcinoma. Exp. Cell Res. 2021;407:112815. doi: 10.1016/j.yexcr.2021.112815. PubMed DOI
Zhou D., Ding L., Xu M., Liu X., Xue J., Zhang X., Du X., Zhou J., Cui X., Cheng Z. Musashi-1 and miR-147 Precursor Interaction Mediates Synergistic Oncogenicity Induced by Co-Infection of Two Avian Retroviruses. Cells. 2022;11:3312. doi: 10.3390/cells11203312. PubMed DOI PMC
Biggs P.M., Milne B.S., Frazier J.A., McDougall J.S., Stuart J.C. Lymphoproliferative disease in turkeys; Proceedings of the 15th World Poultry Congress, World Poultry Science Association; Washington, DC, USA. 11–16 August 1974; pp. 55–56.
Rous P. A sarcoma of the fowl transmissible by an agent separable from the tumor cells. J. Exp. Med. 1911;13:397–411. doi: 10.1084/jem.13.4.397. PubMed DOI PMC
Baltimore D. Viral RNA-Dependent DNA Polymerase: RNA-Dependent DNA Polymerase in Virions of RNA Tumour Viruses. Nature. 1970;226:1209–1211. doi: 10.1038/2261209a0. PubMed DOI
Temin H.M., Mizutani S. RNA-Dependent DNA Polymerase in Virions of Rous Sarcoma Virus. Nature. 1970;226:1211–1213. doi: 10.1038/2261211a0. PubMed DOI
Stehelin D., Varmus H.E., Bishop J.M., Vogt P.K. DNA Related to the Transforming Gene(s) of Avian Sarcoma Viruses Is Present in Normal Avian DNA. Nature. 1976;260:170–173. doi: 10.1038/260170a0. PubMed DOI
Raji L., Tetteh A., Amin A.R.M.R. Role of C-Src in Carcinogenesis and Drug Resistance. Cancers. 2023;16:32. doi: 10.3390/cancers16010032. PubMed DOI PMC
Bauer A.N., Majumdar N., Williams F., Rajput S., Pokhrel L.R., Cook P.P., Akula S.M. MicroRNAs: Small but Key Players in Viral Infections and Immune Responses to Viral Pathogens. Biology. 2023;12:1334. doi: 10.3390/biology12101334. PubMed DOI PMC
Gallo A., Miceli V., Bulati M., Iannolo G., Contino F., Conaldi P.G. Viral miRNAs as Active Players and Participants in Tumorigenesis. Cancers. 2020;12:358. doi: 10.3390/cancers12020358. PubMed DOI PMC
Islam M.S., Islam A.B.M.M.K. Viral miRNAs Confer Survival in Host Cells by Targeting Apoptosis Related Host Genes. Inform. Med. Unlocked. 2021;22:100501. doi: 10.1016/j.imu.2020.100501. DOI
Paul S., Saikia M., Chakraborty S. Identification of Novel microRNAs in Rous Sarcoma Virus (RSV) and Their Target Sites in Tumor Suppressor Genes of Chicken. Infect. Genet. Evol. 2021;96:105139. doi: 10.1016/j.meegid.2021.105139. PubMed DOI
Brown C.J., Lain S., Verma C.S., Fersht A.R., Lane D.P. Awakening Guardian Angels: Drugging the P53 Pathway. Nat. Rev. Cancer. 2009;9:862–873. doi: 10.1038/nrc2763. PubMed DOI
Cavanagh H., Rogers K.M.A. The Role of BRCA1 and BRCA2 Mutations in Prostate, Pancreatic and Stomach Cancers. Hered. Cancer Clin. Pract. 2015;13:16. doi: 10.1186/s13053-015-0038-x. PubMed DOI PMC
Khare V.M., Saxena V.K., Tomar A., Singh K.P., Singh K.B., Tiwari A.K. MHC-B Haplotypes Impact Susceptibility and Resistance to RSV-A Infection. Front. Biosci. Elite Ed. 2018;10:506–519. doi: 10.2741/e837. PubMed DOI
Wilkinson N.G., Kopulos R.T., Yates L.M., Briles W.E., Taylor R.L. Research Note: Rous Sarcoma Growth Differs among Congenic Lines Containing Major Histocompatibility (B) Complex Recombinants. Poult. Sci. 2021;100:101335. doi: 10.1016/j.psj.2021.101335. PubMed DOI PMC
Khare V.M., Saxena V.K., Tomar A., Nyinawabera A., Singh K.B., Ashby C.R., Jr., Tiwari A.K. Cytokine Gene Expression Following RSV-A Infection. Front. Biosci.-Landmark. 2019;24:463–481. doi: 10.2741/4729. PubMed DOI
Khare V.M., Saxena V.K., Pasternak M.A., Nyinawabera A., Singh K.B., Ashby C.R., Tiwari A.K., Tang Y. The Expression Profiles of Chemokines, Innate Immune and Apoptotic Genes in Tumors Caused by Rous Sarcoma Virus (RSV-A) in Chickens. Genes Immun. 2022;23:12–22. doi: 10.1038/s41435-021-00158-0. PubMed DOI
Mucksová J., Plachý J., Staněk O., Hejnar J., Kalina J., Benešová B., Trefil P. Cytokine Response to the RSV Antigen Delivered by Dendritic Cell-Directed Vaccination in Congenic Chicken Lines. Vet. Res. 2017;48:18. doi: 10.1186/s13567-017-0423-8. PubMed DOI PMC
Frossard J. Retroviridae. In: McVey D.S., Kennedy M., Chengappa M.M., Wilkes R., editors. Veterinary Microbiology. John Wiley & Sons, Inc.; Hoboken, NJ, USA: 2022. pp. 698–727.
Beard J.W. Avian Virus Growths And Theri Etiologic Agents. Adv. Cancer Res. 1963;7:1–127. doi: 10.1016/s0065-230x(08)60982-3. PubMed DOI
Engelke U., Lipsick J.S. Transformation of myelomonocytic cells by the avian myeloblastosis virus is determined by the v-myb oncogene, not by the unique long terminal repeats of the virus. J. Virol. 1994;68:2752–2755. doi: 10.1128/jvi.68.4.2752-2755.1994. PubMed DOI PMC
Ivanov X., Mladenov Z., Nedyalkov S., Todorov T.G. Experimental investigations into avian leucoses. I. Transmission experiments of certain diseases of the avian leukosis complex, found in Bulgaria. Bull. Inst. Path. Comp. Anim. Acad. Bulg. Sci. 1962;9:5–36.
Oh I.H., Reddy E.P. The myb gene family in cell growth, differentiation and apoptosis. Oncogene. 1999;18:3017–3033. doi: 10.1038/sj.onc.1202839. PubMed DOI
Davidson C.J., Guthrie E.E., Lipsick J.S. Duplication and maintenance of the Myb genes of vertebrate animals. Biol. Open. 2013;2:101–110. doi: 10.1242/bio.20123152. PubMed DOI PMC
Li Y., Jin K., van Pelt G.W., van Dam H., Yu X., Mesker W.E., Ten Dijke P., Zhou F., Zhang L. c-Myb Enhances Breast Cancer Invasion and Metastasis through the Wnt/β-Catenin/Axin2 Pathway. Cancer Res. 2016;76:3364–3375. doi: 10.1158/0008-5472.CAN-15-2302. PubMed DOI
Mansour M.R., Abraham B.J., Anders L., Berezovskaya A., Gutierrez A., Durbin A.D., Etchin J., Lawton L., Sallan S.E., Silverman L.B., et al. Oncogene regulation. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science. 2014;346:1373–1377. doi: 10.1126/science.1259037. PubMed DOI PMC
Williams B.B., Wall M., Miao R.Y., Williams B., Bertoncello I., Kershaw M.H., Mantamadiotis T., Haber M., Norris M.D., Gautam A., et al. Induction of T cell-mediated immunity using a c-Myb DNA vaccine in a mouse model of colon cancer. Cancer Immunol. Immunother. 2008;57:1635–1645. doi: 10.1007/s00262-008-0497-2. PubMed DOI PMC
Sun S.S., Fu Y., Lin J.Y. Upregulation of MYBL2independently predicts a poorer prognosis in patients with clear cell renal cell carcinoma. Oncol. Lett. 2020;19:2765–2772. doi: 10.3892/ol.2020.11408. PubMed DOI PMC
Klein G. Herpesviruses and Oncogenesis. Proc. Natl. Acad. Sci. USA. 1972;69:1056–1064. doi: 10.1073/pnas.69.4.1056. PubMed DOI PMC
Chang P.-C., Campbell M., Robertson E.S. Human Oncogenic Herpesvirus and Post-Translational Modifications—Phosphorylation and SUMOylation. Front. Microbiol. 2016;7:962. doi: 10.3389/fmicb.2016.00962. PubMed DOI PMC
Bertzbach L.D., Conradie A.M., You Y., Kaufer B.B. Latest Insights into Marek’s Disease Virus Pathogenesis and Tumorigenesis. Cancers. 2020;12:647. doi: 10.3390/cancers12030647. PubMed DOI PMC
Weiss R.A. The Oncologist’s Debt to the Chicken. Avian Pathol. 1998;27:S8–S15. doi: 10.1080/03079459808419287. DOI
Vishwanatha R., Nair V. Reference Module in Life Sciences. Elsevier; Amsterdam, The Netherlands: 2019. Avian Herpesviruses.
McGeoch D.J., Davison A.J. Chapter 17—The Molecular Evolutionary History of the Herpesviruses. In: Domingo E., Webster R., Holland J., editors. Origin and Evolution of Viruses. Academic Press; London, UK: 1999. pp. 441–465.
Davison A.J. Herpesvirus Systematics. Vet. Microbiol. 2010;143:52–69. doi: 10.1016/j.vetmic.2010.02.014. PubMed DOI PMC
Yu G., Hatta A., Periyannan S., Lagudah E., Wulff B.B.H. Wheat Rust Diseases: Methods and Protocols. Volume 1659. Humana Press; New York, NY, USA: 2017. Isolation of Wheat Genomic DNA for Gene Mapping and Cloning; pp. 207–213. PubMed DOI
Tulman E.R., Afonso C.L., Lu Z., Zsak L., Rock D.L., Kutish G.F. The Genome of a Very Virulent Marek’s Disease Virus. J. Virol. 2000;74:7980–7988. doi: 10.1128/JVI.74.17.7980-7988.2000. PubMed DOI PMC
Osterrieder N., Kamil J.P., Schumacher D., Tischer B.K., Trapp S. Marek’s Disease Virus: From Miasma to Model. Nat. Rev. Microbiol. 2006;4:283–294. doi: 10.1038/nrmicro1382. PubMed DOI
Boodhoo N., Gurung A., Sharif S., Behboudi S. Marek’s Disease in Chickens: A Review with Focus on Immunology. Vet. Res. 2016;47:119. doi: 10.1186/s13567-016-0404-3. PubMed DOI PMC
Witter R.L. Increased Virulence of Marek’s Disease Virus Field Isolates. Avian Dis. 1997;41:149–163. doi: 10.2307/1592455. PubMed DOI
Roh J.H., Kang M., Wei B., Yoon R.H., Seo H.S., Bahng J.Y., Kwon J.T., Cha S.Y., Jang H.K. Efficacy of HVT-IBD vector vaccine compared to attenuated live vaccine using in-ovo vaccination against a Korean very virulent IBDV in commercial broiler chickens. Poult. Sci. 2016;95:1020–1024. doi: 10.3382/ps/pew042. PubMed DOI
Baaten B.J.G., Staines K.A., Smith L.P., Skinner H., Davison T.F., Butter C. Early Replication in Pulmonary B Cells after Infection with Marek’s Disease Herpesvirus by the Respiratory Route. Viral Immunol. 2009;22:431–444. doi: 10.1089/vim.2009.0047. PubMed DOI
Lantier I., Mallet C., Souci L., Larcher T., Conradie A.M., Courvoisier K., Trapp S., Pasdeloup D., Kaufer B.B., Denesvre C. In Vivo Imaging Reveals Novel Replication Sites of a Highly Oncogenic Avian Herpesvirus in Chickens. PLoS Pathog. 2022;18:e1010745. doi: 10.1371/journal.ppat.1010745. PubMed DOI PMC
Calnek B.W., Adldinger H.K., Kahn D.E. Feather Follicle Epithelium: A Source of Enveloped and Infectious Cell-Free Herpesvirus from Marek’s Disease. Avian Dis. 1970;14:219–233. doi: 10.2307/1588466. PubMed DOI
Lee L.F., Zhang H., Heidari M., Lupiani B., Reddy S.M. Evaluation of Factors Affecting Vaccine Efficacy of Recombinant Marek’s Disease Virus Lacking the Meq Oncogene in Chickens. Avian Dis. 2011;55:172–179. doi: 10.1637/9575-101510-Reg.1. PubMed DOI
Baigent S.J., Smith L.P., Nair V.K., Currie R.J.W. Vaccinal Control of Marek’s Disease: Current Challenges, and Future Strategies to Maximize Protection. Vet. Immunol. Immunopathol. 2006;112:78–86. doi: 10.1016/j.vetimm.2006.03.014. PubMed DOI
Lipsick J. A History of Cancer Research: Tumor Viruses. Cold Spring Harb. Perspect. Biol. 2021;13:a035774. doi: 10.1101/cshperspect.a035774. PubMed DOI PMC
Becsei-Kilborn E. Scientific Discovery and Scientific Reputation: The Reception of Peyton Rous’ Discovery of the Chicken Sarcoma Virus. J. Hist. Biol. 2010;43:111–157. doi: 10.1007/s10739-008-9171-y. PubMed DOI
González-Herrero I., Rodríguez-Hernández G., Luengas-Martínez A., Isidro-Hernández M., Jiménez R., García-Cenador M.B., García-Criado F.J., Sánchez-García I., Vicente-Dueñas C. The Making of Leukemia. Int. J. Mol. Sci. 2018;19:1494. doi: 10.3390/ijms19051494. PubMed DOI PMC
Vogt P.K. Retroviral Oncogenes: A Historical Primer. Nat. Rev. Cancer. 2012;12:639–648. doi: 10.1038/nrc3320. PubMed DOI PMC
Mui U.N., Haley C.T., Tyring S.K. Viral Oncology: Molecular Biology and Pathogenesis. J. Clin. Med. 2017;6:111. doi: 10.3390/jcm6120111. PubMed DOI PMC
Campbell K. Infectious Causes of Cancer. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2010. Herpesviruses (Herpesviridae) pp. 91–105.
Javier R.T., Butel J.S. The History of Tumor Virology. Cancer Res. 2008;68:7693–7706. doi: 10.1158/0008-5472.CAN-08-3301. PubMed DOI PMC
M’Fadyan J., Hobday F. Note on the experimental “transmission of warts in the dog”. J. Comp. Pathol. Ther. 1898;11:341–343. doi: 10.1016/S0368-1742(98)80056-8. DOI
Hausen H., Fox J., Wang T.C., Parsonnet J. Infections Causing Human Cancer. John Wiley & Sons; Hoboken, NJ, USA: 2006. p. 517.
Institute of Medicine . To Improve Human Health: A History of the Institute of Medicine. National Academies Press; Washington, DC, USA: 1998. PubMed
White M.K., Pagano J.S., Khalili K. Viruses and Human Cancers: A Long Road of Discovery of Molecular Paradigms. Clin. Microbiol. Rev. 2014;27:463–481. doi: 10.1128/CMR.00124-13. PubMed DOI PMC
Giunta S. Decoding Human Cancer with Whole Genome Sequencing: A Review of PCAWG Project Studies Published in February 2020. Cancer Metastasis Rev. 2021;40:909–924. doi: 10.1007/s10555-021-09969-z. PubMed DOI PMC
Schiller J.T., Lowy D.R. Vaccines to Prevent Infections by Oncoviruses. Annu. Rev. Microbiol. 2010;64:23–41. doi: 10.1146/annurev.micro.112408.134019. PubMed DOI PMC
Shuro A. Review Paper on Approaches in Developing Inbred Lines in Cross-Pollinated Crops. Biochem. Mol. Biol. 2017;2:40. doi: 10.11648/j.bmb.20170204.12. DOI
Xu L., He Y., Ding Y., Liu G.E., Zhang H., Cheng H.H., Taylor R.L., Jr., Song J. Genetic assessment of inbred chicken lines indicates genomic signatures of resistance to Marek’s disease. J. Anim. Sci. Biotechnol. 2018;9:65. doi: 10.1186/s40104-018-0281-x. PubMed DOI PMC
Gul H., Habib G., Khan I.M., Rahman S.U., Khan N.M., Wang H., Khan N.U., Liu Y. Genetic resilience in chickens against bacterial, viral and protozoal pathogens. Front. Vet. Sci. 2022;9:1032983. doi: 10.3389/fvets.2022.1032983. PubMed DOI PMC
Silva A.P.D., Gallardo R.A. The Chicken MHC: Insights into Genetic Resistance, Immunity, and Inflammation Following Infectious Bronchitis Virus Infections. Vaccines. 2020;8:637. doi: 10.3390/vaccines8040637. PubMed DOI PMC
Lengyel E., Burdette J.E., Kenny H.A., Matei D., Pilrose J., Haluska P., Nephew K.P., Hales D.B., Stack M.S. Epithelial ovarian cancer experimental models. Oncogene. 2014;33:3619–3633. doi: 10.1038/onc.2013.321. PubMed DOI PMC
Karnezis A.N., Cho K.R. Preclinical Models of Ovarian Cancer: Pathogenesis, Problems, and Implications for Prevention. Clin. Obstet. Gynecol. 2017;60:789–800. doi: 10.1097/GRF.0000000000000312. PubMed DOI PMC
Tudrej P., Kujawa K.A., Cortez A.J., Lisowska K.M. Characteristics of in Vivo Model Systems for Ovarian Cancer Studies. Diagnostics. 2019;9:120. doi: 10.3390/diagnostics9030120. PubMed DOI PMC
Hawkridge A.M. The Chicken Model of Spontaneous Ovarian Cancer. Proteom. Clin. Appl. 2014;8:689–699. doi: 10.1002/prca.201300135. PubMed DOI PMC
Bernardo A.D.M., Thorsteinsdóttir S., Mummery C.L. Advantages of the Avian Model for Human Ovarian Cancer. Mol. Clin. Oncol. 2015;3:1191–1198. doi: 10.3892/mco.2015.619. PubMed DOI PMC
Fredrickson T.N. Ovarian tumors of the hen. Environ. Health Perspect. 1987;73:35–51. doi: 10.1289/ehp.877335. PubMed DOI PMC
Barnes M.N., Berry W.D., Straughn J.M.J., Kirby T.O., Leath C.A., Huh W.K., Grizzle W.E., Partridge E.E. A Pilot Study of Ovarian Cancer Chemoprevention Using Medroxyprogesterone Acetate in an Avian Model of Spontaneous Ovarian Carcinogenesis. Gynecol. Oncol. 2002;87:57–63. doi: 10.1006/gyno.2002.6806. PubMed DOI
King S.M., Burdette J.E. Evaluating the Progenitor Cells of Ovarian Cancer: Analysis of Current Animal Models. BMB Rep. 2011;44:435–445. doi: 10.5483/BMBRep.2011.44.7.435. PubMed DOI PMC
Barua A., Abramowicz J.S., Bahr J.M., Bitterman P., Dirks A., Holub K.A., Sheiner E., Bradaric M.J., Edassery S.L., Luborsky J.L. Detection of ovarian tumors in chicken by sonography: A step toward early diagnosis in humans? J. Ultrasound Med. 2007;26:909–919. doi: 10.7863/jum.2007.26.7.909. PubMed DOI
Barua A., Bitterman P., Abramowicz J.S., Dirks A.L., Bahr J.M., Hales D.B., Bradaric M.J., Edassery S.L., Rotmensch J., Luborsky J.L. Histopathology of ovarian tumors in laying hens: A preclinical model of human ovarian cancer. Int. J. Gynecol. Cancer. 2009;19:531–539. doi: 10.1111/IGC.0b013e3181a41613. PubMed DOI PMC
Jackson E., Anderson K., Ashwell C., Petitte J., Mozdziak P.E. CA125 Expression in Spontaneous Ovarian Adenocarcinomas from Laying Hens. Gynecol. Oncol. 2007;104:192–198. doi: 10.1016/j.ygyno.2006.07.024. PubMed DOI
Barua A., Bahr J.M. Ovarian Cancer: Applications of Chickens to Humans. Annu. Rev. Anim. Biosci. 2022;10:241–257. doi: 10.1146/annurev-animal-021419-084001. PubMed DOI
Hasan N., Ohman A.W., Dinulescu D.M. The Promise and Challenge of Ovarian Cancer Models. Transl. Cancer Res. 2015;4 doi: 10.3978/j.issn.2218-676X.2015.01.02. PubMed DOI PMC
Ansenberger K., Zhuge Y., Lagman J.A.J., Richards C., Barua A., Bahr J.M., Hales D.B. E-Cadherin Expression in Ovarian Cancer in the Laying Hen, Gallus Domesticus, Compared to Human Ovarian Cancer. Gynecol. Oncol. 2009;113:362–369. doi: 10.1016/j.ygyno.2009.02.011. PubMed DOI PMC
Hakim A.A., Barry C.P., Barnes H.J., Anderson K.E., Petitte J., Whitaker R., Lancaster J.M., Wenham R.M., Carver D.K., Turbov J., et al. Ovarian Adenocarcinomas in the Laying Hen and Women Share Similar Alterations in P53, Ras, and HER-2/Neu. Cancer Prev. Res. 2009;2:114–121. doi: 10.1158/1940-6207.CAPR-08-0065. PubMed DOI
Choi P.-W., So W.W., Yang J., Liu S., Tong K.K., Kwan K.M., Kwok J.S.-L. MicroRNA-200 Family Governs Ovarian Inclusion Cyst Formation and Mode of Ovarian Cancer Spread. Oncogene. 2020;39:4045–4061. doi: 10.1038/s41388-020-1264-x. PubMed DOI
Stammer K., Edassery S.L., Barua A., Bitterman P., Bahr J.M., Hales D.B., Luborsky J. Selenium-Binding Protein 1 Expression in Ovaries and Ovarian Tumors of in the Laying Hen, a Spontaneous Model of Human Ovarian Cancer. Gynecol. Oncol. 2008;109:115–121. doi: 10.1016/j.ygyno.2007.12.030. PubMed DOI PMC
Pal P., Starkweather K.N., Hales K.H., Hales D.B. A Review of Principal Studies on the Development and Treatment of Epithelial Ovarian Cancer in the Laying Hen Gallus Gallus. Comp. Med. 2021;71:271–284. doi: 10.30802/AALAS-CM-20-000116. PubMed DOI PMC
Eilati E., Pan L., Bahr J.M., Hales D.B. Age Dependent Increase in Prostaglandin Pathway Coincides with Onset of Ovarian Cancer in Laying Hens. Prostaglandins Leukot. Essent. Fat. Acids. 2012;87:177–184. doi: 10.1016/j.plefa.2012.09.003. PubMed DOI PMC
Kain K.H., Miller J.W.I., Jones-Paris C.R., Thomason R.T., Lewis J.D., Bader D.M., Barnett J.V., Zijlstra A. The Chick Embryo as an Expanding Experimental Model for Cancer and Cardiovascular Research. Dev. Dyn. 2014;243:216–228. doi: 10.1002/dvdy.24093. PubMed DOI PMC
Sahin K., Yenice E., Tuzcu M., Orhan C., Mizrak C., Ozercan I.H., Sahin N., Yilmaz B., Bilir B., Ozpolat B., et al. Lycopene Protects Against Spontaneous Ovarian Cancer Formation in Laying Hens. J. Cancer Prev. 2018;23:25–36. doi: 10.15430/JCP.2018.23.1.25. PubMed DOI PMC
Sahin K., Yenice E., Bilir B., Orhan C., Tuzcu M., Sahin N., Ozercan I.H., Kabil N., Ozpolat B., Kucuk O. Genistein Prevents Development of Spontaneous Ovarian Cancer and Inhibits Tumor Growth in Hen Model. Cancer Prev. Res. 2019;12:135–146. doi: 10.1158/1940-6207.CAPR-17-0289. PubMed DOI
Dikshit A., Hales K., Hales D.B. Whole Flaxseed Diet Alters Estrogen Metabolism to Promote 2-Methoxtestradiol-Induced Apoptosis in Hen Ovarian Cancer. J. Nutr. Biochem. 2017;42:117–125. doi: 10.1016/j.jnutbio.2017.01.002. PubMed DOI PMC
Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337:816–821. doi: 10.1126/science.1225829. PubMed DOI PMC
Lee K.Y., Choi H.J., Park K.J., Woo S.J., Kim Y.M., Han J.Y. Development and characterization of a CRISPR/Cas9-mediated RAG1 knockout chicken model lacking mature B and T cells. Front. Immunol. 2022;13:892476. doi: 10.3389/fimmu.2022.892476. PubMed DOI PMC
Oishi I., Yoshii K., Miyahara D., Kagami H., Tagami T. Targeted mutagenesis in chicken using CRISPR/Cas9 system. Sci. Rep. 2016;6:23980. doi: 10.1038/srep23980. PubMed DOI PMC
Oishi I., Yoshii K., Miyahara D., Tagami T. Efficient production of human interferon beta in the white of eggs from ovalbumin gene–targeted hens. Sci. Rep. 2018;8:10203. doi: 10.1038/s41598-018-28438-2. PubMed DOI PMC
Rieblinger B., Sid H., Duda D., Bozoglu T., Klinger R., Schlickenrieder A., Lengyel K., Flisikowski K., Flisikowska T., Simm N., et al. Cas9-expressing chickens and pigs as resources for genome editing in livestock. Proc. Natl. Acad. Sci. USA. 2021;118:e2022562118. doi: 10.1073/pnas.2022562118. PubMed DOI PMC
Orelli B.J., Logsdon J.M., Jr., Bishop D.K. Nine novel conserved motifs in BRCA1 identified by the chicken orthologue. Oncogene. 2001;20:4433–4438. doi: 10.1038/sj.onc.1204485. PubMed DOI
Takata M., Tachiiri S., Fujimori A., Thompson L.H., Miki Y., Hiraoka M., Takeda S., Yamazoe M. Conserved domains in the chicken homologue of BRCA2. Oncogene. 2002;21:1130–1134. doi: 10.1038/sj.onc.1205168. PubMed DOI
Prakash V., Carson B.B., Feenstra J.M., Dass R.A., Sekyrova P., Hoshino A., Petersen J., Guo Y., Parks M.M., Kurylo C.M., et al. Ribosome Biogenesis during Cell Cycle Arrest Fuels EMT in Development and Disease. Nat. Commun. 2019;10:2110. doi: 10.1038/s41467-019-10100-8. PubMed DOI PMC
DeBord L.C., Pathak R.R., Villaneuva M., Liu H.-C., Harrington D.A., Yu W., Lewis M.T., Sikora A.G. The Chick Chorioallantoic Membrane (CAM) as a Versatile Patient-Derived Xenograft (PDX) Platform for Precision Medicine and Preclinical Research. Am. J. Cancer Res. 2018;8:1642–1660. PubMed PMC
Palmer T.D., Lewis J., Zijlstra A. Quantitative Analysis of Cancer Metastasis Using an Avian Embryo Model. J. Vis. Exp. 2011;51:2815. doi: 10.3791/2815. PubMed DOI PMC
Bader A.G., Kang S., Vogt P.K. Cancer-Specific Mutations in PIK3CA Are Oncogenic in Vivo. Proc. Natl. Acad. Sci. USA. 2006;103:1475–1479. doi: 10.1073/pnas.0510857103. PubMed DOI PMC
Chambers A.F., Shafir R., Ling V. A Model System for Studying Metastasis Using the Embryonic Chick. Cancer Res. 1982;42:4018–4025. PubMed
Deryugina E.I., Kiosses W.B. Intratumoral Cancer Cell Intravasation Can Occur Independent of Invasion into the Adjacent Stroma. Cell Rep. 2017;19:601–616. doi: 10.1016/j.celrep.2017.03.064. PubMed DOI PMC
Murphy J.B. Transplantability of tissues to the embryo of foreign species: Its bearing on questions of tissue specificity and tumor immunity. J. Exp. Med. 1913;17:482–493. doi: 10.1084/jem.17.4.482. PubMed DOI PMC
Ribatti D. The Chick Embryo Chorioallantoic Membrane as a Model for Tumor Biology. Exp. Cell Res. 2014;328:314–324. doi: 10.1016/j.yexcr.2014.06.010. PubMed DOI
Chen L., Wang S., Feng Y., Zhang J., Du Y., Zhang J., Van Ongeval C., Ni Y., Li Y. Utilisation of Chick Embryo Chorioallantoic Membrane as a Model Platform for Imaging-Navigated Biomedical Research. Cells. 2021;10:463. doi: 10.3390/cells10020463. PubMed DOI PMC
Pawlikowska P., Tayoun T., Oulhen M., Faugeroux V., Rouffiac V., Aberlenc A., Pommier A.L., Honore A., Marty V., Bawa O., et al. Exploitation of the Chick Embryo Chorioallantoic Membrane (CAM) as a Platform for Anti-Metastatic Drug Testing. Sci. Rep. 2020;10:16876. doi: 10.1038/s41598-020-73632-w. PubMed DOI PMC
Ribatti D. The Chick Embryo Chorioallantoic Membrane (CAM) Assay. Reprod. Toxicol. 2017;70:97–101. doi: 10.1016/j.reprotox.2016.11.004. PubMed DOI
Cao J., Liu X., Yang Y., Wei B., Li Q., Mao G., He Y., Li Y., Zheng L., Zhang Q., et al. Decylubiquinone Suppresses Breast Cancer Growth and Metastasis by Inhibiting Angiogenesis via the ROS/P53/ BAI1 Signaling Pathway. Angiogenesis. 2020;23:325–338. doi: 10.1007/s10456-020-09707-z. PubMed DOI
Delloye-Bourgeois C., Bertin L., Thoinet K., Jarrosson L., Kindbeiter K., Buffet T., Tauszig-Delamasure S., Bozon M., Marabelle A., Combaret V., et al. Microenvironment-Driven Shift of Cohesion/Detachment Balance within Tumors Induces a Switch toward Metastasis in Neuroblastoma. Cancer Cell. 2017;32:427–443.e8. doi: 10.1016/j.ccell.2017.09.006. PubMed DOI
Jarrosson L., Dalle S., Costechareyre C., Tang Y., Grimont M., Plaschka M., Lacourrège M., Teinturier R., Le Bouar M., Maucort-Boulch D., et al. An In Vivo Avian Model of Human Melanoma to Perform Rapid and Robust Preclinical Studies. EMBO Mol. Med. 2023;15:e16629. doi: 10.15252/emmm.202216629. PubMed DOI PMC
Leene W., Duyzings M.J., van Steeg C. Lymphoid Stem Cell Identification in the Developing Thymus and Bursa of Fabricius of the Chick. Z. Zellforsch. Mikrosk. Anat. 1973;136:521–533. doi: 10.1007/BF00307368. PubMed DOI
Auerbach R., Akhtar N., Lewis R.L., Shinners B.L. Angiogenesis Assays: Problems and Pitfalls. Cancer Metastasis Rev. 2000;19:167–172. doi: 10.1023/A:1026574416001. PubMed DOI