FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Viruses / Establishment of a Three-Dimensional In Vitro Model of Equin...
Viruses2021; 13(7); 1404; doi: 10.3390/v13071404

Establishment of a Three-Dimensional In Vitro Model of Equine Papillomavirus Type 2 Infection.

Abstract: There is growing evidence that equine papillomavirus type 2 (EcPV2) infection is etiologically associated with the development of genital squamous cell carcinoma (SCC) and precursor lesions in equids. However, the precise mechanisms underlying neoplastic progression remain unknown. To allow the study of EcPV2-induced carcinogenesis, we aimed to establish a primary equine cell culture model of EcPV2 infection. Three-dimensional (3D) raft cultures were generated from equine penile perilesional skin, plaques and SCCs. Using histological, molecular biological and immunohistochemical methods, rafts versus corresponding natural tissue sections were compared with regard to morphology, presence of EcPV2 DNA, presence and location of EcPV2 gene transcripts and expression of epithelial, mesenchymal and tumor/proliferation markers. Raft cultures from perilesional skin harboring only a few EcPV2-positive (EcPV2+) cells accurately recapitulated the differentiation process of normal skin, whilst rafts from EcPV2+ penile plaques were structurally organized but showed early hyperplasia. Rafts from EcPV2+ SCCs exhibited pronounced hyperplasia and marked dysplasia. Raft levels of EcPV2 oncogene transcription (E6/E7) and expression of tumor/proliferation markers p53, Ki67 and MCM7 expression positively correlated with neoplastic progression, again reflecting the natural situation. Three-dimensional raft cultures accurately reflected major features of corresponding ex vivo material, thus constituting a valuable new research model to study EcPV2-induced carcinogenesis.
Get Full Text
Publication Date: 2021-07-19 PubMed ID: 34372610PubMed Central: PMC8310375DOI: 10.3390/v13071404Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research aims to understand the mechanisms of equine papillomavirus type 2 (EcPV2)-induced carcinogenesis by establishing a three-dimensional (3D) culture model from equine penile skin cells. Researchers noted that the cell culture mirrored natural conditions, showing potential as a tool for further study on the matter.

Objective of the Research

  • The objective of this research was to establish a useful 3D in vitro model to study the mechanism of EcPV2-induced carcinogenesis, linked to the development of genital squamous cell carcinoma (SCC) and precursor lesions in equids.

Methodology

  • Three-dimensional raft cultures were generated from equine penile perilesional skin, plaques, and SCCs.
  • The researchers used histological, molecular biological, and immunohistochemical methods to compare rafts versus natural tissue sections in terms of morphology, presence of EcPV2 DNA, presence and location of EcPV2 gene transcripts, and expression of epithelial, mesenchymal, and tumor/proliferation markers.

Findings

  • Raft cultures from perilesional skin with very few EcPV2-positive cells accurately mirrored the differentiation process of normal skin.
  • Rafts from EcPV2-positive penile plaques were structurally organized but showed signs of early hyperplasia (overgrowth of cells).
  • Rafts developed from EcPV2-positive SCCs showed severe hyperplasia and marked dysplasia (abnormal cell growth).
  • There was a positive correlation between raft levels of EcPV2 oncogene transcription (E6/E7) and expression of tumor/proliferation markers, such as p53, Ki67, and MCM7, with neoplastic progression. This again reflected the conditions naturally observed.

Conclusion

  • The research concluded that the 3D raft cultures successfully mirrored the primary features of the corresponding ex vivo material and hence could serve as a valuable research model for studying EcPV2-induced carcinogenesis.

Cite This Article

APA
Ramsauer AS, Wachoski-Dark GL, Fraefel C, Ackermann M, Brandt S, Grest P, Knight CG, Favrot C, Tobler K. (2021). Establishment of a Three-Dimensional In Vitro Model of Equine Papillomavirus Type 2 Infection. Viruses, 13(7), 1404. https://doi.org/10.3390/v13071404

Publication

Viruses
ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 13
Issue: 7
PII: 1404

Researcher Affiliations

Ramsauer, Anna Sophie
  • Institute of Virology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.
  • Dermatology Unit, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.
  • Internal Medicine, University Equine Clinic, University of Veterinary Medicine, 1210 Vienna, Austria.
Wachoski-Dark, Garrett Louis
  • Department of Veterinary Clinical and Diagnostic Sciences, Faculty of Veterinary Medicine, University of Calgary, Calgary, AB T2N 1N4, Canada.
Fraefel, Cornel
  • Institute of Virology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.
Ackermann, Mathias
  • Institute of Virology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.
Brandt, Sabine
  • Research Group Oncology, University Equine Clinic, University of Veterinary Medicine, 1210 Vienna, Austria.
Grest, Paula
  • Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.
Knight, Cameron Greig
  • Department of Veterinary Clinical and Diagnostic Sciences, Faculty of Veterinary Medicine, University of Calgary, Calgary, AB T2N 1N4, Canada.
Favrot, Claude
  • Dermatology Unit, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.
Tobler, Kurt
  • Institute of Virology, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland.

MeSH Terms

  • Animals
  • Carcinogenesis
  • Carcinoma, Squamous Cell / virology
  • Cell Culture Techniques / methods
  • DNA, Viral / genetics
  • Horse Diseases / virology
  • Horses
  • Hyperplasia / veterinary
  • Hyperplasia / virology
  • Male
  • Papillomaviridae / classification
  • Papillomaviridae / genetics
  • Papillomaviridae / pathogenicity
  • Papillomavirus Infections / complications
  • Papillomavirus Infections / veterinary
  • Papillomavirus Infections / virology
  • Penis / cytology
  • Penis / virology

Conflict of Interest Statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

This article includes 50 references
  1. Campo MS. Papillomavirus Research: From Natural History to Vaccines and Beyond.. 1st ed. Caister Academic Press; Norfolk, UK: 2006. Introduction; pp. 1–2.
  2. Campo MS. Animal models of papillomavirus pathogenesis.. Virus Res 2002 Nov;89(2):249-61.
    doi: 10.1016/S0168-1702(02)00193-4pubmed: 12445664google scholar: lookup
  3. Doorbar J. The papillomavirus life cycle.. J Clin Virol 2005 Mar;32 Suppl 1:S7-15.
    doi: 10.1016/j.jcv.2004.12.006pubmed: 15753007google scholar: lookup
  4. Day PM, Lowy DR, Schiller JT. Papillomaviruses infect cells via a clathrin-dependent pathway.. Virology 2003 Mar 1;307(1):1-11.
    doi: 10.1016/S0042-6822(02)00143-5pubmed: 12667809google scholar: lookup
  5. Giroglou T, Florin L, Schäfer F, Streeck RE, Sapp M. Human papillomavirus infection requires cell surface heparan sulfate.. J Virol 2001 Feb;75(3):1565-70.
    doi: 10.1128/JVI.75.3.1565-1570.2001pmc: PMC114064pubmed: 11152531google scholar: lookup
  6. Spoden G, Freitag K, Husmann M, Boller K, Sapp M, Lambert C, Florin L. Clathrin- and caveolin-independent entry of human papillomavirus type 16--involvement of tetraspanin-enriched microdomains (TEMs).. PLoS One 2008 Oct 2;3(10):e3313.
    doi: 10.1371/journal.pone.0003313pmc: PMC2561052pubmed: 18836553google scholar: lookup
  7. Graham S. Papillomavirus Research: From Natural History to Vaccines and Beyond.. 1st ed. Caister Academic Press; Norfolk, UK: 2006. Late events in the life cycle of human papillomaviruses; pp. 193–212.
  8. Chambers G, Ellsmore VA, O'Brien PM, Reid SWJ, Love S, Campo MS, Nasir L. Association of bovine papillomavirus with the equine sarcoid.. J Gen Virol 2003 May;84(Pt 5):1055-1062.
    doi: 10.1099/vir.0.18947-0pubmed: 12692268google scholar: lookup
  9. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, Stanley MA. The biology and life-cycle of human papillomaviruses.. Vaccine 2012 Nov 20;30 Suppl 5:F55-70.
    doi: 10.1016/j.vaccine.2012.06.083pubmed: 23199966google scholar: lookup
  10. Van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D, Liou D, Sun Q, Kaur R, Huyen Y, McBride AA. The Papillomavirus Episteme: a major update to the papillomavirus sequence database.. Nucleic Acids Res 2017 Jan 4;45(D1):D499-D506.
    doi: 10.1093/nar/gkw879pmc: PMC5210616pubmed: 28053164google scholar: lookup
  11. Dayyani F, Etzel CJ, Liu M, Ho CH, Lippman SM, Tsao AS. Meta-analysis of the impact of human papillomavirus (HPV) on cancer risk and overall survival in head and neck squamous cell carcinomas (HNSCC).. Head Neck Oncol 2010 Jun 29;2:15.
    doi: 10.1186/1758-3284-2-15pmc: PMC2908081pubmed: 20587061google scholar: lookup
  12. Scott DW, Miller WH Jr. Equine Dermatology.. 1st ed. Saunders Elsevier; St. Louis, MO, USA: 2003. Squamous cell carcinoma; pp. 707–712.
  13. Knottenbelt DC, Patterson-Kane JC, Snalune KL. Squamous Cell Carcinoma.. Elsevier BV; Amsterdam, The Netherlands: 2015. pp. 220–236.
  14. Bogaert L, Willemsen A, Vanderstraeten E, Bracho MA, De Baere C, Bravo IG, Martens A. EcPV2 DNA in equine genital squamous cell carcinomas and normal genital mucosa.. Vet Microbiol 2012 Jul 6;158(1-2):33-41.
    doi: 10.1016/j.vetmic.2012.02.005pubmed: 22397936google scholar: lookup
  15. Knight CG, Munday JS, Peters J, Dunowska M. Equine penile squamous cell carcinomas are associated with the presence of equine papillomavirus type 2 DNA sequences.. Vet Pathol 2011 Nov;48(6):1190-4.
    doi: 10.1177/0300985810396516pubmed: 21282669google scholar: lookup
  16. Lange CE, Tobler K, Lehner A, Grest P, Welle MM, Schwarzwald CC, Favrot C. EcPV2 DNA in equine papillomas and in situ and invasive squamous cell carcinomas supports papillomavirus etiology.. Vet Pathol 2013 Jul;50(4):686-92.
    doi: 10.1177/0300985812463403pubmed: 23064881google scholar: lookup
  17. Scase T, Brandt S, Kainzbauer C, Sykora S, Bijmholt S, Hughes K, Sharpe S, Foote A. Equus caballus papillomavirus-2 (EcPV-2): an infectious cause for equine genital cancer?. Equine Vet J 2010 Nov;42(8):738-45.
    doi: 10.1111/j.2042-3306.2010.00311.xpubmed: 21039805google scholar: lookup
  18. Sykora S, Brandt S. Papillomavirus infection and squamous cell carcinoma in horses.. Vet J 2017 May;223:48-54.
    doi: 10.1016/j.tvjl.2017.05.007pubmed: 28671071google scholar: lookup
  19. Sykora S, Jindra C, Hofer M, Steinborn R, Brandt S. Equine papillomavirus type 2: An equine equivalent to human papillomavirus 16?. Vet J 2017 Jul;225:3-8.
    doi: 10.1016/j.tvjl.2017.04.014pubmed: 28720295google scholar: lookup
  20. Ramsauer AS, Kubacki J, Favrot C, Ackermann M, Fraefel C, Tobler K. RNA-seq analysis in equine papillomavirus type 2-positive carcinomas identifies affected pathways and potential cancer markers as well as viral gene expression and splicing events.. J Gen Virol 2019 Jun;100(6):985-998.
    doi: 10.1099/jgv.0.001267pubmed: 31084699google scholar: lookup
  21. Kainzbauer C, Rushton J, Tober R, Scase T, Nell B, Sykora S, Brandt S. Bovine papillomavirus type 1 and Equus caballus papillomavirus 2 in equine squamous cell carcinoma of the head and neck in a Connemara mare.. Equine Vet J 2012 Jan;44(1):112-5.
    doi: 10.1111/j.2042-3306.2010.00358.xpubmed: 21668491google scholar: lookup
  22. Alloway E, Linder K, May S, Rose T, DeLay J, Bender S, Tucker A, Luff J. A Subset of Equine Gastric Squamous Cell Carcinomas Is Associated With Equus Caballus Papillomavirus-2 Infection.. Vet Pathol 2020 May;57(3):427-431.
    doi: 10.1177/0300985820908797pmc: PMC7335262pubmed: 32180540google scholar: lookup
  23. Knight CG, Dunowska M, Munday JS, Peters-Kennedy J, Rosa BV. Comparison of the levels of Equus caballus papillomavirus type 2 (EcPV-2) DNA in equine squamous cell carcinomas and non-cancerous tissues using quantitative PCR.. Vet Microbiol 2013 Sep 27;166(1-2):257-62.
    doi: 10.1016/j.vetmic.2013.06.004pubmed: 23845733google scholar: lookup
  24. Wilson R, Laimins LA. Differentiation of HPV-containing cells using organotypic "raft" culture or methylcellulose.. Methods Mol Med 2005;119:157-69.
    pubmed: 16350403doi: 10.1385/1-59259-982-6:157google scholar: lookup
  25. Liu X, Krawczyk E, Suprynowicz FA, Palechor-Ceron N, Yuan H, Dakic A, Simic V, Zheng YL, Sripadhan P, Chen C, Lu J, Hou TW, Choudhury S, Kallakury B, Tang DG, Darling T, Thangapazham R, Timofeeva O, Dritschilo A, Randell SH, Albanese C, Agarwal S, Schlegel R. Conditional reprogramming and long-term expansion of normal and tumor cells from human biospecimens.. Nat Protoc 2017 Feb;12(2):439-451.
    doi: 10.1038/nprot.2016.174pmc: PMC6195120pubmed: 28125105google scholar: lookup
  26. Alkhilaiwi F, Wang L, Zhou D, Raudsepp T, Ghosh S, Paul S, Palechor-Ceron N, Brandt S, Luff J, Liu X, Schlegel R, Yuan H. Long-term expansion of primary equine keratinocytes that maintain the ability to differentiate into stratified epidermis.. Stem Cell Res Ther 2018 Jul 4;9(1):181.
    doi: 10.1186/s13287-018-0918-xpmc: PMC6032561pubmed: 29973296google scholar: lookup
  27. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, Haddad BR, Rhim JS, Dritschilo A, Riegel A, McBride A, Schlegel R. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells.. Am J Pathol 2012 Feb;180(2):599-607.
    doi: 10.1016/j.ajpath.2011.10.036pmc: PMC3349876pubmed: 22189618google scholar: lookup
  28. Ramsauer AS, Wachoski-Dark GL, Fraefel C, Tobler K, Brandt S, Knight CG, Favrot C, Grest P. Paving the way for more precise diagnosis of EcPV2-associated equine penile lesions.. BMC Vet Res 2019 Oct 22;15(1):356.
    doi: 10.1186/s12917-019-2097-0pmc: PMC6805557pubmed: 31640696google scholar: lookup
  29. Zhu KW, Affolter VK, Gaynor AM, Dela Cruz FN Jr, Pesavento PA. Equine Genital Squamous Cell Carcinoma: In Situ Hybridization Identifies a Distinct Subset Containing Equus caballus Papillomavirus 2.. Vet Pathol 2015 Nov;52(6):1067-72.
    doi: 10.1177/0300985815583095pubmed: 25967135google scholar: lookup
  30. Matoltsy AG. Keratinization.. J Invest Dermatol 1976 Jul;67(1):20-5.
    doi: 10.1111/1523-1747.ep12512473pubmed: 778293google scholar: lookup
  31. Guiraud B, Hernandez-Pigeon H, Ceruti I, Mas S, Palvadeau Y, Saint-Martory C, Castex-Rizzi N, Duplan H, Bessou-Touya S. Characterization of a human epidermis model reconstructed from hair follicle keratinocytes and comparison with two commercially models and native skin.. Int J Cosmet Sci 2014 Oct;36(5):485-93.
    doi: 10.1111/ics.12150pubmed: 25065839google scholar: lookup
  32. Balansin Rigon R, Kaessmeyer S, Wolff C, Hausmann C, Zhang N, Sochorová M, Kováčik A, Haag R, Vávrová K, Ulrich M, Schäfer-Korting M, Zoschke C. Ultrastructural and Molecular Analysis of Ribose-Induced Glycated Reconstructed Human Skin.. Int J Mol Sci 2018 Nov 8;19(11).
    doi: 10.3390/ijms19113521pmc: PMC6275002pubmed: 30413126google scholar: lookup
  33. Cerrato S, Ramió-Lluch L, Brazís P, Rabanal RM, Fondevila D, Puigdemont A. Development and characterization of an equine skin-equivalent model.. Vet Dermatol 2014 Oct;25(5):475-e77.
    doi: 10.1111/vde.12134pubmed: 25041278google scholar: lookup
  34. Isaacson Wechsler E, Wang Q, Roberts I, Pagliarulo E, Jackson D, Untersperger C, Coleman N, Griffin H, Doorbar J. Reconstruction of human papillomavirus type 16-mediated early-stage neoplasia implicates E6/E7 deregulation and the loss of contact inhibition in neoplastic progression.. J Virol 2012 Jun;86(11):6358-64.
    doi: 10.1128/JVI.07069-11pmc: PMC3372204pubmed: 22457518google scholar: lookup
  35. Anacker D, Moody C. Generation of organotypic raft cultures from primary human keratinocytes.. J Vis Exp 2012 Feb 22;(60).
    doi: 10.3791/3668pmc: PMC3376940pubmed: 22395296google scholar: lookup
  36. Deng H, Hillpot E, Mondal S, Khurana KK, Woodworth CD. HPV16-Immortalized Cells from Human Transformation Zone and Endocervix are More Dysplastic than Ectocervical Cells in Organotypic Culture.. Sci Rep 2018 Oct 18;8(1):15402.
    doi: 10.1038/s41598-018-33865-2pmc: PMC6194146pubmed: 30337615google scholar: lookup
  37. Srivastava K, Pickard A, McDade S, McCance DJ. p63 drives invasion in keratinocytes expressing HPV16 E6/E7 genes through regulation of Src-FAK signalling.. Oncotarget 2017 Mar 7;8(10):16202-16219.
    doi: 10.18632/oncotarget.3892pmc: PMC5369957pubmed: 26001294google scholar: lookup
  38. Evans MF, Peng Z, Clark KM, Adamson CS, Ma XJ, Wu X, Wang H, Luo Y, Cooper K. HPV E6/E7 RNA in situ hybridization signal patterns as biomarkers of three-tier cervical intraepithelial neoplasia grade.. PLoS One 2014;9(3):e91142.
    doi: 10.1371/journal.pone.0091142pmc: PMC3953338pubmed: 24625757google scholar: lookup
  39. Johansson C, Schwartz S. Regulation of human papillomavirus gene expression by splicing and polyadenylation.. Nat Rev Microbiol 2013 Apr;11(4):239-51.
    doi: 10.1038/nrmicro2984pubmed: 23474685google scholar: lookup
  40. Gilles C, Polette M, Piette J, Delvigne AC, Thompson EW, Foidart JM, Birembaut P. Vimentin expression in cervical carcinomas: association with invasive and migratory potential.. J Pathol 1996 Oct;180(2):175-80.
    doi: 10.1002/(SICI)1096-9896(199610)180:2<175::AID-PATH630>3.0.CO;2-Gpubmed: 8976877google scholar: lookup
  41. Franke WW, Schmid E, Winter S, Osborn M, Weber K. Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates.. Exp Cell Res 1979 Oct 1;123(1):25-46.
    doi: 10.1016/0014-4827(79)90418-Xpubmed: 114401google scholar: lookup
  42. Virtanen I, Lehto VP, Lehtonen E, Vartio T, Stenman S, Kurki P, Wager O, Small JV, Dahl D, Badley RA. Expression of intermediate filaments in cultured cells.. J Cell Sci 1981 Aug;50:45-63.
    doi: 10.1242/jcs.50.1.45pubmed: 7033254google scholar: lookup
  43. Steenbergen RD, Parker JN, Isern S, Snijders PJ, Walboomers JM, Meijer CJ, Broker TR, Chow LT. Viral E6-E7 transcription in the basal layer of organotypic cultures without apparent p21cip1 protein precedes immortalization of human papillomavirus type 16- and 18-transfected human keratinocytes.. J Virol 1998 Jan;72(1):749-57.
    doi: 10.1128/JVI.72.1.749-757.1998pmc: PMC109431pubmed: 9420282google scholar: lookup
  44. Silva DC, Gonçalves AK, Cobucci RN, Mendonça RC, Lima PH, Cavalcanti G Júnior. Immunohistochemical expression of p16, Ki-67 and p53 in cervical lesions - A systematic review.. Pathol Res Pract 2017 Jul;213(7):723-729.
    doi: 10.1016/j.prp.2017.03.003pubmed: 28554769google scholar: lookup
  45. Gariglio P, Organista-Nava J, Alvarez-Rios E. Role of HR-HPVs E6 and E7 Oncoproteins in Cervical Carcinogenesis.. J. Mol. Genet. Med. 2016;2016:1–11.
    doi: 10.4172/1747-0862.1000216google scholar: lookup
  46. Kho EY, Wang HK, Banerjee NS, Broker TR, Chow LT. HPV-18 E6 mutants reveal p53 modulation of viral DNA amplification in organotypic cultures.. Proc Natl Acad Sci U S A 2013 May 7;110(19):7542-9.
    doi: 10.1073/pnas.1304855110pmc: PMC3651465pubmed: 23572574google scholar: lookup
  47. Martinez-Zapien D, Ruiz FX, Poirson J, Mitschler A, Ramirez J, Forster A, Cousido-Siah A, Masson M, Vande Pol S, Podjarny A, Travé G, Zanier K. Structure of the E6/E6AP/p53 complex required for HPV-mediated degradation of p53.. Nature 2016 Jan 28;529(7587):541-5.
    doi: 10.1038/nature16481pmc: PMC4853763pubmed: 26789255google scholar: lookup
  48. Brimer N, Drews CM, Vande Pol SB. Association of papillomavirus E6 proteins with either MAML1 or E6AP clusters E6 proteins by structure, function, and evolutionary relatedness.. PLoS Pathog 2017 Dec;13(12):e1006781.
    doi: 10.1371/journal.ppat.1006781pmc: PMC5760104pubmed: 29281732google scholar: lookup
  49. Murnyák B, Hortobágyi T. Immunohistochemical correlates of TP53 somatic mutations in cancer.. Oncotarget 2016 Oct 4;7(40):64910-64920.
    doi: 10.18632/oncotarget.11912pmc: PMC5323125pubmed: 27626311google scholar: lookup
  50. Ando K, Oki E, Saeki H, Yan Z, Tsuda Y, Hidaka G, Kasagi Y, Otsu H, Kawano H, Kitao H, Morita M, Maehara Y. Discrimination of p53 immunohistochemistry-positive tumors by its staining pattern in gastric cancer.. Cancer Med 2015 Jan;4(1):75-83.
    doi: 10.1002/cam4.346pmc: PMC4312120pubmed: 25354498google scholar: lookup

Citations

This article has been cited 2 times.
  1. Hainisch EK, Jindra C, Kirnbauer R, Brandt S. Papillomavirus-like Particles in Equine Medicine. Viruses 2023 Jan 25;15(2).
    doi: 10.3390/v15020345pubmed: 36851559google scholar: lookup
  2. Strohmayer C, Klang A, Kummer S, Walter I, Jindra C, Weissenbacher-Lang C, Redmer T, Kneissl S, Brandt S. Tumor Cell Plasticity in Equine Papillomavirus-Positive Versus-Negative Squamous Cell Carcinoma of the Head and Neck. Pathogens 2022 Feb 18;11(2).
    doi: 10.3390/pathogens11020266pubmed: 35215208google scholar: lookup
Subscribe to our newsletter
Join 99,105 horse owners like you who receive our email updates on horse health and nutrition.