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Viruses2023; 15(2); 345; doi: 10.3390/v15020345

Papillomavirus-like Particles in Equine Medicine.

Abstract: Papillomaviruses (PVs) are a family of small DNA tumor viruses that can induce benign lesions or cancer in vertebrates. The observation that animal PV capsid-proteins spontaneously self-assemble to empty, highly immunogenic virus-like particles (VLPs) has led to the establishment of vaccines that efficiently protect humans from specific PV infections and associated diseases. We provide an overview of PV-induced tumors in horses and other equids, discuss possible routes of PV transmission in equid species, and present recent developments aiming at introducing the PV VLP-based vaccine technology into equine medicine.
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Publication Date: 2023-01-25 PubMed ID: 36851559PubMed Central: PMC9966523DOI: 10.3390/v15020345Google Scholar: Lookup
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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 article covers the phenomenon of Papillomaviruses (PVs) causing benign lesions or cancer in vertebrates, with a particular focus on horses and other equids. The paper also discusses the development of vaccines that use virus-like particles (VLPs), derived from PV capside-proteins, for the efficient protection against PV infections.

Papillomaviruses and Their Effect on Equids

  • The focus of this research paper is on a specific family of small DNA tumor viruses known as Papillomaviruses (PVs). These viruses are known for their ability to induce benign lesions or cancer in vertebrates, including horses and other equids.
  • These PV-induced tumors are a consequential matter in equine species, as the research sheds light on this specific issue.

Transmission Routes of PV in Equid Species

  • Apart from discussing the effect of PVs on equids, the paper also explores possible routes through which these viruses might be transmitted among equid species.
  • This understanding is crucial in preventive procedures and in curbing the spread of these viruses within the equid population.

Virus-Like Particles (VLPs) based Vaccine

  • The most notable feature of PVs that the study highlights is their method of defense against the capsid-proteins of PVs, which spontaneously self-assemble to form empty, highly immunogenic virus-like particles (VLPs).
  • These VLPs have led to the creation of effective vaccines that can protect human beings from specific PV infections and their associated diseases.
  • The paper discusses recent developments concerning the adaptation of this PV VLP-based vaccine technology for use within equine medicine.

Cite This Article

APA
Hainisch EK, Jindra C, Kirnbauer R, Brandt S. (2023). Papillomavirus-like Particles in Equine Medicine. Viruses, 15(2), 345. https://doi.org/10.3390/v15020345

Publication

Viruses
ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 15
Issue: 2
PII: 345

Researcher Affiliations

Hainisch, Edmund K
  • Research Group Oncology (RGO), Clinical Unit of Equine Surgery, Department for Companion Animals and Horses, Veterinary University, 1210 Vienna, Austria.
Jindra, Christoph
  • Research Group Oncology (RGO), Clinical Unit of Equine Surgery, Department for Companion Animals and Horses, Veterinary University, 1210 Vienna, Austria.
  • Division of Molecular Oncology and Haematology, Karl Landsteiner University of Health Sciences, 3500 Krems an der Donau, Austria.
Kirnbauer, Reinhard
  • Laboratory of Viral Oncology (LVO), Department of Dermatology, Medical University, 1090 Vienna, Austria.
Brandt, Sabine
  • Research Group Oncology (RGO), Clinical Unit of Equine Surgery, Department for Companion Animals and Horses, Veterinary University, 1210 Vienna, Austria.

MeSH Terms

  • Animals
  • Capsid
  • Capsid Proteins / genetics
  • Capsid Proteins / immunology
  • Horses
  • Papillomaviridae / genetics
  • Vaccines, Virus-Like Particle
  • Papillomavirus Infections / prevention & control
  • Papillomavirus Infections / transmission
  • Horse Diseases / prevention & control
  • Horse Diseases / transmission
  • Horse Diseases / virology

Grant Funding

  • P50 CA098252 / NCI NIH HHS

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 93 references
  1. Howley PM, Lowy DR. Papillomaviruses and their replication. Fields Virol 2001;2:2197–2230.
  2. Campo MS. Introduction. Papillomavirus Research: From Natural History to Vaccines and Beyond Caister Academic Press; Norfolk, UK: 2006. pp. 1–2.
  3. 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
  4. 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
  5. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses.. Virology 2004 Jun 20;324(1):17-27.
    doi: 10.1016/j.virol.2004.03.033pubmed: 15183049google scholar: lookup
  6. De Falco F, Cutarelli A, Cuccaro B, Catoi C, De Carlo E, Roperto S. Evidence of a novel cross-species transmission by ovine papillomaviruses.. Transbound Emerg Dis 2022 Nov;69(6):3850-3857.
    doi: 10.1111/tbed.14756pubmed: 36335589google scholar: lookup
  7. Borzacchiello G, Roperto F, Nasir L, Campo MS. Human papillomavirus research: do we still need animal models?. Int J Cancer 2009 Aug 1;125(3):739-40.
    doi: 10.1002/ijc.24430pubmed: 19441096google scholar: lookup
  8. Bosch FX, Burchell AN, Schiffman M, Giuliano AR, de Sanjose S, Bruni L, Tortolero-Luna G, Kjaer SK, Muñoz N. Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia.. Vaccine 2008 Aug 19;26 Suppl 10:K1-16.
    doi: 10.1016/j.vaccine.2008.05.064pubmed: 18847553google scholar: lookup
  9. Campo MS. Bovine papillomavirus and cancer.. Vet J 1997 Nov;154(3):175-88.
    doi: 10.1016/S1090-0233(97)80019-6pubmed: 9414951google scholar: lookup
  10. Daudt C, Da Silva FRC, Lunardi M, Alves CBDT, Weber MN, Cibulski SP, Alfieri AF, Alfieri AA, Canal CW. Papillomaviruses in ruminants: An update.. Transbound Emerg Dis 2018 Oct;65(5):1381-1395.
    doi: 10.1111/tbed.12868pubmed: 29603890google scholar: lookup
  11. Lowy DR. History of papillomavirus research. Papillomaviruses 2010;1:13–44.
  12. Munday JS, Kiupel M. Papillomavirus-associated cutaneous neoplasia in mammals.. Vet Pathol 2010 Mar;47(2):254-64.
    doi: 10.1177/0300985809358604pubmed: 20106770google scholar: lookup
  13. Muñoz N. Human papillomavirus and cancer: the epidemiological evidence.. J Clin Virol 2000 Oct;19(1-2):1-5.
    doi: 10.1016/S1386-6532(00)00125-6pubmed: 11091143google scholar: lookup
  14. Nasir L, Brandt S. Papillomavirus associated diseases of the horse.. Vet Microbiol 2013 Nov 29;167(1-2):159-67.
    doi: 10.1016/j.vetmic.2013.08.003pubmed: 24016387google scholar: lookup
  15. Rector A, Van Ranst M. Animal papillomaviruses.. Virology 2013 Oct;445(1-2):213-23.
    doi: 10.1016/j.virol.2013.05.007pubmed: 23711385google scholar: lookup
  16. The Papillomavirus Episteme. [(accessed on 18 January 2023)]; Available online: https://pave.niaid.nih.gov.
  17. 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
  18. Lunardi M, Alfieri AA, Otonel RA, de Alcântara BK, Rodrigues WB, de Miranda AB, Alfieri AF. Genetic characterization of a novel bovine papillomavirus member of the Deltapapillomavirus genus.. Vet Microbiol 2013 Feb 22;162(1):207-13.
    doi: 10.1016/j.vetmic.2012.08.030pubmed: 22999523google scholar: lookup
  19. Lunardi M, de Alcântara BK, Otonel RA, Rodrigues WB, Alfieri AF, Alfieri AA. Bovine papillomavirus type 13 DNA in equine sarcoids.. J Clin Microbiol 2013 Jul;51(7):2167-71.
    doi: 10.1128/JCM.00371-13pmc: PMC3697707pubmed: 23637294google scholar: lookup
  20. 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
  21. 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
  22. Hainisch EK, Brandt S. Equine Sarcoids. Robinson’s Current Therapy in Equine Medicine Volume 1. Saunders Elsevier; St. Louis, MO, USA: 2015.
    doi: 10.1016/B978-1-4557-4555-5.00214-4google scholar: lookup
  23. Knottenbelt DC. A suggested clinical classification for the equine sarcoid. Clin. Tech. Equine Pract. 2005;4:278–295.
    doi: 10.1053/j.ctep.2005.10.008google scholar: lookup
  24. Knottenbelt DC. The Equine Sarcoid: Why Are There so Many Treatment Options?. Vet Clin North Am Equine Pract 2019 Aug;35(2):243-262.
    doi: 10.1016/j.cveq.2019.03.006pubmed: 31097356google scholar: lookup
  25. Scott DW, Miller WH Jr. Equine Dermatology. Saunders Elsevier St. Louis, MO, USA: 2011. Sarcoid; pp. 479–488.
  26. Nasir L, Reid SWJ. Bovine papillomaviruses and equine sarcoids. Papillomavirus Research: From Natural History to Vaccines and Beyond Caister Academic Press; Norfolk, UK: 2006. pp. 389–397.
  27. OLSON C Jr, COOK RH. Cutaneous sarcoma-like lesions of the horse caused by the agent of bovine papilloma.. Proc Soc Exp Biol Med 1951 Jun;77(2):281-4.
    doi: 10.3181/00379727-77-18750pubmed: 14854020google scholar: lookup
  28. Petti L, DiMaio D. Specific interaction between the bovine papillomavirus E5 transforming protein and the beta receptor for platelet-derived growth factor in stably transformed and acutely transfected cells.. J Virol 1994 Jun;68(6):3582-92.
    doi: 10.1128/jvi.68.6.3582-3592.1994pmc: PMC236862pubmed: 8189497google scholar: lookup
  29. Venuti A, Paolini F, Nasir L, Corteggio A, Roperto S, Campo MS, Borzacchiello G. Papillomavirus E5: the smallest oncoprotein with many functions.. Mol Cancer 2011 Nov 11;10:140.
    doi: 10.1186/1476-4598-10-140pmc: PMC3248866pubmed: 22078316google scholar: lookup
  30. Borzacchiello G. Bovine papillomavirus on the scene of crime: is E5 oncogene the only guilty party?. Infect Agent Cancer 2013 Jul 5;8(1):26.
    doi: 10.1186/1750-9378-8-26pmc: PMC3704702pubmed: 23829702google scholar: lookup
  31. Borzacchiello G, Roperto F. Bovine papillomaviruses, papillomas and cancer in cattle.. Vet Res 2008 Sep-Oct;39(5):45.
    doi: 10.1051/vetres:2008022pubmed: 18479666google scholar: lookup
  32. Marchetti B, Gault EA, Cortese MS, Yuan Z, Ellis SA, Nasir L, Campo MS. Bovine papillomavirus type 1 oncoprotein E5 inhibits equine MHC class I and interacts with equine MHC I heavy chain.. J Gen Virol 2009 Dec;90(Pt 12):2865-2870.
    doi: 10.1099/vir.0.014746-0pubmed: 19675187google scholar: lookup
  33. De Falco F, Cutarelli A, Catoi AF, Uberti BD, Cuccaro B, Roperto S. Bovine delta papillomavirus E5 oncoprotein negatively regulates the cGAS-STING signaling pathway in cattle in a spontaneous model of viral disease.. Front Immunol 2022;13:937736.
    doi: 10.3389/fimmu.2022.937736pmc: PMC9597257pubmed: 36311756google scholar: lookup
  34. De Falco F, Cutarelli A, Gentile I, Cerino P, Uleri V, Catoi AF, Roperto S. Bovine Delta Papillomavirus E5 Oncoprotein Interacts With TRIM25 and Hampers Antiviral Innate Immune Response Mediated by RIG-I-Like Receptors.. Front Immunol 2021;12:658762.
    doi: 10.3389/fimmu.2021.658762pmc: PMC8223750pubmed: 34177899google scholar: lookup
  35. DeMasi J, Huh KW, Nakatani Y, Münger K, Howley PM. Bovine papillomavirus E7 transformation function correlates with cellular p600 protein binding.. Proc Natl Acad Sci U S A 2005 Aug 9;102(32):11486-91.
    doi: 10.1073/pnas.0505322102pmc: PMC1182553pubmed: 16081543google scholar: lookup
  36. Knottenbelt DC. Pascoe’s Principles and Practice of Equine Dermatology. Saunders Elsevier London, UK: 2009. Squamous cell carcinoma; pp. 427–433.
  37. Scott DW, Miller WH Jr. Equine Dermatology. Saunders Elsevier St. Louis, MO, USA: 2011. Squamous cell carcinoma; pp. 473–476.
  38. Mair TS, Walmsley JP, Phillips TJ. Surgical treatment of 45 horses affected by squamous cell carcinoma of the penis and prepuce.. Equine Vet J 2000 Sep;32(5):406-10.
    doi: 10.2746/042516400777591093pubmed: 11037262google scholar: lookup
  39. Scott DW, Miller WH Jr. Equine Dermatology. Saunders Elsevier St. Louis, MO, USA: 2003. Squamous cell carcinoma; pp. 707–712.
  40. van den Top JG, de Heer N, Klein WR, Ensink JM. Penile and preputial squamous cell carcinoma in the horse: a retrospective study of treatment of 77 affected horses.. Equine Vet J 2008 Sep;40(6):533-7.
    doi: 10.2746/042516408X281171pubmed: 18487102google scholar: lookup
  41. Gardiol D, Kühne C, Glaunsinger B, Lee SS, Javier R, Banks L. Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation.. Oncogene 1999 Sep 30;18(40):5487-96.
    doi: 10.1038/sj.onc.1202920pubmed: 10523825google scholar: lookup
  42. Armando F, Mecocci S, Orlandi V, Porcellato I, Cappelli K, Mechelli L, Brachelente C, Pepe M, Gialletti R, Ghelardi A, Passeri B, Razzuoli E. Investigation of the Epithelial to Mesenchymal Transition (EMT) Process in Equine Papillomavirus-2 (EcPV-2)-Positive Penile Squamous Cell Carcinomas.. Int J Mol Sci 2021 Sep 30;22(19).
    doi: 10.3390/ijms221910588pmc: PMC8508821pubmed: 34638929google scholar: lookup
  43. 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
  44. 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/pathogens11020266pmc: PMC8875230pubmed: 35215208google scholar: lookup
  45. 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
  46. Ramsauer AS, Wachoski-Dark GL, Fraefel C, Ackermann M, Brandt S, Grest P, Knight CG, Favrot C, Tobler K. Establishment of a Three-Dimensional In Vitro Model of Equine Papillomavirus Type 2 Infection.. Viruses 2021 Jul 19;13(7).
    doi: 10.3390/v13071404pmc: PMC8310375pubmed: 34372610google scholar: lookup
  47. Sykora S, Samek L, Schönthaler K, Palm F, Borzacchiello G, Aurich C, Brandt S. EcPV-2 is transcriptionally active in equine SCC but only rarely detectable in swabs and semen from healthy horses.. Vet Microbiol 2012 Jul 6;158(1-2):194-8.
    doi: 10.1016/j.vetmic.2012.02.006pubmed: 22386674google scholar: lookup
  48. 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
  49. Aksoy P, Gottschalk EY, Meneses PI. HPV entry into cells.. Mutat Res Rev Mutat Res 2017 Apr-Jun;772:13-22.
    doi: 10.1016/j.mrrev.2016.09.004pmc: PMC5443120pubmed: 28528686google scholar: lookup
  50. 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
  51. 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
  52. Roden RB, Kirnbauer R, Jenson AB, Lowy DR, Schiller JT. Interaction of papillomaviruses with the cell surface.. J Virol 1994 Nov;68(11):7260-6.
    doi: 10.1128/jvi.68.11.7260-7266.1994pmc: PMC237166pubmed: 7933109google scholar: lookup
  53. Roden RB, Lowy DR, Schiller JT. Papillomavirus is resistant to desiccation.. J Infect Dis 1997 Oct;176(4):1076-9.
    doi: 10.1086/516515pubmed: 9333171google scholar: lookup
  54. Campo MS. Bovine papillomavirus: Old system, new lessons. Papillomavirus Research: From Natural History to Vaccines and Beyond Caister Academic Press; Norfolk, UK: 2006. pp. 373–387.
  55. Amtmann E, Müller H, Sauer G. Equine connective tissue tumors contain unintegrated bovine papilloma virus DNA.. J Virol 1980 Sep;35(3):962-4.
    doi: 10.1128/jvi.35.3.962-964.1980pmc: PMC288890pubmed: 6252350google scholar: lookup
  56. Robl MG, Gordon DE, Lee KP, Olson C. Intracranial fibroblastic neoplasms in the hamster from bovine papilloma virus.. Cancer Res 1972 Oct;32(10):2221-5.
    pubmed: 4343012
  57. Brandt S, Haralambus R, Shafti-Keramat S, Steinborn R, Stanek C, Kirnbauer R. A subset of equine sarcoids harbours BPV-1 DNA in a complex with L1 major capsid protein.. Virology 2008 Jun 5;375(2):433-41.
    doi: 10.1016/j.virol.2008.02.014pubmed: 18395238google scholar: lookup
  58. Wilson AD, Armstrong ELR, Gofton RG, Mason J, De Toit N, Day MJ. Characterisation of early and late bovine papillomavirus protein expression in equine sarcoids.. Vet Microbiol 2013 Mar 23;162(2-4):369-380.
    doi: 10.1016/j.vetmic.2012.10.010pubmed: 23123175google scholar: lookup
  59. Bogaert L, Martens A, Kast WM, Van Marck E, De Cock H. Bovine papillomavirus DNA can be detected in keratinocytes of equine sarcoid tumors.. Vet Microbiol 2010 Dec 15;146(3-4):269-75.
    doi: 10.1016/j.vetmic.2010.05.032pubmed: 21095508google scholar: lookup
  60. Brandt S, Tober R, Corteggio A, Burger S, Sabitzer S, Walter I, Kainzbauer C, Steinborn R, Nasir L, Borzacchiello G. BPV-1 infection is not confined to the dermis but also involves the epidermis of equine sarcoids.. Vet Microbiol 2011 May 12;150(1-2):35-40.
    doi: 10.1016/j.vetmic.2010.12.021pubmed: 21242040google scholar: lookup
  61. Hartl B, Hainisch EK, Shafti-Keramat S, Kirnbauer R, Corteggio A, Borzacchiello G, Tober R, Kainzbauer C, Pratscher B, Brandt S. Inoculation of young horses with bovine papillomavirus type 1 virions leads to early infection of PBMCs prior to pseudo-sarcoid formation.. J Gen Virol 2011 Oct;92(Pt 10):2437-2445.
    doi: 10.1099/vir.0.033670-0pmc: PMC5034893pubmed: 21715602google scholar: lookup
  62. Gobeil P, Gault EA, Campo MS, Gow J, Morgan IM, Nasir L. Equine sarcoids are not induced by an infectious cell line.. Equine Vet J 2007 Mar;39(2):189-91.
    doi: 10.2746/042516407X179879pubmed: 17378450google scholar: lookup
  63. Nasir L, Campo MS. Bovine papillomaviruses: their role in the aetiology of cutaneous tumours of bovids and equids.. Vet Dermatol 2008 Oct;19(5):243-54.
    doi: 10.1111/j.1365-3164.2008.00683.xpubmed: 18927950google scholar: lookup
  64. Abel-Reichwald H, Hainisch EK, Zahalka S, Corteggio A, Borzacchiello G, Massa B, Merlone L, Nasir L, Burden F, Brandt S. Epidemiologic analysis of a sarcoid outbreak involving 12 of 111 donkeys in Northern Italy.. Vet Microbiol 2016 Nov 30;196:85-92.
    doi: 10.1016/j.vetmic.2016.10.021pubmed: 27939161google scholar: lookup
  65. Bogaert L, Martens A, De Baere C, Gasthuys F. Detection of bovine papillomavirus DNA on the normal skin and in the habitual surroundings of horses with and without equine sarcoids.. Res Vet Sci 2005 Dec;79(3):253-8.
    doi: 10.1016/j.rvsc.2004.12.003pubmed: 16054896google scholar: lookup
  66. Finlay M, Yuan Z, Burden F, Trawford A, Morgan IM, Campo MS, Nasir L. The detection of Bovine Papillomavirus type 1 DNA in flies.. Virus Res 2009 Sep;144(1-2):315-7.
    doi: 10.1016/j.virusres.2009.04.015pubmed: 19409942google scholar: lookup
  67. Kemp-Symonds JG. The Detection and Sequencing of Bovine Papillomavirus Type 1 and 2 DNA from Musca autumnalis (Diptera: Muscidae) Face Flies Infesting Sarcoid-Affected Horses. Royal Veterinary College; London, UK: 2000.
  68. Knottenbelt DC. Sarcoid. Pascoe’s Principles and Practice of Equine Dermatology Saunders Elsevier; London, UK: 2009. pp. 387–407.
  69. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic.. Proc Natl Acad Sci U S A 1992 Dec 15;89(24):12180-4.
    doi: 10.1073/pnas.89.24.12180pmc: PMC50722pubmed: 1334560google scholar: lookup
  70. Suzich JA, Ghim SJ, Palmer-Hill FJ, White WI, Tamura JK, Bell JA, Newsome JA, Jenson AB, Schlegel R. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas.. Proc Natl Acad Sci U S A 1995 Dec 5;92(25):11553-7.
    doi: 10.1073/pnas.92.25.11553pmc: PMC40440pubmed: 8524802google scholar: lookup
  71. Breitburd F, Kirnbauer R, Hubbert NL, Nonnenmacher B, Trin-Dinh-Desmarquet C, Orth G, Schiller JT, Lowy DR. Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection.. J Virol 1995 Jun;69(6):3959-63.
    doi: 10.1128/jvi.69.6.3959-3963.1995pmc: PMC189126pubmed: 7745754google scholar: lookup
  72. Christensen ND, Reed CA, Cladel NM, Han R, Kreider JW. Immunization with viruslike particles induces long-term protection of rabbits against challenge with cottontail rabbit papillomavirus.. J Virol 1996 Feb;70(2):960-5.
    doi: 10.1128/jvi.70.2.960-965.1996pmc: PMC189900pubmed: 8551636google scholar: lookup
  73. Kirnbauer R, Chandrachud LM, O'Neil BW, Wagner ER, Grindlay GJ, Armstrong A, McGarvie GM, Schiller JT, Lowy DR, Campo MS. Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization.. Virology 1996 May 1;219(1):37-44.
    doi: 10.1006/viro.1996.0220pubmed: 8623552google scholar: lookup
  74. Kirnbauer R. Papillomavirus-like particles for serology and vaccine development.. Intervirology 1996;39(1-2):54-61.
    doi: 10.1159/000150475pubmed: 8957670google scholar: lookup
  75. Schiller JT. Papillomavirus Vaccines. Papillomaviruses 2007;1:337–369.
  76. Markowitz LE, Schiller JT. Human Papillomavirus Vaccines.. J Infect Dis 2021 Sep 30;224(12 Suppl 2):S367-S378.
    doi: 10.1093/infdis/jiaa621pmc: PMC8577198pubmed: 34590141google scholar: lookup
  77. Hainisch EK, Brandt S, Shafti-Keramat S, Van den Hoven R, Kirnbauer R. Safety and immunogenicity of BPV-1 L1 virus-like particles in a dose-escalation vaccination trial in horses.. Equine Vet J 2012 Jan;44(1):107-11.
    doi: 10.1111/j.2042-3306.2011.00390.xpmc: PMC3939654pubmed: 21895749google scholar: lookup
  78. Shafti-Keramat S, Schellenbacher C, Handisurya A, Christensen N, Reininger B, Brandt S, Kirnbauer R. Bovine papillomavirus type 1 (BPV1) and BPV2 are closely related serotypes.. Virology 2009 Oct 10;393(1):1-6.
    doi: 10.1016/j.virol.2009.07.036pmc: PMC3792341pubmed: 19729180google scholar: lookup
  79. Hainisch EK, Abel-Reichwald H, Shafti-Keramat S, Pratscher B, Corteggio A, Borzacchiello G, Wetzig M, Jindra C, Tichy A, Kirnbauer R, Brandt S. Potential of a BPV1 L1 VLP vaccine to prevent BPV1- or BPV2-induced pseudo-sarcoid formation and safety and immunogenicity of EcPV2 L1 VLPs in horse.. J Gen Virol 2017 Feb;98(2):230-241.
    doi: 10.1099/jgv.0.000673pubmed: 28284277google scholar: lookup
  80. Schellenbacher C, Shafti-Keramat S, Huber B, Fink D, Brandt S, Kirnbauer R. Establishment of an in vitro equine papillomavirus type 2 (EcPV2) neutralization assay and a VLP-based vaccine for protection of equids against EcPV2-associated genital tumors.. Virology 2015 Dec;486:284-90.
    doi: 10.1016/j.virol.2015.08.016pubmed: 26519597google scholar: lookup
  81. Harnacker J, Hainisch EK, Shafti-Keramat S, Kirnbauer R, Brandt S. Type-specific L1 virus-like particle-mediated protection of horses from experimental bovine papillomavirus 1-induced pseudo-sarcoid formation is long-lasting.. J Gen Virol 2017 Jun;98(6):1329-1333.
    doi: 10.1099/jgv.0.000791pubmed: 28635592google scholar: lookup
  82. Stanley M, Pinto LA, Trimble C. Human papillomavirus vaccines--immune responses.. Vaccine 2012 Nov 20;30 Suppl 5:F83-7.
    doi: 10.1016/j.vaccine.2012.04.106pubmed: 23199968google scholar: lookup
  83. Brandt S. Immune response to bovine papillomavirus type 1 in equine sarcoid.. Vet J 2016 Oct;216:107-8.
    doi: 10.1016/j.tvjl.2016.07.012pubmed: 27687935google scholar: lookup
  84. Stanley M. Immunobiology of HPV and HPV vaccines.. Gynecol Oncol 2008 May;109(2 Suppl):S15-21.
    doi: 10.1016/j.ygyno.2008.02.003pubmed: 18474288google scholar: lookup
  85. Mueller SN, Mackay LK. Tissue-resident memory T cells: local specialists in immune defence.. Nat Rev Immunol 2016 Feb;16(2):79-89.
    doi: 10.1038/nri.2015.3pubmed: 26688350google scholar: lookup
  86. Pinto LA, Edwards J, Castle PE, Harro CD, Lowy DR, Schiller JT, Wallace D, Kopp W, Adelsberger JW, Baseler MW, Berzofsky JA, Hildesheim A. Cellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles.. J Infect Dis 2003 Jul 15;188(2):327-38.
    doi: 10.1086/376505pubmed: 12854090google scholar: lookup
  87. Pinto LA, Viscidi R, Harro CD, Kemp TJ, García-Piñeres AJ, Trivett M, Demuth F, Lowy DR, Schiller JT, Berzofsky JA, Hildesheim A. Cellular immune responses to HPV-18, -31, and -53 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles.. Virology 2006 Sep 30;353(2):451-62.
    doi: 10.1016/j.virol.2006.06.021pubmed: 16863657google scholar: lookup
  88. 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
  89. Roden RB, Weissinger EM, Henderson DW, Booy F, Kirnbauer R, Mushinski JF, Lowy DR, Schiller JT. Neutralization of bovine papillomavirus by antibodies to L1 and L2 capsid proteins.. J Virol 1994 Nov;68(11):7570-4.
    doi: 10.1128/jvi.68.11.7570-7574.1994pmc: PMC237204pubmed: 7523700google scholar: lookup
  90. Campo MS, Grindlay GJ, O'Neil BW, Chandrachud LM, McGarvie GM, Jarrett WF. Prophylactic and therapeutic vaccination against a mucosal papillomavirus.. J Gen Virol 1993 Jun;74 ( Pt 6):945-53.
    doi: 10.1099/0022-1317-74-6-945pubmed: 8389809google scholar: lookup
  91. Ashrafi GH, Piuko K, Burden F, Yuan Z, Gault EA, Müller M, Trawford A, Reid SWJ, Nasir L, Campo MS. Vaccination of sarcoid-bearing donkeys with chimeric virus-like particles of bovine papillomavirus type 1.. J Gen Virol 2008 Jan;89(Pt 1):148-157.
    doi: 10.1099/vir.0.83267-0pubmed: 18089738google scholar: lookup
  92. Mattil-Fritz S, Scharner D, Piuko K, Thönes N, Gissmann L, Müller H, Müller M. Immunotherapy of equine sarcoid: dose-escalation trial for the use of chimeric papillomavirus-like particles.. J Gen Virol 2008 Jan;89(Pt 1):138-147.
    doi: 10.1099/vir.0.83266-0pubmed: 18089737google scholar: lookup
  93. Schiller JT, Lowy DR. Virus infection and human cancer: an overview.. Recent Results Cancer Res 2014;193:1-10.
    doi: 10.1007/978-3-642-38965-8_1pubmed: 24008290google scholar: lookup

Citations

This article has been cited 3 times.
  1. Maggi R, De Paolis L, De Santis D, Vellone VG, De Ciucis CG, Fruscione F, Mazzocco K, Ghelardi A, Marruchella G, Razzuoli E. Bovine Papillomavirus Type 1 Infection in an Equine Congenital Papilloma. Pathogens 2023 Aug 18;12(8).
    doi: 10.3390/pathogens12081059pubmed: 37624019google scholar: lookup
  2. Mirmiran SD, Li X, Li X, Qian P. Isolation and characterization of Salmonella phages for controlling bacterial infections. Front Vet Sci 2025;12:1695255.
    doi: 10.3389/fvets.2025.1695255pubmed: 41394913google scholar: lookup
  3. De Falco F, Cutarelli A, Pellicanò R, Brandt S, Roperto S. Molecular Detection and Quantification of Ovine Papillomavirus DNA in Equine Sarcoid. Transbound Emerg Dis 2024;2024:6453158.
    doi: 10.1155/2024/6453158pubmed: 40303025google scholar: lookup
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