FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Sci Rep / Equine penile squamous cell carcinoma: expression of biomark...
Scientific reports2020; 10(1); 7863; doi: 10.1038/s41598-020-64014-3

Equine penile squamous cell carcinoma: expression of biomarker proteins and EcPV2.

Abstract: Equine penile squamous cell carcinoma (EpSCC) is a relatively common cutaneous neoplasm with a poor prognosis. In this study, we aimed to determine the protein expression and colocalisation of FRA1, c-Myc, Cyclin D1, and MMP7 in normal (NT), tumour (T), hyperplastic epidermis and/or squamous papilloma (Hyp/Pap), poorly-differentiated (PDSCC), or well-differentiated (WDSCC) EpSCC using a tissue array approach. Further objectives were to correlate protein expression to (i) levels of inflammation, using a convolutional neural network (ii) equine papillomavirus 2 (EcPV2) infection, detected using PCR amplification. We found an increase in expression of FRA1 in EpSCC compared to NT samples. c-Myc expression was higher in Hyp/Pap and WDSCC but not PDSCC whereas MMP7 was reduced in WDSCC compared with NT. There was a significant increase in the global intersection coefficient (GIC) of FRA1 with MMP7, c-Myc, and Cyclin D1 in EpSCC. Conversely, GIC for MMP7 with c-Myc was reduced in EpSCC tissue. Inflammation was positively associated with EcPV2 infection in both NT and EpSCC but not Hyp/Pap. Changes in protein expression could be correlated with EcPV2 for Cyclin D1 and c-Myc. Our results evaluate novel biomarkers of EpSCC and a putative correlation between the expression of biomarkers, EcPV2 infection and inflammation.
Get Full Text
Publication Date: 2020-05-12 PubMed ID: 32398763PubMed Central: PMC7217868DOI: 10.1038/s41598-020-64014-3Google 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 given research article investigates the protein expression relevant to equine penile squamous cell carcinoma (EpSCC) and its relation to inflammation and equine papillomavirus 2 (EcPV2) infection. The study also examines the potential contributions of variations in these protein levels to EpSCC.

Methods and Materials

  • The analysis was conducted by assessing protein expression and co-localization of FRA1, c-Myc, Cyclin D1, and MMP7 in different types of tissue samples. They used tissue samples that were normal (NT), cancerous (T), had hyperplastic epidermis and/or squamous papilloma (Hyp/Pap), poorly differentiated EpSCC (PDSCC), or well-differentiated EpSCC (WDSCC).
  • A tissue array approach was used for the mentioned assessment.
  • The other objectives of the study were to explore the relationship between protein expression and inflammation levels, and the presence of EcPV2 infection. Inflammation was measured using a computational method called a convolutional neural network, and the EcPV2 infection was detected through a lab technique called PCR amplification.

Results

  • Results of this study showed an increase in the expression of the protein FRA1 in EpSCC compared to NT samples. Also, c-Myc expression was found to be higher in Hyp/Pap and WDSCC but not in PDSCC samples. Moreover, the expression of MMP7 was reduced in WDSCC compared with NT samples.
  • The findings indicated an important increase in the global intersection coefficient (GIC) of FRA1 along with MMP7, c-Myc, and Cyclin D1 in EpSCC tissues. However, the GIC for MMP7 and c-Myc was reduced in the tissues affected by EpSCC.
  • They found that inflammation was positively related to EcPV2 infection in both, the NT and EpSCC samples but not in the Hyp/Pap samples.
  • Furthermore, the alterations in the expression of Cyclin D1 and c-Myc proteins could be associated with the presence of EcPV2.

Conclusion

  • The study concluded that novel biomarkers that could be influential in evaluating EpSCC were discovered and the results indicated a probable correlation between the expression of specific biomarkers, EcPV2 infection, and inflammation levels.

Cite This Article

APA
Arthurs C, Suarez-Bonnet A, Willis C, Xie B, Machulla N, Mair TS, Cao K, Millar M, Thrasivoulou C, Priestnall SL, Ahmed A. (2020). Equine penile squamous cell carcinoma: expression of biomarker proteins and EcPV2. Sci Rep, 10(1), 7863. https://doi.org/10.1038/s41598-020-64014-3

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 10
Issue: 1
Pages: 7863
PII: 7863

Researcher Affiliations

Arthurs, Callum
  • Prostate Cancer Research Centre at the Centre for Stem Cells and Regenerative Medicine, King's College London, London, United Kingdom.
Suarez-Bonnet, Alejandro
  • Department of Pathobiology and Population Sciences, Royal Veterinary College, Hertfordshire, UK.
Willis, Claire
  • Department of Pathobiology and Population Sciences, Royal Veterinary College, Hertfordshire, UK.
Xie, Boyu
  • Prostate Cancer Research Centre at the Centre for Stem Cells and Regenerative Medicine, King's College London, London, United Kingdom.
Machulla, Natalie
  • Prostate Cancer Research Centre at the Centre for Stem Cells and Regenerative Medicine, King's College London, London, United Kingdom.
Mair, Tim S
  • Bell Equine Veterinary Clinic, Maidstone, UK.
Cao, Kevin
  • Prostate Cancer Research Centre at the Centre for Stem Cells and Regenerative Medicine, King's College London, London, United Kingdom.
Millar, Michael
  • Queen's Medical Research Institute, University of Edinburgh, Edinburgh, United Kingdom.
Thrasivoulou, Christopher
  • Research Department of Cell and Developmental Biology, The Centre for Cell and Molecular Dynamics, Rockefeller Building, University College London, London, United Kingdom.
Priestnall, Simon L
  • Department of Pathobiology and Population Sciences, Royal Veterinary College, Hertfordshire, UK.
Ahmed, Aamir
  • Prostate Cancer Research Centre at the Centre for Stem Cells and Regenerative Medicine, King's College London, London, United Kingdom. aamir.ahmed@kcl.ac.uk.

MeSH Terms

  • Animals
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Carcinoma, Squamous Cell / diagnosis
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / virology
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • Gene Expression Regulation, Neoplastic
  • Horses
  • Male
  • Matrix Metalloproteinase 7 / genetics
  • Matrix Metalloproteinase 7 / metabolism
  • Papillomaviridae / isolation & purification
  • Papillomaviridae / physiology
  • Papillomavirus Infections / diagnosis
  • Papillomavirus Infections / genetics
  • Papillomavirus Infections / virology
  • Penile Neoplasms / diagnosis
  • Penile Neoplasms / genetics
  • Penile Neoplasms / virology
  • Protein Binding
  • Proto-Oncogene Proteins c-fos / genetics
  • Proto-Oncogene Proteins c-fos / metabolism
  • Proto-Oncogene Proteins c-myc / genetics
  • Proto-Oncogene Proteins c-myc / metabolism
  • ROC Curve
  • Tissue Array Analysis / methods

Grant Funding

  • MR/N022556/1 / Medical Research Council

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 67 references
  1. Valentine BA. Survey of equine cutaneous neoplasia in the Pacific Northwest.. J Vet Diagn Invest 2006 Jan;18(1):123-6.
    doi: 10.1177/104063870601800121pubmed: 16566271google scholar: lookup
  2. 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
  3. Scott D, Miller W. Neoplasms, cysts, hamartomas and keratoses. Equine dermatology 468-516 (2011).
  4. Van Den Top JG, Ensink JM, Gröne A, Klein WR, Barneveld A, Van Weeren PR. Penile and preputial tumours in the horse: literature review and proposal of a standardised approach.. Equine Vet J 2010 Nov;42(8):746-57.
    doi: 10.1111/j.2042-3306.2010.00290.xpubmed: 21039806google scholar: lookup
  5. Theilen GH, Madewell BR. Veterinary cancer medicine. Lea & Febiger Philadelphia, 1987.
  6. Knowles EJ, Tremaine WH, Pearson GR, Mair TS. A database survey of equine tumours in the United Kingdom.. Equine Vet J 2016 May;48(3):280-4.
    doi: 10.1111/evj.12421pubmed: 25594351google scholar: lookup
  7. 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
  8. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent.. Cancer Cell 2005 May;7(5):411-23.
    doi: 10.1016/j.ccr.2005.04.014pubmed: 15894262google scholar: lookup
  9. Grivennikov SI, Karin M. Inflammation and oncogenesis: a vicious connection.. Curr Opin Genet Dev 2010 Feb;20(1):65-71.
    doi: 10.1016/j.gde.2009.11.004pmc: PMC2821983pubmed: 20036794google scholar: lookup
  10. Dürst M, Gissmann L, Ikenberg H, zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions.. Proc Natl Acad Sci U S A 1983 Jun;80(12):3812-5.
    doi: 10.1073/pnas.80.12.3812pmc: PMC394142pubmed: 6304740google scholar: lookup
  11. Chaturvedi AK. Beyond cervical cancer: burden of other HPV-related cancers among men and women.. J Adolesc Health 2010 Apr;46(4 Suppl):S20-6.
    doi: 10.1016/j.jadohealth.2010.01.016pubmed: 20307840google scholar: lookup
  12. Elce Y. The aetiopathogenesis of squamous cell carcinomas in horses. Where are we?. Equine Veterinary Education 2009;21:17–18.
    doi: 10.2746/095777309X390272google scholar: lookup
  13. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Muñoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide.. J Pathol 1999 Sep;189(1):12-9.
    pubmed: 10451482doi: 10.1002/(sici)1096-9896(199909)189:1<12::aid-path431>3.0.co;2-fgoogle scholar: lookup
  14. Postey RC, Appleyard GD, Kidney BA. Evaluation of equine papillomas, aural plaques, and sarcoids for the presence of Equine papillomavirus DNA and Papillomavirus antigen.. Can J Vet Res 2007 Jan;71(1):28-33.
    pmc: PMC1635997pubmed: 17193879
  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. Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments.. Virology 2010 May 25;401(1):70-9.
    doi: 10.1016/j.virol.2010.02.002pmc: PMC3400342pubmed: 20206957google scholar: lookup
  18. Arya M, Thrasivoulou C, Henrique R, Millar M, Hamblin R, Davda R, Aare K, Masters JR, Thomson C, Muneer A, Patel HR, Ahmed A. Targets of Wnt/ß-catenin transcription in penile carcinoma.. PLoS One 2015;10(4):e0124395.
    doi: 10.1371/journal.pone.0124395pmc: PMC4406530pubmed: 25901368google scholar: lookup
  19. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors.. J Biol Chem 2006 Aug 11;281(32):22429-33.
    doi: 10.1074/jbc.R600015200pubmed: 16793760google scholar: lookup
  20. Novellasdemunt L, Antas P, Li VS. Targeting Wnt signaling in colorectal cancer. A Review in the Theme: Cell Signaling: Proteins, Pathways and Mechanisms.. Am J Physiol Cell Physiol 2015 Oct 15;309(8):C511-21.
    doi: 10.1152/ajpcell.00117.2015pmc: PMC4609654pubmed: 26289750google scholar: lookup
  21. Moparthi L, Koch S. Wnt signaling in intestinal inflammation.. Differentiation 2019 Jul-Aug;108:24-32.
    pubmed: 30718056doi: 10.1016/j.diff.2019.01.002google scholar: lookup
  22. Bergers G, Graninger P, Braselmann S, Wrighton C, Busslinger M. Transcriptional activation of the fra-1 gene by AP-1 is mediated by regulatory sequences in the first intron.. Mol Cell Biol 1995 Jul;15(7):3748-58.
    doi: 10.1128/MCB.15.7.3748pmc: PMC230613pubmed: 7791782google scholar: lookup
  23. Zenz R, Eferl R, Scheinecker C, Redlich K, Smolen J, Schonthaler HB, Kenner L, Tschachler E, Wagner EF. Activator protein 1 (Fos/Jun) functions in inflammatory bone and skin disease.. Arthritis Res Ther 2008;10(1):201.
    doi: 10.1186/ar2338pmc: PMC2374460pubmed: 18226189google scholar: lookup
  24. Young MR, Colburn NH. Fra-1 a target for cancer prevention or intervention.. Gene 2006 Sep 1;379:1-11.
    doi: 10.1016/j.gene.2006.05.001pubmed: 16784822google scholar: lookup
  25. Young MR, Li JJ, Rincón M, Flavell RA, Sathyanarayana BK, Hunziker R, Colburn N. Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion.. Proc Natl Acad Sci U S A 1999 Aug 17;96(17):9827-32.
    doi: 10.1073/pnas.96.17.9827pmc: PMC22295pubmed: 10449779google scholar: lookup
  26. Zhang D, Ma QY, Hu HT, Zhang M. β2-adrenergic antagonists suppress pancreatic cancer cell invasion by inhibiting CREB, NFκB and AP-1.. Cancer Biol Ther 2010 Jul 1;10(1):19-29.
    doi: 10.4161/cbt.10.1.11944pubmed: 20424515google scholar: lookup
  27. Hein S, Mahner S, Kanowski C, Löning T, Jänicke F, Milde-Langosch K. Expression of Jun and Fos proteins in ovarian tumors of different malignant potential and in ovarian cancer cell lines.. Oncol Rep 2009 Jul;22(1):177-83.
    pubmed: 19513521doi: 10.3892/or_00000422google scholar: lookup
  28. Symes AJ, Eilertsen M, Millar M, Nariculam J, Freeman A, Notara M, Feneley MR, Patel HR, Masters JR, Ahmed A. Quantitative analysis of BTF3, HINT1, NDRG1 and ODC1 protein over-expression in human prostate cancer tissue.. PLoS One 2013;8(12):e84295.
    doi: 10.1371/journal.pone.0084295pmc: PMC3874000pubmed: 24386364google scholar: lookup
  29. Giuliano A, Swift R, Arthurs C, Marote G, Abramo F, McKay J, Thomson C, Beltran M, Millar M, Priestnall S, Dobson J, Costantino-Casas F, Petrou T, McGonnell IM, Davies AJ, Weetman M, Garden OA, Masters JR, Thrasivoulou C, Ahmed A. Quantitative Expression and Co-Localization of Wnt Signalling Related Proteins in Feline Squamous Cell Carcinoma.. PLoS One 2016;11(8):e0161103.
    doi: 10.1371/journal.pone.0161103pmc: PMC4999089pubmed: 27559731google scholar: lookup
  30. Arthurs C, Murtaza BN, Thomson C, Dickens K, Henrique R, Patel HRH, Beltran M, Millar M, Thrasivoulou C, Ahmed A. Expression of ribosomal proteins in normal and cancerous human prostate tissue.. PLoS One 2017;12(10):e0186047.
    doi: 10.1371/journal.pone.0186047pmc: PMC5634644pubmed: 29016636google scholar: lookup
  31. Cao K, Arthurs C, Atta-Ul A, Millar M, Beltran M, Neuhaus J, Horn LC, Henrique R, Ahmed A, Thrasivoulou C. Quantitative Analysis of Seven New Prostate Cancer Biomarkers and the Potential Future of the 'Biomarker Laboratory'.. Diagnostics (Basel) 2018 Jul 27;8(3).
    pmc: PMC6163663pubmed: 30060509doi: 10.3390/diagnostics8030049google scholar: lookup
  32. Kikuchi A, Kishida S, Yamamoto H. Regulation of Wnt signaling by protein-protein interaction and post-translational modifications.. Exp Mol Med 2006 Feb 28;38(1):1-10.
    doi: 10.1038/emm.2006.1pubmed: 16520547google scholar: lookup
  33. Gera JF, Mellinghoff IK, Shi Y, Rettig MB, Tran C, Hsu JH, Sawyers CL, Lichtenstein AK. AKT activity determines sensitivity to mammalian target of rapamycin (mTOR) inhibitors by regulating cyclin D1 and c-myc expression.. J Biol Chem 2004 Jan 23;279(4):2737-46.
    doi: 10.1074/jbc.M309999200pubmed: 14576155google scholar: lookup
  34. Asano T, Yao Y, Zhu J, Li D, Abbruzzese JL, Reddy SA. The PI 3-kinase/Akt signaling pathway is activated due to aberrant Pten expression and targets transcription factors NF-kappaB and c-Myc in pancreatic cancer cells.. Oncogene 2004 Nov 11;23(53):8571-80.
    doi: 10.1038/sj.onc.1207902pubmed: 15467756google scholar: lookup
  35. Shan G, Tang T. Expression of cyclin D1 and cyclin E in urothelial bladder carcinoma detected in tissue chips using a quantum dot immunofluorescence technique.. Oncol Lett 2015 Sep;10(3):1271-1276.
    doi: 10.3892/ol.2015.3436pmc: PMC4533711pubmed: 26622662google scholar: lookup
  36. Xu S, Gu G, Ni Q, Li N, Yu K, Li X, Liu C. The expression of AEG-1 and Cyclin D1 in human bladder urothelial carcinoma and their clinicopathological significance.. Int J Clin Exp Med 2015;8(11):21222-8.
    pmc: PMC4723903pubmed: 26885058
  37. Bolenz C, Knauf D, John A, Erben P, Steidler A, Schneider SW, Günes C, Gorzelanny C. Decreased Invasion of Urothelial Carcinoma of the Bladder by Inhibition of Matrix-Metalloproteinase 7.. Bladder Cancer 2018 Jan 20;4(1):67-75.
    doi: 10.3233/BLC-170124pmc: PMC5798526pubmed: 29430508google scholar: lookup
  38. Liu JY, Dai YB, Li X, Cao K, Xie D, Tong ZT, Long Z, Xiao H, Chen MK, Ye YL, Liu B, Tan J, Tang J, Xu ZZ, Gan Y, Zhou YH, Deng F, He LY. Solute carrier family 12 member 5 promotes tumor invasion/metastasis of bladder urothelial carcinoma by enhancing NF-κB/MMP-7 signaling pathway.. Cell Death Dis 2017 Mar 23;8(3):e2691.
    doi: 10.1038/cddis.2017.118pmc: PMC5386524pubmed: 28333147google scholar: lookup
  39. Tao L, Li Z, Lin L, Lei Y, Hongyuan Y, Hongwei J, Yang L, Chuize K. MMP1, 2, 3, 7, and 9 gene polymorphisms and urinary cancer risk: a meta-analysis.. Genet Test Mol Biomarkers 2015 Oct;19(10):548-55.
    doi: 10.1089/gtmb.2015.0123pmc: PMC4599389pubmed: 26301605google scholar: lookup
  40. Li Y, Liu H, Lai C, Du X, Su Z, Gao S. The Lin28/let-7a/c-Myc pathway plays a role in non-muscle invasive bladder cancer.. Cell Tissue Res 2013 Nov;354(2):533-41.
    doi: 10.1007/s00441-013-1715-6pubmed: 24036903google scholar: lookup
  41. Massari F, Bria E, Ciccarese C, Munari E, Modena A, Zambonin V, Sperduti I, Artibani W, Cheng L, Martignoni G, Tortora G, Brunelli M. Prognostic Value of Beta-Tubulin-3 and c-Myc in Muscle Invasive Urothelial Carcinoma of the Bladder.. PLoS One 2015;10(6):e0127908.
    doi: 10.1371/journal.pone.0127908pmc: PMC4457798pubmed: 26046361google scholar: lookup
  42. Jeong KC, Kim KT, Seo HH, Shin SP, Ahn KO, Ji MJ, Park WS, Kim IH, Lee SJ, Seo HK. Intravesical instillation of c-MYC inhibitor KSI-3716 suppresses orthotopic bladder tumor growth.. J Urol 2014 Feb;191(2):510-8.
    doi: 10.1016/j.juro.2013.07.019pubmed: 23872029google scholar: lookup
  43. Zhang L, Liu H, Mu X, Cui J, Peng Z. Dysregulation of Fra1 expression by Wnt/β-catenin signalling promotes glioma aggressiveness through epithelial-mesenchymal transition.. Biosci Rep 2017 Apr 28;37(2).
    pmc: PMC5469333pubmed: 28232512doi: 10.1042/bsr20160643google scholar: lookup
  44. Kim JH, Park SY, Jun Y, Kim JY, Nam JS. Roles of Wnt Target Genes in the Journey of Cancer Stem Cells.. Int J Mol Sci 2017 Jul 25;18(8).
    pmc: PMC5577996pubmed: 28757546doi: 10.3390/ijms18081604google scholar: lookup
  45. Gaffen SL. Structure and signalling in the IL-17 receptor family.. Nat Rev Immunol 2009 Aug;9(8):556-67.
    doi: 10.1038/nri2586pmc: PMC2821718pubmed: 19575028google scholar: lookup
  46. Zhong G, Chen X, Fang X, Wang D, Xie M, Chen Q. Fra-1 is upregulated in lung cancer tissues and inhibits the apoptosis of lung cancer cells by the P53 signaling pathway.. Oncol Rep 2016 Jan;35(1):447-53.
    doi: 10.3892/or.2015.4395pubmed: 26549498google scholar: lookup
  47. Motrich RD, Castro GM, Caputto BL. Old players with a newly defined function: Fra-1 and c-Fos support growth of human malignant breast tumors by activating membrane biogenesis at the cytoplasm.. PLoS One 2013;8(1):e53211.
    pmc: PMC3534677pubmed: 23301044doi: 10.1371/journal.pone.0053211google scholar: lookup
  48. Sayan AE, Stanford R, Vickery R, Grigorenko E, Diesch J, Kulbicki K, Edwards R, Pal R, Greaves P, Jariel-Encontre I, Piechaczyk M, Kriajevska M, Mellon JK, Dhillon AS, Tulchinsky E. Fra-1 controls motility of bladder cancer cells via transcriptional upregulation of the receptor tyrosine kinase AXL.. Oncogene 2012 Mar 22;31(12):1493-503.
    doi: 10.1038/onc.2011.336pubmed: 21822309google scholar: lookup
  49. Kireva T, Erhardt A, Tiegs G, Tilg H, Denk H, Haybaeck J, Aigner E, Moschen A, Distler JH, Schett G, Zwerina J. Transcription factor Fra-1 induces cholangitis and liver fibrosis.. Hepatology 2011 Apr;53(4):1259-69.
    doi: 10.1002/hep.24175pubmed: 21480331google scholar: lookup
  50. Gao D, Chen HQ. Specific knockdown of HOXB7 inhibits cutaneous squamous cell carcinoma cell migration and invasion while inducing apoptosis via the Wnt/β-catenin signaling pathway.. Am J Physiol Cell Physiol 2018 Nov 1;315(5):C675-C686.
    pubmed: 30067384doi: 10.1152/ajpcell.00291.2017google scholar: lookup
  51. Chen YP, Wang YQ, Lv JW, Li YQ, Chua MLK, Le QT, Lee N, Colevas AD, Seiwert T, Hayes DN, Riaz N, Vermorken JB, O'Sullivan B, He QM, Yang XJ, Tang LL, Mao YP, Sun Y, Liu N, Ma J. Identification and validation of novel microenvironment-based immune molecular subgroups of head and neck squamous cell carcinoma: implications for immunotherapy.. Ann Oncol 2019 Jan 1;30(1):68-75.
    pubmed: 30407504doi: 10.1093/annonc/mdy470google scholar: lookup
  52. Bleeker MC, Heideman DA, Snijders PJ, Horenblas S, Dillner J, Meijer CJ. Penile cancer: epidemiology, pathogenesis and prevention.. World J Urol 2009 Apr;27(2):141-50.
    doi: 10.1007/s00345-008-0302-zpubmed: 18607597google scholar: lookup
  53. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 2001 Feb 17;357(9255):539-45.
    doi: 10.1016/S0140-6736(00)04046-0pubmed: 11229684google scholar: lookup
  54. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing.. N Engl J Med 1986 Dec 25;315(26):1650-9.
    doi: 10.1056/NEJM198612253152606pubmed: 3537791google scholar: lookup
  55. Kidd JG, Rous P. CANCERS DERIVING FROM THE VIRUS PAPILLOMAS OF WILD RABBITS UNDER NATURAL CONDITIONS.. J Exp Med 1940 Mar 31;71(4):469-94.
    doi: 10.1084/jem.71.4.469pmc: PMC2135089pubmed: 19870976google scholar: lookup
  56. Hölters S. Histopathologic and prognostic correlations regarding human papillomavirus (HPV) infection in penile squamous cell carcinomas (SCC) considering the novel 2016 WHO classification. European Urology Supplements 2017;16:e1242.
    doi: 10.1016/S1569-9056(17)30771-6google scholar: lookup
  57. Newkirk KM, Hendrix DV, Anis EA, Rohrbach BW, Ehrhart EJ, Lyons JA, Kania SA. Detection of papillomavirus in equine periocular and penile squamous cell carcinoma.. J Vet Diagn Invest 2014 Jan;26(1):131-5.
    doi: 10.1177/1040638713511618pubmed: 24323055google scholar: lookup
  58. Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation.. Annu Rev Immunol 2009;27:591-619.
    doi: 10.1146/annurev.immunol.021908.132706pmc: PMC2740335pubmed: 19132916google scholar: lookup
  59. Dupuy d'Angeac A, Monier S, Jorgensen C, Gao Q, Travaglio-Encinoza A, Bologna C, Combe B, Sany J, Rème T. Increased percentage of CD3+, CD57+ lymphocytes in patients with rheumatoid arthritis. Correlation with duration of disease.. Arthritis Rheum 1993 May;36(5):608-12.
    pubmed: 7683880doi: 10.1002/art.1780360506google scholar: lookup
  60. Yndestad A, Holm AM, Müller F, Simonsen S, Frøland SS, Gullestad L, Aukrust P. Enhanced expression of inflammatory cytokines and activation markers in T-cells from patients with chronic heart failure.. Cardiovasc Res 2003 Oct 15;60(1):141-6.
    doi: 10.1016/S0008-6363(03)00362-6pubmed: 14522416google scholar: lookup
  61. Blanchard-Channell M, Moore PF, Stott JL. Characterization of monoclonal antibodies specific for equine homologues of CD3 and CD5.. Immunology 1994 Aug;82(4):548-54.
    pmc: PMC1414917pubmed: 7530685
  62. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis.. Nat Methods 2012 Jul;9(7):671-5.
    doi: 10.1038/nmeth.2089pmc: PMC5554542pubmed: 22930834google scholar: lookup
  63. Chollet F. Keras. 2015.
  64. Abadi M. Tensorflow: Large-scale machine learning on heterogeneous distributed systems. arXiv preprint arXiv:1603.04467 (2016).
  65. Komura D, Ishikawa S. Machine Learning Methods for Histopathological Image Analysis.. Comput Struct Biotechnol J 2018;16:34-42.
    doi: 10.1016/j.csbj.2018.01.001pmc: PMC6158771pubmed: 30275936google scholar: lookup
  66. Fulton AJ, Nemec A, Murphy BG, Kass PH, Verstraete FJ. Risk factors associated with survival in dogs with nontonsillar oral squamous cell carcinoma 31 cases (1990-2010).. J Am Vet Med Assoc 2013 Sep 1;243(5):696-702.
    doi: 10.2460/javma.243.5.696pubmed: 23971850google scholar: lookup
  67. Alcover A, Alarcón B, Di Bartolo V. Cell Biology of T Cell Receptor Expression and Regulation.. Annu Rev Immunol 2018 Apr 26;36:103-125.
    doi: 10.1146/annurev-immunol-042617-053429pubmed: 29261409google scholar: lookup

Citations

This article has been cited 5 times.
  1. Xie B, Zuhair H, Henrique R, Millar M, Robson T, Thrasivoulou C, Dickens K, Pendjiky J, Muneer A, Patel H, Ahmed A. Opposite changes in the expression of clathrin and caveolin-1 in normal and cancerous human prostate tissue: putative clathrin-mediated recycling of EGFR.. Histochem Cell Biol 2023 Jun;159(6):489-500.
    doi: 10.1007/s00418-023-02183-8pubmed: 36869937google scholar: lookup
  2. 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/ijms221910588pubmed: 34638929google scholar: lookup
  3. Mecocci S, Porcellato I, Armando F, Mechelli L, Brachelente C, Pepe M, Gialletti R, Passeri B, Modesto P, Ghelardi A, Cappelli K, Razzuoli E. Equine Genital Squamous Cell Carcinoma Associated with EcPV2 Infection: RANKL Pathway Correlated to Inflammation and Wnt Signaling Activation.. Biology (Basel) 2021 Mar 21;10(3).
    doi: 10.3390/biology10030244pubmed: 33801021google scholar: lookup
  4. Medeiros-Fonseca B, Cubilla A, Brito H, Martins T, Medeiros R, Oliveira P, Gil da Costa RM. Experimental Models for Studying HPV-Positive and HPV-Negative Penile Cancer: New Tools for An Old Disease.. Cancers (Basel) 2021 Jan 26;13(3).
    doi: 10.3390/cancers13030460pubmed: 33530343google scholar: lookup
  5. Porcellato I, Mecocci S, Mechelli L, Cappelli K, Brachelente C, Pepe M, Orlandi M, Gialletti R, Passeri B, Ferrari A, Modesto P, Ghelardi A, Razzuoli E. Equine Penile Squamous Cell Carcinomas as a Model for Human Disease: A Preliminary Investigation on Tumor Immune Microenvironment.. Cells 2020 Oct 27;9(11).
    doi: 10.3390/cells9112364pubmed: 33121116google scholar: lookup
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.