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Pathogens (Basel, Switzerland)2022; 11(2); 266; doi: 10.3390/pathogens11020266

Tumor Cell Plasticity in Equine Papillomavirus-Positive Versus-Negative Squamous Cell Carcinoma of the Head and Neck.

Abstract: Squamous cell carcinoma of the head and neck (HNSCC) is a common malignant tumor in humans and animals. In humans, papillomavirus (PV)-induced HNSCCs have a better prognosis than papillomavirus-unrelated HNSCCs. The ability of tumor cells to switch from epithelial to mesenchymal, endothelial, or therapy-resistant stem-cell-like phenotypes promotes disease progression and metastasis. In equine HNSCC, PV-association and tumor cell phenotype switching are poorly understood. We screened 49 equine HNSCCs for equine PV (EcPV) type 2, 3 and 5 infection. Subsequently, PV-positive versus -negative lesions were analyzed for expression of selected epithelial (keratins, β-catenin), mesenchymal (vimentin), endothelial (COX-2), and stem-cell markers (CD271, CD44) by immunohistochemistry (IHC) and immunofluorescence (IF; keratins/vimentin, CD44/CD271 double-staining) to address tumor cell plasticity in relation to PV infection. Only EcPV2 PCR scored positive for 11/49 equine HNSCCs. IHC and IF from 11 EcPV2-positive and 11 EcPV2-negative tumors revealed epithelial-to-mesenchymal transition events, with vimentin-positive cells ranging between 50%. CD44- and CD271-staining disclosed the intralesional presence of infiltrative tumor cell fronts and double-positive tumor cell subsets independently of the PV infection status. Our findings are indicative of (partial) epithelial-mesenchymal transition events giving rise to hybrid epithelial/mesenchymal and stem-cell-like tumor cell phenotypes in equine HNSCCs and suggest CD44 and CD271 as potential malignancy markers that merit to be further explored in the horse.
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Publication Date: 2022-02-18 PubMed ID: 35215208PubMed Central: PMC8875230DOI: 10.3390/pathogens11020266Google Scholar: Lookup
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  • Journal Article

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.

This study explores the cell behavior or ‘plasticity’ in horse head and neck squamous cell carcinoma (HNSCC), identifying variances between those positive and negative for equine papillomavirus infection. The findings reveal that infection status does not prevent the tumor cells from changing their phenotype in a way that could promote disease progression and metastasis.

Background of the Study

  • The research takes a focus on squamous cell carcinoma of the head and neck (HNSCC), which is a common malignant tumor in both humans and animals.
  • In humans, HNSCCs induced by papillomavirus (PV) have been observed to have a better prognosis than those unrelated to papillomavirus.
  • Crucial to the research is the concept of tumor cell plasticity, which refers to the ability of tumor cells to switch from epithelial to mesenchymal, endothelial, or therapy-resistant stem-cell-like phenotypes, a process that is understood to promote disease progression and metastasis.
  • The understanding of papillomavirus association and tumor cell phenotype switching in equine HNSCC has up until now been poorly understood.

Results of the Study

  • A total of 49 equine HNSCCs were studied for equine papillomavirus (EcPV) type 2, 3, and 5 infection. Out of these, only 11 were found to be positive for EcPV2 — the others showed no presence of equine papillomavirus types 2, 3 or 5.
  • Both EcPV2-positive and EcPV2-negative tumors were observed to experience epithelial-to-mesenchymal transition events, characterized by vimentin-positive cells ranging between less than 10% and more than 50%.
  • CD44 and CD271 staining, markers of stem cell activity, decrypted the presence of invasive tumor cell fronts and double-positive tumor cell subsets, regardless of the tumors’ papillomavirus infection status.

Interpretation and Potential Implications

  • The findings of the research suggest that (partial) epithelial-mesenchymal transition events cause the emergence of hybrid epithelial/mesenchymal and stem-cell-like tumor cell phenotypes in equine HNSCCs.
  • Interestingly, these transitions occurred irrespective of papillomavirus infection status, indicating that other factors may drive cell plasticity in this type of cancer.
  • Markers CD44 and CD271 may be potential indicators of malignancy in equine HNSCC and merit further exploration.

Cite This Article

APA
Strohmayer C, Klang A, Kummer S, Walter I, Jindra C, Weissenbacher-Lang C, Redmer T, Kneissl S, Brandt S. (2022). Tumor Cell Plasticity in Equine Papillomavirus-Positive Versus-Negative Squamous Cell Carcinoma of the Head and Neck. Pathogens, 11(2), 266. https://doi.org/10.3390/pathogens11020266

Publication

Pathogens (Basel, Switzerland)
ISSN: 2076-0817
NlmUniqueID: 101596317
Country: Switzerland
Language: English
Volume: 11
Issue: 2
PII: 266

Researcher Affiliations

Strohmayer, Carina
  • Clinical Unit of Diagnostic Imaging, Department for Companion Animals and Horses, University of Veterinary Medicine, 1210 Vienna, Austria.
Klang, Andrea
  • Institute of Pathology, Department of Pathobiology, University of Veterinary Medicine, 1210 Vienna, Austria.
Kummer, Stefan
  • VetCore Facility for Research, University of Veterinary Medicine, 1210 Vienna, Austria.
Walter, Ingrid
  • VetCore Facility for Research, University of Veterinary Medicine, 1210 Vienna, Austria.
  • Institute of Morphology, Department of Pathobiology, University of Veterinary Medicine, 1210 Vienna, Austria.
Jindra, Christoph
  • Research Group Oncology (RGO), Clinical Unit of Equine Surgery, Department for Companion Animals and Horses, University of Veterinary Medicine, 1210 Vienna, Austria.
Weissenbacher-Lang, Christiane
  • Institute of Pathology, Department of Pathobiology, University of Veterinary Medicine, 1210 Vienna, Austria.
Redmer, Torben
  • Institute of Medical Biochemistry, Department of Biomedical Sciences, University of Veterinary Medicine, 1210 Vienna, Austria.
Kneissl, Sibylle
  • Clinical Unit of Diagnostic Imaging, Department for Companion Animals and Horses, University of Veterinary Medicine, 1210 Vienna, Austria.
Brandt, Sabine
  • Research Group Oncology (RGO), Clinical Unit of Equine Surgery, Department for Companion Animals and Horses, University of Veterinary Medicine, 1210 Vienna, Austria.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 75 references
  1. 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
  2. Gissmann L. Linking human papillomaviruses to cervical cancer: A long and winding road. In: Campo M.S., editor. Papillomavirus Research: From Natural History to Vaccines and Beyond. Caister Academic Press; Wymondham, UK: 2006. pp. 3–9.
  3. Ashrafi GH, Brown DR, Fife KH, Campo MS. Down-regulation of MHC class I is a property common to papillomavirus E5 proteins.. Virus Res 2006 Sep;120(1-2):208-11.
    doi: 10.1016/j.virusres.2006.02.005pubmed: 16780984google scholar: lookup
  4. Pullos AN, Castilho RM, Squarize CH. HPV Infection of the Head and Neck Region and Its Stem Cells.. J Dent Res 2015 Nov;94(11):1532-43.
    doi: 10.1177/0022034515605456pubmed: 26353884google scholar: lookup
  5. Secretan B, Straif K, Baan R, Grosse Y, El Ghissassi F, Bouvard V, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V. A review of human carcinogens--Part E: tobacco, areca nut, alcohol, coal smoke, and salted fish.. Lancet Oncol 2009 Nov;10(11):1033-4.
    doi: 10.1016/S1470-2045(09)70326-2pubmed: 19891056google scholar: lookup
  6. Kikuchi K, Inoue H, Miyazaki Y, Ide F, Kojima M, Kusama K. Epstein-Barr virus (EBV)-associated epithelial and non-epithelial lesions of the oral cavity.. Jpn Dent Sci Rev 2017 Aug;53(3):95-109.
    doi: 10.1016/j.jdsr.2017.01.002pmc: PMC5501733pubmed: 28725300google scholar: lookup
  7. Fleming JC, Woo J, Moutasim K, Mellone M, Frampton SJ, Mead A, Ahmed W, Wood O, Robinson H, Ward M, Woelk CH, Ottensmeier CH, King E, Kim D, Blaydes JP, Thomas GJ. HPV, tumour metabolism and novel target identification in head and neck squamous cell carcinoma.. Br J Cancer 2019 Feb;120(3):356-367.
    doi: 10.1038/s41416-018-0364-7pmc: PMC6353968pubmed: 30655616google scholar: lookup
  8. Scott D.W., Miller W.H. Jr.. Squamous cell carcinoma. In: Scott D.W., Miller W.H. Jr., editors. Equine Dermatology. 2nd ed. Saunders Elsevier; St. Louis, MO, USA: 2011. pp. 473–476.
  9. 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
  10. 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
  11. Lassaline M, Cranford TL, Latimer CA, Bellone RR. Limbal squamous cell carcinoma in Haflinger horses.. Vet Ophthalmol 2015 Sep;18(5):404-8.
    doi: 10.1111/vop.12229pubmed: 25312447google scholar: lookup
  12. 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
  13. 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
  14. Yuan S, Norgard RJ, Stanger BZ. Cellular Plasticity in Cancer.. Cancer Discov 2019 Jul;9(7):837-851.
    doi: 10.1158/2159-8290.CD-19-0015pmc: PMC6606363pubmed: 30992279google scholar: lookup
  15. Baum B, Settleman J, Quinlan MP. Transitions between epithelial and mesenchymal states in development and disease.. Semin Cell Dev Biol 2008 Jun;19(3):294-308.
    doi: 10.1016/j.semcdb.2008.02.001pubmed: 18343170google scholar: lookup
  16. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis.. Dev Cell 2008 Jun;14(6):818-29.
    doi: 10.1016/j.devcel.2008.05.009pubmed: 18539112google scholar: lookup
  17. Greenburg G, Hay ED. Epithelia suspended in collagen gels can lose polarity and express characteristics of migrating mesenchymal cells.. J Cell Biol 1982 Oct;95(1):333-9.
    doi: 10.1083/jcb.95.1.333pmc: PMC2112361pubmed: 7142291google scholar: lookup
  18. Greenburg G, Hay ED. Cytodifferentiation and tissue phenotype change during transformation of embryonic lens epithelium to mesenchyme-like cells in vitro.. Dev Biol 1986 Jun;115(2):363-79.
    doi: 10.1016/0012-1606(86)90256-3pubmed: 3519318google scholar: lookup
  19. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease.. Cell 2009 Nov 25;139(5):871-90.
    doi: 10.1016/j.cell.2009.11.007pubmed: 19945376google scholar: lookup
  20. Chen C, Wei Y, Hummel M, Hoffmann TK, Gross M, Kaufmann AM, Albers AE. Evidence for epithelial-mesenchymal transition in cancer stem cells of head and neck squamous cell carcinoma.. PLoS One 2011 Jan 27;6(1):e16466.
    doi: 10.1371/journal.pone.0016466pmc: PMC3029362pubmed: 21304586google scholar: lookup
  21. Chen C, Zimmermann M, Tinhofer I, Kaufmann AM, Albers AE. Epithelial-to-mesenchymal transition and cancer stem(-like) cells in head and neck squamous cell carcinoma.. Cancer Lett 2013 Sep 10;338(1):47-56.
    doi: 10.1016/j.canlet.2012.06.013pubmed: 22771535google scholar: lookup
  22. Mandal M, Myers JN, Lippman SM, Johnson FM, Williams MD, Rayala S, Ohshiro K, Rosenthal DI, Weber RS, Gallick GE, El-Naggar AK. Epithelial to mesenchymal transition in head and neck squamous carcinoma: association of Src activation with E-cadherin down-regulation, vimentin expression, and aggressive tumor features.. Cancer 2008 May 1;112(9):2088-100.
    doi: 10.1002/cncr.23410pubmed: 18327819google scholar: lookup
  23. Nijkamp MM, Span PN, Hoogsteen IJ, van der Kogel AJ, Kaanders JH, Bussink J. Expression of E-cadherin and vimentin correlates with metastasis formation in head and neck squamous cell carcinoma patients.. Radiother Oncol 2011 Jun;99(3):344-8.
    doi: 10.1016/j.radonc.2011.05.066pubmed: 21684617google scholar: lookup
  24. Saitoh M. Involvement of partial EMT in cancer progression.. J Biochem 2018 Oct 1;164(4):257-264.
    doi: 10.1093/jb/mvy047pubmed: 29726955google scholar: lookup
  25. Liao C, Wang Q, An J, Long Q, Wang H, Xiang M, Xiang M, Zhao Y, Liu Y, Liu J, Guan X. Partial EMT in Squamous Cell Carcinoma: A Snapshot.. Int J Biol Sci 2021;17(12):3036-3047.
    doi: 10.7150/ijbs.61566pmc: PMC8375241pubmed: 34421348google scholar: lookup
  26. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells.. Cell 2008 May 16;133(4):704-15.
    doi: 10.1016/j.cell.2008.03.027pmc: PMC2728032pubmed: 18485877google scholar: lookup
  27. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors.. Nat Genet 2008 May;40(5):499-507.
    doi: 10.1038/ng.127pmc: PMC2912221pubmed: 18443585google scholar: lookup
  28. Vitale I, Manic G, De Maria R, Kroemer G, Galluzzi L. DNA Damage in Stem Cells.. Mol Cell 2017 May 4;66(3):306-319.
    doi: 10.1016/j.molcel.2017.04.006pubmed: 28475867google scholar: lookup
  29. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL, Clarke MF. Association of reactive oxygen species levels and radioresistance in cancer stem cells.. Nature 2009 Apr 9;458(7239):780-3.
    doi: 10.1038/nature07733pmc: PMC2778612pubmed: 19194462google scholar: lookup
  30. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer.. Cell 2007 May 4;129(3):465-72.
    doi: 10.1016/j.cell.2007.04.019pmc: PMC3150586pubmed: 17482542google scholar: lookup
  31. Oshimori N. Cancer stem cells and their niche in the progression of squamous cell carcinoma.. Cancer Sci 2020 Nov;111(11):3985-3992.
    doi: 10.1111/cas.14639pmc: PMC7648029pubmed: 32888236google scholar: lookup
  32. Vidal A, Redmer T. Decoding the Role of CD271 in Melanoma.. Cancers (Basel) 2020 Aug 31;12(9).
    doi: 10.3390/cancers12092460pmc: PMC7564075pubmed: 32878000google scholar: lookup
  33. Nassar D, Blanpain C. Cancer Stem Cells: Basic Concepts and Therapeutic Implications.. Annu Rev Pathol 2016 May 23;11:47-76.
    doi: 10.1146/annurev-pathol-012615-044438pubmed: 27193450google scholar: lookup
  34. Bourguignon LY, Earle C, Wong G, Spevak CC, Krueger K. Stem cell marker (Nanog) and Stat-3 signaling promote MicroRNA-21 expression and chemoresistance in hyaluronan/CD44-activated head and neck squamous cell carcinoma cells.. Oncogene 2012 Jan 12;31(2):149-60.
    doi: 10.1038/onc.2011.222pmc: PMC3179812pubmed: 21685938google scholar: lookup
  35. Bourguignon LY, Wong G, Earle C, Chen L. Hyaluronan-CD44v3 interaction with Oct4-Sox2-Nanog promotes miR-302 expression leading to self-renewal, clonal formation, and cisplatin resistance in cancer stem cells from head and neck squamous cell carcinoma.. J Biol Chem 2012 Sep 21;287(39):32800-24.
    doi: 10.1074/jbc.M111.308528pmc: PMC3463333pubmed: 22847005google scholar: lookup
  36. Gomez KE, Wu F, Keysar SB, Morton JJ, Miller B, Chimed TS, Le PN, Nieto C, Chowdhury FN, Tyagi A, Lyons TR, Young CD, Zhou H, Somerset HL, Wang XJ, Jimeno A. Cancer Cell CD44 Mediates Macrophage/Monocyte-Driven Regulation of Head and Neck Cancer Stem Cells.. Cancer Res 2020 Oct 1;80(19):4185-4198.
    doi: 10.1158/0008-5472.CAN-20-1079pmc: PMC8146866pubmed: 32816856google scholar: lookup
  37. Keysar SB, Le PN, Miller B, Jackson BC, Eagles JR, Nieto C, Kim J, Tang B, Glogowska MJ, Morton JJ, Padilla-Just N, Gomez K, Warnock E, Reisinger J, Arcaroli JJ, Messersmith WA, Wakefield LM, Gao D, Tan AC, Serracino H, Vasiliou V, Roop DR, Wang XJ, Jimeno A. Regulation of Head and Neck Squamous Cancer Stem Cells by PI3K and SOX2.. J Natl Cancer Inst 2017 Jan;109(1).
    doi: 10.1093/jnci/djw189pmc: PMC5025278pubmed: 27634934google scholar: lookup
  38. Suárez-Bonnet A, Willis C, Pittaway R, Smith K, Mair T, Priestnall SL. Molecular carcinogenesis in equine penile cancer: A potential animal model for human penile cancer.. Urol Oncol 2018 Dec;36(12):532.e9-532.e18.
    doi: 10.1016/j.urolonc.2018.09.004pubmed: 30270026google scholar: lookup
  39. 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
  40. Armando F, Godizzi F, Razzuoli E, Leonardi F, Angelone M, Corradi A, Meloni D, Ferrari L, Passeri B. Epithelial to Mesenchymal Transition (EMT) in a Laryngeal Squamous Cell Carcinoma of a Horse: Future Perspectives.. Animals (Basel) 2020 Dec 7;10(12).
    doi: 10.3390/ani10122318pmc: PMC7762370pubmed: 33297475google scholar: lookup
  41. Lange CE, Tobler K, Ackermann M, Favrot C. Identification of two novel equine papillomavirus sequences suggests three genera in one cluster.. Vet Microbiol 2011 Apr 21;149(1-2):85-90.
    doi: 10.1016/j.vetmic.2010.10.019pubmed: 21109367google scholar: lookup
  42. Lange CE, Vetsch E, Ackermann M, Favrot C, Tobler K. Four novel papillomavirus sequences support a broad diversity among equine papillomaviruses.. J Gen Virol 2013 Jun;94(Pt 6):1365-1372.
    doi: 10.1099/vir.0.052092-0pubmed: 23486670google scholar: lookup
  43. Moll R, Divo M, Langbein L. The human keratins: biology and pathology.. Histochem Cell Biol 2008 Jun;129(6):705-33.
    doi: 10.1007/s00418-008-0435-6pmc: PMC2386534pubmed: 18461349google scholar: lookup
  44. Moll R, Franke WW, Schiller DL, Geiger B, Krepler R. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells.. Cell 1982 Nov;31(1):11-24.
    doi: 10.1016/0092-8674(82)90400-7pubmed: 6186379google scholar: lookup
  45. Makarova G, Bette M, Schmidt A, Jacob R, Cai C, Rodepeter F, Betz T, Sitterberg J, Bakowsky U, Moll R, Neff A, Sesterhenn A, Teymoortash A, Ocker M, Werner JA, Mandic R. Epidermal growth factor-induced modulation of cytokeratin expression levels influences the morphological phenotype of head and neck squamous cell carcinoma cells.. Cell Tissue Res 2013 Jan;351(1):59-72.
    doi: 10.1007/s00441-012-1500-ypubmed: 23111772google scholar: lookup
  46. Kudo Y, Kitajima S, Ogawa I, Hiraoka M, Sargolzaei S, Keikhaee MR, Sato S, Miyauchi M, Takata T. Invasion and metastasis of oral cancer cells require methylation of E-cadherin and/or degradation of membranous beta-catenin.. Clin Cancer Res 2004 Aug 15;10(16):5455-63.
    doi: 10.1158/1078-0432.CCR-04-0372pubmed: 15328184google scholar: lookup
  47. Stenner M, Yosef B, Hrs CU, Preuss SF, Dienes HP, Speel EJ, Odenthal M, Klussmann JP. Nuclear translocation of β-catenin and decreased expression of epithelial cadherin in human papillomavirus-positive tonsillar cancer: an early event in human papillomavirus-related tumour progression?. Histopathology 2011 Jun;58(7):1117-26.
    doi: 10.1111/j.1365-2559.2011.03805.xpubmed: 21438909google scholar: lookup
  48. Wang W, Wen Q, Luo J, Chu S, Chen L, Xu L, Zang H, Alnemah MM, Li J, Zhou J, Fan S. Suppression Of β-catenin Nuclear Translocation By CGP57380 Decelerates Poor Progression And Potentiates Radiation-Induced Apoptosis in Nasopharyngeal Carcinoma.. Theranostics 2017;7(7):2134-2149.
    doi: 10.7150/thno.17665pmc: PMC5485425pubmed: 28656063google scholar: lookup
  49. Usman S, Waseem NH, Nguyen TKN, Mohsin S, Jamal A, Teh MT, Waseem A. Vimentin Is at the Heart of Epithelial Mesenchymal Transition (EMT) Mediated Metastasis.. Cancers (Basel) 2021 Oct 5;13(19).
    doi: 10.3390/cancers13194985pmc: PMC8507690pubmed: 34638469google scholar: lookup
  50. Watanabe Y, Imanishi Y, Ozawa H, Sakamoto K, Fujii R, Shigetomi S, Habu N, Otsuka K, Sato Y, Sekimizu M, Ito F, Ikari Y, Saito S, Kameyama K, Ogawa K. Selective EP2 and Cox-2 inhibition suppresses cell migration by reversing epithelial-to-mesenchymal transition and Cox-2 overexpression and E-cadherin downregulation are implicated in neck metastasis of hypopharyngeal cancer.. Am J Transl Res 2020;12(3):1096-1113.
    pmc: PMC7137058pubmed: 32269737
  51. Sadasivam S, Subramanian R. A perspective on challenges and opportunities in characterizing oral cancer stem cells.. Front Biosci (Landmark Ed) 2020 Mar 1;25(6):1011-1021.
    doi: 10.2741/4845pubmed: 32114422google scholar: lookup
  52. Murillo-Sauca O, Chung MK, Shin JH, Karamboulas C, Kwok S, Jung YH, Oakley R, Tysome JR, Farnebo LO, Kaplan MJ, Sirjani D, Divi V, Holsinger FC, Tomeh C, Nichols A, Le QT, Colevas AD, Kong CS, Uppaluri R, Lewis JS Jr, Ailles LE, Sunwoo JB. CD271 is a functional and targetable marker of tumor-initiating cells in head and neck squamous cell carcinoma.. Oncotarget 2014 Aug 30;5(16):6854-66.
    doi: 10.18632/oncotarget.2269pmc: PMC4196168pubmed: 25149537google scholar: lookup
  53. Gale N, Poljak M, Zidar N. Update from the 4th Edition of the World Health Organization Classification of Head and Neck Tumours: What is New in the 2017 WHO Blue Book for Tumours of the Hypopharynx, Larynx, Trachea and Parapharyngeal Space.. Head Neck Pathol 2017 Mar;11(1):23-32.
    doi: 10.1007/s12105-017-0788-zpmc: PMC5340729pubmed: 28247231google scholar: lookup
  54. Scott D.W., Miller W.H. Jr.. Squamous cell carcinoma. In: Scott D.W., Miller W.H. Jr., editors. Equine Dermatology. 1st ed. Saunders Elsevier; St. Louis, MO, USA: 2003. pp. 707–712.
  55. Knottenbelt D.C.. Squamous cell carcinoma. In: Knottenbelt D.C., editor. Pascoe’s Principles and Practice of Equine Dermatology. 2nd ed. Saunders Elsevier; London, UK: 2009. pp. 427–433.
  56. Pascoe R.R., Knottenbelt D.C.. Squamous cell carcinoma. In: Saunders W.B., editor. Manual of Equine Dermatology. Harcourt Publishers; London, UK: 1999. pp. 261–266.
  57. Budras K.-D., Sack W.O., Röck S.. Anatomy of the Horse. 6th ed. Schlütersche Verlagsgesellschaft; Hannover, Germany: 2011. Head.
  58. Hibi H, Hatama S, Obata A, Shibahara T, Kadota K. Laryngeal squamous cell carcinoma and papilloma associated with Equus caballus papillomavirus 2 in a horse.. J Vet Med Sci 2019 Jul 19;81(7):1029-1033.
    doi: 10.1292/jvms.18-0461pmc: PMC6656819pubmed: 31167980google scholar: lookup
  59. 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
  60. 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
  61. 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
  62. 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
  63. Van der Velden L.A.. Expression of cytokeratin subtypes and vimentin in squamous cell carcinoma of the floor of the mouth and the mobile tongue. Otorhinolaryngol. Nova 2001;11:186–192.
    doi: 10.1159/000063015google scholar: lookup
  64. Jung A, Schrauder M, Oswald U, Knoll C, Sellberg P, Palmqvist R, Niedobitek G, Brabletz T, Kirchner T. The invasion front of human colorectal adenocarcinomas shows co-localization of nuclear beta-catenin, cyclin D1, and p16INK4A and is a region of low proliferation.. Am J Pathol 2001 Nov;159(5):1613-7.
    doi: 10.1016/S0002-9440(10)63007-6pmc: PMC1867079pubmed: 11696421google scholar: lookup
  65. Gómez-Valenzuela F, Escobar E, Pérez-Tomás R, Montecinos VP. The Inflammatory Profile of the Tumor Microenvironment, Orchestrated by Cyclooxygenase-2, Promotes Epithelial-Mesenchymal Transition.. Front Oncol 2021;11:686792.
    doi: 10.3389/fonc.2021.686792pmc: PMC8222670pubmed: 34178680google scholar: lookup
  66. Subbaramaiah K, Dannenberg AJ. Cyclooxygenase-2 transcription is regulated by human papillomavirus 16 E6 and E7 oncoproteins: evidence of a corepressor/coactivator exchange.. Cancer Res 2007 Apr 15;67(8):3976-85.
    doi: 10.1158/0008-5472.CAN-06-4273pubmed: 17440114google scholar: lookup
  67. Dawood S, Austin L, Cristofanilli M. Cancer stem cells: implications for cancer therapy.. Oncology (Williston Park) 2014 Dec;28(12):1101-7, 1110.
    pubmed: 25510809
  68. Chung MK, Jung YH, Lee JK, Cho SY, Murillo-Sauca O, Uppaluri R, Shin JH, Sunwoo JB. CD271 Confers an Invasive and Metastatic Phenotype of Head and Neck Squamous Cell Carcinoma through the Upregulation of Slug.. Clin Cancer Res 2018 Feb 1;24(3):674-683.
    doi: 10.1158/1078-0432.CCR-17-0866pmc: PMC6713647pubmed: 29208672google scholar: lookup
  69. Elkashty OA, Abu Elghanam G, Su X, Liu Y, Chauvin PJ, Tran SD. Cancer stem cells enrichment with surface markers CD271 and CD44 in human head and neck squamous cell carcinomas.. Carcinogenesis 2020 Jun 17;41(4):458-466.
    doi: 10.1093/carcin/bgz182pmc: PMC7298622pubmed: 31742606google scholar: lookup
  70. Boiko AD, Razorenova OV, van de Rijn M, Swetter SM, Johnson DL, Ly DP, Butler PD, Yang GP, Joshua B, Kaplan MJ, Longaker MT, Weissman IL. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271.. Nature 2010 Jul 1;466(7302):133-7.
    doi: 10.1038/nature09161pmc: PMC2898751pubmed: 20596026google scholar: lookup
  71. Huang SD, Yuan Y, Liu XH, Gong DJ, Bai CG, Wang F, Luo JH, Xu ZY. Self-renewal and chemotherapy resistance of p75NTR positive cells in esophageal squamous cell carcinomas.. BMC Cancer 2009 Jan 10;9:9.
    doi: 10.1186/1471-2407-9-9pmc: PMC2637890pubmed: 19134212google scholar: lookup
  72. Imai T, Tamai K, Oizumi S, Oyama K, Yamaguchi K, Sato I, Satoh K, Matsuura K, Saijo S, Sugamura K, Tanaka N. CD271 defines a stem cell-like population in hypopharyngeal cancer.. PLoS One 2013;8(4):e62002.
    pmc: PMC3633921pubmed: 23626764doi: 10.1371/journal.pone.0062002google scholar: lookup
  73. Okumura T, Shimada Y, Imamura M, Yasumoto S. Neurotrophin receptor p75(NTR) characterizes human esophageal keratinocyte stem cells in vitro.. Oncogene 2003 Jun 26;22(26):4017-26.
    doi: 10.1038/sj.onc.1206525pubmed: 12821936google scholar: lookup
  74. Weissenbacher-Lang C, Kristen T, Mendel V, Brunthaler R, Schwarz L, Weissenböck H. Porcine circovirus type 2 (PCV2) genotyping in Austrian pigs in the years 2002 to 2017.. BMC Vet Res 2020 Jun 15;16(1):198.
    doi: 10.1186/s12917-020-02413-4pmc: PMC7294622pubmed: 32539835google scholar: lookup
  75. Brandt S, Haralambus R, Schoster A, Kirnbauer R, Stanek C. Peripheral blood mononuclear cells represent a reservoir of bovine papillomavirus DNA in sarcoid-affected equines.. J Gen Virol 2008 Jun;89(Pt 6):1390-1395.
    doi: 10.1099/vir.0.83568-0pubmed: 18474554google scholar: lookup

Citations

This article has been cited 9 times.
  1. Altamura G, Borzacchiello G. Feline oral squamous cell carcinoma and Felis catus papillomavirus: is it time to walk the path of human oncology?. Front Vet Sci 2023;10:1148673.
    doi: 10.3389/fvets.2023.1148673pubmed: 37266382google scholar: lookup
  2. 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
  3. Miglinci L, Reicher P, Nell B, Koch M, Jindra C, Brandt S. Detection of Equine Papillomaviruses and Gamma-Herpesviruses in Equine Squamous Cell Carcinoma. Pathogens 2023 Jan 23;12(2).
    doi: 10.3390/pathogens12020179pubmed: 36839451google scholar: lookup
  4. Schwarz S, Kummer S, Klang A, Walter I, Nell B, Brandt S. Detection of vasculogenic mimicry in equine ocular, oronasal, and genital squamous cell carcinoma. PLoS One 2026;21(1):e0328584.
    doi: 10.1371/journal.pone.0328584pubmed: 41490689google scholar: lookup
  5. Brodesser DM, Kummer S, Eichberger JA, Schlangen K, Corteggio A, Borzacchiello G, Bertram CA, Brandt S, Pratscher B. Deregulation of Metalloproteinase Expression in Gray Horse Melanoma Ex Vivo and In Vitro. Cells 2024 May 31;13(11).
    doi: 10.3390/cells13110956pubmed: 38891088google scholar: lookup
  6. Tuomisto L, Virtanen J, Kegler K, Levanov L, Sukura A, Sironen T, Kareskoski M. Equus caballus papillomavirus type 2 (EcPV2)-associated benign penile lesions and squamous cell carcinomas. Vet Med Sci 2024 Jan;10(1):e1342.
    doi: 10.1002/vms3.1342pubmed: 38227707google scholar: lookup
  7. Kummer S, Klang A, Strohmayer C, Walter I, Jindra C, Kneissl S, Brandt S. Feline SCCs of the Head and Neck Display Partial Epithelial-Mesenchymal Transition and Harbor Stem Cell-like Cancer Cells. Pathogens 2023 Oct 27;12(11).
    doi: 10.3390/pathogens12111288pubmed: 38003753google scholar: lookup
  8. Luff J, Weingart S, May S, Murphy B. A subset of equine oral squamous cell carcinomas is associated with Equus caballus papillomavirus 2 infection. J Comp Pathol 2023 Aug;205:1-6.
    doi: 10.1016/j.jcpa.2023.06.003pubmed: 37478800google scholar: lookup
  9. King RE, Bilger A, Rademacher J, Lambert PF, Thibeault SL. Preclinical Models of Laryngeal Papillomavirus Infection: A Scoping Review. Laryngoscope 2023 Dec;133(12):3256-3268.
    doi: 10.1002/lary.30762pubmed: 37227124google scholar: lookup
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