E-Cadherin Immunostaining in Equine Melanocytic Tumors
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Tissue Samples
2.2. Clinical Information
2.3. Histopathological Evaluation
2.4. Immunohistochemistry
2.5. Immunohistochemical Evaluation
2.6. Statistical Analysis
3. Results
3.1. Clinical Information
3.2. Histopathologic Results
3.3. Immunohistochemical Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Nishiya, A.T.; Massoco, C.O.; Felizzola, C.R.; Perlmann, E.; Batschinski, K.; Tedardi, M.V.; Garcia, J.S.; Mendonça, P.P.; Teixeira, T.F.; Dagli, M.L.Z. Comparative Aspects of Canine Melanoma. Vet. Sci. 2016, 3, 7. [Google Scholar] [CrossRef] [Green Version]
- Wong, K.; van der Weyden, L.; Schott, C.R.; Foote, A.; Constantino-Casas, F.; Smith, S.; Dobson, J.M.; Murchison, E.P.; Wu, H.; Yeh, I.; et al. Cross-Species Genomic Landscape Comparison of Human Mucosal Melanoma with Canine Oral and Equine Melanoma. Nat. Commun. 2019, 10, 353. [Google Scholar] [CrossRef]
- Resende, L.; Moreira, J.; Prada, J.; Queiroga, F.L.; Pires, I. Current Insights Into Canine Cutaneous Melanocytic Tumours Diagnosis. In Melanoma—Current Clinical Management and Future Therapeutics; Intech: London, UK, 2015. [Google Scholar]
- van der Weyden, L.; Patton, E.E.; Wood, G.A.; Foote, A.K.; Brenn, T.; Arends, M.J.; Adams, D.J. Cross-Species Models of Human Melanoma. J. Pathol. 2016, 238, 152–165. [Google Scholar] [CrossRef] [Green Version]
- Phillips, J.C.; Lembcke, L.M. Equine Melanocytic Tumors. Vet. Clin. N. Am. Equine Pract. 2013, 29, 673–687. [Google Scholar] [CrossRef]
- Moore, J.S.; Shaw, C.; Shaw, E.; Buechner-Maxwell, V.; Scarratt, W.K.; Crisman, M.; Furr, M.; Robertson, J. Melanoma in Horses: Current Perspectives. Equine Vet. Educ. 2013, 25, 144–151. [Google Scholar] [CrossRef]
- Teixeira, R.B.C.; Rendahl, A.K.; Anderson, S.M.; Mickelson, J.R.; Sigler, D.; Buchanan, B.R.; Coleman, R.J.; Mccue, M.E. Coat Color Genotypes and Risk and Severity of Melanoma in Gray Quarter Horses. J. Vet. Intern. Med. 2013, 27, 1201–1208. [Google Scholar] [CrossRef]
- Rosengren Pielberg, G.; Golovko, A.; Sundström, E.; Curik, I.; Lennartsson, J.; Seltenhammer, M.H.; Druml, T.; Binns, M.; Fitzsimmons, C.; Lindgren, G.; et al. A Cis-Acting Regulatory Mutation Causes Premature Hair Graying and Susceptibility to Melanoma in the Horse. Nat. Genet. 2008, 40, 1004–1009. [Google Scholar] [CrossRef]
- Albanese, V.; Newton, J.C.; Waguespack, R.W. Malignant Melanoma of the Third Eyelid in a Horse. Equine Vet. Educ. 2015, 27, e15–e19. [Google Scholar] [CrossRef]
- Strauss, R.A.; Allbaugh, R.A.; Haynes, J.; Ben-Shlomo, G. Primary Corneal Malignant Melanoma in a Horse. Equine Vet. Educ. 2019, 31, 403–409. [Google Scholar] [CrossRef]
- Va Metcalfe, L.; O’brien, P.J.; Papakonstantinou, S.; Cahalan, S.D.; Mcallister, H.; Duggan, V.E. Malignant Melanoma in a Grey Horse: Case Presentation and Review of Equine Melanoma Treatment Options. Ir. Vet. J. 2013, 66, 22. [Google Scholar] [CrossRef] [Green Version]
- Valentine, B.A.; Calderwood Mays, M.B.; Cheramie, H.S. Anaplastic Malignant Melanoma of the Tail in Non-Grey Horses. Equine Vet. Educ. 2014, 26, 156–158. [Google Scholar] [CrossRef]
- Cavalleri, J.M.V.; Mählmann, K.; Steinig, P.; Feige, K. Aetiology, Clinical Presentation and Current Treatment Options of Equine Malignant Melanoma—A Review of the Literature. Pferdeheilkunde 2014, 30, 455–460. [Google Scholar] [CrossRef] [Green Version]
- Hsu, M.Y.; Meier, F.E.; Nesbit, M.; Hsu, J.Y.; Van Belle, P.; Elder, D.E.; Herlyn, M. E-Cadherin Expression in Melanoma Cells Restores Keratinocyte-Mediated Growth Control and down-Regulates Expression of Invasion-Related Adhesion Receptors. Am. J. Pathol. 2000, 156, 1515–1525. [Google Scholar] [CrossRef] [Green Version]
- D’arcy, C.; Kiel, C. Cell Adhesion Molecules in Normal Skin and Melanoma. Biomolecules 2021, 11, 1213. [Google Scholar] [CrossRef]
- Eddy, K.; Shah, R.; Chen, S. Decoding Melanoma Development and Progression: Identification of Therapeutic Vulnerabilities. Front. Oncol. 2021, 10, 626129. [Google Scholar] [CrossRef]
- Vandyck, H.H.; Hillen, L.M.; Bosisio, F.M.; Van Den Oord, J.; Zur Hausen, A.; Winnepenninckx, V. Rethinking the Biology of Metastatic Melanoma: A Holistic Approach. Cancer Metastasis Rev. 2021, 40, 603–624. [Google Scholar] [CrossRef]
- Smart, J.A.; Oleksak, J.E.; Hartsough, E.J. Cell Adhesion Molecules in Plasticity and Metastasis. Mol. Cancer Res. 2021, 19, 25–37. [Google Scholar] [CrossRef]
- Haass, N.K.; Smalley, K.S.M.; Li, L.; Herlyn, M. Adhesion, Migration and Communication in Melanocytes and Melanoma. Pigment. Cell Res. 2005, 18, 150–159. [Google Scholar] [CrossRef]
- Han, J.I.; Kim, Y.; Kim, D.Y.; Na, K.J. Alteration in E-Cadherin/β-Catenin Expression in Canine Melanotic Tumors. Vet. Pathol. 2013, 50, 274–280. [Google Scholar] [CrossRef] [Green Version]
- Dane, E.; Vries, T.; Morandini, R.; Ghanem, G.; Ruiter, D.; Muijen, G. E Cadherin Expression in Human Melanoma. Melanoma Res. 1996, 6, 127–131. [Google Scholar] [CrossRef]
- Silvestri, S.; Porcellato, I.; Mechelli, L.; Menchetti, L.; Iussich, S.; De Maria, R.; Sforna, M.; Bongiovanni, L.; Brachelente, C. E-Cadherin Expression in Canine Melanocytic Tumors: Histological, Immunohistochemical, and Survival Analysis. Vet. Pathol. 2020, 57, 608–619. [Google Scholar] [CrossRef]
- Burandt, E.; Lübbersmeyer, F.; Gorbokon, N.; Büscheck, F.; Luebke, A.M.; Menz, A.; Kluth, M.; Hube-Magg, C.; Hinsch, A.; Höflmayer, D.; et al. E-Cadherin Expression in Human Tumors: A Tissue Microarray Study on 10,851 Tumors. Biomark. Res. 2021, 9, 44. [Google Scholar] [CrossRef]
- Pisamai, S.; Rungsipipat, A.; Kalpravidh, C.; Suriyaphol, G. Gene Expression Profiles of Cell Adhesion Molecules, Matrix Metalloproteinases and Their Tissue Inhibitors in Canine Oral Tumors. Res. Vet. Sci. 2017, 113, 94–100. [Google Scholar] [CrossRef]
- Pires, I.; Gomes, J.; Prada, J.; Pereira, D.; Queiroga, F.L. MMP-2 and MMP-9 Expression in Canine Cutaneous Melanocytic Tumours: Evidence of a Relationship with Tumoural Malignancy. In Recent Advances in the Biology, Therapy and Management of Melanoma; InTech: London, UK, 2013. [Google Scholar] [CrossRef] [Green Version]
- Campagne, C.; Julé, S.; Bernex, F.; Estrada, M.; Aubin-Houzelstein, G.; Panthier, J.-J.; Egidy, G. RACK1, a Clue to the Diagnosis of Cutaneous Melanomas in Horses. BMC Vet. Res. 2012, 8, 95. [Google Scholar] [CrossRef] [Green Version]
- Pires, I.; Queiroga, F.; Alves, A.; Silva, F.; Lopes, C. Decrease of E-Cadherin Expression in Canine Cutaneous Histiocytoma Appears to Be Related to Its Spontaneous Regression. Anticancer Res. 2009, 29, 2713–2718. [Google Scholar]
- Sáez-Ayala, M.; Montenegro, M.F.; Sánchez-del-Campo, L.; Fernández-Pérez, M.P.; Chazarra, S.; Freter, R.; Middleton, M.; Piñero-Madrona, A.; Cabezas-Herrera, J.; Goding, C.R.; et al. Directed Phenotype Switching as an Effective Antimelanoma Strategy. Cancer Cell 2013, 24, 105–119. [Google Scholar] [CrossRef] [Green Version]
- Pearlman, R.L.; de Oca, M.K.M.; Pal, H.C.; Afaq, F. Potential Therapeutic Targets of Epithelial–Mesenchymal Transition in Melanoma. Cancer Lett. 2017, 391, 125–140. [Google Scholar] [CrossRef] [Green Version]
- Kreizenbeck, G.M.; Berger, A.J.; Subtil, A.; Rimm, D.L.; Gould Rothberg, B.E. Prognostic Significance of Cadherin-Based Adhesion Molecules in Cutaneous Malignant Melanoma. Cancer Epidemiol. Biomark. Prev. 2008, 17, 949–958. [Google Scholar] [CrossRef] [Green Version]
- Veloso, E.S.; Gonçalves, I.N.N.; Silveira, T.L.; Espirito Santo, J.T.; Figueiredo, L.V.; Varaschin, M.S.; Cassali, G.D.; Del Puerto, H.L.; Ferreira, E. ZEB and Snail Expression Indicates Epithelial-Mesenchymal Transition in Canine Melanoma. Res. Vet. Sci. 2020, 131, 7–14. [Google Scholar] [CrossRef]
- Armando, F.; Mazzola, F.; Ferrari, L.; Corradi, A. An Overview of Epithelial-to-Mesenchymal Transition and Mesenchymal-to-Epithelial Transition in Canine Tumors: How Far Have We Come? Vet. Sci. 2023, 10, 19. [Google Scholar] [CrossRef]
- Schmid, F.; Brodesser, D.; Reifinger, M.; Forte, S.; Semp, P.; Eberspächer-Schweda, M.C.; Wolschek, M.; Brandt, S.; Kleiter, M.; Pratscher, B. Canine Oral Primary Melanoma Cells Exhibit Shift to Mesenchymal Phenotype and Phagocytic Behaviour. Vet. Comp. Oncol. 2019, 17, 211–220. [Google Scholar] [CrossRef]
- Loh, C.Y.; Chai, J.Y.; Tang, T.F.; Wong, W.F.; Sethi, G.; Shanmugam, M.K.; Chong, P.P.; Looi, C.Y. The E-Cadherin and n-Cadherin Switch in Epithelial-to-Mesenchymal Transition: Signaling, Therapeutic Implications, and Challenges. Cells 2019, 8, 1118. [Google Scholar] [CrossRef] [Green Version]
- Knottenbelt, D.C.; Patterson-Kane, J.C.; Snalune, K.L. Melanocytic Neoplasms. In Clinical Equine Oncology; Elsevier: Amsterdam, The Netherlands, 2015; pp. 237–246. ISBN 978-0-7020-4266-9. [Google Scholar]
- Seltenhammer, M.H.; Simhofer, H.; Scherzer, S.; Zechner, P.; Curik, I.; Sölkner, J.; Brandt, S.M.; Jansen, B.; Pehamberger, H.; Eisenmenger, E. Equine Melanoma in a Population of 296 Grey Lipizzaner Horses. Equine Vet. J. 2003, 35, 153–157. [Google Scholar] [CrossRef]
- Sundström, E.; Imsland, F.; Mikko, S.; Wade, C.; Sigurdsson, S.; Rosengren Pielberg, G.; Golovko, A.; Curik, I.; Seltenhammer, M.H.; Sölkner, J.; et al. Copy Number Expansion of the STX17 Duplication in Melanoma Tissue from Grey Horses. BMC Genom. 2012, 13, 365. [Google Scholar] [CrossRef] [Green Version]
- Curik, I.; Druml, T.; Seltenhammer, M.; Sundström, E.; Pielberg, G.R.; Andersson, L.; Sölkner, J. Complex Inheritance of Melanoma and Pigmentation of Coat and Skin in Grey Horses. PLoS Genet. 2013, 9, e1003248. [Google Scholar] [CrossRef] [Green Version]
- Peres, J.; Damerell, V.; Chauhan, J.; Popovic, A.; Desprez, P.Y.; Galibert, M.D.; Goding, C.R.; Prince, S. TBX3 Promotes Melanoma Migration by Transcriptional Activation of ID1, Which Prevents Activation of E-Cadherin by MITF. J. Investig. Dermatol. 2021, 141, 2250–2260.e2. [Google Scholar] [CrossRef]
- Hartman, M.L.; Czyz, M. MITF in Melanoma: Mechanisms behind Its Expression and Activity. Cell. Mol. Life Sci. 2015, 72, 1249–1260. [Google Scholar] [CrossRef] [Green Version]
- Dilshat, R.; Fock, V.; Kenny, C.; Gerritsen, I.; Lasseur, R.M.J.; Travnickova, J.; Eichhoff, O.; Cerny, P.; Möller, K.; Sigurbjörnsdóttir, S.; et al. Mitf Reprograms the Extracellular Matrix and Focal Adhesion in Melanoma. eLife 2021, 10, e63093. [Google Scholar] [CrossRef]
- Vachtenheim, J.; Ondrušová, L. Microphthalmia-Associated Transcription Factor Expression Levels in Melanoma Cells Contribute to Cell Invasion and Proliferation. Exp. Dermatol. 2015, 24, 481–484. [Google Scholar] [CrossRef] [Green Version]
- Joshi, S.S.; Hornyak, T.J. Cellular Phenotypic Plasticity of Cutaneous Melanoma: A Complex Puzzle. J. Investig. Dermatol. 2020, 140, 743–745. [Google Scholar] [CrossRef] [Green Version]
- Bockhorn, M.; Jain, R.K.; Munn, L.L. Active versus Passive Mechanisms in Metastasis: Do Cancer Cells Crawl into Vessels, or Are They Pushed? Lancet Oncol. 2007, 8, 444–448. [Google Scholar] [CrossRef] [Green Version]
- Bønnelykke-Behrndtz, M.L.; Steiniche, T.; Damsgaard, T.E.; Georgsen, J.B.; Danielsen, A.; Bastholt, L.; Møller, H.J.; Nørgaard, P.H.; Schmidt, H. MelanA-Negative Spindle-Cell Associated Melanoma, a Distinct Inflammatory Phenotype Correlated with Dense Infiltration of CD163 Macrophages and Loss of E-Cadherin. Melanoma Res. 2015, 25, 113–118. [Google Scholar] [CrossRef] [PubMed]
- Seltenhammer, M.H.; Heere-Ress, E.; Brandt, S.; Druml, T.; Jansen, B.; Pehamberger, H.; Niebauer, G.W. Comparative Histopathology of Grey-Horse-Melanoma and Human Malignant Melanoma. Pigment. Cell Res. 2004, 17, 674–681. [Google Scholar] [CrossRef] [PubMed]
- Smedley, R.C.; Spangler, W.L.; Esplin, D.G.; Kitchell, B.E.; Bergman, P.J.; Ho, H.Y.; Bergin, I.L.; Kiupel, M. Prognostic Markers for Canine Melanocytic Neoplasms: A Comparative Review of the Literature and Goals for Future Investigation. Vet. Pathol. 2011, 48, 54–72. [Google Scholar] [CrossRef]
- Sullins, K.E. Melanocytic Tumours in Horses. Equine Vet. Educ. 2020, 32, 624–630. [Google Scholar] [CrossRef]
- Pilsworth, R.C.; Knottenbelt, D. Skin Diseases Refresher Melanoma. Equine Vet. Educ. 2006, 18, 296–340. [Google Scholar]
- Knottenbelt, D.C.; Patterson-Kane, J.C.; Snalune, K.L. Tumours of the Skin. In Clinical Equine Oncology; Elsevier: Amsterdam, The Netherlands, 2015; pp. 544–584. ISBN 978-0-7020-4266-9. [Google Scholar]
- Bellenghi, M.; Puglisi, R.; Pontecorvi, G.; De Feo, A.; Carè, A.; Mattia, G. Sex and Gender Disparities in Melanoma. Cancers 2020, 12, 1819. [Google Scholar] [CrossRef] [PubMed]
- Burden, K. Melanomas and Their Effect on the Grey Horse. Young Sci. J. 2011, 4, 75. [Google Scholar] [CrossRef] [Green Version]
Histological Classification | Nuclear Grade | Nucleolar Size | Mitotic Count | Tumor Vascular Emboli | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|
I | II | III | Small | Medium | Large | 0 | <10 | >10 | Absent | Present | |
Benign | 26 | 5 | 0 | 28 | 3 | 0 | 31 | 0 | 0 | 31 | 0 |
Malignant | 0 | 10 | 31 | 9 | 29 | 3 | 28 | 3 | 10 | 13 | 28 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pimenta, J.; Pires, I.; Prada, J.; Cotovio, M. E-Cadherin Immunostaining in Equine Melanocytic Tumors. Animals 2023, 13, 2216. https://doi.org/10.3390/ani13132216
Pimenta J, Pires I, Prada J, Cotovio M. E-Cadherin Immunostaining in Equine Melanocytic Tumors. Animals. 2023; 13(13):2216. https://doi.org/10.3390/ani13132216
Chicago/Turabian StylePimenta, José, Isabel Pires, Justina Prada, and Mário Cotovio. 2023. "E-Cadherin Immunostaining in Equine Melanocytic Tumors" Animals 13, no. 13: 2216. https://doi.org/10.3390/ani13132216