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Novel Molecular Targets for Feline Oral Squamous Cell Carcinoma

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Novel Molecular Targets for Feline Oral Squamous Cell Carcinoma Novel Molecular Targets for Feline Oral Squamous Cell Carcinoma DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Wachiraphan Supsavhad Graduate Program in Comparative and Veterinary Medicine The Ohio State University 2016 Dissertation Committee Thomas J. Rosol, Advisor James DeWille Ramiro Toribio Gwendolen Lorch Theodore M. Brasky Copyrighted by Wachiraphan Supsavhad 2016 Abstract Feline oral squamous cell carcinoma (FOSCC) is the most common oral cancer in cats. This cancer is very aggressive and has the ability to invade into the adjacent bone resulting in poor quality of life and a grave prognosis in affected cats. FOSCC has been shown to be comparable to human OSCC in many aspects. However, the pathogenesis of FOSCC remains unclear. Similar to human OSCC, FOSCCs respond poorly to the available standard therapy. Therefore, novel molecular targets as well as effective therapies are required for this cancer. The usefulness of p16, p53, and pRb immunohistochemistry (IHC) for human OSCC classification has been reported. Low p16 frequently associates with non-viral- associated OSCCs, while high p16 with low p53 and pRb usually occurs in HPV- associated OSCC. In addition, a favorable prognosis was found in patients with HPV- associated OSCC and a grave prognosis was observed in patients with non-viral- associated OSCC. In this study, the IHC pattern of p16, p53, and pRb in FOSCC was investigated. We found that low p16 IHC is common in FOSCCs and high p16 IHC is present in a subset of patients with this cancer. However feline papillomavirus was not detected in these samples. These results indicate that FOSCCs have more than one type of classification and a variation in pathogenesis may occur in FOSCC. Increased osteoprotegerin (OPG) has been found to reduce tumor size and bone invasion in many human bone-invasive cancers. Low levels of feline OPG (fOPG) ii mRNA expression were previously observed in a bone-invasive FOSCC cell line (SCCF2). The role of fOPG in bone-invasive FOSCC in vitro and in vivo was investigated using a novel bone-invasive FOSCC cell line with high fOPG mRNA expression (SCCF2-OPGv.1).We found that overexpression of fOPG reduced tumor growth and inhibited bone invasion in bone-invasive FOSCC in vivo. Thus, fOPG could be effective adjuvant therapy for FOSCC-associated bone lysis. Telomerase, a protein complex with cell immortalization activity, has been speculated as a novel therapeutic target for human cancers. Telomerase transcriptase catalytic subunit (TERT) and the non-coding RNA template are the main components of this protein. Pre-mRNA alternative splicing occurs in human TERT gene and more than 20 human TERT alternative splice variants were identified. In this study, high levels of telomerase activity were observed in FOSCC cells (SCCF1, SCCF2, and SCCF3) and in 2 of 3 FOSCC tumors. Full-length and 10 novel feline TERT (fTERT) alternative splice variants were identified. Full-length and the deletion of exon 10 (Del-e10) splice variant of fTERT were the two common variants in FOSCCs with high telomerase activity found in this study. These findings suggest that alternative splicing is important for the regulation of telomerase activity and provide critical information to further the understanding of telomerase in feline cancers. iii Acknowledgments I would like to take this opportunity to give special thanks to people who have contributed to my success. First and foremost, I would like to sincerely express my gratitude to my advisor, Dr. Thomas J. Rosol who has given me an opportunity to pursue my studies at the Ohio State University. The wonderful experience, constant guidance and support that I have received during my study prepared me well for more challenges in my future career. I would like to take this chance to thank to Drs. James DeWille, Ramiro Toribio, and Gwendolen Lorch, members of my dissertation committee, for their valuable technical advice. My gratitude is extended to Dr. Wessel Dirksen, Rosol lab manager, for significant contributions on day-to-day problem solving related to experimental work, suggestions, and considerable editorial help on this dissertation. In addition, I would like to thank all of the previous and present Rosol lab members (Dr. Eason Hildreth, Dr. Jessica Simmons, Dr. Said Elshafae, Dr. Bardes Hassan, Dr. Nicole Kohart, Dr. Aylin Demirer, Lucas Altstadt, James Feller and Taylor Wickware) for their support and for contributing to a pleasant working environment during my study. I am very thankful for the staff in the Histology/Immunohistochemistry Core Lab, College of Veterinary Medicine, The Ohio State University for the wonderful histopathology slides. This work could not be done without their help. iv I am grateful for the tuition scholarship from the Faculty of Veterinary Medicine at Kasetsart University, Thailand, during the first two and half years of my Ph.D. study and the fellowship from the Department of Defense (DOD) for during last 1.5 year. Without this support, it would not have been possible to complete my studies successfully. Last but not least, I cannot forget to thank my family members and my beloved husband for the unconditional love, care, and encouragement. I would never come this far without their constant support. v Vita 1999................................................................Chinat Pittayakom High School 2005................................................................D.V.M., Kasetsart University, Thailand 2012................................................................M.S. Comparative and Veterinary Medicine. The Ohio State University 2012 to 2015 ..................................................Graduate Student Department of Veterinary Biosciences, The Ohio State University 2015 to present ...............................................Post Doctoral Fellow Department of Veterinary Biosciences, The Ohio State University Publications W. Supsavhad, W.P. Dirksen, C.K. Martin, T.J. Rosol. Animal models of head and neck squamous cell carcinoma. The Veterinary Journal. 210: 7-16. October 2015 B.E. Hildreth, K.M. Hernon, W.P. Dirksen, J. Leong, W. Supsavhad, P.N. Boyaka, T.J. Rosol, R.E. Toribio. Deletion of the nuclear localization sequence and C-terminus of parathyroid hormone-related protein decreases osteogenesis and chondrogenesis but increases adipogenesis and myogenesis in murine bone marrow stromal cells. Journal of Tissue Engineering. 6. October 2015; DOI: 10.1177/2041731415609298 vi J.K. Simmons, B.E. III Hildreth, W. Supsavhad, S.M. Elshafae, B.B. Hassan, W.P. Dirksen, R.E. Toribio, T.J. Rosol. Animal model of bone metastasis. Veterinary Pathology. 52(5). May 2015 S.M. Elshafae, B.B. Hassan, W. Supsavhad, W.P. Dirksen, R.Y. Camiener, H. Ding, M. F. Tweedle, T. J Rosol. Gastrin-releasing peptide receptor (GRPr) promotes EMT, growth, and invasion in canine prostate cancer. The Prostate. 76(9). March 2016 B.B. Hassan, S.M. Elshafae, W. Supsavhad, J.K. Simmons, W.P. Dirksen, S.M. Sokkar, T.J. Rosol. Feline mammary cancer: novel nude mouse model and molecular characterization of invasion and metastasis genes. Veterinary Pathology. June 2016 Fields of Study Major Field: Comparative and Veterinary Medicine vii Table of Contents Abstract ............................................................................................................................... ii Acknowledgments.............................................................................................................. iv Vita ..................................................................................................................................... vi List of Tables ................................................................................................................... xiii List of Figures .................................................................................................................. xiv Chapter 1: Animal Models of Head and Neck Squamous Cell Carcinoma ........................ 1 Abstract ........................................................................................................................... 1 Introduction ..................................................................................................................... 2 Hamster model of HNSCC .............................................................................................. 5 Rodent models of HNSCC .............................................................................................. 7 Rat and mouse chemically-induced carcinogenesis model ......................................... 7 Xenograft transplantation models of HNSCC ............................................................. 9 Transgenic mouse models of HNSCC ....................................................................... 11 Domestic animal models of spontaneous HNSCC ........................................................ 13 Dog model of HNSCC ............................................................................................... 14 viii Cat model of HNSCC ................................................................................................ 15 Conclusions ................................................................................................................... 22 Chapter 2: p16, pRb, and p53 in Feline Oral Squamous Cell Carcinoma ........................ 33 Abstract ........................................................................................................................
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