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In Vitro and in Vivo Development of a Topical Drug for the Treatment Of Lisa Annabel Weber In vitro DQGin vivo GHYHORSPHQWRIDWRSLFDOGUXJIRUWKH WUHDWPHQWRIHTXLQHVNLQFDQFHU±EDVHGRQQDWXUDOO\ RFFXUULQJDQGV\QWKHWLFDOO\PRGLILHG VXEVWDQFHVLQSODQHEDUN Cuvillier Verlag Göttingen Internationaler wissenschaftlicher Fachverlag %LEOLRJUDILVFKH,QIRUPDWLRQGHU'HXWVFKHQ1DWLRQDOELEOLRWKHN 'LH'HXWVFKH1DWLRQDOELEOLRWKHNYHU]HLFKQHWGLHVH3XEOLNDWLRQLQGHU 'HXWVFKHQ1DWLRQDOELEOLRJUDILHGHWDLOOLHUWHELEOLRJUDSKLVFKH'DWHQVLQGLP,QWHUQHW EHUKWWSGQEGQEGHDEUXIEDU $XIO*|WWLQJHQ&XYLOOLHU =XJO+DQQRYHU 7L+R 8QLY'LVV &89,//,(59(5/$**|WWLQJHQ 1RQQHQVWLHJ*|WWLQJHQ 7HOHIRQ 7HOHID[ ZZZFXYLOOLHUGH $OOH5HFKWHYRUEHKDOWHQ2KQHDXVGUFNOLFKH*HQHKPLJXQJGHV9HUODJHVLVW HVQLFKWJHVWDWWHWGDV%XFKRGHU7HLOHGDUDXVDXIIRWRPHFKDQLVFKHP:HJ )RWRNRSLH0LNURNRSLH ]XYHUYLHOIlOWLJHQ $XIODJH *HGUXFNWDXIXPZHOWIUHXQGOLFKHPVlXUHIUHLHP3DSLHUDXVQDFKKDOWLJHU )RUVWZLUWVFKDIW ,6%1 H,6%1 University of Veterinary Medicine Hannover Clinic for Horses In vitro and in vivo development of a topical drug for the treatment of equine skin cancer – based on naturally occurring and synthetically modified substances in plane bark THESIS Submitted in partial fulfilment of the requirements for the degree DOCTOR OF PHILOSOPHY (PhD) awarded by the University of Veterinary Medicine Hannover by Lisa Annabel Weber born in Idar-Oberstein Hannover, Germany 2020 Main supervisor: Prof. Dr. Karsten Feige Supervision group: Prof. Dr. Karsten Feige Prof. Dr. Manfred Kietzmann Prof. Dr. Jessika-M.V. Cavalleri 1st evaluation: Prof. Dr. Karsten Feige University of Veterinary Medicine Hannover, Foundation Clinic for Horses Bünteweg 9 30559 Hannover (Germany) Prof. Dr. Manfred Kietzmann University of Veterinary Medicine Hannover, Foundation Department of Pharmacology, Toxicology and Pharmacy Bünteweg 17 30559 Hannover (Germany) Prof. Dr. Jessika-M.V. Cavalleri University of Veterinary Medicine Vienna University Equine Clinic Veterinärplatz 1 1210 Vienna (Austria) 2nd evaluation: Prof. Dr. Wolfgang Bäumer Free University of Berlin – Department of Veterinary Medicine Institute of Pharmacology and Toxicology Koserstraße 20 14195 Berlin (Germany) Date of final exam: 26 October 2020 Sponsorship: Financial support was provided by the Federal Ministry for Economic Affairs and Energy based on a decision by the German Bundestag (Specific grant number: TopiDrugHorse 16KN051526 BMWI) Parts of this thesis have been previously published or communicated: Publications in peer-reviewed journals Weber LA, Meißner J, Delarocque J, Kalbitz J, Feige K, Kietzmann M, Michaelis A, Paschke R, Michael J, Pratscher B, Cavalleri JMV. Betulinic acid shows anticancer activity against equine melanoma cells and permeates isolated equine skin in vitro. BMC Vet Res 2020;16(44):1-9. DOI: 10.1186/s12917-020-2262-5 Weber LA, Funtan A, Paschke R, Meißner J, Delarocque J, Kalbitz J, Feige K, Kietzmann M, Cavalleri JMV. In vitro assessment of triterpenoids NVX-207 and betulinyl-bis-sulfamate as a topical treatment for equine skin cancer. PLoS ONE 2020;15(11):1-22. DOI: 10.1371/journal.pone.0241448 Weber LA, Puff C, Kalbitz J, Kietzmann M, Feige K, Bosse K, Rohn K, Cavalleri JMV. Concentration profiles and safety of topically applied betulinic acid and NVX-207 in eight healthy horses – A randomized, blinded, placebo-controlled, crossover pilot study. J vet Pharmacol Therap 2020;00:1-11. DOI: 10.1111/JVP.12903 Oral communications at conferences 27th Annual Conference “Internal Medicine and Clinical Laboratory Diagnostics (InnLab)” of the DVG, Feb 1-2, 2019 Munich, Germany Weber LA, Meißner J, Delarocque J, Michaelis A, Paschke R, Michael J, Feige K, Kietzmann M, Cavalleri JMV “Antiproliferative and cytotoxic effects of betulinic acid on equine melanoma cells and percutaneous permeation of betulinic acid through equine skin in vitro” Abstract: Tierarztl Prax Ausg K 2019;47(01): 66. DOI: 10.1055/s-0039-1678436 31st European Veterinary Dermatology Congress, Sept 26-28, 2019 Liverpool, United Kingdom Weber LA, Meißner J, Kietzmann M, Delarocque J, Kalbitz J, Feige K, Michaelis A, Paschke R, Cavalleri JMV “Anticancer effects of betulinic acid derivative NVX-207 on equine melanoma cells and percutaneous permeation through isolated equine skin in vitro” Abstract: Vet Dermatol 2019;30(6): 468–469. DOI: 10.1111/vde.12812 12th European College of Equine Internal Medicine Congress, Nov 22-23, 2019 Valencia, Spain Weber LA, Meißner J, Feige K, Kietzmann M, Kalbitz J, Delarocque J, Michaelis A, Paschke R, Brandt S, Cavalleri JMV “In vitro assessment of betulinic acid derivative NVX-207 as a topical treatment for equine sarcoids” 12th Graduate School Days, Nov 29-30, 2019 Bad Salzdetfurth, Germany Weber LA, Kalbitz J, Meißner J, Feige K, Kietzmann M, Puff C, Cavalleri JMV “Betulinic acid derivative NVX-207: In vitro and in vivo permeation studies on equine skin” Poster presentations at conferences 11th European College of Equine Internal Medicine Congress, Nov 9-10, 2018 Ghent, Belgium Weber LA, Meißner J, Delarocque J, Kalbitz J, Feige K, Kietzmann M, Michaelis A, Paschke R., Michael J, Pratscher B, Cavalleri JMV “Antiproliferative and cytotoxic effects of betulinic acid and derivatives on equine melanoma cells” Abstract: J Vet Intern Med 2019; 33(3):1555–1556. DOI: 10.1111/jvim.15447 11th Graduate School Days, Nov 30-Dec 1, 2018 Hannover, Germany Weber LA, Meißner J, Delarocque J, Kalbitz J, Feige K, Kietzmann M, Michaelis A, Paschke R, Michael J, Pratscher B, Cavalleri JMV “Trees against equine skin cancer? - Antiproliferative and cytotoxic effects of betulinic acid and derivatives on equine melanoma cells” Für meine Familie TABLE OF CONTENTS LIST OF ABBREVIATIONS .................................................................................................. I SUMMARY .............................................................................................................................. II ZUSAMMENFASSUNG........................................................................................................ IV 1. Introduction......................................................................................................................... 1 1.1. The equine malignant melanoma .................................................................................. 1 1.1.1. Tumor classification ........................................................................................... 2 1.1.2. Etiology............................................................................................................... 2 1.1.3. Gross pathology and diagnosis ........................................................................... 3 1.1.4. Clinical signs in diseased horses......................................................................... 3 1.1.5. Current treatment options ................................................................................... 4 1.2. The equine sarcoid: an overview................................................................................... 5 1.3. Topical drug application ............................................................................................... 5 1.3.1. Why the topical (epicutaneous) approach to treat equine skin cancer? .............. 5 1.3.2. Drug transport across the skin ............................................................................ 6 1.4. Naturally occurring substances in plane bark and their synthetically modified derivatives ..................................................................................................................... 7 1.4.1. Betulinic acid ...................................................................................................... 8 1.4.2. Betulinic acid derivative NVX-207 .................................................................... 9 1.4.3. Betulin derivative betulinyl-bis-sulfamate ......................................................... 9 1.5. Hypotheses and aims of the thesis .............................................................................. 10 2. Manuscript I: Betulinic acid shows anticancer activity against equine melanoma cells and permeates isolated equine skin in vitro............................................................ 13 2.1. Supplemental data ....................................................................................................... 23 3. Manuscript II: In vitro assessment of triterpenoids NVX-207 and betulinyl-bis- sulfamate as a topical treatment for equine skin cancer ............................................... 25 4. Manuscript III: Concentration profiles and safety of topically applied betulinic acid and NVX-207 in eight healthy horses – A randomized, blinded, placebo- controlled, crossover pilot study ...................................................................................... 49 5. Manuscript IV: Effects of topically applied betulinic acid and NVX-207 on early stage equine melanoma – A prospective, randomized, double-blind, placebo- controlled pilot study ........................................................................................................ 63 6. General discussion ............................................................................................................ 85 6.1. Summarized findings .................................................................................................. 85 6.2. Interpretation of the findings ....................................................................................... 85 6.2.1. In vitro cell culture experiments ......................................................................
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