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Thesis Reference Thesis Role of oxidative stress and calcium regulation in Duchenne muscular dystrophy: pharmacological investigations ISMAIL, Hesham Abstract Duchenne Muscular Dystrophy (DMD) is the most common and most severe myopathy. Currently, no cure exists for DMD and novel pharmacotherapy holds the promise of being the fastest route for reaching the patients until a curative genetic therapy is delivered. Towards this end, three drug candidates were evaluated in DMD models. The first was doxorubicin which inhibited phospholipase A2 activity and reduced Ca2+ influx through stretch-activated channels, both reported to be overactive in dystrophic cells. Dystrophic muscles treated with doxorubicin were protected from damaging eccentric contractions. We have also tested the classical NADPH oxidase inhibitor apocynin and its synthetic dimer, diapocynin. Our in vitro and in vivo results show that diapocynin holds a superior therapeutic potential. In conclusion, the work presented in this thesis presents novel drug candidates that can be developed further as potential pharmacotherapeutic treatment for DMD. It also sheds light on the pathways involved in DMD pathogenesis. Reference ISMAIL, Hesham. Role of oxidative stress and calcium regulation in Duchenne muscular dystrophy: pharmacological investigations. Thèse de doctorat : Univ. Genève, 2013, no. Sc. 4607 URN : urn:nbn:ch:unige-321331 DOI : 10.13097/archive-ouverte/unige:32133 Available at: http://archive-ouverte.unige.ch/unige:32133 Disclaimer: layout of this document may differ from the published version. 1 / 1 UNIVERSITÉ DE GENÈVE FACULTÉ DES SCIENCES Section de Sciences Pharmaceutiques Professeur Urs T. Ruegg Pharmacologie Professeur Leonardo Scapozza Role of oxidative stress and calcium regulation in Duchenne muscular dystrophy: Pharmacological investigations THÈSE présentée à la Faculté des sciences de l’Université de Genève pour obtenir le grade de Docteur ès sciences, mention sciences pharmaceutiques par Hesham Mohamed Ismail HAMED du Caire (Egypte) These N°: 4607 Genève Atelier de reproduction Repromail 2013 ii Acknowledgments I would like to start my acknowledgments by expressing my sincere gratitude to Professor Urs Ruegg & Leonardo Scapozza as well as Dr. Olivier Dorchies for supervising my work. Urs, Thank you for giving me the chance to be a part of your lab team and for the joyful atmosphere and discussions we always have. Thank you for giving me much freedom of choosing my topics, trying out new techniques and experiments and for your generosity. I would have had a lot of difficulties supervising a student like me. Leonardo, I cannot thank you enough for accepting me as a part of your lab after Urs’ retirement and for your continuous support without which most of the work in this study would not have been completed. You made me feel as one of your own team. Also thank you for your support and encouragement for my future plans and projects. Olivier, all these results would not have existed if it was not for your help. Your remarks, pointers, discussions and suggestions redirected my work towards the better continuously. Your encouragement after every progress report I gave was very supportive. Having you in the empty lab after Urs’ retirement was really fun. I would like to thank the jury members, including Professors Natalia Shirokova, Karl Heinz Krause, and Gérard Hopfgartner for accepting to review my thesis and for their time spent in this process. To the ex-members of the lab of pharmacology, Chiara, Colette, Dominique, George, Julie, Karin, Miriam, Olivier, Ophélie, Piter, Yoshiko and Youssef……you are the best! Thank you for the lovely times we spent together inside the lab and outside. It would not have been the same without you. And a special thank you goes to Dominique who has been my legal advisor, lawyer, translator, facilitator among many others. I would be in a mess if it weren’t for you. For all of those in FABIP and the rest of the section, you really created a lovely atmosphere to work in, I enjoyed the coffee breaks , outings and courses and I hope we keep in touch even after all will go their own way. Prof. Khayyal, I consider you more a family member than my undergraduate professor, my M.S.c. supervisor and a jury member of my PhD thesis. I thank you very much for your support and encouragement at every step of the way and I hope to live up to your expectations even further. Finally to my family, to my mother, words cannot describe how much I am in debt to you for molding me through the years to be where I am today. Father, you lived up to be my role model, I just hope I will be close to achieving your expectations. My son Yousef whom I was blessed with during the work on this PhD thesis, thank you for finally accepting that my laptop is off limits! And Nesrin, I cannot thank you enough for supporting me not only through the ups and downs, of which there were a lot, during the work on my thesis but also throughout our marriage. Thank you for being who you are, I am truly blessed by you. iii iv Table of Contents Acknowledgments........................................................................................................................ iii Table of Contents ......................................................................................................................... iv List of figures and tables .............................................................................................................. vi Abbreviations .............................................................................................................................. vii Author Bibliography ................................................................................................................... viii Summary ...................................................................................................................................... ix Résumé......................................................................................................................................... xi Introduction ................................................................................................................................. 1 1.1 Skeletal Muscles ............................................................................................................ 3 1.1.1 Skeletal muscle organization and structure .......................................................... 3 1.1.2 Skeletal muscle function ........................................................................................ 5 1.1.3 Calcium handling in skeletal muscles .................................................................... 8 1.2 Duchenne muscular dystrophy (DMD) ........................................................................ 13 1.2.1 Clinical features and genetic aspects of DMD ..................................................... 13 1.2.2 Dystrophin and dystrophin-associated proteins complex ................................... 14 1.2.3 Pathogenesis of DMD .......................................................................................... 15 1.2.4 Therapeutic approaches for DMD ....................................................................... 21 Aim of the work ......................................................................................................................... 29 Chapter 2: Inhibition of iPLA2β and of stretch-activated channels by doxorubicin alters dystrophic muscle function .......................................................................................................................... 30 Chapter 3: Diapocynin, a NADPH oxidase inhibitor, reduces ROS production and prevents force loss in eccentrically contracting dystrophic muscle ......................................................................... 74 Chapter 4: Diapocynin, a putative NADPH oxidase inhibitor, ameliorates the phenotype of a mouse model of Duchenne muscular dystrophy ................................................................. 110 Chapter 5: General discussion and conclusions ................................................................... 142 Chapter 6: References ............................................................................................................ 148 v List of figures and tables Figure 1-1, Structure of skeletal muscle ...................................................................................... 4 Figure 1-2, Myosin, actin and the regulatory proteins ................................................................ 6 Figure 1-3, Phasic and tetanic contractions ................................................................................. 7 Figure 1-4, Force-velocity relationship in skeletal muscle........................................................... 8 Figure 1-5, Calcium handling in skeletal muscle cells ................................................................ 12 Figure 1-6, Dystrophin associated protein complex .................................................................. 15 Figure 1-7, Structure of group VIA-2 phospholipase A2 ............................................................. 18 Figure 1-8, NOX isoforms expressed in skeletal muscles .......................................................... 20 Figure 1-9, NOX2 and its assembly upon activation .................................................................. 21 Figure 1-10, Exon skipping technology in DMD ......................................................................... 23 Figure 5-11 Conversion of apocynin into
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