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3.1 Publication I Evolution of Novel Antibiotic Scaffolds Targeting the Nucleic Acid Machineries RNA Polymerase, DNA Gyrase, and Topoisomerase IV Dissertation zur Erlangung des Grades des Doktors der Naturwissenschaften der Naturwissenschaftlich-Technischen Fakultät III Chemie, Pharmazie, Bio- und Werkstoffwissenschaften der Universität des Saarlandes von MSc. Walid Ali Mahmoud Elgaher Saarbrücken 2016 II „Gedruckt mit Unterstützung des Deutschen Akademischen Austauschdienstes“ Tag des Kolloquiums: 08. November 2016 Dekan: Prof. Dr. Dirk Bähre Vorsitz: Prof. Dr. Rolf Müller Berichterstatter: Prof. Dr. Rolf W. Hartmann Prof. Dr. Andreas Speicher Akad. Mitarbeiter: Dr. Silke Wenzel III Die vorliegende Arbeit wurde von April 2012 bis März 2016 unter Anleitung von Herrn Prof. Dr. Rolf W. Hartmann in der Fachrichtung 8.2 Pharmazeutische und Medizinische Chemie der Naturwissenschaftlich-Technischen Fakultät III der Universität des Saarlandes sowie am Helmholtz Institut für Pharmazeutische Forschung Saarland (HIPS) angefertigt. IV „Wer folgte einem Pfad Wissen darin zu suchen, erleichtert Allah für ihn einen Weg zum Paradies.“ Prophet Mohammad V Acknowledgment To Allah almighty who supported, blessed, and granted me everything I have. All my sincere appreciations and everlasting thanks to my PhD supervisor Prof. Dr. Rolf W. Hartmann for giving me the honor to work under his supervision and assigning attractive projects to me. Thanks for the golden advices, valuable instructions, experienced decisions, continuous encouragement, efficient assistance, and a lot of things I learned from him that changed my professional and life perspectives as well. I am greatly indebted to Prof. Dr. Andreas Speicher for his scientific support, constructive comments, and fruitful discussions during my doctorate study. I express my thanks and gratitude to Dr. Matthias Groh for his sincere training and transfer of knowledge in synthetic chemistry as well as for orchestrating numerous scientific and further tasks in a friendly atmosphere. I would like to thank Dr. Jörg Haupenthal for the good management and performance of some biological experiments of the RNAP project. My special thanks to Dr. Mostafa Hamed for the smart management and sincere help in the cystobactamids project. I am grateful to Prof. Dr. Rolf Müller, Prof. Dr. Andreas Kirschning, Dr. Sascha Baumman, Dr. Jennifer Herrmann, Dr. María Moreno, and Lorenz Siebenbürger for their precious efforts in the cystobactamids project. Great thanks are presented to Prof. Dr. Yves Mély and his team in particular Dr. Kamal Sharma and Dr. Francesco Saladini for the successful collaboration in the dual RNAP/RT inhibitors project. I also appreciate Dr. Martina Fruth, Dr. Kristina Hüsecken, Jeaninne Jung, and Jannine Ludwig for their assistance in the biological evaluations of the RNAP project. Deep thanks are expressed to Dr. Josef Zapp for running and optimizing hundreds of NMR experiments, and Dr. Volker Huch for determination of several X-ray crystal structures as well as Dr. Stefan Boettcher for his help in LC/MS analysis. I am very thankful to Prof. Dr. Uli Kazmaier for the admission in the Interdisciplinary Graduate School of Natural Product Research and financing participation in conferences. VI My endless thanks to the German academic exchange service (DAAD) for the full scholarship and support to get my PhD degree in Germany. Sincere thanks are to Dr. Matthias Engel, Dr. Martin Frotscher, Dr. Ahmed S. Abdelsamie, Katrin Schmitt, May Concepcion, and Lothar Jager who helped me before the journey to and during the stay in Germany. Many thanks to all current and former colleagues and employees at the working group of Prof. Hartmann and Helmholtz Institute for Pharmaceutical Research Saarland (HIPS) who are not mentioned by name here for the cooperative atmosphere. Finally, I would like to present all my thanks to my beloved family: my parents Ali and Samia, my sisters Samar and Norhan, my brother Mohammad, my wife Weam and my children Nermin and Mohammad, who stand beside me in every moment to relief my pains and share my joy feelings. When I see you or hear your voices, I feel like being in heaven and without you, I am lost. To you I dedicate this thesis. Walid Ali M. Elgaher August 2016 VII Abstract The magic bullets for treating bacterial infection are getting less potent in face of the growing resistance. This warning situation urges for rapid development of new antibacterial weapons effective against resistant pathogens. In this thesis, novel antibiotic scaffolds with low resistance frequency were developed by two strategies. First, targeting a vital binding site (the switch region) of bacterial RNA polymerase: Following analog design approaches, six ureido-heterocycle-carboxylic acid classes were synthesized based on a previous class. The new compounds show potent activity against Gram-positive pathogens as well as the Gram-negative E. coli TolC strain. They are characterized by no cross- resistance with the clinically used RNAP inhibitor rifampicin, lower rate of resistance development, and marginal cytotoxicity to human cells. These features were employed to target the closely related NNRTI binding site of HIV-1 reverse transcriptase. By structure-based optimization, the first small molecule dual anti- infectives were discovered exhibiting antibacterial and antiretroviral activities on HIV-1 wild type and resistant strains. Second, optimization of novel natural antibiotics (the cystobactamids) that target DNA gyrase and topoisomerase IV: Pursuing an interactive de novo design, both target and antibacterial activities of cystobactamid 507 were enhanced. The new congeners display an outstanding metabolic stability. Moreover, the synthetic route was markedly improved. VIII Zusammenfassung Angesichts einer ständig wachsenden Resistenzentwicklung werden die therapeutischen Optionen zur Behandlung bakterieller Infektionen ständig schlechter. Deshalb sind neue Antibiotika gegen resistente Bakterien dringend notwendig. In dieser Doktorarbeit werden neue antibiotisch wirksame Scaffolds durch zwei Strategien entwickelt. Erstens Hemmstoffe der bakteriellen RNA Polymerase, die an die Switch Region binden: mittels Analog Design wurden Substanzen in sechs Klassen von Ureido-Heterocyclus- Carbonsäuren erhalten. Die Verbindungen zeigten eine starke antibakterielle Aktivität, keine Kreuzresistenz zu dem klinisch verwendeten Rifampicin, eine niedrigere Resistenz- Entwicklungsrate und eine nur geringfügige Toxizität gegenüber humanen Zellen. In einem weiteren Projekt wurde die Tatsache ausgenutzt, dass die NNRTI Bindestelle der HIV-1 Reversen Transkriptase strukturelle Ähnlichkeiten zur Switch Region hat. Geeignete, oben entwickelte Wirkstoffe wurden nun weiter strukturell optimiert und duale Hemmstoffe mit antibakterieller und antiretroviraler Aktivität an Wildtyp und resistenten Stämmen erhalten. Zweitens wurde eine Optimierung des natürlich vorkommenden Cystobactamids 507 hinsichtlich DNA Gyrase und Topoisomerase IV unternommen. Diese Ziele und eine Erhöhung der antibakteriellen Aktivität wurde durch interaktives de novo Design erreicht. Die neuen Derivate zeigten auch eine verbesserte metabolische Stabilität. Außerdem wurde der synthetische Zugang verbessert. IX Papers and Manuscripts Included in This Thesis This thesis is divided into three publications and one manuscript, which are referred to in the text by their numbers I–IV, respectively. I Expanding the Scaffold for Bacterial RNA Polymerase Inhibitors: Design, Synthesis and Structure–Activity Relationships of Ureido-Heterocyclic-Carboxylic Acids Walid A. M. Elgaher, Martina Fruth, Matthias Groh, Jörg Haupenthal and Rolf W. Hartmann RSC Adv., 2014, 4, 2177–2194. II Discovery and Structure-Based Optimization of 2-Ureidothiophene-3-Carboxylic Acids as Dual Bacterial RNA Polymerase and Viral Reverse Transcriptase Inhibitors Walid A. M. Elgaher, Kamal K. Sharma, Jörg Haupenthal, Francesco Saladini, Manuel Pires, Eleonore Real, Yves Mély, and Rolf W. Hartmann J. Med. Chem., 2016, 59, 7212–7222. III Synthesis and Biological Evaluation of Cystobactamid 507: A Bacterial Topoisomerase Inhibitor from Cystobacter sp. María Moreno, Walid A. M. Elgaher, Jennifer Herrmann, Nadin Schläger, Mostafa M. Hamed, Sascha Baumann, Rolf Müller, Rolf W. Hartmann, and Andreas Kirschning Synlett, 2015, 26, 1175–1178. IV Cystobactamid 507: Concise Synthesis and Design of Non-Covalently Bonded Rigid Analogs Boost Bacterial Topoisomerases IIA Inhibition, Antibacterial Activity and Disclose the Bioactive Conformation (Manuscript in Submission). X Contribution Report The author would like to declare his contributions to the papers/manuscript I–IV included in this thesis. I The author designed, synthesized and characterized most of the compounds. He performed all the molecular modelling studies (similarity analysis, flexible alignment and molecular docking). Furthermore, he performed the minimum inhibitory concentration (MIC) assays of selected compounds, and studied the role of cell wall and efflux pumps for the uptake of the compounds into the Gram-negative E. coli. In addition, he interpreted the results of the biological experiments, and he conceived and wrote the manuscript. II The author designed, synthesized and characterized most of the compounds. He performed all the molecular modelling studies (molecular docking, similarity analysis, and quantitative structure–activity relationship (QSAR) model). Furthermore, he interpreted the results of the biological experiments, and he conceived and
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