AMINOGLYCOSIDE ANTIBIOTICS
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1 AMINOGLYCOSIDE ANTIBIOTICS
2
3 AMINOGLYCOSIDE ANTIBIOTICS From Chemical Biology to Drug Discovery DEV P. ARYA Clemson University WILEY-INTERSCIENCE A John Wiley & Sons, Inc., Publication
4 Copyright 2007 by John Wiley & Sons, Inc. All rights reserved. Published by John Wiley & Sons, Inc., Hoboken, New Jersey. Published simultaneously in Canada. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, (978) , fax (978) , or on the web at Requests to the Publisher for permission should be addressed to the Permissions Department, John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, (201) , fax (201) , or online at Limit of Liability/Disclaimer of Warranty: While the publisher and author have used their best efforts in preparing this book, they make no representations or warranties with respect to the accuracy or completeness of the contents of this book and specifically disclaim any implied warranties of merchantability or fitness for a particular purpose. No warranty may be created or extended by sales representatives or written sales materials. The advice and strategies contained herein may not be suitable for your situation. You should consult with a professional where appropriate. Neither the publisher nor author shall be liable for any loss of profit or any other commercial damages, including but not limited to special, incidental, consequential, or other damages. For general information on our other products and services or for technical support, please contact our Customer Care Department within the United States at (800) , outside the United States at (317) or fax (317) Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic formats. For more information about Wiley products, visit our web site at Wiley Bicentennial Logo: Richard J. Pacifico Library of Congress Cataloging-in-Publication Data: ISBN Printed in the United States of America
5 CONTENTS Preface Contributors vii ix 1. In the Beginning There Was Streptomycin 1 Julian Davies 2. The Biochemistry and Genetics of Aminoglycoside Producers 15 Wolfgang Piepersberg, Khaled M. Aboshanab, Heike Schmidt-Beißner, and Udo F. Wehmeier 3. Mechanisms of Aminoglycoside Antibiotic Resistance 119 Tushar Shakya and Gerard D. Wright 4. Design, Chemical Synthesis, and Antibacterial Activity of Kanamycin and Neomycin Class Aminoglycoside Antibiotics 141 Jinhua Wang and Cheng-Wei Tom Chang 5. NMR Structural Studies of Aminoglycoside: RNA Interaction 181 R. Andrew Marshall and Joseph D. Puglisi v
6 vi CONTENTS 6. Structural Comparisons Between Prokaryotic and Eukaryotic Ribosomal Decoding A Sites Free and Complexed with Aminoglycosides 209 Jiro Kondo and Eric Westhof 7. Binding of Antibiotics to the Aminoacyl-tRNA Site of Bacterial Ribosome 225 Dale Kling, Christine Chow, and Shahriar Mobashery 8. Metalloaminoglycosides: Chemistry and Biological Relevance 235 Nikhil Gokhale, Anjali Patwardhan, and J. A. Cowan 9. Adverse Effects of Aminoglycoside Therapy 255 Andra E. Talaska and Jochen Schacht 10. Targeting HIV-1 RNA with Aminoglycoside Antibiotics and Their Derivatives 267 Lev Elson-Schwab and Yitzhak Tor 11. Novel Targets for Aminoglycosides 289 Dev P. Arya, Nicholas Shaw, and Hongjuan Xi Index 315
7 PREFACE Since Selman Waksman s discovery of streptomycin in 1944, aminoglycosides have been at the forefront of antibacterial drug treatment. Advances in carbohydrate chemistry and biochemistry, coupled with other technological advances in nucleic acid synthesis, biochemistry and structure analysis have led to a substantial increase in aminoglycoside research among both chemists and biochemists. While by no means exhaustive, this endeavor attempts to chronicle the advances made in aminoglycoside-related work over the last two decades to assist new researchers in the field of aminoglycoside research while also offering a reference guide for the expert. Any omission of work is unintentional and due partly to the time constraints always present in such a venture. In the introduction, Dr. Davies narrative of aminoglycoside research provides us with an elegant historical perspective on aminoglycoside discovery and the mechanism of action over the past 50 years. Chapter 2 illustrates the progress made in the elucidation of the biosynthetic pathways for aminoglycoside synthesis. Piepersburg and coworkers have outlined the major pathways and their work should serve as an important reference guide for years to come. A major problem in aminoglycoside therapy has been drug resistance and in Chapter 3 are the findings of Shakya and Wright regarding their articulation of the major mechanisms of aminoglycoside resistance and the possible methods for overcoming these pathways. To get past the resistance mechanisms, chemistry and biology must come together and in Chapter 4, Wang and Chang summarize the synthetic advances made in aminoglycoside chemistry over the past decade and their uses in the development of improved antibiotics. A large interest among chemists and biochemists in aminoglycosides stems also from the fact that their molecular RNA target of therapeutic action has been identified. Chapters 5 7 provide a broad overview of the interaction of vii
8 viii PREFACE aminoglycoside with RNA focusing particularly on the A-site, their ribosomal target. In Chapter 5, Marshall and Puglisi first summarize the advances made in the NMR-based structural investigation of aminoglycosides with RNA, including the A-site. In Chapter 6, Kondo and Westhof detail the progress made in the crystallographic investigations of RNA aminoglycoside interactions and how that has been used to decipher the differences between eukaryotic and prokaryotic ribosomal drug targets. Kling, Chow and Mobashery summarize the different approaches regarding the further comprehension of this important nucleic-acid interaction. Together, these accounts should provide an excellent reference guide for students and established researchers interested in the field of aminoglycoside biochemistry, biophysics, chemical biology or medicinal chemistry. In Chapter 8, Cowan and coworkers review the state of the art on the metalmediated aminoglycoside research resulting in possible metallozymes that can be developed as novel drugs and tools for DNA and RNA cleavage. A major issue preventing the development of aminoglycoside therapies has to do with their toxicity. As the mechanisms causing these aminoglycoside toxicities (ototoxicity and nephrotoxicity) become clearer, molecular mechanisms to circumvent the propagation of these toxicities are being proposed. Talaska and Schacht discuss these proposed mechanisms and the possible role of iron-mediated free radical damage leading to oxidative stress. For other molecular mechanisms in the genetic basis of aminoglycoside ototoxicity, the reader is advised to consult the references at the end of Chapter 1. In Chapter 10, Elson-Schwab and Tor describe the use of aminoglycosides in other medicinally relevant RNA targets, specifically those involved in HIV therapy. The work elegantly illustrates how the congruence of chemistry and biology can lead to novel paradigms in drug development. Finally, Arya and coworkers summarize the recent work in some non-rna targets discovered for aminoglycoside-based recognition and how chemical manipulations can be used to tailor aminoglycoside specificities. Aminoglycoside research is now a legitimate aspect of scientific endeavor; with much knowledge, yet unknown, that we can learn. Aminoglycosides have brought together a number of different disciplines (and many more disciplines are expected to be positively affected by aminoglycoside research). It is my hope that this book will assist in both the continuing progress and expansion of aminoglycoside research into drug development, chemical biology, biophysics, microbiology, toxicology, molecular recognition and carbohydrate chemistry. I wish to thank all the authors for their wholehearted collaboration in this endeavor. Without them this book would not have been possible. Dev Priya Arya Clemson
9 CONTRIBUTORS Khaled M. Aboshanab, BU Wuppertal, Chemical Microbiology, D Wuppertal, Germany Dev P. Arya, Laboratory of Medicinal Chemistry, Department of Chemistry, Clemson University, Clemson, SC Cheng-Wei Tom Chang, Department of Chemistry and Biochemistry, Utah State University, Logan, UT Christine Chow, Department of Chemistry, Wayne State University, Detroit, MI J. A. Cowan, Department of Chemistry, Ohio State University, Columbus, OH Julian Davies, Department of Microbiology and Immunology, University of British Columbia 1 Life Sciences Institute, 2 Vancouver BC V6T 1Z3, Canada Lev Elson-Schwab, Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA Nikhil Gokhale, Department of Chemistry, Ohio State University, Columbus, OH Dale Kling, Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN Jiro Kondo, Institut de Biologie Moléculaire et Cellulaire, UPR9002 CNRS, Université Louis Pasteur, Strasbourg, France R. Andrew Marshall, Department of Chemistry, Stanford University, Stanford, CA Shahriar Mobashery, Department of Chemistry and Biochemistry, University of Notre Dame, Notre Dame, IN ix
10 x CONTRIBUTORS Anjali Patwardhan, Department of Chemistry, Ohio State University, Columbus, OH Wolfgang Piepersberg, BU Wuppertal, Chemical Microbiology, D Wuppertal, Germany Joseph D. Puglisi, Department of Structural Biology, Stanford University, Stanford, CA Jochen Schacht, Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, MI Heike Schmidt-Beißner, BU Wuppertal, Chemical Microbiology, D Wuppertal, Germany Tushar Shakya, Antimicrobial Research Centre, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada, L8N 3Z5 Nicholas Shaw, Laboratory of Medicinal Chemistry, Department of Chemistry, Clemson University, Clemson, SC Andra E. Talaska, Kresge Hearing Research Institute, Department of Otolaryngology, University of Michigan, Ann Arbor, MI Yitzhak Tor, Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, CA Jinhua Wang, Department of Chemistry and Biochemistry, Utah State University, Logan, UT Udo F. Wehmeier, BU Wuppertal, Chemical Microbiology, D Wuppertal, Germany Eric Westhof, Institut de Biologie Moléculaire et Cellulaire, UPR9002 CNRS, Université Louis Pasteur, Strasbourg, France Gerard D. Wright, Antimicrobial Research Centre, Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada, L8N 3Z5 Hongjuan Xi, Laboratory of Medicinal Chemistry, Department of Chemistry, Clemson University, Clemson, SC
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