Photosensitisers in Biomedicine
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1 Photosensitisers in Biomedicine Mark Wainwright School of Pharmacy and Chemistry, Liverpool John Moores University, UK AJohn Wiley & Sons, Ltd., Publication
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3 Photosensitisers in Biomedicine
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5 Photosensitisers in Biomedicine Mark Wainwright School of Pharmacy and Chemistry, Liverpool John Moores University, UK AJohn Wiley & Sons, Ltd., Publication
6 This edition first published 2009 Ó 2009 John Wiley & Sons Ltd. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley s global Scientific, Technical and Medical business with Blackwell Publishing. Registered office John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK Other Editorial Offices 9600 Garsington Road, Oxford, OX4 2DQ, UK 111 River Street, Hoboken, NJ , USA For details of our global editorial offices, for customer services and for information about how to apply for permission to reuse the copyright material in this book please see our website at The right of the author to be identified as the author of this work has been asserted in accordance with the Copyright, Designs and Patents Act All rights reserved. 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 or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The publisher is not associated with any product or vendor mentioned in this book. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold on the understanding that the publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional should be sought. Library of Congress Cataloging-in-Publication Data Wainwright, Mark. Photosensitisers in biomedicine / authored by Mark Wainwright. p. ; cm. Includes bibliographical references and index. ISBN (cloth) 1. Photosensitizing compounds. 2. Photochemotherapy. I. Title. [DNLM: 1. Photosensitizing Agents chemistry. 2. Photosensitizing Agents therapeutic use. 3. Photochemotherapy. QV 240 W142p 2009] RM666.P73W dc A catalogue record for this book is available from the British Library. ISBN Set in 10.5/12.5pt Times by Integra Software Services Pvt. Ltd, Pondicherry, India. Printed in Great Britain by Antony Rowe Ltd, Chippenham, Wiltshire. First [Impression] 2009
7 To Bernadette, Michael, Lauren and Kate. There can be no richer man than a husband and father.
8
9 Contents Author s introduction xi PART I Introduction 1 1 Light Electromagnetic radiation in everyday life Radiation and tissue Light, electrons and molecules Photoreaction Dental/plastics curing Photoaging/photofading/photobleaching 12 References 12 2 Dyes and stains Dye use Textile dyeing and biological staining Biological stains and biomedical photosensitisers The human factor Dyes and drug development Dyes and stains and photosensitiser design 25 References 25 3 Photosensitisers and photosensitisation Photosensitiser action The photodynamic effect and cell death Photosensitising drug discovery Fitness for purpose Organic versus inorganic photosensitisers 40 References 41 PART II Chemistry of photosensitisers 43 4 Azines Acridines Acridine synthesis 50
10 viii CONTENTS 4.3 Rationale Acridines in photodynamic therapy Phenanthridines Phenaziniums Phenoxaziniums Phenothiazinium derivatives Reduction oxidation activity Hydrophilicity lipophilicity Molecular planarity Benzannelated derivatives Synthetic approaches 69 References 74 5 Triarylmethanes and xanthenes Triarylmethanes Victoria blue series Structure and photoproperties in triarylmethanes extending the long-wavelength absorption Synthesis Xanthene derivatives Biological uses Rhodamines Rosamines Pyrylium compounds Pyronines 107 References Porphyrins Central metals Meso compounds Amino derivatives Hetero-porphyrins Chlorins Benzoporphyrin derivative Temoporfin Tookad Purpurins Texaphyrins Porphycenes Aminolaevulinic acid Esters 139 References 141
11 CONTENTS ix 7 Phthalocyanines General features Phthalocyanine synthesis Photosens Naphthalocyanines Hetero-fused systems Silicon derivatives Photoantimicrobial activity 162 References Cyanines Synthesis Merocyanine N,N -Bis(2-ethyl-1,3-dioxolane)kryptocyanine Indocyanine green Structural improvement Squaric and croconic acid derivatives Functional cyanines 186 References Natural product photosensitisers Condensed aromatic pigments: perylene- and phenanthroperylenequinones Hypericin-type photosensitisers Hypocrellins Anthraquinones Psoralens (furocoumarins) Isoquinoline alkaloid photosensitisers Riboflavin Terthiophenes 207 References 208 PART III Applications Photodynamic therapy in oncology Photosensitisers for use in photodynamic therapy Indications for photodynamic therapy Skin Head and neck Gastrointestinal tract Breast Lung Genitourinary tract and prostate 223
12 x CONTENTS 10.9 Brain Haematological disease (leukaemia and lymphoma) Targeting/formulation Liposomes Biomolecular conjugation Dendrimers Nanoparticles Magnetic targeting Light in photodynamic therapy 231 References Antimicrobial application photodynamic antimicrobial chemotherapy Antimicrobial and photoantimicrobial action Applications Blood Thionin/light þ low-dose UVB for the decontamination of platelet concentrates The cellular problem A role for photodynamic antimicrobial chemotherapy in tropical medicine? 252 References Non-oncological applications Age-related macular degeneration Atherosclerosis Endometreosis Port wine stain Arthritis and autoimmune disorders Photodynamic diagnosis Photocytotoxics and photochemical internalisation 264 References 266 Index 269
13 Author s introduction Introduction I am often puzzled that authors wait until the end of a piece of work to thank those involved or those who inspired or supported the work. This may only be tradition, but it does, occasionally, seem like an afterthought. I shall therefore thank and send my best wishes to all those who have supported and inspired my work at the outset of this piece. Research is often a long drawn-out process requiring considerable help, understanding and forbearance from family and colleagues, often with little tangible reward. At least you can find my gratitude here without having to wade through the introduction! Photodynamic therapy (PDT) has been a clinical reality, with many thankful recipients, for around 25 years at the time of writing. Cancer is a terrible and terrifying disease, and its therapy is often quite as frightening in terms of side effects. In many cases, the application of a photosensitising drug and subsequent illumination of the tumour site has been sufficient to remove the malignant tissue without scarring or disfigurement either to the body or to the psyche and this is a major and continuing strength of the approach. The reliance of cancer PDT on porphyrins and porphyrin-based photosensitisers is a constant theme in my writing on the subject area. This is not a personal bias, and I hope that the many photodynamicists who have quite happily never gone beyond working with haematoporphyrin derivative, in whichever form, do not see my views as such. Rather, I am interested in the exploration of new avenues regarding photosensitiser development, as this is, in my own view again, the best way to make progress in drug discovery. Indeed, many who concentrate on porphyrin photosensitisers are not involved in drug discovery or development, but in optimising the use of clinically accepted compounds. In my own research since 1990, I have consciously stayed away from porphyrins as there have always been many others involved already. The antimicrobial application of photosensitisers, i.e. to infection control, is usually seen as a development of cancer PDT. Again, in writing on this subject I am usually at pains to point out that Oskar Raab s photodestruction of unicellular organisms pre-dates the first anticancer reports, but it is an inescapable fact that anticancer PDT was first to be clinically accepted. Photoantimicrobial agents are only now, in the early twenty-first century, taking their first proper clinical steps, although it is to be hoped that photodynamic antimicrobial chemotherapy (PACT) achieves a rather quicker acceptance from clinicians than did PDT itself. Really the evolution of photosensitisers for use in PDT and PACT should mirror the conventional drug development pattern seen with beta-lactams, fluoroquinolones, etc.
14 xii AUTHOR S INTRODUCTION However, one of the reasons for the continuing reliance on porphyrins lies in the lack of funding for drug discovery: Given the small amount available, it makes sense to optimise proven methods and preparations. While this may be logical, it does not improve the chances for novelty, nor is it likely to provide great strides in photosensitiser application. Perhaps we should take heart from Howard Florey s struggles in funding penicillin development in the early 1940s! There is an additional drawback in photosensitiser development, of course: the drug - dye relationship. Neither the pharmacological industry nor the clinicians are enthusiastic about coloured therapeutics, and yet the use of biological stains- either for pathology or for in vivo use during surgery is quite acceptable. Consider the following two statements. Biological stains work by their selective uptake by target cells and the resulting difference in colour between these and non-target cells. Photosensitisers work by their selective uptake by target cells and the resulting difference in colour between these and non-target cells. Admittedly this is a simplistic view, but the difference between these two approaches is that we use light to view the former and light to alter the latter. Of course there is a danger of over-simplification here. A considerable difference exists between staining and fixing cells on a microscope slide and, for example, triggering apoptosis in tumour cells in an older patient s prostate or bacterial cell wall destruction in an MRSA-colonised wound. Here, as a systemic approach, there are considerations at least in pharmacology, pharmacokinetics and light delivery. However, in line with several PDT protocols, PACT is not proposed, in its current form at least, as a systemic approach. The local application of a photosensitiser followed by local, superficial illumination means that the aforementioned considerations do not apply. The evolution of clinical photosensitisers from dyestuffs rather than natural precursors is another problem besetting the unwary fund-seeking researcher. It is pointless to deny the link, but the fact remains that although some standard dyes are also photosensitisers (methylene blue for one), most photosensitisers intended for clinical use would be of no use in textile dyeing. In addition, the idea that the synthesis of photosensitisers employs bucket chemistry techniques is also misguided given the paucity of chemists among the various photodynamic research groups worldwide, a considerable amount of novel, elegant synthetic work has been published. Target molecules unattainable via new methodologies obviously require the old, dye chemistry routes, but even here product purity requirements result in differences in separation and isolation. All things being equal, the only significant difference between getting a photoantibacterial candidate and a conventional antibiotic to clinic trial should be the light activation requirement for the former. Photosensitisers must offer advantages over conventional therapy, in whichever field. Thus, within anticancer therapy, the benefits lie mainly in the lack of side effects and
15 AUTHOR S INTRODUCTION xiii excellent post-treatment cosmesis. For the antimicrobial application, the efficacy of cationic photosensitisers against conventional drug-resistant organisms is the obvious gain, particularly in view of the small number of new alternatives available from the pharmaceutical industry. In both the anticancer and the antimicrobial application, of course, the photosensitisers involved operate via multiple rather than singular sites within the target cell. This must be considered a strength, particularly from the point of view of potential resistance development. With both applications, however, the problem of systemic light delivery remains we cannot yet say that any malignant or microbial disease treatable by conventional chemotherapy can also be successfully treated with photosensitisers and light. The range of treatable tumours is increasing year on year and photoantimicrobials are in clinical trials or have been very recently licensed, but this does not represent front-line therapy. There are more rapid methods of progress, for example where no efficient or affordable therapeutics exist. Consequently, researchers involved in PACT may be less affected than more conventional workers by the ongoing fiscal crises of health providers and/or the continuing rise of the bacterial superbug! In writing this book, I am attempting the impossible: to cover all aspects of photosensitisers in some depth. Plainly, there will be omissions after over a century of research and more than 25 years of clinical PDT. However, the main intention is to encourage further efforts in the field particularly in chromophore diversification and so, hopefully, to aid in moving more of the research into the clinical arena. The book is intentionally different in area and approach to Raymond Bonnett s Chemical Aspects of Photodynamic Therapy of 2000, covering the full range of photosensitisers and all applications, rather than concentrating on porphyrins and phthalocyanines. In a world where the cost of launching a new therapeutic is often prohibitive, it is incumbent on those involved in drug discovery to produce the optimal derivative for use. In my opinion, this means investigating as many candidates as possible before making decisions. There are classes of photosensitiser that are mainly ignored by the majority involved in photosensitiser drug development. I hope this book will act as a reminder that there are many possible answers to our current questions in the antimicrobial and anticancer fields. Mark Wainwright Lea, Preston October 2008
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