Parvoviruses This page intentionally left blank Parvoviruses Edited by Jonathan R. Kerr MD, PhD, FRCPath Sir Joseph Hotung Senior Lecturer in Inflammation, Dept of Cellular & Molecular Medicine, St George’s University of London, London, UK Susan F. Cotmore PhD Senior Research Scientist, Department of Laboratory Medicine, Yale University School of Medicine, New Haven, USA Marshall E. Bloom MD Associate Director for Rocky Mountain Laboratories, National Institute of Allergy and Infectious Disease, National Institutes of Health, Hamilton, USA R. Michael Linden PhD Associate Professor, Department of Gene and Cell Medicine, and Department of Microbiology, Mount Sinai School of Medicine, New York, USA Colin R. Parrish PhD Professor of Virology, J.A. Baker Institute, College of Veterinary Medicine, Cornell University, Ithaca, USA Hodder Arnold AMEMBER OF THE HODDER HEADLINE GROUP First published in Great Britain in 2006 by Hodder Arnold, an imprint of Hodder Education and a member of the Hodder Headline Group 338 Euston Road, London NW1 3BH http://www.hoddereducation.com Distributed in the United States of America by Oxford University Press Inc. 198 Madison Avenue, New York, NY10016 Oxford is a registered trademark of Oxford University Press ©2006 Edward Arnold (Publishers) Ltd All rights reserved. Apart from any use permitted under UK copyright law, this publication may only be reproduced, stored or transmitted, in any form, or by any means with prior permission in writing of the publishers or in the case of reprographic production in accordance with the terms of licences issued by the Copyright Licensing Agency. 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Please visit our website at www.hoddereducation.com Dedication Jacov Tal (1940–2005):An Appreciation As this book is being readied for press we have received the laboratory at NIH in Bethesda and contributed to some of news of the sudden and untimely passing in February of the initial studies on the trans-regulation ofAAV transcrip- our friend and colleague Jacov Tal.It was a profound shock tion by the AAV rep gene. for us all to hear of the dreadful circumstances of Jacov’s In addition to his accomplishments as a scientist, the illness, made even more so because he was in such good enduring memory and impact of Jacov as a friend, col- health and fine spirit at the Xth Parvovirus Workshop in league,collaborator,and mentor to his students,is his love Florida last September 2004. of interaction with others, his extraordinary positive Jacov was a long-time member and contributor,and a impact upon them,his perpetual questions,his great sense very integral part of,the world wide parvovirus commu- of humor and his wonderful story-telling.This emanated nity from the time when this was quite a small group.He from an inner philosophy that he had about life,that we are will be greatly missed but very fondly remembered.We all all here to achieve useful things and that we can best do this have wonderful memories ofJacov,and many will remem- by constantly asking questions and seeking the answers ber the parvovirus workshop that he organized in Israel in together. Based upon these beliefs, Jacov had a highly 1989.I personally have many wonderful memories ofhim developed sense ofcommunity and fairness,so that he held as a scientist and friend,and particularly the two years he strong but well-reasoned opinions that he never failed to spent with us at NIH. express. Nevertheless, his opinions were always presented Jacov’s initial training in Israel was in biochemistry,first as an undergraduate at The Hebrew University in Jerusalem and then as a graduate student at the Weitzman Institute in Uri Littauer’s lab.However,following his stud- ies on tRNA with Littauer and obtaining his PhD in Biochemistry in 1971,he set out on a career as a virologist and worked on several classes ofviruses,although he ulti- mately spent most of his career devoted to parvoviruses. He first studied adenovirus RNA transcription as a postdoc with Heschal Raskas in St Louis.He then went to the labo- ratory of Michael Bishop and Harold Varmus at The University of California, San Francisco, to study retro- viruses where he analyzed the structures of avian tumor viruses genes and their cellular counterparts. Jacov then returned to Israel to the fledgling Ben Gurion University of the Negev in Beer Sheva and established studies in virology and retained a faculty position there for the rest of his career as Head ofVirology. Upon his return to Israel, Jacov took up the study of parvoviruses and initially was interested in MVM and its transcription in studies he did with the late Yossi Aloni.He also began to study the biology of MVM and its host cell tropism and,in many ofthese studies over the years,he col- laborated with Peter Tattersall at Yale or Jean Rommelaere in Europe.In the mid-1980s he spent a 2-year period in my vi Dedication in a most constructive way and we are all individually and The CCU was housed in Harvard Hospital,which was a collectively the better for hearing them. gift from the USA to the UK in time ofwar.It was built in The photo accompanying these comments beautifully 1940 from pre-fabricated materials shipped from the USA, captures the essence ofJacov,the man,and the occasion of and was equipped and staffed by Harvard University in the publication ofthis book is a wonderful opportunity to Boston and the American Red Cross.Harvard Hospital was memorialize him.So,although we feel a profound sadness designed and run as an infectious disease hospital, and at Jacov’s passing,we also celebrate his life and the wonder- after the war ended,it was given to the MRC and became ful community that he created around him. the CCU in 1946.The creation and the continuation ofthe CCU was due critically to the support at the MRC of Sir Barrie Carter,March 2005 Christopher Andrewes,an influenza virus researcher,who had greatly inspired David. Under his direction,the CCU began to uncover the spe- David A.J.Tyrrell (1925–2005) cific viral causes ofthe common cold,its global epidemiol- ogy,some possible treatments and the important role played David Tyrrell began his research into the common cold by emotional stress in the genesis of symptomatic infec- shortly after the end of the Second World War at a time tion.The involved the use ofhuman volunteers (a total of when knowledge ofits causes was inaccurate and conflict- 20000),many ofwhom visited the unit on an annual basis ing,and went on to reveal virtually all ofits mysteries:that in return for a 10 day holiday on Harnham Hill, a small it was caused by several hundred viruses which were trans- stipend and a dose ofcold virus,delivered intranasally. mitted by aerosol droplets, and how the viruses actually An important dimension ofthe work was David’s skill in cause disease; interactions with other diseases; and the motivating and bringing people together towards a common effect ofcertain predisposing factors.He also tested several goal, and this applied at local, national and international candidate treatments,but as more and more ‘cold viruses’ levels in the initiation and maintenance of collaborations were revealed, it became clear why no single treatment with the World Health Organization (WHO), National could be expected to work consistently. Institutes of Health (NIH) and others which led to an David Arthur John Tyrrell was born on 19 June 1925 and international network offriends and collaborators. graduated with distinction in Medicine at the University of In the early 1960s,David was involved in planning the Sheffield in 1948 and upon the encouragement of Clinical Research Centre which was closely integrated with Professor (later Sir) Charles Stuart-Harris, became inter- Northwick Park Hospital in Harrow in north-west London ested in the novel area ofvirus research,and joined a group and opened in stages between 1970 and 1975.As Head ofthe studying influenza viruses.In 1951,he began a three-year Division ofCommunicable Diseases and Deputy Director, attachment to the Rockefeller Institute for Medical Research he was later involved in developing and running the gen- in New York, working with Frank Horsfall on influenza eral medical and infectious disease services ofthe CRC. viruses, and returned to Sheffield University in 1954. In He was elected FRS in 1970 and appointed CBE in 1980. 1957,he was invited to run the MRC Common Cold Unit In the early 1980s,he hosted the seminal studies ofparvovirus (CCU) in Salisbury, by Sir Harold Himsworth, then B19 infection in human volunteers, a collaboration with Secretary ofthe MRC.He accepted and took up the post on Professor (later Sir) John Pattison,which provided some firm 1 April 1957. Figure 1 David checking cell cultures using a light microscope in the virus laboratory. Figure 2 Aerial view of the Common Cold Unit, Salisbury, Wiltshire. Dedication vii foundations in our knowledge of the way this virus causes success,never lost the common touch.In his undertakings, disease,and upon which much further work was based. the best interests of people was always foremost in his David retired from the CCU in 1990 but continued to motivation; patients,colleagues,friends,family and com- contribute in new ways.He chaired the government’s BSE munity at all levels. committee (1989–1995) and the Taskforce on Chronic David was also a devoted husband and father to three Fatigue Syndrome (CFS)/myalgic encephalomyelitis (ME) children; he enjoyed gardening and read very widely. He (1994). From 1994, he served as Vice-Chairman of the lived a Christian faith,and was the President of both the Research Committee ofthe CFSResearch Foundation and Christian Medical Fellowship and the Friends of the became its Chairman in 2000. During this time, he was Christian Medical College at Ludhiana,India.He was also involved in studies outlining the role ofparvovirus B19 as the organist and choirmaster at All Saints Church, a trigger for CFS and in setting up a program ofresearch in Whiteparish,Wiltshire. to the ongoing physical causes of CFS using gene expres- He is survived by his wife,Moyra,and two daughters, sion and proteomics.This work continues today,with the Frances and Sue. ultimate aim of developing a diagnostic test and effective treatments for CFS sufferers. Jonathan Kerr,June 2005 David was a refined and elusive man who was sparkling with ideas,a wonderful sense ofhumor and who,despite his This page intentionally left blank Contents Contributors xiii Foreword xvii Introduction xix Acknowledgments xxiii Abbreviations xxv The color plate section appears between pages 164 and 165. PART 1 BIOLOGY OF THE VIRUS FAMILY 01 Section A Virus groups and evolution of the family 03 1 The evolution of parvovirus taxonomy 05 Peter Tattersall 2 The genus Dependovirus 15 Dawn E. Bowles, Joseph E. Rabinowitz, and R. Jude Samulski 3 The genus Erythrovirus 25 Kevin E. Brown 4 Autonomous parvovirus variation and evolution 47 Colin R. Parrish 5 Evolution of densoviruses 55 P. Tijssen, H. Bando, Y. Li, F.-X. Jousset, Z. Zádori, G. Fédière, M. El-Far, J. Szelei, and M. Bergoin Section B The rugged virion 69 6 Introduction 71 Susan F. Cotmore and Peter Tattersall 7 Structure and organization of the viral genome 73 Susan F. Cotmore and Peter Tattersall 8 Phospholipase A domains in structural proteins of parvoviruses 95 2 P. Tijssen, J. Szelei, and Z. Zádori 9 Atomic structure of viral particles 107 Michael S. Chapman and Mavis Agbandje-McKenna 10 Correlating structure with function in the viral capsid 125 Mavis Agbandje-McKenna and Michael S. Chapman Section C Viral life cycles: molecular interactions between virus and host cell 141 11 The parvovirus life cycle: an introduction to molecular interactions important for infection 143 Matthew D. Weitzman 12 Cell infection processes of autonomous parvoviruses 157 Maija Vihinen-Ranta and Colin R. Parrish 13 Looking down the rabbit hole: understanding the binding, entry, and trafficking patterns of AAV particles in the cell 165 John A. Chiorini
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