Encyclopedia of virology 3rd ed b mahy, m van regenmortel (elsevier, 2008) 5 volumes 1

University of Oklahoma Health Sciences Center,Oklahoma City, OK, USA National Institute for Biotechnology and Genetic Engineering, Faisalabad, Pakistan H AttouiFaculte´ de Me´decine de M

Encyclopedia of VIROLOGY

THIRD EDITION

Encyclopedia of VIROLOGY

Linacre House, Jordan Hill, Oxford, OX2 8DP, UK

525 B Street, Suite 1900, San Diego, CA 92101-4495, USA

Copyrightã 2008 Elsevier Inc All rights reserved

The following articles are US government works in the public domain and are not subject to copyright:

Bovine Viral Diarrhea Virus, Coxsackieviruses, Prions of Yeast and Fungi, Human Respiratory Syncytial Virus,Fish Rhabdoviruses, Varicella-Zoster Virus: General Features, Viruses and Bioterrorism, Bean Common MosaicVirus and Bean Common Mosaic Necrosis Virus, Metaviruses, Crimean-Congo Hemorrhagic Fever Virus and OtherNairoviruses, AIDS: Global Epidemiology, Papaya Ringspot Virus, Transcriptional Regulation in Bacteriophage.Nepovirus, Canadian Crown Copyright 2008

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PRINTED AND BOUND IN SLOVENIA

08 09 10 11 10 9 8 7 6 5 4 3 2 1

Brian W J Mahy MA PhD ScD DSc

Senior Scientific Advisor,

Division of Emerging Infections and Surveillance Services,

Centers for Disease Control and Prevention,

Atlanta GA, USA

Marc H V Van Regenmortel PhD

Emeritus Director at the CNRS,

French National Center for Scientific Research,

Biotechnology School of the University of Strasbourg,

Illkirch, France

v

Dennis H Bamford, Ph.D.

Department of Biological and Environmental Sciences

and Institute of Biotechnology, Biocenter 2,

P.O Box 56 (Viikinkaari 5),

00014 University of Helsinki,

Finland

Charles Calisher, B.S., M.S., Ph.D

Arthropod-borne and Infectious Diseases Laboratory

Department of Microbiology, Immunology and Pathology

College of Veterinary Medicine and Biomedical Sciences

Colorado State University

ILTAB/Donald Danforth Plant Science Center

975 North Warson Road

Department of Pathology and Laboratory Medicine, and

Emory Vaccine Center

2205 Tech Dr

Evanston

IL 60208-3500USA

Olivier Le GallIPV, UMR GDPP, IBVM,INRA Bordeaux-Aquitaine, BP 81,F-33883 Villenave d’Ornon CedexFRANCE

Vincent Racaniello, Ph.D

Department of MicrobiologyColumbia UniversityNew York, NY 10032USA

David A Theilmann, Ph.D., B.Sc., M.ScPacific Agri-Food Research CentreAgriculture and Agri-Food CanadaBox 5000, 4200 Highway 97Summerland

BC V0H 1Z0Canada

Peter J Walker, B.Sc., Ph.D

CSIRO Livestock IndustriesAustralian Animal Health Laboratory (AAHL)Private Bag 24

GeelongVIC 3220Australia

vii

This third edition of the Encyclopedia of Virology is being published nine years after the second edition, a period which hasseen enormous growth both in our understanding of virology and in our recognition of the viruses themselves, many ofwhich were unknown when the second edition was prepared Considering viruses affecting human hosts alone, theworldwide epidemic of severe acute respiratory syndrome (SARS), caused by a previously unknown coronavirus, led tothe discovery of other human coronaviruses such as HKU1 and NL63 As many as seven chapters are devoted to theAIDS epidemic and to human immunodeficiency viruses In addition, the development of new molecular technologiesled to the discovery of viruses with no obvious disease associations, such as torque-teno virus (one of the most ubiquitousviruses in the human population), human bocavirus, human metapneumovirus, and three new human polyomaviruses.Other new developments of importance to human virology have included the introduction of a virulent strain of WestNile virus from Israel to North America in 1999 Since that time the virus has become established in mosquito, bird andhorse populations throughout the USA, the Caribbean and Mexico as well as the southern regions of Canada

As in the two previous editions, we have tried to include information about all known species of virus infectingbacteria, fungi, invertebrates, plants and vertebrates, as well as descriptions of related topics in virology such as antiviraldrug development, cell- and antibody-mediated immunity, vaccine development, electron microscopy and molecularmethods for virus characterization and identification Many chapters are devoted to the considerable economicimportance of virus diseases of cereals, legumes, vegetable crops, fruit trees and ornamentals, and new approaches tocontrol these diseases are reviewed

General issues such as the origin, evolution and phylogeny of viruses are also discussed as well as the history of thedifferent groups of viruses

To cover all these subjects and new developments, we have had to increase the size of the Encyclopedia from three to fivevolumes

Throughout this work we have relied upon the 8th Report of the International Committee on Taxonomy of Virusespublished in 2005, which lists more than 6000 viruses classified into some 2000 virus species distributed among morethan 390 different genera and families In recent years the criteria for placing viruses in different taxa have shifted awayfrom traditional serological methods and increasingly rely upon molecular techniques, particularly the nucleotidesequence of the virus genome This has changed many of the previous groupings of viruses, and is reflected in thisthird edition

Needless to say, a work of this magnitude has involved many expert scientists, who have given generously of their time

to bring it to fruition We extend our grateful thanks to all contributors and associate editors for their excellent andtimely contributions

Brian W J MahyMarc H V van Regenmortel

ix

Structure of the Encyclopedia

The major topics discussed in detail in the text are presented in alphabetical order (see the Alphabetical Contents listwhich appears in all five volumes)

Finding Specific Information

Information on specific viruses, virus diseases and other matters can be located by consulting the General Index at theend of Volume 5

Taxonomic Groups of Viruses

For locating detailed information on the major taxonomic groups of viruses, namely virus genera, families and orders, theTaxonomic Index in Volume 5 (page .) should be consulted

Further Reading sections

The articles do not feature bibliographic citations within the body of the article text itself The articles are intended to be

a first introduction to the topic, or a ‘refresher’, readable from beginning to end without referring the reader outside ofthe encyclopedia itself Bibliographic references to external literature are grouped at the end of each article in a FurtherReading section, containing review articles, ‘seminal’ primary articles and book chapters These point users to the nextlevel of information for any given topic

Cross referencing between articles

The ‘‘See also’’ section at the end of each article directs the reader to other entries on related topics For example Theentry Lassa, Junin, Machupo and Guanarito Viruses includes the following cross-references:

See also: Lymphocytic Choriomeningitis Virus: General Features

xi

University of Oklahoma Health Sciences Center,

Oklahoma City, OK, USA

National Institute for Biotechnology and Genetic

Engineering, Faisalabad, Pakistan

H AttouiFaculte´ de Me´decine de Marseilles,Etablissement Franc¸ais Du Sang, Marseilles, France

H AttouiUniversite´ de la Me´diterrane´e, Marseille, France

H AttouiInstitute for Animal Health, Pirbright, UK

L AurelianUniversity of Maryland School of Medicine, Baltimore,

MD, USA

L A BabiukUniversity of Alberta, Edmonton, AB, Canada

S BabiukNational Centre for Foreign Animal Disease, Winnipeg,

MB, Canada

A G BaderThe Scripps Research Institute, La Jolla, CA, USA

S C BakerLoyola University of Chicago, Maywood, IL, USA

T S BakerUniversity of California, San Diego, La Jolla, CA, USA

J K H BamfordUniversity of Jyva¨skyla¨, Jyva¨skyla¨, Finland

Y BaoNational Institutes of Health, Bethesda, MD, USA

M Bar-JosephThe Volcani Center, Bet Dagan, Israel

H BarkerScottish Crop Research Institute, Dundee, UK

A D T BarrettUniversity of Texas Medical Branch, Galveston, TX, USA

J W BarrettThe University of Western Ontario, London, ON,Canada

xiii

Veterinary Medical Research Institute, Hungarian

Academy of Sciences, Budapest, Hungary

Aaron Diamond AIDS Research Center, The Rockefeller

University, New York, NY, USA

B A BlacklawsUniversity of Cambridge, Cambridge, UK

C D BlairColorado State University, Fort Collins, CO, USA

S BlancINRA–CIRAD–AgroM, Montpellier, France

R BlawidInstitute of Plant Diseases and Plant Protection,Hannover, Germany

G W BlissardBoyce Thompson Institute at Cornell University, Ithaca,

NY, USA

S BlomqvistNational Public Health Institute (KTL), Helsinki, Finland

J F BolLeiden University, Leiden, The NetherlandsJ-R Bonami

CNRS, Montpellier, France

L BosWageningen University and Research Centre (WUR),Wageningen, The Netherlands

H R Bose Jr

University of Texas at Austin, Austin, TX, USA

H BourhyInstitut Pasteur, Paris, France

P R BowserCornell University, Ithaca, NY, USA

D B BoyleCSIRO Livestock Industries, Geelong, VIC,Australia

C BragardUniversite´ Catholique de Louvain, Leuven, Belgium

J N BraggUniversity of California, Berkeley, Berkeley, CA, USA

R W BriddonNational Institute for Biotechnology and GeneticEngineering, Faisalabad, Pakistan

M A BrintonGeorgia State University, Atlanta, GA, USA

P BrittonInstitute for Animal Health, Compton, UK

J K BrownThe University of Arizona, Tucson, AZ, USA

K S BrownUniversity of Manitoba, Winnipeg, MB, Canada

Northern Illinois University, DeKalb, IL, USA and Polish

Academy of Sciences, Poznan, Poland

S CasjensUniversity of Utah School of Medicine, Salt Lake City, UT,USA

R CattaneoMayo Clinic College of Medicine, Rochester, MN, USA

D CavanaghInstitute for Animal Health, Compton, UK

A ChahroudiUniversity of Pennsylvania School of Medicine,Philadelphia, PA, USA

S ChakrabortyJawaharlal Nehru University, New Delhi, India

T J ChambersSaint Louis University School of Medicine, St Louis, MO,USA

Y ChangUniversity of Pittsburgh Cancer Institute, Pittsburgh, PA,USA

J T ChangBaylor College of Medicine, Houston, TX, USA

D ChapmanInstitute for Animal Health, Pirbright, UK

D ChattopadhyayUniversity of Calcutta, Kolkata, India

M ChenUniversity of Arizona, Tucson, AZ, USA

J E CherwaUniversity of Arizona, Tucson, AZ, USA

V G ChincharUniversity of Mississippi Medical Center, Jackson, MS,USA

A V ChintakuntlawarUniversity of Oklahoma Health Sciences Center,Oklahoma City, OK, USA

W ChiuBaylor College of Medicine, Houston, TX, USA

J ChodoshUniversity of Oklahoma Health Sciences Center,Oklahoma City, OK, USA

I-R ChoiInternational Rice Research Institute, Los Ban˜os, ThePhilippines

P D ChristianNational Institute of Biological Standards and Control,South Mimms, UK

M G CiufoliniIstituto Superiore di Sanita`, Rome, Italy

Contributors xv

Johns Hopkins University Schools of Public Health and

Medicine, Baltimore, MD, USA

R J Clem

Kansas State University, Manhattan, KS, USA

C J Clements

The Macfarlane Burnet Institute for Medical Research and

Public Health Ltd., Melbourne, VIC, Australia

University of Wisconsin School of Medicine

and Public Health, Madison, WI, USA

L A DayThe Public Health Research Institute, Newark, NJ, USA

J C de la TorreThe Scripps Research Institute, La Jolla, CA, USA

X de LamballerieFaculte´ de Me´decine de Marseille, Marseilles, France

M de VegaUniversidad Auto´noma, Madrid, Spain

P DelfosseCentre de Recherche Public-Gabriel Lippmann, Belvaux,Luxembourg

B DelmasINRA, Jouy-en-Josas, France

M DengUniversity of California, Berkeley, CA, USA

J DeRisiUniversity of California, San Francisco,San Francisco, CA, USA

C DesbiezInstitut National de la Recherche Agronomique (INRA),Station de Pathologie Ve´ge´tale, Montfavet, France

R C DesrosiersNew England Primate Research Center, Southborough,

MA, USA

A K DharAdvanced BioNutrition Corp, Columbia, MD, USA

R G DietzgenThe University of Queensland, St Lucia, QLD, Australia

S P Dinesh-KumarYale University, New Haven, CT, USA

L K DixonInstitute for Animal Health, Pirbright, UK

C DogimontINRA, Montfavet, France

A DomanskaUniversity of Helsinki, Helsinki, Finland

L L DomierUSDA–ARS, Urbana, IL, USA

L L DomierUSDA-ARS, Urbana-Champaign, IL, USA

A DotzauerUniversity of Bremen, Bremen, Germany

T W DreherOregon State University, Corvallis, OR, USA

S DreschersUniversity of Duisburg–Essen, Essen, Germany

Instituto de Microbiologı´a Bioquı´mica CSIC/University de

Salamanca, Salamanca, Spain

R EstebanInstituto de Microbiologı´a Bioquı´mica CSIC/University ofSalamanca, Salamanca, Spain

J L Van EttenUniversity of Nebraska–Lincoln, Lincoln, NE, USA

D J EvansUniversity of Warwick, Coventry, UK

Ø EvensenNorwegian School of Veterinary Science, Oslo,Norway

D FalzaranoUniversity of Manitoba, Winnipeg, MB, Canada

B A FaneUniversity of Arizona, Tucson, AZ, USAR-X Fang

Chinese Academy of Sciences, Beijing, People’sRepublic of China

D FargetteIRD, Montpellier, France

A Fath-GoodinUniversity of Kentucky, Lexington, KY, USA

C M FauquetDanforth Plant Science Center, St Louis, MO, USA

B A FedericiUniversity of California, Riverside, CA, USA

H FeldmannNational Microbiology Laboratory, Public Health Agency

of Canada, Winnipeg, MB, Canada

H FeldmannPublic Health Agency of Canada, Winnipeg, MB,Canada

F FennerAustralian National University, Canberra, ACT, Australia

S A FerreiraUniversity of Hawaii at Manoa, Honolulu, HI, USA

H J FieldUniversity of Cambridge, Cambridge, UK

K FischerUniversity of California, San Francisco,San Francisco, CA, USA

J A FishmanMassachusetts General Hospital, Boston, MA, USA

B FleckensteinUniversity of Erlangen – Nu¨rnberg, Erlangen, Germany

R FloresInstituto de Biologı´a Molecular y Celular de Plantas(UPV-CSIC), Valencia, Spain

Contributors xvii

Instituto de Microbiologı´a Bioquı´mica CSIC/University of

Salamanca, Salamanca, Spain

National Emerging Infectious Diseases Laboratories,

Boston, MA, USA

MD, USA

M GlasaSlovak Academy of Sciences, Bratislava, Slovakia

Y GlebaIcon Genetics GmbH, Weinbergweg, Germany

U A GompelsUniversity of London, London, UK

D GonsalvesUSDA, Pacific Basin Agricultural Research Center, Hilo,

HI, USA

M M GoodinUniversity of Kentucky, Lexington, KY, USA

T J D GoodwinUniversity of Otago, Dunedin, New Zealand

A E GorbalenyaLeiden University Medical Center, Leiden, TheNetherlands

E A GouldUniversity of Reading, Reading, UK

A GrakouiEmory University School of Medicine, Atlanta, GA, USAM-A Grandbastien

INRA, Versailles, France

R GrassmannUniversity of Erlangen – Nu¨rnberg, Erlangen, Germany

M GravellNational Institutes of Health, Bethesda, MD, USA

M V GravesUniversity of Massachusetts–Lowell, Lowell, MA, USA

K Y GreenNational Institutes of Health, Bethesda, MD, USA

H B GreenbergStanford University School of Medicine andVeterans Affairs Palo Alto Health Care System, Palo Alto,

CA, USA

B M GreenbergJohns Hopkins School of Medicine, Baltimore, MD, USA

I Greiser-WilkeSchool of Veterinary Medicine, Hanover, Germany

D E GriffinJohns Hopkins Bloomberg School of Public Health,Baltimore, MD, USA

T S GritsunUniversity of Reading, Reading, UK

R J de GrootUtrecht University, Utrecht, The Netherlands

Johns Hopkins University Schools of Public Health and

Medicine, Baltimore, MD, USA

D Hariri

INRA – De´partement Sante´ des Plantes et

Environnement, Versailles, France

Aaron Diamond AIDS Research Center, The Rockefeller

University, New York, NY, USA

F van HeuverswynUniversity of Montpellier 1, Montpellier, France

J HilliardGeorgia State University, Atlanta, GA, USA

B I HillmanRutgers University, New Brunswick, NJ, USA

S HiltonUniversity of Warwick, Warwick, UK

D M HintonNational Institutes of Health, Bethesda, MD, USA

A HinzUMR 5233 UJF-EMBL-CNRS, Grenoble, France

A E HoetThe Ohio State University, Columbus, OH, USA

S A HogenhoutThe John Innes Centre, Norwich, UK

T HohnBasel university, Institute of Botany, Basel,Switzerland

J S HongSeoul Women’s University, Seoul, South Korea

M C HorzinekUtrecht University, Utrecht, The Netherlands

T HoviNational Public Health Institute (KTL), Helsinki, Finland

A M HugerInstitute for Biological Control, Darmstadt, Germany

L E HughesUniversity of St Andrews, St Andrews, UK

R HullJohn Innes Centre, Colney, UK

E HunterEmory University Vaccine Center, Atlanta, GA, USA

A D HyattAustralian Animal Health Laboratory, Geelong, VIC,Australia

T Hyypia¨

University of Turku, Turku, Finland

T IwanamiNational Institute of Fruit Tree Science, Tsukuba, Japan

A O JacksonUniversity of California, Berkeley, CA, USA

P JardineUniversity of Minnesota, Minneapolis, MN, USA

J A JehleDLR Rheinpfalz, Neustadt, Germany

Contributors xix

Murdoch Childrens Research Institute Royal Children’s

Hospital, Melbourne, VIC, Australia

University of Pennsylvania School of Medicine,

Philadelphia, PA, USA

R G KleespiesInstitute for Biological Control, Darmstadt, Germany

D F KlessigBoyce Thompson Institute for Plant Research, Ithaca, NY,USA

W B KlimstraLouisiana State University Health Sciences Center atShreveport, Shreveport, LA, USA

V KlimyukIcon Genetics GmbH, Weinbergweg, Germany

N KnowlesInstitute for Animal Health, Pirbright, UK

R KoenigBiologische Bundesanstalt fu¨r Land- und Forstwirtschaft,Brunswick, Germany

R KoenigInstitut fu¨r Pflanzenvirologie, Mikrobiologie undbiologische Sicherheit, Brunswick, Germany

G Konate´

INERA, Ouagadougou, Burkina Faso

C N KottonMassachusetts General Hospital, Boston, MA, USA

L D KramerWadsworth Center, New York State Department ofHealth, Albany, NY, USA

P J KrellUniversity of Guelph, Guelph, ON, Canada

J KreuzeInternational Potato Center (CIP), Lima, Peru

M J KuehnertCenters for Disease Control and Prevention, Atlanta, GA,USA

R J KuhnPurdue University, West Lafayette, IN, USA

G KurathWestern Fisheries Research Center, Seattle, WA, USA

I Kusterssanofi pasteur, Lyon, France

I V KuzminCenters for Disease Control and Prevention, Atlanta,

GA, USA

M E LairdNew England Primate Research Center, Southborough,

MA, USA

R A LambHoward Hughes Medical Institute at NorthwesternUniversity, Evanston, IL, USA

P F LambertUniversity of Wisconsin School of Medicineand Public Health, Madison, WI, USA

A S Lang

Memorial University of Newfoundland, St John’s, NL,

Canada

H D Lapierre

INRA – De´partement Sante´ des Plantes et

Environnement, Versailles, France

Institut National de la Recherche Agronomique (INRA),

Station de Pathologie Ve´ge´tale, Montfavet, France

University of Medicine and Dentistry of New Jersey

(UMDNJ), Piscataway, NJ, USA

Western Australian Department of Health, Mount

Claremont, WA, Australia

R Ling

University of Warwick, Coventry, UK

M L LinialFred Hutchinson Cancer Research Center, Seattle, WA,USA

D C LiottaEmory University, Atlanta, GA, USA

W Ian LipkinColumbia University, New York, NY, USA

H L LiptonUniversity of Illinois at Chicago, Chicago, IL, USA

A S LissUniversity of Texas at Austin, Austin, TX, USA

J J Lo´pez-MoyaInstituto de Biologı´a Molecular de Barcelona (IBMB),CSIC, Barcelona, Spain

G LoebensteinAgricultural Research Organization, Bet Dagan, IsraelC-F Lo

National Taiwan University, Taipei, Republic of China

S A LommelNorth Carolina State University, Raleigh, NC, USA

G P LomonossoffJohn Innes Centre, Norwich, UK

M LuoUniversity of Alabama at Birmingham, Birmingham, AL,USA

S A MacFarlaneScottish Crop Research Institute, Dundee, UK

J S MackenzieCurtin University of Technology, Shenton Park, WA,Australia

R MahieuxPasteur Institute, CNRS URA 3015, Paris, France

B W J MahyCenters for Disease Control and Prevention, Atlanta, GA,USA

E MaissInstitute of Plant Diseases and Plant Protection,Hannover, Germany

E O MajorNational Institutes of Health, Bethesda, MD, USA

V G MalathiIndian Agricultural Research Institute, New Delhi,India

A MankertzRobert Koch-Institut, Berlin, Germany

S MansoorNational Institute for Biotechnology and GeneticEngineering, Faisalabad, Pakistan

Contributors xxi

W A O’BrienUniversity of Texas Medical Branch – Galveston,Galveston, TX, USA

D J O’CallaghanLouisiana State University Health Sciences Center,Shreveport, LA, USA

W F OchoaUniversity of California, San Diego, La Jolla, CA, USA

M R OdomUniversity of Alabama at Birmingham, Birmingham, AL,USA

M M van OersWageningen University, Wageningen, The Netherlands

M B A OldstoneThe Scripps Research Institute, La Jolla, CA, USA

G OlingerUSAMRIID, Fort Detrick, MD, USA

K E OlsonColorado State University, Fort Collins, CO, USA

A OlspertTallinn University of Technology, Tallinn, Estonia

G OrthInstitut Pasteur, Paris, France

J E OsorioUniversity of Wisconsin, Madison, WI, USA

N OsterriederCornell University, Ithaca, NY, USA

S A OvermanUniversity of Missouri – Kansas City, Kansas City,

MO, USA

R A OwensBeltsville Agricultural Research Center, Beltsville, MD,USA

M S PadmanabhanYale University, New Haven, CT, USA

S PaesslerUniversity of Texas Medical Branch, Galveston, TX, USA

P PaleseMount Sinai School of Medicine, New York, NY, USA

M A PallanschCenters for Disease Control and Prevention, Atlanta, GA,USA

M PalmariniUniversity of Glasgow Veterinary School, Glasgow, UK

P PalukaitisScottish Crop Research Institute, Invergowrie, Dundee, UK

Virginia Polytechnic Institute and State University,

Blacksburg, VA, USA

H MeyerBundeswehr Institute of Microbiology, Munich, Germany

R F MeyerCenters for Disease Control and Prevention, Atlanta, GA,USA

P de MiccoEtablissement Franc¸ais du Sang Alpes-Me´diterrane´e,Marseilles, France

B R MillerCenters for Disease Control and Prevention (CDC), FortCollins, CO, USA

C J MillerUniversity of California, Davis, Davis, CA, USA

R G MilneIstituto di Virologia Vegetale CNR, Torino, Italy

P D MinorNIBSC, Potters Bar, UK

S MjaalandNorwegian School of Veterinary Science, Oslo, Norway

E S MocarskiEmory University School of Medicine, Atlanta, GA, USA

E S Mocarski, Jr

Emory University School of Medicine, Emory, GA, USA

V MoennigSchool of Veterinary Medicine, Hanover, Germany

P MoffettBoyce Thompson Institute for Plant Research, Ithaca, NY,USA

T P MonathKleiner Perkins Caufield and Byers, Menlo Park, CA, USA

R C MontelaroUniversity of Pittsburgh School of Medicine, Pittsburgh,

PA, USA

P S MooreUniversity of Pittsburgh Cancer Institute, Pittsburgh,

PA, USA

F J MoralesInternational Center for Tropical Agriculture, Cali,Colombia

H MoriyamaTokyo University of Agriculture and Technology, Fuchu,Japan

T J MorrisUniversity of Nebraska, Lincoln, NE, USA

S A MorseCenters for Disease Control and Prevention, Atlanta, GA,USA

xxii Contributors

A M PowersCenters for Disease Control and Prevention, Fort Collins,

CO, USA

D PrangishviliInstitut Pasteur, Paris, France

C M PrestonMedical Research Council Virology Unit, Glasgow, UK

S L QuackenbushColorado State University, Fort Collins, CO, USA

F QuUniversity of Nebraska, Lincoln, NE, USA

B C RamirezCNRS, Paris, France

A RaposeUniversity of Texas Medical Branch – Galveston,Galveston, TX, USA

D V R ReddyHyderabad, India

A J RedwoodThe University of Western Australia,Crawley, WA, Australia

M RegnerAustralian National University, Canberra, ACT, Australia

W K ReisenUniversity of California, Davis, CA, USA

T RenaultIFREMER, La Tremblade, France

P A RevillVictorian Infectious Diseases Reference Laboratory,Melbourne, VIC, Australia

A RezaianUniversity of Adelaide, Adelaide, SA, Australia

J F RidpathUSDA, Ames, IA, USA

B K RimaThe Queen’s University of Belfast, Belfast, UK

E RimstadNorwegian School of Veterinary Science, Oslo,Norway

F J RixonMRC Virology Unit, Glasgow, UKY-T Ro

Konkuk University, Seoul, South Korea

C M RobinsonUniversity of Oklahoma Health Sciences Center,Oklahoma City, OK, USA

Louisiana State University Health Sciences Center at

Shreveport, Shreveport, LA, USA

K D Ryman

Louisiana State University Health Sciences Center,

Shreveport, LA, USA

C E SampleThe Pennsylvania State University College of Medicine,Hershey, PA, USA

R M Sandri-GoldinUniversity of California, Irvine, Irvine, CA, USA

H Sanfac¸onPacific Agri-Food Research Centre, Summerland, BC,Canada

R Sanjua´nInstituto de Biologı´a Molecular y Cellular de Plantas,CSIC-UPV, Valencia, Spain

N SantiNorwegian School of Veterinary Science, Oslo, Norway

C SarmientoTallinn University of Technology, Tallinn, Estonia

T SasayaNational Agricultural Research Center, Ibaraki, Japan

Q J SattentauUniversity of Oxford, Oxford, UK

C Savolainen-KopraNational Public Health Institute (KTL), Helsinki, Finland

B SchaffhausenTufts University School of Medicine, Boston, MA, USA

K ScheetsOklahoma State University, Stillwater, OK, USA

M J SchmittUniversity of the Saarland, Saarbru¨cken, Germany

A SchneemannThe Scripps Research Institute, La Jolla, CA, USA

G SchoehnCNRS, Grenoble, France

J E SchoelzUniversity of Missouri, Columbia, MO, USA

L B SchonbergerCenters for Disease Control and Prevention, Atlanta, GA,USA

U SchubertKlinikum der Universita¨t Erlangen-Nu¨rnberg, Erlangen,Germany

D A SchultzJohns Hopkins University School of Medicine, Baltimore,

MD, USA

S Schultz-CherryUniversity of Wisconsin – Madison, Madison, WI, USA

T F SchulzHannover Medical School, Hannover, Germany

Contributors xxv

The University of Western Australia,

Crawley, WA, Australia

Centex Shrimp and Center for Genetic Engineering and

Biotechnology, Bangkok, Thailand

The University of Western Australia,

Crawley, WA, Australia

J StanleyJohn Innes Centre, Colney, UK

K M StedmanPortland State University, Portland, OR, USA

D StephanInstitute of Plant Diseases and Plant Protection,Hannover, Germany

C C M M StijgerWageningen University and Research Centre, Naaldwijk,The Netherlands

L StitzFederal Research Institute for Animal Health, Tuebingen,Gemany

P G StockleyUniversity of Leeds, Leeds, UK

M R StrandUniversity of Georgia, Athens, GA, USA

M J StuddertThe University of Melbourne, Parkville, VIC, Australia

C A SuttleUniversity of British Columbia, Vancouver, BC,Canada

N SuzukiOkayama University, Okayama, Japan

J Y SuzukiUSDA, Pacific Basin Agricultural Research Center, Hilo,

HI, USA

R SwanepoelNational Institute for Communicable Diseases,Sandringham, South Africa

S J SymesThe University of Melbourne, Parkville, VIC, Australia

G SzittyaAgricultural Biotechnology Center, Godollo, Hungary

M TalianskyScottish Crop Research Institute, Dundee, UK

P TattersallYale University Medical School, New Haven, CT, USA

T TatusovaNational Institutes of Health, Bethesda, MD, USA

S TavantzisUniversity of Maine, Orono, ME, USA

J M TaylorFox Chase Cancer Center, Philadelphia, PA, USA

D A TheilmannAgriculture and Agri-Food Canada, Summerland, BC,Canada

Virginia Polytechnic Institute and State University,

Blacksburg, VA, USA

University of California, San Francisco,

San Francisco, CA, USA

N K Van AlfenUniversity of California, Davis, CA, USA

R A A Van der VlugtWageningen University and Research Centre,Wageningen, The Netherlands

M H V Van RegenmortelCNRS, Illkirch, France

P A VenterThe Scripps Research Institute, La Jolla, CA, USA

J Verchot-LubiczOklahoma State University, Stillwater, OK, USA

R A Vere HodgeVere Hodge Antivirals Ltd., Reigate, UK

H J VettenFederal Research Centre for Agriculture and Forestry(BBA), Brunswick, Germany

L P VillarrealUniversity of California, Irvine, Irvine, CA, USA

J M VlakWageningen University, Wageningen, The Netherlands

P K VogtThe Scripps Research Institute, La Jolla, CA, USA

L E VolkmanUniversity of California, Berkeley, Berkeley, CA, USA

J VottelerKlinikum der Universita¨t Erlangen-Nu¨rnberg, Erlangen,Germany

D F VoytasIowa State University, Ames, IA, USA

J D F WadsworthUniversity College London, London, UK

E K WagnerUniversity of California, Irvine, Irvine, CA, USA

P J WalkerCSIRO Australian Animal Health Laboratory, Geelong,VIC, Australia

A L WangUniversity of California, San Francisco, CA, USA

X WangUniversity of Wisconsin – Madison, Madison, WI, USA

C C WangUniversity of California, San Francisco, CA, USA

Contributors xxvii

University of Oklahoma Health Sciences Center,

Oklahoma City, OK, USA

United States Army Medical Research Institute of

Infectious Diseases, Frederick, MD, USA

R B Wickner

National Institutes of Health, Bethesda, MD, USA

R G WillWestern General Hospital, Edinburgh, UK

T WilliamsInstituto de Ecologı´a A.C., Xalapa, Mexico

K WilloughbyMoredun Research Institute, Edinburgh, UK

S WinterDeutsche Sammlung fu¨r Mikroorganismen undZellkulturen, Brunswick, Germany

J WintonWestern Fisheries Research Center, Seattle, WA, USA

J K YamamotoUniversity of Florida, Gainesville, FL, USA

M YoshidaUniversity of Tokyo, Chiba, Japan

N YoshikawaIwate University, Ueda, Japan

L S YoungUniversity of Birmingham, Birmingham, UK

R F Young,IIITexas A&M University, College Station, TX, USA

T M YuillUniversity of Wisconsin, Madison, WI, USA

A J ZajacUniversity of Alabama at Birmingham, Birmingham, AL,USA

S K ZavrievShemyakin and Ovchinnikov Institute of BioorganicChemistry, Russian Academy of Sciences,Moscow, Russia

J ZiebuhrThe Queen’s University of Belfast, Belfast, UK

E I ZunigaThe Scripps Research Institute, La Jolla, CA, USA

Adenoviruses: General Features B Harrach 1Adenoviruses: Malignant Transformation and Oncology A S Turnell 9Adenoviruses: Molecular Biology K N Leppard 17Adenoviruses: Pathogenesis M Benko˝ 24African Cassava Mosaic Disease J P Legg 30African Horse Sickness Viruses P S Mellor and P P C Mertens 37African Swine Fever Virus L K Dixon and D Chapman 43AIDS: Disease Manifestation A Rapose, J East, M Sova and W A O’Brien 51AIDS: Global Epidemiology P J Peters, P H Kilmarx and T D Mastro 58AIDS: Vaccine Development N C Sheppard and Q J Sattentau 69Akabane Virus P S Mellor and P D Kirkland 76Alfalfa Mosaic Virus J F Bol 81Algal Viruses K Nagasaki and C P D Brussaard 87Allexivirus S K Zavriev 96Alphacryptovirus and Betacryptovirus R Blawid, D Stephan and E Maiss 98Anellovirus P Biagini and P de Micco 104Animal Rhabdoviruses H Bourhy, A J Gubala, R P Weir and D B Boyle 111Antigen Presentation E I Zuniga, D B McGavern and M B A Oldstone 121Antigenic Variation G M Air and J T West 127Antigenicity and Immunogenicity of Viral Proteins M H V Van Regenmortel 137

xxix

Antiviral Agents H J Field and R A Vere Hodge 142Apoptosis and Virus Infection J R Clayton and J M Hardwick 154Aquareoviruses M St J Crane and G Carlile 163Arboviruses B R Miller 170Arteriviruses M A Brinton and E J Snijder 176Ascoviruses B A Federici and Y Bigot 186Assembly of Viruses: Enveloped Particles C K Navaratnarajah, R Warrier and R J Kuhn 193Assembly of Viruses: Nonenveloped Particles M Luo 200Astroviruses L Moser and S Schultz-Cherry 204

B

Baculoviruses: Molecular Biology of Granuloviruses S Hilton 211Baculoviruses: Molecular Biology of Mosquito Baculoviruses J J Becnel and C L Afonso 219Baculoviruses: Molecular Biology of Sawfly Baculoviruses B M Arif 225Baculoviruses: Apoptosis Inhibitors R J Clem 231Baculoviruses: Expression Vector F J Haines, R D Possee and L A King 237Baculoviruses: General Features P J Krell 247Baculoviruses: Molecular Biology of Nucleopolyhedroviruses D A Theilmann and G W Blissard 254Baculoviruses: Pathogenesis L E Volkman 265Banana Bunchy Top Virus J E Thomas 272Barley Yellow Dwarf Viruses L L Domier 279Barnaviruses P A Revill 286Bean Common Mosaic Virus and Bean Common Mosaic Necrosis Virus R Jordan and J Hammond 288Bean Golden Mosaic Virus F J Morales 295Beet Curly Top Virus J Stanley 301

Bunyaviruses: General Features R M Elliott 390Bunyaviruses: Unassigned C H Calisher 399

C

Cacao Swollen Shoot Virus E Muller 403Caliciviruses M J Studdert and S J Symes 410Capillovirus, Foveavirus, Trichovirus, Vitivirus N Yoshikawa 419Capripoxviruses R P Kitching 427Capsid Assembly: Bacterial Virus Structure and Assembly S Casjens 432Cardioviruses C Billinis and O Papadopoulos 440Carlavirus K H Ryu and B Y Lee 448Carmovirus F Qu and T J Morris 453Caulimoviruses: General Features J E Schoelz 457Caulimoviruses: Molecular Biology T Hohn 464Central Nervous System Viral Diseases R T Johnson and B M Greenberg 469Cereal Viruses: Maize/Corn P A Signoret 475Cereal Viruses: Rice F Morales 482Cereal Viruses: Wheat and Barley H D Lapierre and D Hariri 490Chandipura Virus S Basak and D Chattopadhyay 497Chrysoviruses S A Ghabrial 503Circoviruses A Mankertz 513Citrus Tristeza Virus M Bar-Joseph and W O Dawson 520Classical Swine Fever Virus V Moennig and I Greiser-Wilke 525Coltiviruses H Attoui and X de Lamballerie 533Common Cold Viruses S Dreschers and C Adams 541Coronaviruses: General Features D Cavanagh and P Britton 549Coronaviruses: Molecular Biology S C Baker 554Cotton Leaf Curl Disease S Mansoor, I Amin and R W Briddon 563Cowpea Mosaic Virus G P Lomonossoff 569Cowpox Virus M Bennett, G L Smith and D Baxby 574Coxsackieviruses M S Oberste and M A Pallansch 580Crenarchaeal Viruses: Morphotypes and Genomes D Prangishvili, T Basta and R A Garrett 587Crimean–Congo Hemorrhagic Fever Virus and Other Nairoviruses C A Whitehouse 596Cryo-Electron Microscopy W Chiu, J T Chang and F J Rixon 603Cucumber Mosaic Virus F Garcı´a-Arenal and P Palukaitis 614Cytokines and Chemokines D E Griffin 620Cytomegaloviruses: Murine and Other Nonprimate Cytomegaloviruses A J Redwood, L M Smith and

Cytomegaloviruses: Simian Cytomegaloviruses D J Alcendor and G S Hayward 634

Contents XXXI

VOLUME 2 D

Defective-Interfering Viruses L Roux 1Dengue Viruses D J Gubler 5Diagnostic Techniques: Microarrays K Fischer, A Urisman and J DeRisi 14Diagnostic Techniques: Plant Viruses R Koenig, D-E Lesemann, G Adam and S Winter 18Diagnostic Techniques: Serological and Molecular Approaches R Vainionpa¨a¨ and P Leinikki 29Dicistroviruses P D Christian and P D Scotti 37Disease Surveillance N Noah 44DNA Vaccines S Babiuk and L A Babiuk 51

C Savolainen-Kopra and M Roivainen 130Entomopoxviruses M N Becker and R W Moyer 136Epidemiology of Human and Animal Viral Diseases F A Murphy 140Epstein–Barr Virus: General Features L S Young 148Epstein–Barr Virus: Molecular Biology J T Sample and C E Sample 157Equine Infectious Anemia Virus J K Craigo and R C Montelaro 167Evolution of Viruses L P Villarreal 174

F

Feline Leukemia and Sarcoma Viruses J C Neil 185Filamentous ssDNA Bacterial Viruses S A Overman and G J Thomas Jr 190Filoviruses G Olinger, T W Geisbert and L E Hensley 198Fish and Amphibian Herpesviruses A J Davison 205Fish Retroviruses T A Paul, R N Casey, P R Bowser, J W Casey, J Rovnak and S L Quackenbush 212

Fish Rhabdoviruses G Kurath and J Winton 221Fish Viruses J C Leong 227Flaviviruses of Veterinary Importance R Swanepoel and F J Burt 234Flaviviruses: General Features T J Chambers 241Flexiviruses M J Adams 253Foamy Viruses M L Linial 259Foot and Mouth Disease Viruses D J Rowlands 265Fowlpox Virus and Other Avipoxviruses M A Skinner 274Fungal Viruses S A Ghabrial and N Suzuki 284

H

Henipaviruses B T Eaton and L-F Wang 321Hepadnaviruses of Birds A R Jilbert and W S Mason 327Hepadnaviruses: General Features T J Harrison 335Hepatitis A Virus A Dotzauer 343Hepatitis B Virus: General Features P Karayiannis and H C Thomas 350Hepatitis B Virus: Molecular Biology T J Harrison 360Hepatitis C Virus R Bartenschlager and S Bu¨hler 367Hepatitis Delta Virus J M Taylor 375Hepatitis E Virus X J Meng 377Herpes Simplex Viruses: General Features L Aurelian 383Herpes Simplex Viruses: Molecular Biology E K Wagner and R M Sandri-Goldin 397Herpesviruses of Birds S Trapp and N Osterrieder 405Herpesviruses of Horses D J O’Callaghan and N Osterrieder 411Herpesviruses: Discovery B Ehlers 420Herpesviruses: General Features A J Davison 430Herpesviruses: Latency C M Preston 436History of Virology: Bacteriophages H-W Ackermann 442History of Virology: Plant Viruses R Hull 450History of Virology: Vertebrate Viruses F J Fenner 455

Contents XXXIII

Hordeivirus J N Bragg, H-S Lim and A O Jackson 459Host Resistance to Retroviruses T Hatziioannou and P D Bieniasz 467Human Cytomegalovirus: General Features E S Mocarski Jr and R F Pass 474Human Cytomegalovirus: Molecular Biology W Gibson 485Human Eye Infections J Chodosh, A V Chintakuntlawar and C M Robinson 491Human Herpesviruses 6 and 7 U A Gompels 498Human Immunodeficiency Viruses: Antiretroviral Agents A W Neuman and D C Liotta 505Human Immunodeficiency Viruses: Molecular Biology J Votteler and U Schubert 517Human Immunodeficiency Viruses: Origin F van Heuverswyn and M Peeters 525Human Immunodeficiency Viruses: Pathogenesis N R Klatt, A Chahroudi and G Silvestri 534Human Respiratory Syncytial Virus P L Collins 542Human Respiratory Viruses J E Crowe Jr 551Human T-Cell Leukemia Viruses: General Features M Yoshida 558Human T-Cell Leukemia Viruses: Human Disease R Mahieux and A Gessain 564Hypovirulence N K Van Alfen and P Kazmierczak 574

VOLUME 3 I

Icosahedral dsDNA Bacterial Viruses with an Internal Membrane J K H Bamford and S J Butcher 1Icosahedral Enveloped dsRNA Bacterial Viruses R Tuma 6Icosahedral ssDNA Bacterial Viruses B A Fane, M Chen, J E Cherwa and A Uchiyama 13Icosahedral ssRNA Bacterial Viruses P G Stockley 21Icosahedral Tailed dsDNA Bacterial Viruses R L Duda 30Idaeovirus A T Jones and H Barker 37

Immune Response to Viruses: Antibody-Mediated Immunity A R Neurath 56Immune Response to Viruses: Cell-Mediated Immunity A J Zajac and L E Harrington 70Immunopathology M B A Oldstone and R S Fujinami 78Infectious Pancreatic Necrosis Virus Ø Evensen and N Santi 83Infectious Salmon Anemia Virus B H Dannevig, S Mjaaland and E Rimstad 89

Interfering RNAs K E Olson, K M Keene and C D Blair 148Iridoviruses of Vertebrates A D Hyatt and V G Chinchar 155Iridoviruses of Invertebrates T Williams and A D Hyatt 161Iridoviruses: General Features V G Chinchar and A D Hyatt 167

Lassa, Junin, Machupo and Guanarito Viruses J B McCormick 203

Leishmaniaviruses R Carrion Jr, Y-T Ro and J L Patterson 220Leporipoviruses and Suipoxviruses G McFadden 225Luteoviruses L L Domier and C J D’Arcy 231Lymphocytic Choriomeningitis Virus: General Features R M Welsh 238Lymphocytic Choriomeningitis Virus: Molecular Biology J C de la Torre 243Lysis of the Host by Bacteriophage R F Young III and R L White 248

M

Machlomovirus K Scheets 259Maize Streak Virus D P Martin, D N Shepherd and E P Rybicki 263Marburg Virus D Falzarano and H Feldmann 272Marnaviruses A S Lang and C A Suttle 280Measles Virus R Cattaneo and M McChesney 285Membrane Fusion A Hinz and W Weissenhorn 292

Mimivirus J-M Claverie 311Molluscum Contagiosum Virus J J Bugert 319Mononegavirales A J Easton and R Ling 324Mouse Mammary Tumor Virus J P Dudley 334Mousepox and Rabbitpox Viruses M Regner, F Fenner and A Mu¨llbacher 342Movement of Viruses in Plants P A Harries and R S Nelson 348

Contents XXXV

Mumps Virus B K Rima and W P Duprex 356Mungbean Yellow Mosaic Viruses V G Malathi and P John 364Murine Gammaherpesvirus 68 A A Nash and B M Dutia 372Mycoreoviruses B I Hillman 378

N

Nanoviruses H J Vetten 385Narnaviruses R Esteban and T Fujimura 392Nature of Viruses M H V Van Regenmortel 398Necrovirus L Rubino and G P Martelli 403

Neutralization of Infectivity P J Klasse 413Nidovirales L Enjuanes, A E Gorbalenya, R J de Groot, J A Cowley, J Ziebuhr and E J Snijder 419Nodaviruses P A Venter and A Schneemann 430Noroviruses and Sapoviruses K Y Green 438

O

Ophiovirus A M Vaira and R G Milne 447Orbiviruses P P C Mertens, H Attoui and P S Mellor 454Organ Transplantation, Risks C N Kotton, M J Kuehnert and J A Fishman 466Origin of Viruses P Forterre 472Orthobunyaviruses C H Calisher 479Orthomyxoviruses: Molecular Biology M L Shaw and P Palese 483Orthomyxoviruses: Structure of Antigens R J Russell 489Oryctes Rhinoceros Virus J M Vlak, A M Huger, J A Jehle and R G Kleespies 495Ourmiavirus G P Accotto and R G Milne 500

VOLUME 4 P

Papaya Ringspot Virus D Gonsalves, J Y Suzuki, S Tripathi and S A Ferreira 1Papillomaviruses: General Features of Human Viruses G Orth 8Papillomaviruses: Molecular Biology of Human Viruses P F Lambert and A Collins 18Papillomaviruses of Animals A A McBride 26Papillomaviruses: General Features H U Bernard 34Paramyxoviruses of Animals S K Samal 40Parainfluenza Viruses of Humans E Adderson and A Portner 47Paramyxoviruses R E Dutch 52Parapoxviruses D Haig and A A Mercer 57

Partitiviruses of Fungi S Tavantzis 63Partitiviruses: General Features S A Ghabrial, W F Ochoa, T S Baker and M L Nibert 68Parvoviruses of Arthropods M Bergoin and P Tijssen 76Parvoviruses of Vertebrates C R Parrish 85Parvoviruses: General Features P Tattersall 90Pecluvirus D V R Reddy, C Bragard, P Sreenivasulu and P Delfosse 97Pepino Mosaic Virus R A A Van der Vlugt and C C M M Stijger 103Persistent and Latent Viral Infection E S Mocarski and A Grakoui 108Phycodnaviruses J L Van Etten and M V Graves 116Phylogeny of Viruses A E Gorbalenya 125Picornaviruses: Molecular Biology B L Semler and K J Ertel 129Plant Antiviral Defense: Gene Silencing Pathway G Szittya, T Dalmay and J Burgyan 141Plant Reoviruses R J Geijskes and R M Harding 149Plant Resistance to Viruses: Engineered Resistance M Fuchs 156Plant Resistance to Viruses: Geminiviruses J K Brown 164Plant Resistance to Viruses: Natural Resistance Associated with Dominant Genes

P Moffett and D F Klessig 170Plant Resistance to Viruses: Natural Resistance Associated with Recessive Genes

C Caranta and C Dogimont 177Plant Rhabdoviruses A O Jackson, R G Dietzgen, R-X Fang, M M Goodin, S A Hogenhout,

Plant Virus Diseases: Economic Aspects G Loebenstein 197Plant Virus Diseases: Fruit Trees and Grapevine G P Martelli and J K Uyemoto 201Plant Virus Diseases: Ornamental Plants J Engelmann and J Hamacher 207Plant Virus Vectors (Gene Expression Systems) Y Gleba, S Marillonnet and V Klimyuk 229Plum Pox Virus M Glasa and T Candresse 238Poliomyelitis P D Minor 242Polydnaviruses: Abrogation of Invertebrate Immune Systems M R Strand 250Polydnaviruses: General Features A Fath-Goodin and B A Webb 256Polyomaviruses of Humans M Safak and K Khalili 261Polyomaviruses of Mice B Schaffhausen 271Polyomaviruses M Gravell and E O Major 277

Potato Virus Y C Kerlan and B Moury 287Potato Viruses C Kerlan 296Potexvirus K H Ryu and J S Hong 310Potyviruses J J Lo´pez-Moya and J A Garcı´a 313Poxviruses G L Smith, P Beard and M A Skinner 322Prions of Vertebrates J D F Wadsworth and J Collinge 330Prions of Yeast and Fungi R B Wickner, H Edskes, T Nakayashiki, F Shewmaker, L McCann,

A Engel and D Kryndushkin 336

Contents XXXVII

Pseudorabies Virus T C Mettenleiter 341Pseudoviruses D F Voytas 352

S

Satellite Nucleic Acids and Viruses P Palukaitis, A Rezaian and F Garcı´a-Arenal 526Seadornaviruses H Attoui and P P C Mertens 535

Severe Acute Respiratory Syndrome (SARS) J S M Peiris and L L M Poon 552Shellfish Viruses T Renault 560Shrimp Viruses J-R Bonami 567

Sigma Rhabdoviruses D Contamine and S Gaumer 576Simian Alphaherpesviruses J Hilliard 581Simian Gammaherpesviruses A Ensser 585Simian Immunodeficiency Virus: Animal Models of Disease C J Miller and M Marthas 594Simian Immunodeficiency Virus: General Features M E Laird and R C Desrosiers 603Simian Immunodeficiency Virus: Natural Infection I Pandrea, G Silvestri and C Apetrei 611Simian Retrovirus D P A Marx 623Simian Virus 40 A L McNees and J S Butel 630Smallpox and Monkeypox Viruses S Parker, D A Schultz, H Meyer and R M Buller 639Sobemovirus M Meier, A Olspert, C Sarmiento and E Truve 644

St Louis Encephalitis W K Reisen 652Sweetpotato Viruses J Kreuze and S Fuentes 659

VOLUME 5 T

Taura Syndrome Virus A K Dhar and F C T Allnutt 1Taxonomy, Classification and Nomenclature of Viruses C M Fauquet 9

Tetraviruses J A Speir and J E Johnson 27Theiler’s Virus H L Lipton, S Hertzler and N Knowles 37Tick-Borne Encephalitis Viruses T S Gritsun and E A Gould 45Tobacco Mosaic Virus M H V Van Regenmortel 54Tobacco Viruses S A Tolin 60Tobamovirus D J Lewandowski 68Tobravirus S A MacFarlane 72Togaviruses Causing Encephalitis S Paessler and M Pfeffer 76Togaviruses Causing Rash and Fever D W Smith, J S Mackenzie and M D A Lindsay 83Togaviruses Not Associated with Human Disease L L Coffey, 91Togaviruses: Alphaviruses A M Powers 96Togaviruses: Equine Encephalitic Viruses D E Griffin 101Togaviruses: General Features S C Weaver, W B Klimstra and K D Ryman 107Togaviruses: Molecular Biology K D Ryman, W B Klimstra and S C Weaver 116Tomato Leaf Curl Viruses from India S Chakraborty 124Tomato Spotted Wilt Virus H R Pappu 133Tomato Yellow Leaf Curl Virus H Czosnek 138Tombusviruses S A Lommel and T L Sit 145Torovirus A E Hoet and M C Horzinek 151Tospovirus M Tsompana and J W Moyer 157Totiviruses S A Ghabrial 163

Contents XXXIX

Transcriptional Regulation in Bacteriophage R A Weisberg, D M Hinton and S Adhya 174Transmissible Spongiform Encephalopathies E D Belay and L B Schonberger 186Tumor Viruses: Human R Grassmann, B Fleckenstein and H Pfister 193Tymoviruses A-L Haenni and T W Dreher 199

Watermelon Mosaic Virus and Zucchini Yellow Mosaic Virus H Lecoq and C Desbiez 433West Nile Virus L D Kramer 440White Spot Syndrome Virus J-H Leu, J-M Tsai and C-F Lo 450

Y

Yatapoxviruses J W Barrett and G McFadden 461Yeast L-A Virus R B Wickner, T Fujimura and R Esteban 465Yellow Fever Virus A A Marfin and T P Monath 469Yellow Head Virus P J Walker and N Sittidilokratna 476

Adenoviruses: General Features

B Harrach, Veterinary Medical Research Institute, Budapest, Hungary

ã 2008 Elsevier Ltd All rights reserved.

Introduction

Adenoviruses are middle-sized, nonenveloped,

icosahe-dral, double-stranded DNA viruses of animals The prefix

adeno comes from the Greek wordadZn (gland),

reflect-ing the first isolation of a virus of this type from human

adenoid tissue half a century ago Adenoviruses have since

been isolated from a large variety of hosts, including

representatives of every major vertebrate class from fish

to mammals Using polymerase chain reaction (PCR)

technology, a large variety of putative novel

adenoviru-ses have been detected, but isolation of such viruadenoviru-ses and

in vitro propagation is hampered in most cases by the lack

of appropriate permissive cell cultures Some human and

animal adenoviruses can cause diseases or even death, but

most are not pathogenic in non-immuno-compromised,

healthy individuals Adenoviruses have been used as model

organisms in molecular biology, and important findings of

general relevance have emerged from such studies,

includ-ing splicinclud-ing in eukaryotes Adenoviruses have become one

of the most popular vector systems for virus-based gene

therapy and vaccination and have potential as antitumor

tools Wide prevalence in diverse host species and a

substantially conserved genome organization make

ade-noviruses an ideal model for studying virus evolution

Taxonomy

Adenoviruses belong to the family Adenoviridae No higher

taxonomical level has yet been established, despite the fact

that certain bacteriophages (Tectiviridae), the green alga

virus Paramecium bursaria Chlorella virus 1 (Phycodnaviridae),

and a virus of Archaea living in hot springs (sulfolobus

turreted icosahedral virus) seem to have common

evolu-tionary roots with adenoviruses

There are four official genera in the family Two genera

(Mastadenovirus and Aviadenovirus) comprise adenoviruses

that have probably co-evolved with mammals and birds,

respectively The other two genera (Atadenovirus and novirus) have a broader range of hosts Atadenoviruses werenamed after a bias toward high AþTcontent in the genomes

Siade-of the initial representatives, which infect various ruminantand avian hosts, as well as a marsupial Every known reptil-ian adenovirus also belongs to the atadenoviruses, althoughtheir genomes do not show the same bias toward high AþTcontent The very few known siadenoviruses were isolatedfrom or detected by PCR in birds and a frog This genus wasnamed in recognition of the presence of a gene encoding apotential sialidase in the viruses concerned The singleconfirmed fish adenovirus falls into a separate group thatmay eventually found a fifth genus; adenovirus-like parti-cles have been described in additional fish species.Within each genus, the viruses are grouped into species,which are named according to the host first described andsupplemented with letters of the alphabet (Table 1) Hostorigin is only one of several criteria that are used to demar-cate the species Phylogenetic distance is the most signifi-cant criterion, with species defined as separated by morethan 5–10% amino acid sequence divergence of hexon andDNA polymerase (pol), respectively Further importantcharacteristics come into play, especially if DNA sequencedata are not available: DNA hybridization, restriction frag-ment length polymorphism, nucleotide composition, onco-genicity in rodents, growth characteristics, host range,cross-neutralization, ability to recombine, number ofvirus-associated (VA) RNA genes, hemagglutinationproperties, and organization of the genome However, all

of these ancillary data are expected to accord with theresults of phylogenetic calculations Thus, for example,chimpanzee adenoviruses are classified into human ade-novirus species Adenoviruses of humans have been stud-ied far more intensively than those of other animals, andthe six species (Human adenovirus A to Human adenovirus F;abbreviated informally to HAdV-A to HAdV-F) corre-spond to substantial ‘groups’ or ‘subgenera’ defined previ-ously Each human adenovirus serotype is abbreviated toHAdV hyphenated to a number

1

Table 1 The taxonomy of family Adenoviridae a

Mastadenovirus

Bovine adenovirus C BAdV-10

Equine adenovirus A EAdV-1

Equine adenovirus B EAdV-2

Porcine adenovirus B PAdV-4

Goat adenovirus (ts) GAdV-2

Guinea pig adenovirus (ts) GPAdV-1

Murine adenovirus B (ts) MAdV-2

Ovine adenovirus C (ts) OAdV-6

Squirrel adenovirus (ts) SqAdV-1

Aviadenovirus

Duck adenovirus B (ts) DAdV-2

Pigeon adenovirus (ts) PiAdV-1

Turkey adenovirus B (ts) TAdV-1, 2

Psittacine adenovirus? Psittacine adenovirus 1

Falcon adenovirus? Falcon adenovirus 1

Atadenovirus

Bearded dragon adenovirus (ts) BDAdV-1

Bovine adenovirus E (ts) BAdV-6

Bovine adenovirus F (ts) BAdV-7

Cervine adenovirus (ts) Odocoileus adenovirus 1 (OdAdV-1)

Chameleon adenovirus (ts) ChAdV-1

Gekkonid adenovirus(?) Tokay gecko adenovirus

Helodermatid adenovirus(?) Gila monster adenovirus

Scincid adenovirus(?) Blue-tongued skink adenovirus

Genus Siadenovirus

Continued

2 Adenoviruses: General Features

To illustrate the need to proceed carefully in developing

adenovirus taxonomy, the case of the newest adenovirus

isolated from human samples (HAdV-52) is illuminating

This virus seems to be sufficiently different from other

human adenoviruses to merit the erection of a new species

However, it is very similar to some previously characterized

Old World monkey adenoviruses (simian adenoviruses 1 and

7 (SAdV-1, SAdV-7) plus others) One taxonomical proposal

would be to establish a new species, Human adenovirus G,

containing HAdV-52 and the related monkey adenoviruses

Clearly, this would depend on epidemiological data

demon-strating that HAdV-52 is properly a human virus and not an

occasional, opportunistic transfer from monkeys For similar

reasons and others, classification of many nonhuman

adeno-viruses into species is not yet resolved

Virion Morphology and Properties

The icosahedral capsid is 70–90 nm in diameter and

con-sists of 240 nonvertex capsomers (called hexons), each

8–10 nm in diameter, and 12 vertex capsomers (pentons),

each with a protruding fiber 9–77.5 nm in length The

members of genus Aviadenovirus that have been studied

have two fiber proteins per vertex Fowl adenovirus 1

(FAdV-1) even has two, tandem fiber genes of different

lengths, resulting in two fibers of different sizes at each

vertex Members of species Human adenovirus F (and

HAdV-52 and the related monkey viruses) also have two

fiber genes of different lengths, but the fibers are

distributed in single copies alternately on the vertices

The main capsomers (hexons) are formed by the interaction

of three identical polypeptides (designated hexon, and also

as polypeptide II, after a Roman numeral system based on

the relative mobilities of structural proteins under reducing

conditions in sodium dodecyl sulfate-polyacrylamide gel

electrophoresis) Each hexon has two characteristic parts: a

triangular top with three ‘towers’, and a pseudohexagonal

base with a central cavity Hexons, or more exactly their

bases, are packed tightly to form a protein shell that

protects the inner components of the virion

In members of the genus Mastadenovirus 12 copies of

polypeptide IX are found between the nine hexons in the

center of each facet However, polypeptide IX is not

present in the members of any other genus Two mers of polypeptide IIIa penetrate the hexon shell at theedge of each facet, and multiple copies of polypeptide VIform a ring underneath the peripentonal hexons Pentonbases are formed at the vertices by the interaction of fivecopies of polypeptide III, and are tightly associated withone (or, in the aviadenoviruses, two) fibers, each consist-ing of three copies of polypeptide IV in the form of a shaft

mono-of characteristic length with a distal knob PolypeptideVIII is situated at the inner surface of the hexon shell.Polypeptides VI and VIII appear to link the capsid to thevirion core, which consists of a single copy of the DNAgenome complexed with four polypeptides (V, VII, X,TP) Polypeptide V exists only in mastadenoviruses.Adenoviruses are stable on storage in the frozen state.They are stable to mild acid and insensitive to lipidsolvents Heat sensitivity varies among the genera

Nucleic Acid, Genome Organization, and Replication

The adenovirus genome is a linear molecule of stranded DNA (26 163–45 063 bp) containing an invertedterminal repeat (ITR) of 36–368 bp at its termini, with the 50ends of the genome linked covalently to a terminal protein(TP) The nucleotide composition is 33.7–63.8% GþC.The genetic organization of the central part of the genome

double-is conserved throughout the family, whereas the terminalparts show large variations in length and gene content(Figure 1) Splicing was first discovered in adenoviruses,and is a common means of expressing mRNAs in this virusfamily In the conserved region, most late genes areexpressed by splicing from the rightward-oriented majorlate promoter located in the pol gene The early genesencoding pol, the precursor of TP (pTP), and the DNA-binding protein (DBP) are spliced from leftward-orientedpromoters Where it has been examined, splicing is also acommon feature of genes in the nonconserved regions.Replication of various human adenoviruses has beenstudied in detail, in particular with HAdV-2 Virus entrytakes place via interactions of the fiber knob with specificreceptors on the surface of a susceptible cell followed byinternalization via interactions between the penton base

Table 1 Continued

Unassigned Viruses in the Family

a

Official genus and species names as published in the Eighth Report of the ICTV are in italics, and tentative species (ts), proposed species (marked by a query) or single isolates are not Because of confusion in the serotype numbering in some cases (e.g among fowl adenoviruses), certain characteristic strains are shown for easier identification Available full genome sequences are noted by G or by the number of the sequenced serotype(s) if those listed are not all available.