Avian Immunology Avian Immunology Third Edition Edited by Bernd Kaspers Department for Veterinary Sciences, Veterinary Immunology Study Group, University of Munich, Munich, Germany Karel A. Schat Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY, United States Thomas W. Go¨bel Department for Veterinary Sciences, Veterinary Immunology Study Group, University of Munich, Munich, Germany Lonneke Vervelde Division Infection and Immunity, The Roslin Institute and R(D)SVS, The University of Edinburgh, Midlothian, United Kingdom AcademicPressisanimprintofElsevier 125LondonWall,LondonEC2Y5AS,UnitedKingdom 525BStreet,Suite1650,SanDiego,CA92101,UnitedStates 50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom Copyright©2022ElsevierLtd.Allrightsreserved. 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BritishLibraryCataloguing-in-PublicationData AcataloguerecordforthisbookisavailablefromtheBritishLibrary LibraryofCongressCataloging-in-PublicationData AcatalogrecordforthisbookisavailablefromtheLibraryofCongress ISBN:978-0-12-818708-1 ForInformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/books-and-journals Publisher:AndreGerhardWolff AcquisitionsEditor:LindaVersteeg-buschman EditorialProjectManager:SusanIkeda ProductionProjectManager: NiranjanBhaskaran CoverDesigner:ChristianJ.Bilbow BackCoverImagesby‘Karel“Ton”A.Schat’ TypesetbyMPSLimited,Chennai,India Dedication Dedicatedto ProfessorPeteKaiser1964(cid:1)2016 CoeditorSecondEditionAvianImmunology ValuedAvianImmunologistandSorelyMissedbytheEditorsofthe ThirdEditionofAvianImmunology. Contents Listofcontributors xvii 2.3.11 Germinalcenterofthe Foreword xix peripherallymphoidorgans 21 Acknowledgments xxi 2.4 Thespleen 22 2.4.1 Originandanatomy 22 1. The importance of the avian immune 2.4.2 Periarteriolarlymphoidsheath 25 system and its unique features 1 2.4.3 Ellipsoidsandperiellipsoid whitepulp 25 FredDavison 2.4.4 Themarginal-zoneequivalent 1.1 Introduction 1 andantigenhandling 27 1.2 Thecontributionfromavian 2.5 Gut-associatedlymphoidtissue 28 lymphocytes 1 2.5.1 Follicle-associatedepitheliumor 1.3 ContributionofthebursaofFabricius 2 lymphoepithelium 30 1.3.1 Geneconversionandthebursa 4 2.5.2 Esophagealandpylorictonsils 30 1.4 ThecontributionofthechickenMHC 5 2.5.3 Peyer’spatches 31 1.5 Contributionstovaccinology 6 2.5.4 Meckel’sdiverticulum 31 1.5.1 Embryonic(inovo)vaccination 7 2.5.5 Cecaltonsils 32 1.6 Conclusion 8 2.6 Harderiangland 33 References 8 2.7 Murallymphnode 34 2.8 Ectopiclymphatictissueandpineal 2. Structure of the avian lymphoid gland 36 system 11 2.9 Bonemarrow 37 2.10 Blood 38 Na´ndorNagy,ImreOla´hand References 39 LonnekeVervelde 2.1 Introduction 11 3. Development of the avian 2.2 Thethymus 12 hematopoietic and immune 2.2.1 Anatomyandhistological organization 12 systems 45 2.2.2 Thymiccortex 13 LaurentYvernogeau,Na´ndorNagy, 2.2.3 Thymicmedulla 13 DominiqueDunon,CatherineRobinand 2.3 ThebursaofFabricius 15 ThierryJaffredo 2.3.1 Anatomyandhistology 15 3.1 Introduction 45 2.3.2 Bursalsurfaceepithelium 16 3.2 Originsandmigrationroutesof 2.3.3 Bursalfollicle 17 hematopoieticcellsusingquail/chicken 2.3.4 Medulla 18 complementarychimeras 45 2.3.5 Bursalmedullaryepithelial 3.2.1 Lookingforthesourceof cells 18 hematopoeieticcellsduring 2.3.6 Bursalsecretorydendriticcells 19 development 45 2.3.7 Bursalmacrophages 19 3.2.2 Macrophageproductionbythe 2.3.8 Bursallymphocytes 21 yolksac 46 2.3.9 Cortex 21 3.2.3 TheaorticregionproducesHSCs 46 2.3.10 Peripherallymphoidtissueof 3.3 Aorticclustersastheintraembryonic thebursaofFabricius 21 sourceofdefinitivehematopoiesis 46 vii viii Contents 3.3.1 Cellularandmolecular 4. B cells, the bursa of Fabricius, and the identificationoftheclusters 46 generation of antibody repertoires 71 3.3.2 Theparaaorticfoci 46 3.3.3 Tracingtheoriginsandfates MichaelJ.H.RatcliffeandSonjaHa¨rtle oftheaorticclusters 46 4.1 Introduction 71 3.4 Formationoftheaorta:adorsal 4.2 Thegenerationofavianantibody angioblasticlineageandaventral repertoires 71 hemangioblastslineage 48 4.2.1 Immunoglobulinlightchains 71 3.4.1 Twoendotheliallineagesformthe 4.2.2 Immunoglobulinheavychains 72 vascularnetworkoftheembryo 48 4.2.3 GenerationofIgmoleculesby 3.4.2 Chimericoriginoftheaortic V(D)Jrecombination 74 endothelialcells 48 4.2.4 GenerationofIgdiversityby 3.5 Developinganinvitromodelof somaticgeneconversion 75 hemogenicendotheliumcommitment 4.2.5 Implicationsofgeneconversion andendothelial-to-hematopoietic forallelicexclusion 77 transition 50 4.3 ThedevelopmentofavianBcells 77 3.6 Spatiotemporalemergenceand 4.3.1 PrebursalBcelldevelopment 77 organizationofthechickenIAHCs 52 4.3.2 Colonizationofthebursaby 3.7 Ecsofthelatefetus/youngadultbone Bcellprogenitors 78 marrowharborhemogenicpotential 4.3.3 Colonizationoflymphoid andgeneratemultilineage folliclesinthebursa 79 hematopoiesis 54 4.3.4 GrowthofbursalBcellsin 3.8 Spatialtranscriptomicsinthechicken bursalfollicles 82 embryorevealsregulatorsof 4.3.5 Developmentofthebursaafter hematopoiesis 55 hatch 83 3.9 TheavianthymusandT-cell 4.3.6 Roleofcelladhesionmolecules development 57 andchemokinesinbursalcell 3.9.1 Thymicdevelopment 57 development 85 3.9.2 Colonizationofthethymus 57 4.3.7 Developmentofperipheral 3.9.3 T-celldifferentiation 57 Bcellpopulations 87 3.9.4 TCRrearrangement 58 4.3.8 ActivationofperipheralBcells 89 3.10 ThebursaofFabricius,B-cellontogeny, 4.3.9 Plasmacelldevelopment 90 andimmunoglobulins 58 4.3.10 CytokinesinchickenBcell 3.10.1 Bursaldevelopment 58 developmentandactivation 91 3.10.2 Formationofthebursal 4.3.11 ApplicationofBcellcultures 92 epithelialanlage 58 References 93 3.10.3 Hematopoieticcolonization ofthebursalrudimentand 5. Structure and evolution of avian folliclebudformation 60 immunoglobulins 101 3.10.4 Developmentofthefollicle- associatedepitheliumandthe SonjaHa¨rtle,KatharineE.Magor, follicularcortex 62 ThomasW.Go¨bel,FredDavisonand 3.10.5 Immunoglobulins 63 BerndKaspers 3.11 Lymphocyte-differentiating 5.1 Thebasicstructureofimmunoglobulins 101 hormones 63 5.2 Avianimmunoglobulins 102 3.12 Developmentoftheimmune 5.2.1 AvianIgM 102 responses 64 5.2.2 AvianIgY(IgG) 103 3.12.1 Earlyimmuneresponses 64 5.2.3 AvianIgA 104 3.12.2 Antibodyisotypeswitching 5.2.4 AvianhomologuesofIgD andhypersensitivityreaction 64 andIgE 105 3.12.3 Allograftrejection 64 5.2.5 Lchains 105 3.13 Conclusion 64 5.2.6 Genomicorganizationofthe Acknowledgments 65 IgHandIgLlocus 105 References 65 5.3 Ighalf-life 107 Contents ix 5.4 Naturalantibodies 107 7.7 Genecoevolutioninthechicken 5.5 Maternalantibodies 108 majorhistocompatibilitycomplex 142 5.6 Fcreceptors 109 7.8 Otherchickengenesimportantfor 5.6.1 ChickenpolymericIgreceptor 109 themajorhistocompatibility 5.6.2 ChickenFcRnhomologue 110 complex 144 5.6.3 ChickenFcreceptorcluster 110 7.9 Polymorphismandtypingchicken 5.6.4 ggFcR 110 majorhistocompatibilitycomplex 5.6.5 CHIR-AB1 110 genes 145 5.7 Avianantibodyresponses 110 7.10 Avianmajorhistocompatibility 5.8 Thechickeneggasasourceof complexes 146 antibodies 112 7.11 Immunity,diseaseresistance,andthe 5.8.1 Avianantibodiesastoolsfor majorhistocompatibilitycomplexin research 112 wildbirds 148 References 113 7.12 Sexualselectionandthemajor histocompatibilitycomplexinwild 6. Avian T cells: Antigen Recognition birds 149 and Lineages 121 7.13 Originandevolutionoftheimmune system 150 AdrianL.SmithandThomasW.Go¨bel Acknowledgments 151 6.1 Introduction 121 References 151 6.2 Tcellreceptorstructureandlineages 121 6.2.1 SomaticDNArecombination 121 8. Introduction to the avian innate 6.2.2 OrganizationoftheTcell immune system; properties, receptorclusters 123 effects, and integration with other 6.3 CD3signalingcomplex 125 6.3.1 MammalianCD3 125 parts of the immune system 163 6.3.2 ChickenCD3γ/δandCD3ε 126 ThomasW.Go¨belandAdrianL.Smith 6.3.3 ζζhomodimer 126 6.3.4 Tcellreceptorcomplex—structural 8.1 Macrophages and dendritic cells 167 models 126 6.3.5 Tcellreceptorsignaltransduction 127 KateSutton,AdamBalic,BerndKaspersand 6.4 CD4andCD8 127 LonnekeVervelde 6.5 Costimulatorymolecules 128 8.1.1 Introduction 167 6.6 Tcelllineages 129 8.1.1.1 Antigenpresentation 167 6.7 MethodstostudyTcellfunction 130 8.1.1.2 Dendriticcells 168 6.8 Perspectives 130 8.1.1.3 Macrophages 169 References 131 8.1.1.4 Developmentofmyeloid cells 171 7. The avian major histocompatibility 8.1.1.5 Sourcesofavianmacrophages anddendriticcells 172 complex 135 8.1.1.6 Avianmyeloidcelllines 175 JimKaufman 8.1.1.7 Cellsurfacemarkersfor 7.1 Introduction 135 avianmyeloidcells 175 7.2 Thebiologyofthemajor 8.1.1.8 Characterizationof histocompatibilitycomplex 135 macrophagesandDCin 7.3 Themajorhistocompatibilitycomplex: tissuesections 178 agenomicregionorabiologicalunit? 136 8.1.1.9 Functionalpropertiesof 7.4 Thechickenmajorhistocompatibility chickenmacrophages 178 complexandthemajorhistocompatibility 8.1.1.10 Macrophagemigration 178 complexsyntenicregion 137 8.1.1.11 Phagocytosis 179 7.5 Classicalandnonclassicalmajor 8.1.1.12 Respiratoryburstactivity 180 histocompatibilitycomplexmolecules 139 8.1.1.13 Nitricoxideproduction:a 7.6 Chickenclassicalmajor readoutsystemforavian histocompatibilitycomplexmolecules 140 macrophageactivation 180