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Recognition of Foreign Particles by the Protochordate Botrylloides

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Recognition of Foreign Particles by the Protochordate Botrylloides 2l-f Ô'93 RÉCOGN ITION OF FOREIGN PARTICLES BY THE PROTOCHORDA TE Botrvlloides leachii. Deirdre R. Coombe, B.Sc. Hons. (Adelaide) ' Department of ZooIogY, The University of Adelaide. A thesis submitted for the degree of Doctor of Philosophy. lvlarch L983. 'rIf mammals are the "Rolls-Royce or Mercedes-Benzrl model of elaborate inmune I'bicycle'l responsiveness, the " jeeptt and models are now discernible among invertebrates. " Hildemann, L974. (in Uhlenbruck, L9l4). a ABSTRACT This thesis is concerned with the mechanisms by which haemocytes from the ascidian Botrylloides leachii recognise foreign particJ-es. The probJ.em was addressed by investigating the functions of two haemaggtutinins (HA-f & HA-2) and a third non-agglutinating protein (LBP-I) aII of which occur in B. Ieachii haemolymph. The possibíIity that other species of ascidian may also possess molecules similar to the q. leachii agglutinins was examined using haemolymph fron 22 different species belonging to the major families of ascidians. The divalent cation requirements and the aggJ-utinating specificities (sugar inhibition) of samples with a high titre were determj-ned. Column chromatography indicated that haemolymph samples flrom 4 different ascidians had molecules with similar size and specificity to the HA-I. One of these, a sample from Botryllus sp., also contained an t'l1\-2 like" molecule. The BotryJ.Ius sp. agglutinins were affinity purified and compared to the HA-I & HA-2 agglutinins. The Botryllus sp. "HA-l like" molecule lvas slightly smaller than the B. Ieachii l-lA-I. These two molecules exhibited identical sugar binding specificities and divalent cation requirements, but no antigenic cross-reactivity was observed. A Preliminary SDS-PAGE analysis suggested that the Botryllus sp. agglutinin was structurally quite dÍstinct from the l-lA-I agglutinin and LEIP-1. The B. Ieachii l1A-2 molecule and the Botryllus sp. sheep erythrocyte aggJ-utinin lvere antigenically cross-reactive and identical in size and subunit structure, but they diflfered sJ.ight.J.y in binding site specificity. rl_ The possibility that the B. Ieachii agglutinins were opsonins was investigated both in vivo and in vitro. It was found that injecting coLonies with erythrocytes bearing HA-z receptors produced a smal-I but significant increase in the ll{-2 agglutinating titre of haemolymph. Ì'4oreover, this increase was specific. There was no indication of an anamnestic response. The HA-l titre of haemoJ.ymph appeared to some extent to be dependent on environmental stimuli since colonies relocated to a new environment had titres significantJ,y different from those of colonies remaining at the original. location. The effect of environmentaL stimuli was not considered to be the only explanation; the possibility that genetic differences between colonies may al-so affect the level of the FIA-I aggJ.utinin in haemolymph is noted. A medium suitable for the in vitro culture ofl q. Ieachii haemocytes was deveJ-oped. q.. leachii haemocytes were found to bind and phagocytose untreated sheep erythrocytes. Binding was mediated by the HA-2 aggJ-utinin, as shown by the inhibitÍon of adhesion by lactose (which is specific for the HA-2 aggJ-utinin) and an anti-(HA-2) IgG preparation. ImmunoflIourescence studies indicated that HA-z moLecul-es were secreted by the haemocytes; these secreted molecul-es then coated unsensitised erythrocytes causing them to bind haemocytes. No ll{-2 agglutinin could be detected on the surface of the haemoiytes in the absence of erythrocytes but receptors for this molecule were detected. These results suggested that the HA-2 agglutinin could function as a recogni.tion molecu.l-e for particles bearing the appropriate carbohydrate moÍeties on their surface. At l-east one of the other two related proteins (HA-I and LBP-I) also existed on the surface of haemocytes. The function(s) of these molecules is not known. The above findings are discussed in relation to the two major . requirements of a defence system: efficient phagocytosis and the control- of sel-f reactivity. III The possibiJ-ity that a molecule with an opsonic function in a protochordate may be structurally related to immunogl-obulin was investigated by testing the abitity of the HA-2 agglut.inin to act as an opsonin for the recognition of particles by phagocytic cel-ls from a vertebrate. B. leachii haemolymph was found to mediate the adhesion and subsequent phagocytosis of sheep erythrocytes by mouse macrophages; the factor responsible was shown to be the HA-z agglutinin. The HA-I mol-ecule did not bind to macrophages. Both erythrocytes and macrophages could be sensitised for adhesion wj-th the agglutinin and in both instances sensitisation coul,d be reversed with lactose. Hence adhesion appeared to be caused by the aggJ-utinin cross-linking similar lactose-like determinants on the surfaces of both types of cell. There was no evidence to suggest any structural homology with immunogJ-obulin. This result is discussed in view of information on the structure of the HA-2 molecule and current ideas on the evolution of immunoglobuJ-in. ACKNOWLEDGEMENTS . I I wish to thank my supervisors, Dr Alan Butler and Dr Charles Jenkin for their guidence and encouragement during the course of lhis study. Special thanks are due to Dr Peter Ey; his constructive criticism and enthusiastic assistance wele much appreciated. I am grateful to Ann Hallett and NeaI Stead for the preparation of the graphs and line drawings, and to Philip Kempster for his excetlent work with the photographs. For the hours of statistical discussions and the use of his statistical programmes I thank RaIf Engler. I would also like to thank both Craig Procter, flor flrequently coltecting q. l-eachii colonies for ffie, and Dr John Casley-Snith for the use of his word processor. Finally I thank my parents and friends flor their kindness and support. vr, ABBREVIATIONS USED IN THIS THESIS. BCCM Bot lloides cell culture medium. BSA Eþvine serum albumin. t BSS Botrylloides salt solution. EDTA EthyJ-enediaminetetra-acetic acid di-sodium salt. EGTA EthylenegJ-ycol-bis (ß-amino-ethyl ether) N, N-tetra-acetic acid. GpRBC Guinea pig erythrocytes. HA-1 Haemagglutinin One (from B. leachii haemolymph). HA-2 Haemagglutinin Two (f,rom B. Ieachii haemolymph). HAU Haemagglutinating Unit. HEPES N -2-Hy droxye thy lpiperazine-N' -2-e thanesul fonic acid . IgG Immunoglobulin G. LBP-] Lactose Binding Protein Three (from B. leachii haemolymph). mol. wt. l'þIecular l,leight. 0.D. 0ptical Density. PBS Phosphate buffered sal-ine. Saline o.L54 M NaCl. SDS Sodium dodecylsulphate. SDS-PAGE SDS polyacryJ-amide gel electrophoresis. SRBC Sheep erythrocytes. Tris Tris ( hydroxymethy I ) amino +nethane. TSA Tris buffered saline. CONTENTS. Page. ABSTRACT Ì STATEMENT .IV ACXNOI¿'ILEDGETENTS ABBREVIATIONS USED IN THIS THESIS .v1 Chapter l: INIRODUCTION l.I Introduction to the probJ-em I 1.2 Development of a theoretical framework 3 r.3 Evidence pertaining to the model 5 I .l.l The recognition of self . 6 I .3.2 The importance of phagocytosis in invertebrate defence 10 I.3.3 Discrimination by phagocytic cells: The possibiJ-ity of celÌ surface receptors I4 I.3.4 Recognition by phagocytic cells: The involvement of serum opsonj-ns 22 l-.4 Re-examination of the model 30 1.5 The experimental approach undertaken j-n an investigation of cell recognition in B. leachii 35 Chapter 2: I.4ATERIALS AND I'ETHODS 2.L Media and reagents 38 2.2 Collection and storage of animals .39 2.3 Preparation ofl ascidian specimens for dissection and identification 39 2.4 CoIIection of ascidian haemolymph .40 2.4.I B. leachii and Botry1lus sp. .. 40 2.4.2 -otherãsclbian @ . .40 2.5 PreparatÍon of erythrocytes 4L 2.6 Haemagglutination assays 4I 2.7 Inhibition of haemagglutination by sugars .42 Page. Chapter 2: Ì"IATERIALS AND t'ETl-ÐDS cont. 2.8 Concentration of samples by uJ-trafliltration 43 2.9 Iodination of proteins 43 2.10 Column chromatographY 43 2.LO.I Sephacryl 5-200 chromatography of haemolymph 43 2.LO.2 Sephacryl 5-100 chromatography of purified agglutinins ::"::".. 44 2.II Puriflication of agglutinins from B. leachii and Botryllus sp. haemolymph .. ;. .- 44 2.I2 Pteparation of isokinetic sucrose gradients 46 2.lf Immunochemical analysis .. 48 2.L3.1 Rocket immunoelectrophoresis 48 2.L3.2 Ouchterlony tests .. 49 2.L3.f Staining procedure 49 2.L4 Yertebrate cell cul-ture .. 49 2.L4.1 Mouse macrophage monoJ-ayers 49 2.L4.2 Sensitisation of erylhrocytes 50 2.L4.f Adhesion of erythrocytes to macrophage monolayers .. 50 2.L4.4 In vitro phagocytosis assay 50 2.15 Radio-labelling erythrocytes 5I 2.L6 CLearance of radiolabelled erythrocytes from the circulation of mice 51 2.17 Solutions for handling B. leachii haemocytes .. .52 2.L1 J BotryIloides salt sõIulÏõñTBSS) :. .52 2.L7.2 Boe¡Vfmmæ cell bulture medium (BCCM) .53 2.I8 B. leachii haemocyte culture .54 2.L6.r-preparation of coverslips for cell culture 54 2.L8.2 Haemocyte monolayers .. .54 2.LB.f Adherence of sheep erythrocytes to ascidian haemocytes .. 55 2.L9 Production of antisera 55 2.2O Purífication of rabbit IgG .. 56 2.2L Innunofluore scence 56 2.2L.I Fluorescein isothiocyanate (FITC) labelling of agglutinins and IgG .. 56 2.2L.2 Fixation of cells for immunofLuorescence .57 2.2L.f Fixation of fluorescent labelled cells 57 Page. Ch t 3: A COMPARISON OF THE HAEMqGGLUTININS FROM A VARIETY l¡lI THE HA N S 3.I Introduction .. 58 3.2 The haemagglutinins found in the haemolymph of a number of ascidian species .. .. 60 3.3 Sephacryl 5-200 fractionations 62 3.3.I The fractionation of Botryllus sp. haemolymph .62 3.3.2 The fractionation of Polycarpa papilJ-ata haemolymph .
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