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Immunoglobulins of the Lizard, Tiliqua Rugosa

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Immunoglobulins of the Lizard, Tiliqua Rugosa I M MUIL.OSI.OBULIN€I OF EH E LIZÀRÐ, TILIQUA RUGOSA. A thesls submitted to the Unlversity oi Adelaide for the degree of L\octor of Philosophy. by tohn David Wetherall, B-Sc' (Sydney) Department of Microbiology, University of J\delaide - fune, 1969. (f i) TABLE OF CONTENTS (iii) Summary Statement ... (vii) (viü) Abbreviations useci in text CHAPTER l. INTRODUCTION : PI{YLOGEIfY OF ANTIBOÐY PRODUCTION. I CHAPTER 2. INTROÐUCTION : PEIYLOGEITY OF IMMUNOGLOBULIN STRUCTURE. 39 66 CHAPTER 3. IVTATERI,ALS AND fuIETHODS 91 CHAPTER 4. KINETICS OF AÀITIBODY PRODUCTION .. ' CHAPTERS.PREPARAIIoNANDCHARÀCTERISATIoN OF Î.I7.ARD IMMUNOGLOBULINS. lIU CHAPTER 6. STUDIES ON REDUCEÐ TEARD IMMUNOGTOBULINS 141 CHAPTER 7. SOME BIOLOGICAL PROPERTIES OF LUARD IMMUNOGT, OBUTINS t54 17I CHAPTER B. DISCUSSIOIV AND CONCLUDING REMAR¡GS Appendix I. Computer program for calculaLing molecular weights from high speeci sedimentalion equili:-.rrium data . k) (xii) Acknowledgements (xiii) BibliographY (iii) SUMMARY The work described in this thesis consists of two parts. The first part is corìcerned with the immune response of the lizard' Til-iqua rugosa. to the antigens, Salmonella tvphimurium' rat erythrocytes and bovine serum albumi¡ (BSA). The second paft pertains to the isolation and subsequent characterlsation of Ilzard immunoglobulins which contained antibody activity' The antigens mentioned above were found to be immunogenic in &liqua and the formation of humoral antibody was observed' The klnetics of humoral antibody production by this lizard were less vigorous than the correspondtng mammallan responses and were lnfluenced by the envlronmental temperature at which the llzards were maintained. Both the rate of production, and the quantity of anLibody produced fn lizards injected with -Úiþ!rylum or BSA and maintalned at 20o were decreased relative to the response to tltese immunogens at 30o. Lizards injected witþ BS.\ and maintained at either 250 or 30o prociuced the sarne ultimate antibody titre although this took longer to attain at ihe lower temperature ' The catabolic humoral half }ives of purified lizard immunoglobullns were measured and lt was found that the thermodynamic effect (iv) of temperature on protein biosynthesis could not account for the observed immune response of lizards maintained at 20o to either S. tvphimurium or BSA. The lizard synthesised two types of antibody which were readlly dÍstinguishable by their size, (rapÍdly and slowly sedimenting), and susceptibility to reduction with thiols. Immunoglobulins containing antibodles against the immunogens mentioned above were isolated from lizard serum. These purified immunoglobulins were then characterised- It was found that the two puriffed }izard immunoglobulins, whilst antigenically related. were not antigenically identical. The existence of at least tipo classes of lfzard immunoglobulin was thus indicated. Thls hypothesls was substantlated by physico- chemÍcal characterlsation of the immunoglobullns and their constituent Iight and heavY chains. The larger immunoglobulin was a macroglobulin, tlile properties of which were very simllar to those of mammalian 7M ¡ it was designated tizarci 'yM'. Light and hear,ry polypeptide chains could be detecteci in a reduce,l and alkylateci preparation of lizard '7M" Starch gel electrophoresis and a molecular weight cietermination indlcated that the heavy chain of lizard 'yIvI' was similar to the (") mammallan p chain : the lizarci heavy chain was designated a 'Þ' chain on this basis. The smaller iromunoglobulin was a 7S gloiculin which ln many respeÖts was anAlogous to rnammalian yG. It was designated lizarcÍ '?G'. Although lizard '.yM' And mammalian yM were very similar, slgnÍficant differences between lizard '7G' and mam¡nalian yG were observed. When examined by electrophoresis llzard 'yG' had the mobilÍty of a fast y or p globulin. Human yG has a slower mobility and is termed aT2T}lmmunoglobulin. In this respect lizard'7G' pig mouse resembleci the ?I 7G immunoglobulins found in guinea and serum and more recently observed in rabbit serum' Lizard,yG,insalinesolutlonwasfoundtoformaggregates.This reaction was pH dependent and a homogeneous preparation wi'cir respect to size could be cbtainecÍ by decreaslng the pH of the solvent to 6 ' i) or less, or also by aading zllvl urea or 4M guanld-ine hydrochloride to the solverrt. The s|. of lÍzarci 'yG' Ín the presence of 4M urea ¿tJ rw- - '¡¡as 6 .95 . AnLibo<1y, specific for BSA, 'ui¡as isolated from i:he serum of hyperimmunized llzards uslng an insoluble immunoadsorbent' Thls anlibody was shown to possess identical propertles to the purified (vi) lizard'yGt immunoglobulin preparatlon. Lizard immunoglobulins were found to ext¡ibtt opsonic acdvity and promoted the phagocytosis of several anLigens ' In conclusÍon, it has been shown that:- antlbodies; (i) the lizard, -Illlggg-Igggs.A, is capable of synthesising (i¡) antibody production in this species was dependent on the ambient temPerature; 0fi) at least two classes of lizard lmmunoglobr'tltn exist and each may manifest anttbodY activitY; and (iv) the physicochemlcal properties of the purified llzard immuno- globutlns suggest that they are analogous to marimalian yM and YG immunoglobullns ' --o0o-- (vif) This thesis contains no materlal which has been accepted for the award of any other degree or diploma in any UniversiËy and to the best of my knor,vledge and bellef it contalns no materlal previously pubtisheci or written by another person, except when due refererrce is made in the text of the thesis. (I. D. \Metherall) ]une, 1969. (vlii) ABBREVATIONS USED IN TEXI. where posstble abbrevfations, symbols and conventlons recommended by the Editorial Board of the Biochemlstry Journal have been used. Temperatures referrecl tc are in ciegrees Celsius ' The Vforlci i]ealth Organisatlon nomenclature has been used for nrarnmalian imrnunoglobulins, ancl an analcgous nomenclature has been adopted fcr lcwer vertebrate immunc-¡glcbulins since thelr synthesls ls ccntrclled by related genes ' AdcltË.onal abbrevlaticns usect have been clefineci where they first occur ln the text. The following list of abbrevfaLions has been included for convenience. Ab antibodY. AR analYtical reagent ' BCG Bacille calmette - Guerin strain of Mvcobacterium tuberculosls . BGG i:ovine gämma globulln' BSA bovine serum albumin ' CFA comPlete Freund's adjuvant ' CM - cellulose carbox¡¡methyl cellulose ' c'S0complementunitbase<ion5i]%haemolysls. cpm radioactive counts per mf nute ' DEAE-cetlulose diethylamtnoethyl cellulose' EÐtrA ethylened.iamlnotetraacetate ' (ix) El-"/' extincLlon coefficient of ¿ !"/" solution measured r cm' in a I cm. cuvette. H healry chain of an immunoglobulin' ILS fmmunlzed lizard serum' i'm' I trroamuscular or intramuscularly' IM) or intraperitoneally' i:p'IP) I trroaperitoneal KLH keYbole ltmPet hEemocYanin' L light chain of an immunoglobulin' Ioq^T anttbody titres have een reported either as the dilution 'z used(".s.I:l28lorasthelogarithm(base2)ofthe clilution (e . g. Loø rT = 7') ' M molar concentration ' z-ME 2, mercaPtoethanol ' p micron (rÛ-6 meffe)' OD oPtical densitY ' PCA pyrrolicì-2-one-5-carbo>rylic acld' ' PVC PolY,zinYlchloride ' RALantisenrmraisedinrabbitstowholelizardserum. S Svedberg unÍts (I0-I3 seconds)' ,2G.* standard sedimentatlon coefficient' coefficient at infÍnite dilution' "zo,* ^tandardÞ sedimentatlon SDG sucrose density gradlent ultracentrifugation' TCA trichloracetic acld' tris tris (hydro:<vmethyl) aminomethane' tris-HCl buffer a trÍs + hydrochloric acid buffer' pH 8'0' whlch ls0.osMwtthrespecttotris.HClandwhichcontalns 0.20M sodium chlorlde' -1- CHAPTER I Paqe A. PREAI\4BLE 2 B.PHH.oGENETICoRIGINSoFAI{TIBoDYPRoDUcTIoN 3 (i) ÐefinÍtÍon of antibodY -.. '. 3 (fi) PhylelÍc capacity for antibody production " ' 4 (iii) Andbody production within subphylum vertebrata 6 (iv) Evolution of the immune response " ' l5 C. DISSECTION OF AIVTIBODY PRODUCTION IN LOWER VERTEBRÀTES ... .. ". 2A (i) The influence of environnrental temperature on antibodY Prociuction 2T (ii) Evidence for immunological anamnesis ' " 32 (iii) Immuncgenicity in lower vertebrates 35 -2- A. PREAÀ4BTE A phylogenetic approach to -rriological problenis has yielded a great deal of information which is not restrlcted solely to comparatlve biology. A comparative exanrination of certaln bÍological systems has demonstrateci that there is a sLroi;g selective pressure to retaln functional integrily. This is well illusirateci by a Çornparison of Èhe prlmary structures of various polypeptlde chains. An often quoted example is the primarf structure of the haemoglobin polypeptide chalns; ceriain sequences of amino aclds a.re preserved in all specles desplte varfabiliry in o¡her portlons of the molecule. Further, if representaLives of various livlng species are examined, less highly evolved structure- function relatlonships can often be found in lower vertebrates and invertebrates. these have provided moclels which are more amenable to experimentation than the systems found in the rnore higtùy evolved species. The efficacy of this approach is well demonstrated by the extensive studles of bacteria and thelr vlruses which have led to great advances in our understanding of molecular biology in general. The overall complexiry of the antlbody response in mammals has led to a more fundamental expertmental approach to this subJect. It is the hope of finding less complex experir¡rental mociels anci of gaining a better apprecÍatlon of the selective advantages of the immune response that has prompted the
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