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Immunological Mechanisms of the Horseshoe Crab, Limulus Polyphemus John Irvin Stagner Iowa State University

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Immunological Mechanisms of the Horseshoe Crab, Limulus Polyphemus John Irvin Stagner Iowa State University Iowa State University Capstones, Theses and Retrospective Theses and Dissertations Dissertations 1974 Immunological mechanisms of the horseshoe crab, Limulus polyphemus John Irvin Stagner Iowa State University Follow this and additional works at: https://lib.dr.iastate.edu/rtd Part of the Zoology Commons Recommended Citation Stagner, John Irvin, "Immunological mechanisms of the horseshoe crab, Limulus polyphemus " (1974). Retrospective Theses and Dissertations. 5172. https://lib.dr.iastate.edu/rtd/5172 This Dissertation is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Retrospective Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. 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Xerox University Microfilms 300 North Zeeb Road Ann Arbor, Michigan 48106 75-10,507 STAGNER, John Irvin, 1944- IMMUNOLOGICAL MECHANISMS OF THE HORSESHOE CRAB, LIMULUS POLYPHEMUS. Iowa State University, Ph.D., 1974 Zoology Xerox University Microfilms, Ann Arbor, Michigan asios 0 1975 JOHN IRVIN STAGNER ALL RIGHTS RESERVED THIS DISSERTATION HAS BEEN MICROFILMED EXACTLY AS RECEIVED. Immunological mechanisms of the horseshoe crab, Limulus polyphemus by John Irvin Stagner A Dissertation Submitted to the Graduate Faculty in Partial Fulfillment of The Requirements for the Degree of DOCTOR OF PHILOSOPHY Department: Zoology and Entomology Major: Zoology (Physiology) Approved: Signature was redacted for privacy. Chargé of/Major Work Signature was redacted for privacy. For the Major Department Signature was redacted for privacy. For the Graduate College Iowa State University Ames, Iowa 1974 Copyright ©John Irvin Stagner, 1974. All rights reserved. ii TABLE OF CONTENTS Page ABBREVIATIONS iv INTRODUCTION ' 1 LITERATURE REVIEW 3 flATERIALS AND METHODS 20 Animal Collection and Maintenance 20 Collection of Hemolymph and Hemocytes 21 Production of Hypodermal Gland Exudate 21 Preparation of Antibodies and Antibody Tests 23 Gel Chromatography 23 Lysozyme Assay 24 Disc Electrophoresis 25 Bactericidal Preparations and Bactericidal Assays 25 Hemocyte Cultures and Phagocytosis 27 Cellular Encapsulation 28 Protein and Carbohydrate Assays 29 Physical and Chemical Analysis of the Exudate 30 Scanning Electron Microscopy 31 Light Microscopy and Staining 32 Circulatory System 33 Tests for Agglutination 34 Alteration of iii vivo Concentrations of Hemocytes and Blood 34 Protein iii Page RESULTS 36 DISCUSSION 112 SUMMARY AND CONCLUSIONS 127 LITERATURE CITED 131 ACKNOWLEDGMENTS 141 APPENDIX: TABLES 142 iv ABBREVIATIONS Aa Antilysate antibody Hg Hypodermal gland Ag Agglutinin Hm Hepatomarginal trunk Ah Antihemolymph antibody Hw Hemolymph (whole, acellular) AT Anterior lateral artery Is Intestinal sinus Am Anterior marginal artery Isa Inferior spinal artery Ba Bacteri a LI Lysate fraction I Bav Branchial afferent vessel LII Lysate fraction II Be Branchial efferent vessel Lv Lateral ventral vessel Bsa ' Bovine serum albumin M Muscle Bv Blood vessel Mc Median connecting vessel C Crayfish cuticle Mv Median ventral vessel Ca Capsule N Nerve Cr Carmine red Nc Nerve cord Es Esophagus Or Oral ring Gd Gland duct Pa Pseudomonas atlantica G1 Gut lumen PI Posterior lateral artery H Heart Pm Posterior marginal artery HI Hemolymph fraction I Ss Superior spinal artery HI I Hemolymph fraction II Va Ventral aorta Ha Hepatic artery Vs Dorsoventral sinus ric Hemocyte Hcl Hemolymph (clotted) Hey Hemocyani n 1 INTRODUCTION While immunity in vertebrates has been extensively studied, the inves­ tigation of invertebrate immune capabilities has only recently begun. In­ vertebrates extant today have achieved astounding diversity and must have successfully coped with pathogens for millions of years during their evo­ lution to their present state of development. Other than phagocytosis in some phyla, little is known about the defense mechanisms of invertebrates. Much of the difficulty in investigations has been due to the use of anti­ gens which are not found in the animal's habitat, the use of strictly mam­ malian immunological techniques, and the persistent but erroneous search for antibodies and complement as found in vertebrates. No immunity con­ ferring globulins have been found in invertebrate phyla (Briggs, 1964; Gotz, 1973; Hildemann and Reddy, 1973). The study of invertebrate immune systems is important for several rea­ sons. Academically it is important to further investigate the evolution of the inmune response in order to understand the mechanisms involved in both vertebrate and invertebrate systems. Proteins and carbohydrates vary among groups of invertebrates (Acton et al., 1973; Hunt, 1970; Katzman and Jeanloz, 1969). These substances may be characterized and compared struc­ turally and functionally to provide a system to classify animals by chemi­ cal and functional homology. By such investigations, the phylogenetic re­ lationships between animals may be determined with more certainty and by means other than morpr.ology or several often controversial criteria. On an applied level, the importance of determining the immune mechanisms of in- veriecrazes and. If possible, reinforcing them becomes important as man 2 turns more to the sea for food and learns to manage populations of inverte­ brates for purposes of mariculture. This study was undertaken to determine whether a primitive arthropod, Limulus polyphemus which has existed since the Ordovician period (Moore, 1959), has inmune capabilities and to compare them with other, more re­ cently evolved arthropods. 3 LITERATURE REVIEW Until recently the acceptance of an invertebrate immune system or cap­ ability has not been widespread. However, it is clear that invertebrates have been successful in combating pathogens throughout their evolutionary history. Within the last five to six years, reports of invertebrate immune capabilities neve begun to appear in the literature. This sudden influx of positive reports is due to the use of antigens which are common to the experimental animal's habitat and are not completely foreign pathogens which the animal would never encounter. Another reason for success is the abandonment of the search for vertebrate antibody or vertebrate immune sys­ tems among the invertebrata. It is only when one adapts vertebrate insnuno- logical techniques to suit an invertebrates's physiology that any success or degree of reliability can be achieved (Johnson and Chapman, 1970). The actual definition of an immune response should be broad and be based on the functional aspects of the response, namely the recognition of self and not-self and a response to foreign materials by phagocytosis or cellular products which will stop or inhibit an infecting pathogen. The recognition of self has oeen shown to exist at all phylogenetic levels both among vertebrates (Quinn, 1968) and invertebrates {Hildemann and Reddy, 1973; Kahan and Reisfeld, 1972). Several excellent review articles are available by the latter authors and Sparks (1972) regarding inverte- Drate immunology. It has been snown that the cells of cifferent species of sponges will not reaggregate into functional colonies (Hildemann and Reddy, 1973). 4 Such a phenomenon was due to self-recognition at the cell surfaces. A large glycoprotein has been implicated in controlling the reaction and the encapsulation of xenografts (Cheng et al., 1968). Cnidarlans and annelids are known to reject allografts and xenografts (Kahan and Reisfeld, 1972). Annelids have also been shown (Bailey et al., 1971) to possess
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