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Fasciola Hepatica Hemoglobin: Isolation, Characterisation and Induction of Protective Immune Response in Cattle

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Fasciola Hepatica Hemoglobin: Isolation, Characterisation and Induction of Protective Immune Response in Cattle Fasciola hepatica hemoglobin: isolation, characterisation and induction of protective immune response in cattle Thesis presented for the degree of PhD by Sharon Me Gonigle under the supervision of John P. Dalton, PhD. School of Biological Sciences Dublin City University January 1996 I hereby certify that this material, which I submit for assessment on the programme of study leading to the award of PhD is entirely my own work and has not been taken from the work of others save to the extent that such work has been cited and acknowledged within the text of my work. Signed: r i e Date: IG f s f iCib Sharon Me Gonigle Date: To Brigid & Jimmy Me Gonigle Acknowledgements I wish to thank Dr. John P. Dalton for giving me the opportunity to persue this PhD. Thanks for your encouragement, enthusiasm and guidance over the past four years. Thanks to ail in JDs lab, both past and present, for your help, patience and friendship, especially to Paul and Andrew who were there as long as I was. Thanks also to Leda, Angela, John Me, Pepe, Sandra, Ciaran, Aengus, Mary and Susan for all the good times and the unforgettable lab outings. A special thank you to all the post grads in DCU for helping make my time here so enjoyable! In particular I’d like to thank Teresa, Louise and Barbara for their support, encouragement and friendship and for all the crack we had! long may it continue! My sincere thanks also to Anna Marie Turley for being a constant source of support and friendship over the years. Finally, I wish to dedicate this thesis to my parents Brigid & Jimmy, and my family, Philip and Paula, Neil and Maeve, Anne Marie (the best sister in the world), Paul and Stephen, for their patience, encouragement and support throughout the years. Contents Abstract 1 Abbreviations 2 1. Introduction General introduction: life cycle of F hepatica 5 Development of F. hepatica in the primary host: morphological, antigenic and biochemical changes 7 Invertebrate hemoglobins: structural classification 11 Annelid hemoglobins 13 Nematode hemoglobins 15 Platyhelminth hemoglobins 19 Oxidative damage and antioxidants 21 Effects of host oxidants on parasites 25 Protection against oxidative damage 28 Antioxidant enzymes in parasites 30 Superoxide dismutase 31 Catalase 33 Glutathione peroxidase 34 Glutathione S-transferase 36 Novel antioxidant family 41 2. Isolation and characterisation of F. hepatica hemoglobin 2.1 Materials 46 2.2 Methods Preparation of ES products from mature liver flukes 47 Purification of hemoprotein from ES 47 Extraction of hemoprotein from mature liver flukes 48 Polyacrylamide gel analysis of hemoprotein 48 N-terminal sequence determination 48 Light absorption spectra 49 Preparation of hemoprotein antiserum, immunoblotting and ELISA 49 Immunolocalisation studies 50 2.3 Results Purification of hemoprotein 51 Analysis of hemoprotein by electrophoresis 51 N-terminal sequence determination 54 Spectral properties 54 ELISA studies 57 Immunolocalisation studies 59 3. Efficacy of hemoglobin as a vaccine against liver fluke infection 3.1 Materials 63 3.2 Methods Preparation of antigens for vaccine trial 64 Formulation and administration of vaccines 64 Vaccination of cattle 64 Parasite challenge 65 Analysis of antibody response by ELISA 65 Immunoblot analysis of cattle antibody responses 65 Liver enzyme analysis 66 Assessment of protection 66 Estimation of egg viability 66 3.3 Results Purification of vaccine components 68 Studies of immune response by ELISA 68 Immunoblot studies of antibody response 71 Liver enzyme analysis 71 Assessment of protection 74 Viability of recovered eggs 76 4. Immunoscreening of F. hepatica cDNA library and identification of clones 4.1 Materials 79 4.2 Methods Immunoscreening of F. hepatica X gt11 cDNA expression library 80 Preparation of X lysates and isolation of DNA 81 PCR analysis of X DNA 81 Subcloning of PCR fragments 82 Screening of recombinant plasmids 83 Sequencing of plasmid DNA 84 Preparation of fusion protein 84 Preparation of radiolabelled DNA probe 84 Isolation of RNA and northern blotting 85 Assay of mature fluke extract for novel antioxidant activity 87 Time course analysis of antioxidant protection of glutamine synthetase from inactivation by thiol iron oxidation system 87 4.3 Results Immunoscreening of F. hepatica cDNA library and analysis of isolated clones by PCR and restriction digestion 88 Subcloning of phage inserts 90 Sequence analysis of clone D6 90 Sequence analysis of clone B1 90 Expression of fusion protein by clone B1 92 Northern analysis 95 Antioxidant activity of mature fluke extract 95 Time course analysis of antioxidant activity 95 D iscussion Purification and characterisation of liver fluke hemoglobin 102 Cattle vaccine trials with liver fluke hemoglobin 110 Isolation of cDNA clones encoding liver fluke enzymes 120 Conclusion 132 Bibliography 134 A p p e n d ix 161 Abstract A hemoprotein released in vitro by Fasciola hepatica was purified by gel filtration chromatography on Sephacryl S200 followed by ion exchange chromatography on DEAE sepharose. Absorption spectra studies characterised the molecule as hemoglobin. N-terminal amino acid sequence analysis revealed no similarity between the F. hepatica hemoglobin and other vertebrate or invertebrate hemoglobins. Immunolocalisation studies demonstrate that the hemoglobin is present in the vitelline glands and excretory tubules of mature flukes. The hemoglobin was shown to be highly immunogenic in F. hepatica infected bovines. Hemoglobin was included in a cattle vaccine trial to determine its immunoprophylactic potential. Vaccination with partially purified hemoglobin (Hf) yielded a significant level of protection (43.8%) against challenge infection. Protective immunity was increased to 72.4% when Hf was combined with the liver fluke cysteine protease CL2. Vaccination with Hf and CL2 also resulted in reduced liver damage as assessed by serum GLDH and 7GT. Furthermore, eggs recovered from both vaccine groups showed reduced viability. This anti-embryonation effect of vaccination was particularly evident in the group that received Hf / CL2 where >98% of recovered eggs did not embryonate to miracidia. Although both vaccine preparations induced high antibody titres which were boosted following the challenge infection, there was no correlation between antibody titre and protection. The results of these trials demonstrate that Hf and CL2 could form the basis of a molecular vaccine that would not only reduce parasite burden but would also prevent transmission of liver fluke disease. Using sera from cattle vaccinated with Hf to screen an adult F. hepatica cDNA library, genes encoding p tubulin and the novel antioxidant, peroxiredoxin were isolated. The presence of these proteins in the immunising fraction may have contributed towards the induction of the protective response. Peroxiredoxin activity was demonstrated in fluke extracts as the ability to protect glutamine synthetase from oxidative damage by mixed iron thiol oxidation systems. The antioxidant enzyme may play an important role in protecting against oxidative stress in the fluke. 1 Abbreviations AhpC Alkyl Hydroperoxide peroxidase AhpF Alkyl hydroperoxide reductase ADP Adenine diphosphate ATP Adenine triphosphate BCA Bicinchoninic acid BCG Bacille Calmette-Guerin BCIP 5-bromo-5-chloro-3-indolyl phosphate BSA Bovine serum albumin cDNA complementary DNA CL2 Cathepsin L2 DAB 3,3’-diaminobenzidine hydrochloride DEAE Diethylaminoethyl DEPC Diethylpyrocarbonate DTT Dithiothreitol E 64 L-trans-epoxysuccinyl-leucylamido-[4-guanidino]-butane EDTA Ethylenediaminetetraacetic acid ELISA Enzyme linked immunosorbant assay EPO Eosinophil peroxidase ES Excretory / Secretory products g Acceleration due to gravity FCA Freunds complete adjuvant FIA Freunds incomplete adjuvant FITC Fluorescein isothiocyanate GPx Glutathione peroxidase GR Glutathione reductase GSH Glutathione GSSG Glutathione disulphide GST Glutathione S-transferase HEPES N-[2-hydroxyethyl] piperazine-N’[2-ethanesulphonic acid] Hf Hemoglobin fraction yiFN y Interferon IL Interleukin 2 IPTG lsopropyl-(3-D-thiogalactopyranoside LFH Liver fluke homogenate MPO Myeloperoxidase MSL Muscle stage larvae NBL Newborn larvae NBT Nitro blue tetrazolium NEJ Newly excysted juvenile NK Natural killer NKEF Natural killer enhancing factor PAG Proliferation associated gene PAGE Polyacrylamide gel electrophoresis PBS Phosphate buffered saline PCR Polymerase chain reaction PMSF Phenylmethylsulphonylfluoride PVDF Polyvinylidine difluoride (Problott) QAE Quaternary aminoethyl ROOH Hydroperoxide ROS Reactive oxygen species SDS Sodium dodecyl sulphate SOD Superoxide dismutase TH T helper cell P TNF p Tumour necrosis factor T-PBS 0.1% Tween 20 in PBS TPx Thioredoxin peroxidase TR Thioredoxin reductase Tris Tris [hydroxymethylj-aminomethane TSA Thiol-specific antioxidant XGal 5-bromo-4-chloro-3-indolyl-p D-galactopyranoside 3 Chapter 1 Introduction 4 General Introduction: life cycle of Fasciola hepatica The parasitic helminth, Fasciola hepatica, is the causative agent of fascioliasis, or liver fluke disease. The disease is most common in sheep, cattle and goats, but a wide range of mammalian hosts have been reported, including humans. The WHO estimates that 2 million people have become infected with this fluke due mainly to eating contaminated watercress and other aquatic plants (Maurice, 1994). Recent reports indicate that F hepatica is a major human pathogen in South America and China (Mas-Coma and Barques, 1990), and isolated cases of human infection have also been reported
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