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Fasciola Hepatica McDougall, H.C. (2012) Identifying “hidden” antigens in the liver fluke, Fasciola hepatica. PhD thesis. http://theses.gla.ac.uk/3661/ Copyright and moral rights for this thesis are retained by the author A copy can be downloaded for personal non-commercial research or study, without prior permission or charge This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Glasgow Theses Service http://theses.gla.ac.uk/ [email protected] 1 Identifying “hidden” antigens in the liver fluke, Fasciola hepatica Heather Catherine McDougall BSc Hons (Zoology) Submitted in the fulfilment of the requirements for the degree of Doctor of Philosophy at The University of Glasgow Research carried out at The Moredun Research Institute, Edinburgh 2 Abstract Fasciola hepatica is responsible for substantial economic losses and animal welfare issues within the agricultural sector worldwide. The increasing incidence of fasciolosis, coupled with the emergence of flukicide resistance, makes vaccination an attractive alternative control strategy. Hidden antigens extracted from the gut of blood feeding parasites have proven to be excellent vaccine candidates against haematophagous parasites, most notably Haemonchus contortus and Rhipicephalus (Boophilus) microplus. Here, as a first step towards a prototype liverfluke vaccine an attempt to identify hidden gut antigens in F. hepatica was made. Proteomic analysis on extracts of adult F. hepatica was used to identify molecules exclusively found within the membrane-bound fraction including four proteases; cathepsin B2, legumain- 2, a putative lysosomal pro-x-carboxypeptidase precursor and a saposin-like protein. Histological sections of adult F. hepatica were screened with a panel of 21 lectins to identify those with an affinity for glycoproteins on the parasite’s gut and to inform subsequent lectin affinity chromatography. Seven lectins showed affinity for the gut region, with peanut (PNA) and jacalin (JAC) lectins binding to glycoproteins on either the gastrodermal cells or gut lamellae, respectively. PNA and JAC were then used to purify glycoproteins from the crude S3 extract by affinity chromatography. The resultant fractions were separated by SDS-PAGE and the protein profiles analysed by mass spectrometry. The enriched lectin-binding fractions shared a number of proteins but one of note that was exclusively identified in the PNA- binding fraction was a cathepsin D-like aspartyl protease, which had not previously been studied in F. hepatica. The proteolytic activities of three somatic extracts of adult F. hepatica were therefore investigated. The ability of the respective fractions to digest haemoglobin, a potential food source, was measured in the presence/absence of class-specific enzyme inhibitors. These analyses confirmed the presence of cathepsin D-like aspartyl protease activity capable of digesting haemoglobin optimally at pH 2 - 2.5. Further characterisation of the cathepsin D-like aspartyl (FhCatD) protease revealed it to be highly conserved within trematodes, to be localized to the gastrodermis of immature (10 day) and adult fluke, and to be more highly expressed, at the RNA level, in the Newly Excysted Juveniles (NEJ) than adult stages. Western blot analysis of native somatic extracts, enriched lectin-binding fractions and recombinant FhCatD using antisera from naturally infected sheep, showed some recognition of the recombinant FhCatD but did not provide clear evidence that the cathepsin D is strongly antigenic during natural infection. 3 Table of Contents Abstract ....................................................................................................................................... 2 List of Tables............................................................................................................................... 8 List of Figures ............................................................................................................................. 9 Acknowledgements ................................................................................................................... 12 Author’s declaration .................................................................................................................. 13 Abbreviations ............................................................................................................................ 14 1 General Introduction ......................................................................................................... 18 1.1 Fasciola hepatica .................................................................................................. 20 1.2 Liver fluke Life-cycle ............................................................................................ 20 1.3 Pathogenesis and Clinical Signs ............................................................................ 23 1.3.1 Acute Fasciolosis ................................................................................................ 23 1.3.2 Sub-acute Fasciolosis .......................................................................................... 24 1.3.3 Chronic Fasciolosis ............................................................................................. 24 1.4 Control and treatment of Fasciolosis ..................................................................... 25 1.4.1 Pasture management............................................................................................ 25 1.4.2 Snail control ........................................................................................................ 25 1.4.3 Treating infected animals .................................................................................... 26 1.5 Immunology .......................................................................................................... 28 1.5.1 The host immune system ..................................................................................... 28 1.5.2 The host immune response to infection with F. hepatica ................................... 29 1.5.3 Parasite evasion of immune attack ...................................................................... 31 1.5.4 Immunity to infection with F. hepatica .............................................................. 33 1.5.5 Vaccination ......................................................................................................... 34 1.5.6 Vaccination against helminth parasites: Conventional and “Hidden” antigens .. 40 4 1.5.7 The gut of Fasciola hepatica .............................................................................. 42 1.5.8 Project Aims ........................................................................................................ 46 2 Application of proteomics to identify proteins enriched within a membrane-bound fraction of adult Fasciola hepatica ........................................................................................... 48 2.1 Introduction ........................................................................................................... 48 2.2 Materials and Methods .......................................................................................... 52 2.2.1 Analysis of somatic extracts by Liquid Chromatography - Electron Spray Ionisation -Tandem Mass Spectrometry (LC - ESI - MS/MS) ......................................... 52 2.2.2 Laser capture microscopy ................................................................................... 55 2.3 Results ................................................................................................................... 58 2.3.1 Somatic extracts from adult F. hepatica ............................................................. 58 2.3.2 LC- ESI-MS/MS ................................................................................................. 59 2.3.3 Transcripts located within the gut of Fasciola hepatica ..................................... 63 2.4 Discussion ............................................................................................................. 66 3 Exploiting lectins to purify gut antigens from somatic extracts of Fasciola hepatica ..... 70 3.1 Introduction ........................................................................................................... 70 3.2 Materials and methods ........................................................................................... 72 3.2.1 Parasites............................................................................................................... 72 3.2.2 Lectin Screen on histological sections ................................................................ 72 3.2.3 Preparation of somatic extracts from F. hepatica ............................................... 75 3.2.4 Lectin probing of somatic extracts ...................................................................... 75 3.2.5 Lectin affinity purification .................................................................................. 76 3.3 Results ................................................................................................................... 77 3.3.1 Lectin probing of histological sections ..............................................................
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