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Investigation of the Sialidases of Periodontal Pathogens

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Investigation of the Sialidases of Periodontal Pathogens Investigation of the Sialidases of Periodontal Pathogens By: Andrew Frey A thesis submitted for the degree of Doctor of Philosophy The University of Sheffield School of Clinical Dentistry Unit of Oral and Maxillofacial Pathology 31/08/2016 1 I. Contents II. List of Figures ................................................................................................................... 6 III. List of Tables .............................................................................................................. 10 IV. Acknowledgements .................................................................................................... 11 V. Abbreviations ................................................................................................................. 12 VI. Abstract ...................................................................................................................... 14 1 Chapter 1: Introduction ................................................................................................. 16 1.1 Teeth and major oral diseases ............................................................................... 16 1.1.1 Periodontitis ................................................................................................... 16 1.1.2 Periodontitis-A Considerable Burden ............................................................ 18 1.2 Periodontitis-Aetiology .......................................................................................... 19 1.2.1 Bacterial Colonisation of the Periodontium and its Role in Periodontitis ..... 19 1.2.2 The Importance of Inflammation in Periodontitis ......................................... 23 1.2.3 Other Factors in Periodontitis Onset and Progression .................................. 37 1.3 Periodontitis-Systemic influences .......................................................................... 38 1.3.1 Head and Neck Cancer ................................................................................... 38 1.3.2 Heart Disease and Atherosclerosis ................................................................ 39 1.3.3 Rheumatoid Arthritis...................................................................................... 39 1.4 Treatment of Periodontitis .................................................................................... 40 1.5 Virulence Factors of the Periodontal Pathogens ................................................... 41 1.5.1 Porphyromonas gingivalis .............................................................................. 41 1.5.2 Tannerella forsythia ....................................................................................... 43 1.5.3 Fusobacterium nucleatum.............................................................................. 46 1.5.4 Biofilm Formation .......................................................................................... 48 1.6 The Anti-Virulence Approach ................................................................................. 51 1.7 Sialic Acid, Sialidases, and Virulence ...................................................................... 52 1.7.1 Sialic Acid ....................................................................................................... 52 1.7.2 Sialidases ........................................................................................................ 53 1.7.3 Sialic Acid in the Oral Cavity ........................................................................... 56 1.7.4 Sialic Acid and the Immune System ............................................................... 56 1.7.5 Sialidases of Periodontal Pathogens .............................................................. 58 2 1.8 Sialidase Inhibition ................................................................................................. 63 1.8.1 Viral Sialidase-The Driving Force Behind Inhibitor Development .................. 63 1.8.2 Sialidase Inhibitors ......................................................................................... 63 1.8.3 Sialidase Inhibition-Potential Impact on Virulence ........................................ 64 1.8.4 Sialidase Inhibition-Impact on the Host Immune Response .......................... 65 1.8.5 Aims and Hypothesis-The Prospect of Sialidase Inhibitors as a Treatment for Periodontitis ................................................................................................................... 65 2 Chapter 2: Biochemical Characterisation of Periodontal Pathogen Sialidases .............. 68 2.1 Introduction-The Sialidases of P. gingivalis and T. forsythia ................................. 68 2.2 Materials and Methods- Biochemical Characterisation of Periodontal Pathogen Sialidases ............................................................................................................................ 69 2.2.1 Bacterial Strains, Growth Conditions, and Plasmids ...................................... 69 2.2.2 Sialidase Activity of Whole Bacteria............................................................... 71 2.2.3 DNA Extraction ............................................................................................... 72 2.2.4 Polymerase Chain Reaction (PCR) .................................................................. 72 2.2.5 Restriction Endonuclease Digestion of Plasmid DNA or PCR products .......... 73 2.2.6 DNA Ligation .................................................................................................. 73 2.2.7 Bacterial Transformation ............................................................................... 74 2.2.8 Protein Production and Purification by Affinity Chromatography................. 75 2.2.9 BCA Assays ..................................................................................................... 77 2.2.10 Sodium Dodecyl Sulphate-Poly Acrylamide Gel Electrophoresis (SDS-PAGE) 78 2.2.11 Biochemical Studies of Sialidases and Sialidase Subunits .............................. 79 2.2.12 Structural Characterisation of NanH -Crystal Trials ....................................... 82 2.3 Results .................................................................................................................... 83 2.3.1 Bioinformatic Analysis of NanH and SiaPG .................................................... 83 2.3.2 Production of SiaPG-CBM, SiaPG-CT, and NanH-CT ..................................... 102 2.3.3 Production of Periodontal Pathogen Sialidases: NanH and SiaPG ............... 116 2.3.4 Expression and Purification of Other Enzymes ............................................ 127 2.3.5 Sialidase Protein Production-a Summary..................................................... 129 2.3.6 Biochemical Characterisation of Purified Periodontal Pathogen Sialidases 131 2.3.7 Inhibition of Periodontal Pathogen Sialidases by Zanamivir ....................... 148 2.4 Discussion ............................................................................................................. 156 2.4.1 pH, Pathogen Sialidases, and Periodontitis ................................................. 156 2.4.2 The Importance of Sialic Acid Linkage preference for T. forsythia .............. 159 3 2.4.3 The Importance of Sialyl Lewis Ligands for T. forsythia ............................... 162 2.4.4 T. forsythia NanH- the RIP Motif of the Catalytic Domain is Essential for Catalysis, and the N-terminal CBM is involved in Ligand Binding ................................ 162 2.4.5 Zanamivir Inhibits Periodontal Pathogen Sialidases .................................... 163 2.5 Summary .............................................................................................................. 164 3 Chapter 3: Investigating the Targeting of Host Sialoglycans by Periodontal Pathogens- the Effects on Growth and Biofilm Formation, and the Impact of Zanamivir ..................... 168 3.1 Introduction ......................................................................................................... 168 3.2 Materials and Methods- Investigating the Targeting of Host Sialoglycans by Periodontal Pathogens- the effects on Growth and Biofilm Formation, and the Impact of Zanamivir ......................................................................................................................... 171 3.2.1 Enzyme synergy in Sialic Acid Release from Salivary Mucin ........................ 171 3.2.2 Bacterial Strains and Growth Conditions ..................................................... 171 3.2.3 Collection and preparation of Human Saliva ............................................... 172 3.2.4 Culture of Periodontal Pathogens on Defined Media Supplemented with Host Sialic Acid Sources ............................................................................................... 173 3.2.5 Biofilm Assays............................................................................................... 173 3.3 Results .................................................................................................................. 174 3.3.1 Release of Sialic Acid from Mucin glycoproteins by Periodontal Pathogen Sialidases is enhanced by T. forsythia Sialate-O-Acetylesterase ................................. 174 3.3.2 P. gingivalis is Capable of Growth Utilising Host Glycoproteins as Sole Carbon and Nitrogen Sources, and this is Enhanced by NanS .................................................. 178 3.3.3 Biofilm Formation of Periodontal Pathogens on Host Glycoproteins, and
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