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Investigation of Cancerous Tissues by MALDI Mass Spectrometry Imaging - Imaging of Proteolytic Activity in Frozen Tissue and Standardised On- Tissue Digestion

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Investigation of Cancerous Tissues by MALDI Mass Spectrometry Imaging - Imaging of Proteolytic Activity in Frozen Tissue and Standardised On- Tissue Digestion Aus dem Institut für Medizintechnologie der Universität Heidelberg und der Hochschule Mannheim (Geschäftsführender Direktor: Prof. Dr. med. Norbert Gretz) Investigation of Cancerous Tissues by MALDI Mass Spectrometry Imaging - Imaging of proteolytic activity in frozen tissue and standardised on- tissue digestion Inauguraldissertation zur Erlangung des akademischen Grades Doctor scientiarum humanarum (Dr. sc. hum.) der Medizinischen Fakultät Mannheim der Ruprecht-Karls-Universität zu Heidelberg vorgelegt von Katrin Miriam Erich aus Bad Dürkheim a.d.W. 2019 Dekan: Prof. Dr. med. Sergij Goerdt Referent: Prof. Dr. rer. nat. Carsten Hopf Für meine Tochter und meinen Ehemann, die viel Zeit opferten und mich stets unterstützen… TABLE OF CONTENT Page ABBREVIATIONS ....................................................................................................... 1 1 INTRODUCTION .................................................................................................... 3 1.1 Classification of Proteases ............................................................................ 3 1.1.1 The role of proteases in disease ................................................................... 5 1.1.2 Relevant proteases in gastric cancer ............................................................ 6 1.2 Visualization of protease activity.................................................................... 8 1.3 Mass Spectrometry ........................................................................................ 9 1.3.1 The principle of MALDI mass spectrometry..................................................10 1.3.2 MALDI MS Imaging ......................................................................................10 1.3.3 The current method for tissue preservation ..................................................11 1.3.4 On-tissue digestion for MALDI MSI ..............................................................12 1.3.5 Data processing and statistical analysis in MALDI MSI ................................16 2 AIMS .................................................................................................................... 17 3 MATERIALS AND METHODS .............................................................................. 18 3.1 Materials ...................................................................................................... 18 3.2 Tissue samples and ethics approval ............................................................ 23 3.3 Sample Preparation Methods ...................................................................... 24 3.3.1 Preparation of tissue for monitoring endogenous protease activity ..............24 3.3.2 Adaptation of a tissue protease activity assay (TPAA) .................................27 3.3.3 Monitoring protease activity in a gastric tumour mouse model and human biopsy ....................................................................................................................29 3.3.4 Tissue preparation for quantitative proteomics analysis of mouse tissue extracts ....................................................................................................................29 3.3.5 MALDI Matrix application .............................................................................30 3.3.6 Preparation of FFPE tissue for the development of statistical scores ...........31 3.4 MALDI MS imaging data acquisition methods ............................................. 33 3.5 Data processing and statistical methods ..................................................... 35 3.5.1 Statistical analysis for digests by endogenous proteases in mouse stomach .. ....................................................................................................................35 3.5.2 Data processing for FFPE-tissue trypsin digests score development ...........36 I 4 RESULTS ............................................................................................................. 38 4.1 Part I – Visualisation of tissue protease activity using MALDI MSI .............. 38 4.1.1 Development of a score for ideal application of the substrate ......................38 4.1.2 Evaluation of substance P as a universal substrate .....................................39 4.1.3 Time-course of substance P digestion by endogenous tissue proteases .....41 4.1.4 Inhibitor-concentration dependency of proteolytic activity in porcine tissue ..52 4.1.5 Development of a photometric tissue-protease activity assay (TPPA) ..........55 4.1.6 Proteolytic activity of tumorous and non-tumorous tissue.............................57 4.1.7 Proteolytic activity of human gastric biopsy samples ....................................67 4.2 Part II - Development of scores for the assessment of quality factors using FFPE tissue digest ............................................................................................... 71 4.2.1 Score for digest efficiency DE% ...................................................................71 4.2.2 Scores for repeatability and homogeneity ....................................................75 5 DISCUSSION ....................................................................................................... 82 5.1 Optimised substrate application with water sensitive paper test .................. 82 5.2 Mean spectra analysis is restricted to homogeneous tissue ........................ 83 5.3 Observation of C-terminally cleaved substance P peptides ......................... 84 5.4 Development of tissue protease activity assay ............................................ 84 5.5 Imaging of endogenous tissue protease activity by MALDI MSI in clinical routine .................................................................................................................. 85 5.6 A first idea of active proteases..................................................................... 88 5.7 Assessment of the proteolytic tissue analysis in human gastric tumour ...... 89 5.8 Scores for FFPE tissue digests and evaluation of the best FFPE on-tissue digestion method .................................................................................................. 91 6 CONCLUSION ..................................................................................................... 94 7 SUMMARY ........................................................................................................... 95 8 REFERENCES ..................................................................................................... 97 9 PUBLICATIONS ................................................................................................. 114 10 CURRICULUM VITAE ........................................................................................ 115 11 ACKNOWLEDGEMENT ..................................................................................... 117 II Abbreviations ABBREVIATIONS ABC Ammonium bicarbonate ABPP Activity-based protein profiling ACC 7-amino-4-carbamoylmethylcoumarin ACE Acetylcholinesterase ACN Acetonitrile AEBSF 4-(2-aminoethyl)benzenesulfonyl fluoride hydrochloride AMC Asp-7-amino-4-methyl-coumin BCA Bicinchoninic acid BSA Bovine serum albumin CHCA Α-cyano-4-hydroxycinnamic acid CMC Carboxymethyl Cellulose CV Coefficient of variation ddH2O Ultra-pure water DHB 2,5-dihydroxybenzoic acid DMSO Dimethyl sulfoxide ECM Extracellular matrix EDTA Ethylenediaminetetraacetic acid ESI Electrospray ionisation EtOH Ethanol FA Formic acid FFPE Formalin-fixed paraffin-embedded FRET Fluorescence resonance energy transfer FT-ICR Fourier Transform Ion Cyclotron Resonance FWHM Full-width half maximum GIST Gastrointestinal stromal tumour H&E Hematoxylin & Eosin HC Hierarchical clustering HCl Hydrochloric acid IQR Inter-quartile-range ITO Indium Tin Oxide LC-MS/MS Liquid Chromatography-Tandem Mass Spectrometry LFQ Label-free quantification m/z Mass to Charge MAD Mean absolute deviation MALDI Matrix-assisted laser desorption/ionization MeOH Methanol MMP Matrix metalloprotease MRI Magnetic Resonance Imaging MS Mass Spectrometry MSI Mass Spectrometry Imaging NIR Near-infrared ON Overnight PBS Phosphate buffered saline PCA Principal Component Analysis 1 Abbreviations PET Positron emission tomography PIM Protease-inhibitor mixture qPCR Quantitative polymerase-chain reaction RG RapiGest SF Surfactant ROI Region of interest RT Room temperature S/N Signal-to-Noise ratio SDS Sodium dodecyl sulfate SOP Standard operating procedure TCA Trichloroacetic acid TCEA- CEA424-SV40TAg transgenic mice (C57BL6 background) with positive developed tumour TCEP Tris(2-carboxyethyl)phosphine TFA Trifluoroacetic acid TGGA The cancer genome atlas TIC Total Ion Current TIMP Tissue matrix metalloprotease inhibitor TOF Time of Flight TPAA Tissue protease activity assay WHO World health organisation WT Wild-Type 2 Introduction 1 INTRODUCTION 1.1 Classification of Proteases The enzyme class ‘hydrolases’ and their subclass ‘peptidases’ (EC 3.4.-.-), defined by the Enzyme Commission in 1961, comprise any enzyme that hydrolyzes peptide bonds (synonyms: peptide hydrolase, protease, proteinase)1,2. The class is further divided into ‘exopeptidases’, which act at the terminus of the substrate’s polypeptide chain and ‘endopeptidases’ that act internally in the polypeptide chain. Several sub-subclasses are defined, for example for exopeptidases: aminopeptidases (EC 3.4.11.-) that liberate a single amino acid at the N-terminus or dipeptidyl-peptidases and tripeptidyl- peptidases liberating two and three amino acids, respectively
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