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Innate Immune Response in the Streptococcus Suis Infected CSF Compartment University of Veterinary Medicine Hannover Institute for Physiological Chemistry Innate immune response in the Streptococcus suis infected CSF compartment: Role of DNases and antimicrobial peptides THESIS Submitted in partial fulfilment of the requirements for the degree DOCTOR OF PHILOSOPHY (PhD) awarded by the University of Veterinary Medicine Hannover by Marita Meurer Hamburg Hannover, Germany 2020 Supervisor: Prof. Dr. Maren von Köckritz-Blickwede Nicole de Buhr, PhD Supervision Group: Prof. Dr. Maren von Köckritz-Blickwede Prof. Dr. Peter Valentin-Weigand Prof. Dr. Christoph G. Baums 1st evaluation: Prof. Dr. Maren von Köckritz-Blickwede Institute of Physiological Chemistry Department of Infectious Diseases University of Veterinary Medicine Hannover, Germany. Prof. Dr. Peter Valentin-Weigand Institute for Microbiology Department of Infectious Diseases, University of Veterinary Medicine Hannover, Germany. Prof. Dr. Christoph G. Baums Institute of Bacteriology and Mycology Centre for Infectious Diseases Faculty of Veterinary Medicine, University Leipzig, Germany 2nd evaluation: Prof. Dr. Ilse D. Jacobsen Research Group Microbial Immunology Leibniz Institute for Natural Product Research and Infection Biology; Hans Knöll Institute, Jena, Germany Day of final exam: 22.10.2020 Parts of the thesis have already been published previously at scientific meetings, conferences or journals: Oral presentations: Meurer M.; Öhlmann S.; Bonilla M. C.; Valentin-Weigand P.; Beineke A.; Hennig-Pauka I.; Schwerk C.; Schroten H.; Baums C. G.; von Köckritz-Blickwede M.; de Buhr N. “Role of nucleases as NET evasion factor during Streptococcus suis meningitis” Graduate School Day of the University for Veterinary Medicine Hannover, Bad Salzdethfurth 2019 Poster presentations: Meurer M.; Öhlmann S.; Valentin-Weigand P.; Beineke A.; Baums C. G.; von Köckritz- Blickwede M.; 2, de Buhr N. “In vivo characterization of Streptococcus suis nuclease SsnA as NET evasion factor during meningitis in piglets” Fourth N-RENNT Symposium on Neuroinfectiology, Hannover 2018 Meurer M.; Öhlmann S.; Valentin-Weigand P.; Beineke A.; Baums C. G.; von Köckritz- Blickwede M.; de Buhr N. “Formation of neutrophil extracellular traps during Streptococcus suis meningitis in piglets in vivo: Evasion by nuclease SsnA?” Tagung der DVG-Fachgruppe Physiologie und Biochemie, Vienna 2018 Meurer M.; Öhlmann S.; Valentin-Weigand P.; Beineke A.; Baums C. G.; von Köckritz- Blickwede M.; de Buhr N. „Analyse von neutrophilen DNA-Netzen und Nukleasen während einer Streptococcus suis Meningitis beim Schwein“ Tagung der DVG-Fachgruppe Bakteriologie und Mykologie, Hannover 2018 Meurer M.; Öhlmann S.; Valentin-Weigand P.; Beineke A.; Baums C. G.; von Köckritz- Blickwede M.; de Buhr N. “Neutrophil extracellular traps (NETs) during Streptococcus suis meningitis in piglets in vivo: Host mediated stabilization against bacterial nucleases?” 4th German Pneumococcal Symposium, Berlin 2018 Meurer M.; Öhlmann S.; Valentin-Weigand P.; Beineke A.; Schroten H.; Baums C. G.; von Köckritz-Blickwede M.; de Buhr N. “Neutrophil extracellular trap formation in the Streptococcus suis infected cerebrospinal fluid compartment” Graduate School Day of the University for Veterinary Medicine Hannover, Hannover 2018 Meurer M.; Öhlmann S.; Valentin-Weigand P.; Beineke A.; Schroten H.; Baums C. G.; von Köckritz-Blickwede M.; de Buhr N. “Neutrophil extracellular trap formation in the Streptococcus suis infected cerebrospinal fluid compartment” Zentrumstag des Zentrums für Infektionsmedizin, Hannover 2019 Meurer M.; de Buhr N.; Unger L. M.; Bonilla M. C.; Seele J.; Nau R.; Baums C. G.; Gutsmann T.; Schwarz S.; von Köckritz-Blickwede M. Testing cathelicidin susceptibility of the meningitis pathogens Streptococcus (S.) suis and Escherichia (E.) coli in culture medium versus porcine or human cerebrospinal fluid 9th International Meeting on Antimicrobial Peptides (IMAP) Utrecht 2019 Publications [see Chapter 5]: Meurer M.; de Buhr N.; Unger L. M.; Bonilla M. C.; Seele J.; Nau R.; Baums C. G.; Gutsmann T.; Schwarz S.; von Köckritz-Blickwede M. “Comparing Cathelicidin Susceptibility of the Meningitis Pathogens Streptococcus suis and Escherichia coli in Culture Medium in Contrast to Porcine or Human Cerebrospinal Fluid” Frontiers in Microbiology, January 2020, Volume 10, Article 2911., doi: 10.3389/fmicb.2019.02911 Meurer M.; Öhlmann S.; Bonilla M. C.; Valentin-Weigand P.; Beineke A.; Hennig-Pauka I.; Schwerk C.; Schroten H.; Baums C. G.; von Köckritz-Blickwede M.; de Buhr N. “Role of bacterial and host DNases on host-pathogen interaction during Streptococcus suis meningitis” International Journal of Molecular Sciences, July 2020, 21, 5289; doi:10.3390/ijms21155289 Sponsorship: Marita Meurer was funded by the German Research Foundation [Deutsche Forschungsgemeinschaft e.V. (DFG; KO 3552/7-1)] within the framework of the PhD program “Animal and Zoonotic Infections” of the Hannover Graduate School for Veterinary Pathobiology, Neuroinfectiology, and Translational Medicine (HGNI). Meiner Familie Index List of Abbreviations ............................................................................................................. VIII 1 Summary ............................................................................................................................. 1 2 Zusammenfassung ............................................................................................................... 3 3 Introduction ......................................................................................................................... 5 3.1 Neutrophil Granulocytes .............................................................................................. 5 3.1.1 Antimicrobial Peptides in Neutrophil Granulocytes ............................................ 7 3.1.2 Neutrophil Extracellular Traps ............................................................................. 7 3.1.3 DNases ............................................................................................................... 11 3.2 Antimicrobial Peptides .............................................................................................. 13 3.2.1 Cathelicidins ....................................................................................................... 15 3.2.2 Cathelicidins in pigs and humans ....................................................................... 15 3.2.3 Methods for testing the antimicrobial activity of AMPs .................................... 17 3.3 Meningitis .................................................................................................................. 18 3.3.1 Brain barriers ...................................................................................................... 20 3.3.2 Models for the investigation of infected brain barriers ...................................... 21 3.3.3 Streptococcus suis as meningitis pathogen ........................................................ 23 4 Aims of the study .............................................................................................................. 27 5 Results ............................................................................................................................... 29 5.1 Optimized cell culture model of the porcine BCSFB ................................................ 29 5.2 DNases modulate immune response .......................................................................... 32 5.3 S. suis is not susceptible to the cathelicidins LL-37 and PR-39 ................................ 35 6 Discussion ......................................................................................................................... 38 6.1 DNases during S. suis meningitis .............................................................................. 39 6.2 Relevance of physiological test systems ................................................................... 45 6.3 Future Outlook ........................................................................................................... 53 6.4 Concluding Remarks ................................................................................................. 54 7 References ......................................................................................................................... 55 8 Affidavit ............................................................................................................................ 67 9 Acknowledgement ............................................................................................................ 68 List of Abbreviations % Percentage µg Microgram µL Microliter µm Micrometer 3D Three dimensional AMP Antimicrobial peptide AST Antimicrobial susceptibility testing BBB Blood brain barrier BCSFB Blood cerebrospinal fluid barrier BLMB Blood leptomeningeal barrier Ca2+ Calcium ions CA-MHB Cation adjusted Mueller-Hinton Broth CAMP Cathelicidin antimicrobial peptides CLSI Clinical and Laboratory Standards Institute CNS Central nervous system CO2 Carbon dioxide CPS Capsule antigen CSF Cerebrospinal fluid DAPI 4′,6-Diamidin-2-phenylindol DMEM Dulbecco’s Modified Eagle’s Medium DNA Deoxyribonucleic acid DNase Deoxyribonuclease E. Escherichia EF Extracellular factor ELISA Enzyme-linked immunosorbent assay EMA Emergency Management Agency EndA Endonuclease A EndAsuis Endonuclease A of S. suis EUCAST European Committee on Antimicrobial Susceptibility Testing FDA Food and Drug Administration hCAP Human cathelicidin antimicrobial
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