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The Group a Streptococcus M1T1 Clone Post-Transcriptionally Modifies Innate Immune Signalling to Promote Infection

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The Group a Streptococcus M1T1 Clone Post-Transcriptionally Modifies Innate Immune Signalling to Promote Infection Doctor of Philosophy The Group A Streptococcus M1T1 clone post-transcriptionally modifies innate immune signalling to promote infection by Amelia Soderholm Bachelor Science (Honours) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2018 School of Chemistry and Molecular Biosciences ABSTRACT Streptococcus pyogenes, the Group A Streptococcus (GAS), is the most common cause of bacterial pharyngitis in children and adults. Host innate and adaptive immune responses mediate defence against streptococcal pharyngitis and are also central to the clinical manifestation of the disease. The ability of GAS to invade the host and establish infection likely involves subversion of host immune defences, however the signalling pathways and immune responses elicited during streptococcal pharyngitis, particularly by epithelial cells, are currently not well understood. This thesis focuses on characterising the inflammatory responses of primary human tonsil epithelial (TEpi) cells during intracellular infection with two distinct GAS strains; the laboratory-adapted M6 strain JRS4 and the M1T1 clinical isolate 5448. M1T1 is a globally-disseminated GAS clone that is the most commonly isolated serotype (approximately 20% of all isolates) in high income countries (1). This thesis aims to investigate innate immune responses triggered and/or subverted by these different GAS strains in order to uncover why the M1T1 strain is such a successful pathogen. The pharyngeal and tonsil epithelia are important components of innate immune defence against GAS infection. They primarily act as a physical barrier, but also secrete antimicrobial peptides and cytokines/chemokines that have direct antimicrobial effects and/or signal to immune cells. Previous studies have investigated epithelial immune responses to GAS infection by utilising a number of different cell types, largely immortalised and nonpharyngeal-derived cell lines such as HEp-2 and HaCaT cells, which may not respond in the same manner as pharyngeal cells to GAS infection. Nonetheless, several studies that have used tonsil explant tissue or pharyngeal-derived cell lines appear to be congruent with studies that have used nonpharyngeal cell lines to examine a number of immune mediators secreted in response to GAS infection. Next generation Illumina RNA sequencing was employed to characterise the inflammatory gene expression profile of JRS4- and 5448-infected TEpi cells during early intracellular infection, as reported in Chapter 4. I found that, whilst infection with either GAS strain induced the mRNA expression of a similar array of host inflammatory genes, the transcriptional response to 5448- infection was of a much higher magnitude compared to JRS4-infection. Sequential window acquisition of all theoretical fragment ion mass spectra (SWATH-MS) was also employed to characterise changes in the host proteome during early GAS infection, and proteins that significantly changed in abundance during 5448-infection consisted mainly of those involved in metabolic and trafficking pathways, as well as transcriptional regulation. 2 Work in Chapter 5 investigates the role of Streptococcus pyogenes Cell Envelope Protease (SpyCEP; also known as ScpC and PrtS) and its ability to dampen levels of secreted IL-8 during intracellular 5448-infection of TEpi cells. RNA sequencing detected a significant increase in IL-8 mRNA expression during JRS4- and 5448-infection, and pathway analysis revealed differentially expressed genes between mock and JRS4- or 5448-infected TEpi cells were enriched in transcription factor networks that regulate IL-8 expression, such as AP-1, ATF-2 and NFAT. Whilst JRS4-infection resulted in high levels of secreted IL-8, 5448-infection did not, suggesting that 5448 may post- transcriptionally dampen IL-8 production or accumulation. Infection with 5448ΔcepA, an isogenic mutant lacking the IL-8 protease SpyCEP, resulted in levels of secreted IL-8 that were comparable to JRS4 infection, whilst complementation of 5448ΔcepA significantly reduced IL-8 secretion by TEpi cells. These results suggest that intracellular infection with the pathogenic M1T1 strain 5448 induces a strong pro-inflammatory response in primary tonsil epithelial cells but is able to modulate this host response by the expression of SpyCEP, which selectively degrades IL-8. As IL-8 is a neutrophil- recruiting chemokine implicated in the host response to GAS, reducing IL-8 secretion may ultimately benefit GAS infection. Finally, in Chapter 6 the level of IL-6 production during GAS infection of TEpi cells was investigated. Both JRS4- and 5448-infection were found to induce IL-6 mRNA expression, however JRS4-infected TEpi cells secreted high levels of IL-6 in comparison to 5448-infected cells. By screening a collection of 5448-isogenic mutants I identified streptolysin O (SLO) as the GAS protein responsible for suppressing IL-6 secretion. Infection with 5448Δslo, an isogenic mutant lacking SLO, resulted in IL- 6 secretion at levels similar to that of JRS4-infected cells, whilst complementation of 5448Δslo significantly reduced IL-6 secretion during infection. 5448 was also found to induce significantly higher levels of haemolysis than JRS4, suggesting that the SLO-dependent effect on IL-6 may be due to a difference in SLO expression or activity during infection. Overall, this thesis characterises the transcriptome and proteome of TEpi cells during intracellular GAS infection and provides new insight into the roles of SpyCEP and SLO in host immune modulation during infection. I found that IL-8 secretion during 5448-infection was dampened by expression of the serine protease SpyCEP, an IL-8 protease whose production during intracellular infection of primary epithelial cells was previously not well defined. I also found that 5448 post- transcriptionally dampens host IL-6, and this effect was dependent on the expression of SLO; however, the mechanism by which SLO achieves this effect is as yet unknown. My fndings reinforce the hypothesis that the success of the M1T1 clone is due to its ability to modulate host inflammatory 3 responses to benefit infection. Better understanding of the host responses that mediate immunity to GAS infection should ultimately help facilitate the development of effective strategies to combat GAS pharyngitis. 4 DECLARATION BY AUTHOR This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis. I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my research higher degree candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award. I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School. I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis. Amelia Soderholm 1nd June, 2018 5 PUBLICATIONS DURING CANDIDATURE Yang Z, Soderholm AT, Wong Fok Lung T, Giogha C, Hill MM, Brown NF, Hartland E, Teasdale RD. 2015. SseK3 is a Salmonella effector that binds TRIM32 and modulates the host’s NF-κB signaling activity. PLoS ONE 10(9): e0138529. Barnett TC, Lim JY, Soderholm AT, Rivera-Hernandez T, West NP, Walker MJ. 2015. Host- pathogen interaction during bacterial vaccination. Current Opinion in Immunology 36:1-7. Soderholm AT, Barnett TC, Sweet MJ, Walker MJ. 2017. Group A streptococcal pharyngitis: immune responses involved in bacterial clearance and GAS-associated immunopathologies. Journal of Leukocyte Biology. 103:193-213. Soderholm AT, Barnett TC, Korn O, Rivera-Hernandez T, Seymour LM, Schulz B, Nizet V, Wells C, Sweet MJ, Walker MJ. 2018. Group A Streptococcus M1T1 intracellular infection of primary tonsil epithelial cells dampens levels of secreted IL-8 through the action of SpyCEP. Frontiers in Cellular Infection and Microbiology 8:160. Soderholm AT, Walker MJ 2018. A host proteome atlas of Streptococcus pyogenes. Cell Systems. 6:5, 536-538. 6 PUBLICATIONS INCLUDED IN THIS THESIS Soderholm AT, Barnett TC, Sweet MJ, Walker MJ. 2017. Group A streptococcal pharyngitis: immune responses involved in bacterial clearance and GAS-associated immunopathologies. Journal of Leukocyte Biology. Doi:10.1189/jlb.4MR0617-227RR. Incorporated into literature review in Chapter 1. Conceived Wrote and project edited Soderholm AT 10 70 (Candidate) Barnett TC 30 10 Sweet MJ 20 10 Walker MJ 40 10 Total 100 100 Soderholm AT, Barnett TC, Korn O, Rivera-Hernandez T, Seymour LM, Schulz BL,
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