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The Immunomodulatory Properties of L-Rhamnose

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The Immunomodulatory Properties of L-Rhamnose The Immunomodulatory Properties of L-Rhamnose Mimmi Lundahl M.Sc. Immunology Supervisors: Prof. Ed Lavelle and Prof. Eoin Scanlan Report prepared for the degree of Doctor of Philosophy, Immunology School of Biochemistry and Immunology, School of Chemistry Trinity Biomedical Sciences Institute Trinity College Dublin 2020 I hereby certify that this report is entirely my own work, and that the contents have not been published elsewhere in paper or electronic form unless indicated through referencing. i Abstract L-Rhamnose is a non-mammalian monosaccharide ubiquitously found on the surface of both commensal and pathogenic bacteria. Previous publications had identified that L-rhamnose-rich Mycobacterium tuberculosis glycolipids, and their structural derivatives, pHBADs, were able to aid this pathogen’s ability to escape immune elimination by repressing protective immune responses. A key immune cell for combatting M. tuberculosis is the macrophage, an innate immune cell present in essentially all tissues. A distinguishing feature of macrophages is their polarisation combined with plasticity; the ability to adopt distinct phenotypes. These are simplified into the pro-inflammatory and bactericidal, “classically activated” M1 macrophages and the “alternatively activated” Th2-promoting and anti-inflammatory M2 macrophages. To combat M. tuberculosis, M1 macrophage activation is critical. In the research presented herein, it is demonstrated that L-rhamnose skews macrophage polarisation away from a bactericidal phenotype and enhances M2 characteristics. Furthermore, it is revealed that L-rhamnose is capable of inducing macrophage innate memory, causing responses elicited by subsequent stimuli, a week after L-rhamnose incubation, to yield a more anti-inflammatory and anti-bactericidal profile. This is presented both as induction of the regulatory cytokine IL-10, as well as reduced expression of iNOS mRNA. To relate these immunomodulatory properties back to the bacteria, two synthetic chemistry strategies were employed: the conjugation of L-rhamnose onto bacteria-sized particles and the synthesis of pHBAD analogues. The first strategy was used to mimic the bacterial surface presentation of the sugar as a more biorelevant model to investigate immunomodulation by L- rhamnose. The second strategy was used to investigate whether L-rhamnose was an essential structural element for pHBADs to induce immunomodulation. Whilst a particle conjugation protocol was developed, the optimised conditions were not translatable between manufactured batches of particles and thus this strategy had to be abandoned. On the other hand, by investigating synthetic pHBAD analogues it was confirmed that L-rhamnose indeed does confer immunomodulatory properties to the molecule. Summarily, it appears that L-rhamnose confers M. tuberculosis with immunomodulatory properties that protects it from macrophage bactericidal responses. This information can be used in future research, not only to target L- rhamnose containing compounds to ameliorate suffering caused by M. tuberculosis, but also by using L-rhamnose as a starting point, this research could lead to the discovery of more immunomodulatory compounds. ii Abbreviations # 2-DG; 2-deoxy glucose A-B AA; Antimycin-A Abs; absorbance aCD3; anti-CD3 ADCC; antibody-dependent cell-mediated cytotoxicity AKT; protein kinase B ARDS; acute respiratory distress syndrome Arg1; arginase 1 ASGPR; asialoglycprotein receptor ATP; adenosine triphosphate BALF; broncho-alveolar lavage fluid BCG; Bacillus Calmette-Guerin BMDCs; bone marrow-derived DCs BMDMs; bone marrow-derived macrophages BSA; bovine serum albumin C-D C3; complement component 3 CD, cluster of differentiation cGAS; cyclic GMP-AMP synthase COX-2; cyclooxygenase-2 CpG; CpG oligodeoxynucleotide 1826 CR3; complement receptor 3 CT; cycle threshold CTL; cytotoxic T cell CTLA-4; cytotoxic T-lymphocyte-associated Protein 4 DAMPs; danger-associated molecular patterns DAP12; DNAX activating protein 12kDa DC; dentritic cell DCM; dichloromethane Dectin; DC-associated C-type lectin DesTCR; Désiré T cell receptor iii DLS; dynamic light scattering DMEM; Dulbecco’s Modified Eagle Medium dNTPs; deoxy nucleotides triphosphates E-F EAE; experimental autoimmune encephalomyelitis EDC; 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide EDTA; ethylenediaminetetraacetic acid ELISA; enzyme-linked immunosorbent assay ESI; electrospray ionisation ETC; electron transport chain EVLP; ex vivo lung perfusion FACS; fluorescent-activated cell sorting FCCP; carbonyl cyanide-p-trifluoromethoxyphenylhydrazone FCS; foetal calf serum FcγR; Fcγ receptor Fizz1; found in inflammatory zone 1 OR resistin-like alpha G-H G-CSF; granulocyte-colony stimulating factor D-GlcNAc; N-acetyl D-glucosamine GLUT1; glucose transporter 1 H37Rv; Gamma-irradiated whole cells of Mycobacterium tuberculosis, strain H37Rv H3K4me3; histone H3 lysine 4 trimethylation HEK; human embryonic kidney cell line Hib; Haemophilus influenzae Type B HIF-1α; hypoxia-inducible factor 1α HMBC; heteronuclear multiple bond correlation HPRA; Health Products Regulatory Authority HRMS; high-resolution mass spectrometry HRP; horseradish-peroxidase HSQC; Heteronuclear Single Quantum Correlation I-J IBD; inflammatory bowel disease IC50; 50% of maximal inhibitory concentration IFNβ; interferon beta IFNγ; interferon gamma iv Ig; Immunoglobulin IL; interleukin IL-13R; IL-13 receptor IL-4R; IL-4 receptor iNOS; inducible nitric oxide synthase INT; tetrazolium salt IR; infrared IRF; interferon regulatory factor ITAM; immunoreceptor tyrosine-based activation motif ITIM; immunoreceptor tyrosine-based inhibitory motif JAK; janus kinase L-M LDH; lactate dehydrogenase LPS; lipopolysaccharide MALDI; matrix assisted laser desorption ionisation ManLAM; mannose-capped lipoarabinomannan MCP1; monocyte chemotactic protein 1 M-CSF; macrophage colony-stimulating factor M-CSFR; macrophage colony-stimulating factor receptor MFI; mean fluorescence intensity Mgl; macrophage galactose-type C-type lectin MHC I; major histocompatibility complex class I MHC II; major histocompatibility complex class II MIP-2; macrophage inflammatory protein-2 m-p-a; methyl-p-anisate MR; mannose receptor MTA; 5′-methylthioadenosine mTOR; mechanistic target of rapamycin mTORC; mTOR complex MyD88; myeloid differentiation primary response 88 N-O NAD+; nicotinamide adenine dinucleotide NADH; nicotinamide adenine dinucleotide NED; N-1-napthylethylenediamine dihydrochloride NF-κB; nuclear factor kappa-light-chain-enhancer of activated B cells v NHDF; normal human dermal fibroblasts NHS; N-hydroxysuccinimide NK cell; natural killer cell NLRP3; NLR family pyrin domain containing 3 NMR; nuclear magnetic resonance NOD; non-obese diabetic NOD-2; nucleotide-binding oligomerization domain-containing protein 2 OD; optical density OPD; O-phenylenediamine dihydrochloride OVA; ovalbumin oxphos; oxidative phosphorylation P-Q PALS; phase analysis light scattering PAM3CSK4; tripalmitoyl-S-glyceryl-cysteine PAMPs; pathogen-associated molecular patterns PBMC; peripheral blood monocyte PBS; phosphate buffered saline, pH 7.4 PCR; polymerase chain reaction PDI; polydispersity index PDIM; phthiocerol dimycocerosate PD-L2; programmed cell death 1 ligand 2 PEG; polyethylene glycol PGE2; prostaglandin E2 PGL; phenolic glycolipid pHBAD; para hydroxybenzoic acid derivative pIA; pHBAD I analogue PIM; phosphatidyl-myo-inositol mannosides PLA; poly(lactic acid) PLGA; poly(lactic-co-glycolic acid) PPARγ; peroxisome proliferator-activated receptor gamma PRR; pattern-recognition receptor qPCR; quantitative real-time PCR Q-Tof; Q-Tof Premier Waters Maldi-quadrupole time-of-flight R-S L-Rha; L-Rhamnose vi RnaseOUT; Ribonuclease Inhibitor RNS; reactive nitrogen species ROS; reactive oxygen species Rot; rotenone RPMI; Roswell Park Memorial Institute RT; reverse transcription SHP; SH2 domain-containing protein tyrosine phosphatases Siglec; sialic acid-binding immunoglobulin-like lectin STING; cGAS-stimulator of interferon genes SYK; spleen tyrosine kinase T-Y TGF-β; transforming growth factor beta Th; T helper cell TLC; thin layer chromatography TLR; toll-like receptor TNFα; tumour necrosis factor alpha Treg; regulatory T cell TRIF; TIR-domain-containing adapter-inducing interferon-β VEGFa; vascular endothelial growth factor alpha WGP; whole β-glucan particles WNV; west nile virus WT; wild type Ym1; chitinase-like protein 3 Publications M.L.E. Lundahl, E.M. Scanlan, E.C. Lavelle, Therapeutic potential of carbohydrates as regulators of macrophage activation, Biochem. Pharmacol. 146 (2017) 23–41. doi:10.1016/j.bcp.2017.09.003. D.D. Barnes, M.L.E. Lundahl, E.C. Lavelle, E.M. Scanlan, The Emergence of Phenolic Glycans as Virulence Factors in Mycobacterium tuberculosis, ACS Chem. Biol. 12 (2017) 1969–1979. doi:10.1021/acschembio.7b00394. vii Acknowledgements First and foremost I want to thank my two supervisors Ed and Eoin; you both have shown me the utmost respect, given credit when it was due and most importantly believed in me throughout. You gave me chances to improve, and provided guidance, help and support when it was needed. Thank you both for giving me the opportunity to grow into the researcher, presenter and writer I am today, someone with the confidence to face even greater challenges, and to keep learning. To everyone past and present in the Scanlan Lab, thank you for making me feel welcome when I started and for teaching me synthetic chemistry – especially Danielle and Moss – I would have been lost in the columns and NMRs without all of
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