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Anti-Inflammatory and Antibacterial Effects of Kinos from Australian and Papua New Guinean Eucalyptus Species

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Anti-Inflammatory and Antibacterial Effects of Kinos from Australian and Papua New Guinean Eucalyptus Species School of Pharmacy Anti-inflammatory and Antibacterial Effects of Kinos from Australian and Papua New Guinean Eucalyptus Species Martha Yahimbu Mungkaje This thesis is presented for the Degree of Doctor of Philosophy of Curtin University June 2015 DECLARATION To the best of my knowledge and belief this thesis contains no material previously published by any other person except where due acknowledgement has been made. This thesis contains no material which has been accepted for the award of any other degree or diploma in any university. …………………………………………………. June 16, 2015 ii ACKNOWLEDGEMENTS I would like to thank all the people who contributed to this Thesis in every way. First and foremost, I would like to thank my two supervisors, Dr Ricky Lareu and Dr Rima Caccetta for demanding a high quality of work in all my aspects of my PhD program and supporting my attendance at conferences. I would like to thank Dr Andrew S. McWilliam for his initial contributions towards my research. I would also like to thank Dr Simon Fox for his contributions for ensuring all reagents for my experiments were in stock at all times. Dr Connie Jackaman is thanked for her patience in training me on the use of flow cytometer. Ms Irma Larma-Cornwall assisted me with the analysis of the flow cytometry data for the phagocytosis assay. Dr Chi Ndi of University of South Australia is thanked for his assistance with the phytochemical screening of kinos. I would like to thank my fellow PhD colleagues, Mr. Wolfgang Wimmer and Mr. Alex Richards for always working together as a team solving problems related to cell culture, immunology and molecular biology. Ms. Angie Samec and Mr. Giuseppe Luna assisted me with the Microbiology aspects of my research and sub-fractionation of kinos work, respectively, in this thesis. I would like to thank Ms. Gaewyn Ellison for going out of her way from her busy schedule for her experiments for her PhD program to proof-read different chapters of my thesis. Ms. Sangeetha Mathavan, a PhD colleague and a very close friend is thanked for always working together to solve problems for each other‘s research and morally supporting each other. Without a sponsorship, I would not have studied at Curtin University and finally produce this thesis. I am very grateful to the Australian Government for giving me the Australian Leadership Award Scholarship that funded my tuition and living allowances during my 4 years PhD tenure. I would also like to thank the School of Pharmacy for giving me a fee waiver for 3 months when my 4 years sponsorship ended. Finally, I would like to acknowledge family and friends who supported me during my study. First and foremost, I would like to thank my husband and my two daughters, iii my mother, sisters, nephews and nieces for their constant love and support throughout this long academic journey. I would also like to thank Lydia Warubi, Jossie Bakri and Ericka Dawanincura for their friendship and support throughout my study period in Perth, Western Australia. I would like to dedicate this thesis to my late father, my mother who lived up to see the final end-product of this thesis despite having arthritis and my two daughters, Grace Boker Mungkaje and Catherine Autamin Mungkaje. iv LIST OF ABBREVIATIONS AND ACRONYMS Abbreviation/ Full name Acronym APH Acid phosphatase BSA Bovine serum albumin CLSI Clinical and Laboratory Standards Institute DCM Dichloromethane E Escherichia or Eucalyptus E. coli Escherichia coli ELISA Enzyme-linked immunosorbent assay EOs Essential oils E. calophylla Eucalyptus calophylla E. confertiflora Eucalyptus confertiflora ERK Extracellular-signal regulated kinase FACS Fluorescence-activated cell sorting FBS Foetal calf serum AF1 Acidic fraction 1 BF2 Basic fraction 2 DCMF3 Dichloromethane fraction 3 h Hour(s) IкB Inhibitory kappa beta IL Interleukin JAK Janus kinase JNK C-Jun N-terminal kinase LPS Lipopolysaccharide LRP Leukocyte common antigen-related phosphatase MAPK Mitogen-activated protein kinase MBC Minimum bactericidal concentration MHA Mueller-Hinton agar MHB Mueller-Hinton broth v LIST OF ABBREVIATIONS AND ACRONYMS CONTINUED Abbreviation/ Full name Acronym MIC Minimum inhibitory concentration Min Minute(s) μg/mL Microgram per millilitre mg/mL Milligram per millilitre μL Microlitre mL Millilitre NCCLS National Committee for Clinical and Laboratory Standards NF-кB Nuclear factor-kappa beta NO Nitric oxide ONOO- Peroxynitrite P. aeruginosa Pseudomonas aeruginosa pg/mL Picograms per millilitre PGN Peptidoglycan PNG Papua New Guinea(n) RA Rheumatoid arthritis RPMI Roswell Park Memorial Institute ROS Reactive oxygen species S. aureus Staphylococcus aureus TE Total kinos extract TLR Toll-like receptors TMB 3,5,3',5'-tetramethylbenzidine TNF-α Tumour necrosis factor alpha USFDA United States Food and Drug Administration WA Western Australia(n) vi ABSTRACT Kinos are astringent exudates from Eucalyptus species which are used by the first Australians to treat inflammatory conditions and bacterial infections. Tannins are the predominant chemical constituents in kinos as identified by the early investigations of kinos chemistry. The tannins and cathechins (constitutive of flavonoids), major groups of compounds are found in plants. Flavonoids are components of nutrition but have also been extensively investigated for their antimicrobial activities using in vitro and in vivo study models. However, limited antimicrobial studies have been conducted on kinos from Eucalyptus species and therefore, this study sets out to validate claims for their medicinal uses. The main goals were to investigate anti-inflammatory and antibacterial effects of kinos from Western Australian (WA) and Papua New Guinean (PNG) Eucalyptus species using in vitro study models. Kinos from Eucalyptus calophylla (WA) and Eucalyptus confertiflora (PNG) were solubilized in a water-based buffer. Murine RAW264.7 macrophages were used for anti-inflammatory and phagocytosis studies. Gram negative and Gram positive bacteria were tested for their susceptibility to kinos. The level of cytokine secretion by the kinos treated LPS-stimulated macrophages were measured by ELISA, whilst nitric oxide (NO) levels were measured by the Griess method. Phagocytosis was evaluated by fluorescent flow cytometry and antibacterial effects were determined by agar diffusion and microdilution methods. Phytochemical analyses of kinos were conducted using thin layer chromatography and qualitative tests. The RAW264.7 macrophage cells developed vacuoles after being exposed to kinos. The intensity of the vacuoles increased with increasing concentrations of kinos and incubation times. The vacuoles were more pronounced in cells exposed to WA kinos than to the cells exposed to the PNG kinos. The cells were 100% viable for the kinos concentrations lower than 250 µg/mL and they were 80% viable at this concentration. The cell viability decreased in a dose-dependent manner. Secretions of interleukin (IL)-6 and NO were significantly reduced by the kinos in a concentration dependent manner. In contrast, the secretion of tumour necrosis factor alpha was enhanced by the kinos whilst IL-10 was also enhanced by WA kinos but it was reduced by the PNG vii kinos. The phagocytosis of Gram positive and Gram negative bacteria by macrophages was enhanced by the kinos. Gram positive bacteria were inhibited by the kinos with a minimum inhibitory concentration of 1 mg/mL and a minimum bactericidal concentration of 3 mg/mL. Gram negative bacterial growth was not affected by kinos. Phenolics (flavonoids), tannin, and triterpenoid saponins are predominant in the kinos as evaluated by the phytochemical qualitative (flavonoid and triterpenoids saponin tests), quantitative (assays of total phenolics and total tannins) and spot tests (kinos spotted on thin layer chromatography plate). Biological activity was lost for WA kinos by fractionation whilst some fractions of PNG kinos retained activity. This suggests that the biological effects of kino on macrophage activity and potentially on growth and viability of Gram positive bacteria may be multifactorial and possibly synergistic in nature. Through these studies we demonstrate that kinos predominantly induce an anti- inflammatory profile in mouse macrophages and possess antibacterial properties against Gram positive bacteria. Although limited to the in vitro context we provide evidence substantiating some of the claims by traditional medicine. viii TABLE OF CONTENTS Anti-inflammatory and Antibacterial Effects of Kinos from Australian and Papua New Guinean Eucalyptus Species i DECLARATION ii ACKNOWLEDGEMENTS iii LIST OF ABBREVIATIONS AND ACRONYMS v LIST OF ABBREVIATIONS AND ACRONYMS CONTINUED vi ABSTRACT vii TABLE OF CONTENTS ix CHAPTER 1 1 GENERAL INTRODUCTION 1 1.1. Introduction 2 1.2. Natural products 3 1.3. Link between folk medicine and natural products 5 1.4. First Australian traditional medicine 7 Table 1.1 10 1.4.1. Chemistry of kinos and links between their chemical constituents and antimicrobial activity 11 1.5. Antimicrobial effects of Eucalyptus species 13 ix Table 1.2 18 1.6. General methods used in drug discovery research 20 1.7. Innate and adaptive immune systems 22 1.7.1. Innate Immune system 22 Figure 1.1 24 1.7.2. Adaptive Immune system 25 1.7.3. Inflammation and cytokines as the mediators 26 1.8. Pathogenesis of bacteria 29 1.8.1. Factors that enhance pathogenesis of bacteria 30 1.9. Perspective and objectives of this study 34 CHAPTER 2 35 MATERIALS AND METHODS 35 2.1. Introduction 36 2.2. Kinos collection and preparation 37 2.3. Materials 38 Table 2.1 38 Figure 2.1 40 2.4. Cells, cell culture and incubation conditions 41 2.5. Morphology of RAW264.7 cells 41 2.6. Cell viability 41 2.6.1. Acid phosphatase assay 41 2.7. Measurement of cytokines and nitric oxide as mediators of inflammation 42 2.7.1. Tumour necrosis factor alpha (TNF-α) ELISA 42 2.7.2. Interleukin-6 (IL-6) and IL-10 ELISAs 43 2.7.3. Nitric oxide assay 43 x 2.8. Phagocytosis of Gram negative and Gram positive bacteria 44 2.8.1.
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