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Biotechnological Applications of Spider Venom Peptides Sing Yan Er Bachelor of Biotechnology Majored in Microbial Biotechnology (Honours)

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Biotechnological Applications of Spider Venom Peptides Sing Yan Er Bachelor of Biotechnology Majored in Microbial Biotechnology (Honours) Biotechnological Applications of Spider Venom Peptides Sing Yan Er Bachelor of Biotechnology majored in Microbial Biotechnology (Honours) A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2016 Institute for Molecular Bioscience Abstract Spider venoms are a rich source of bioactive compounds with potential biotechnological applications. The overall aim of this project was to isolate and characterise novel spider- venom peptides (SVPs) with potential in two key areas: (1) insect control using orally active insecticidal peptides; (2) improvement of human health with peptide modulators that target acid-sensing ion channels (ASICs). Insect pests are a worldwide problem as they threaten crop yields and spread a multitude of insect-borne diseases. Unfortunately, the armament of commercially available chemical insecticides is rapidly diminishing due to the emergence of insecticide-resistant insect strains as well as deregistrations and use restrictions by regulatory authorities due to environmental and health concerns. This has created an unmet need for new eco-friendly insecticides. Spiders are highly efficient insect predators that utilise venom to rapidly incapacitate prey. As such, many SVPs have potent insecticidal properties. However, as SVPs are injected by the spider, they are generally perceived to lack sufficient oral efficacy to be of practical agrochemical use. Recently, several orally-active insecticidal peptides (OAIP 1–5) were isolated from the venom of the Australian tarantula, Selenotypus plumipes, and shown to be lethal when fed to the termites. Chapter 2 describes the characterisation and structure determination of one of these peptides, OAIP3. The peptide was produced using an efficient E. coli periplasmic expression system that promotes disulfide bond formation in vivo. The insecticidal activity of the recombinant peptide was tested in mealworms, while the structure of the peptide was solved using heteronuclear nuclear magnetic resonance spectroscopy. Structural studies indicated that OAIP3 contains a canonical inhibitor cystine knot motif commonly found in spider venom peptides. In comparison to its native form, recombinant OAIP3 is markedly less potent in mealworms, with ~53% moribund at a dose of 7.6 nmol/g. Sequence and structural homologies with other spider venom peptides indicated that OAIP3 is likely to target insect voltage-gated sodium channels. Spider venoms are a rich source of peptides that target therapeutically-relevant ion channels such as ASICs. Chapter 3 describes the isolation and characterisation of a novel ASIC1a modulator, Hm3a, isolated from spider venom. ASICs are proton-gated ion channels that respond to acidosis. Since their initial discovery more than a decade ago, ii they have been implicated in many neurodegenerative diseases, neuronal damage resulting form ischemia, and pain. Given that spider venoms are a rich source of ion channel modulators, we screened a panel of 30 spider venoms for inhibitory activity on ASIC1a. Through an assay-guided fractionation using reverse-phase high performance liquid chromatography, we isolated a peptide modulator of ASIC1a from the venom of the tarantula Heteroscodra maculata. Recombinant peptide was produced and characterised using two-electrode voltage-clamp electrophysiology studies of ASICs expressed in Xenopus laevis oocytes. The peptide, named π-TRTX-Hm3a (Hm3a), is highly selective for ASIC1a over other ASIC subtypes. Hm3a is a close homolog of PcTx1, sharing similar electrophysiological effects on ASICs, but it proved to be more resistant to high temperatures as well as proteolytic degradation by human serum and cerebrospinal fluid. An engineered variant of Hm3a resulted in improved potency and efficacy on ASIC1a. Since the population of ASIC1a that is therapeutically relevant is located in the brain, an efficient method of administration is needed to deliver the peptide across the blood-brain barrier. Invasive methods are often required to deliver drugs into the brain. An alternative approach is intranasal administration that bypasses the blood-brain barrier and allows direct delivery to the brain via the olfactory bulb. Thus, we hypothesised that intranasal administration may also be an effective method for delivery of ASIC1a modulators into the CNS. As described in Chapter 4, several engineered variants of the prototypical ASIC1a modulator, PcTx1, were produced recombinantly or chemical synthesised. These peptides were then conjugated to moieties for PET, MRI and optical imaging in vivo. The addition of various imaging moieties at the N-terminal of PcTx1 had minimal effect on its activity on ASICs. A pharmacokinetics and biodistribution study of PcTx1 was performed using in vivo PET/CT imaging and traditional ex vivo tissue sampling after intravenous and intranasal administration. We show that brain delivery of PcTx1 in mice can be achieved through intranasal but not intravenous administration. In summary, the work presented in this thesis demonstrates that spider venoms provide a diverse library of peptides with potential biotechnological applications. In addition, we show that unconventional intranasal delivery is a plausible route for delivering peptide drugs to target sites in the CNS. iii 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. iv Publications during candidature RESEARCH ARTICLES Koehn L.M., Dong Q, Er S.Y, Rash L.D., King G.F., Dziegielewska K.M., Saunders N.R. and Habgood M.D. (2016) Selective inhibition of ASIC1a confers functional and morphological neuroprotection following traumatic spinal cord injury. F1000Research 5, 1822. Klint, J.K., Smith, J.J., Vetter, I., Rupasinghe, D.B., Er, S.Y., Senff, S., Herzig, V., Mobli, M., Lewis, R.J., Bosmans, F. and King, G.F. (2015) Seven novel modulators of the analgesic target NaV1.7 uncovered using a high-throughput venom-based discovery approach. British Journal of Pharmacology 172: 2445–2458 CONFERENCE ABSTRACTS Er S.Y., Zoltan D., Klintzing J.R., Lau H.Y., Tesiram Y., Bhalla R., Rash L.D., King G.F. (2015) Developing PcTx1 as an imaging probe for acid-sensing ion channel 1a (ASIC1a). 7th International Peptide Symposium, Biopolis, Singapore. December 9–11 (Poster) Er S.Y., Cristofori-Armstrong B., Escoubas P., King G.F., Rash L.D. (2015) Isolation and pharmacological characterisation of π-TRTX-Hm3a, a potent modulator of acid-sensing ion channel 1a (ASIC1a) from venom of the spider Heteroscodra maculata. 10th Peptide Therapeutic Symposium. Salk Institute, United States. October 22–24 (Poster) Er S.Y., Hardy M., King G.F. (2014) Spider-venom peptides as bioinsecticides: orally active insecticidal peptides from an Australian tarantula. 5th Annual Early Career Researcher Symposium, University of Queensland, Australia. November 24 (Poster) Er S.Y., Hardy M., King G.F. (2014) Spider-venom peptides as bioinsecticides: orally active insecticidal peptides from an Australian tarantula. 5th Venoms to Drugs Meeting, Kingscliff, Australia. October 19–24 (Poster) . v Publications included in this thesis No publications included vi Contributions by others to the thesis Chapter Two: NMR spectra collection and spectral editing of OAIP3 was Dr Mehdi Mobli (Centre for Advance imaging, Australia). Dr Mobli also provided expert guidance and opinions in chemical shift analysis and structure calculations. The insecticidal bioassay on mealworms was performed and the results were verified and recorded by Dr Volker Herzig (Institute for Molecular Bioscience (IMB), Australia). Chapter Three: (Incorporated as manuscript for submission) Collaborative work with Mr Ben Cristofori-Armstrong (IMB) who produced the recombinant peptide, performed the electrophysiology experiments to elucidate the mechanism of actions, on-rates on ASIC1a, activity of the peptide on rASIC1a chimeras and off-targets as well as the stability of Hm3a and hANP in human CSF. The peptide sequence was provided by Dr Pierre Escoubas (VenomeTech, France). Dr Lachlan Rash (University of Queensland
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