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Cyclotides Evolve Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Pharmacy 218 Cyclotides evolve Studies on their natural distribution, structural diversity, and activity SUNGKYU PARK ACTA UNIVERSITATIS UPSALIENSIS ISSN 1651-6192 ISBN 978-91-554-9604-3 UPPSALA urn:nbn:se:uu:diva-292668 2016 Dissertation presented at Uppsala University to be publicly examined in B/C4:301, BMC, Husargatan 3, Uppsala, Friday, 10 June 2016 at 09:00 for the degree of Doctor of Philosophy (Faculty of Pharmacy). The examination will be conducted in English. Faculty examiner: Professor Mohamed Marahiel (Philipps-Universität Marburg). Abstract Park, S. 2016. Cyclotides evolve. Studies on their natural distribution, structural diversity, and activity. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Pharmacy 218. 71 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-554-9604-3. The cyclotides are a family of naturally occurring peptides characterized by cyclic cystine knot (CCK) structural motif, which comprises a cyclic head-to-tail backbone featuring six conserved cysteine residues that form three disulfide bonds. This unique structural motif makes cyclotides exceptionally resistant to chemical, thermal and enzymatic degradation. They also exhibit a wide range of biological activities including insecticidal, cytotoxic, anti-HIV and antimicrobial effects. The cyclotides found in plants exhibit considerable sequence and structural diversity, which can be linked to their evolutionary history and that of their host plants. To clarify the evolutionary link between sequence diversity and the distribution of individual cyclotides across the genus Viola, selected known cyclotides were classified using signature sequences within their precursor proteins. By mapping the classified sequences onto the phylogenetic system of Viola, we traced the flow of cyclotide genes over evolutionary history and were able to estimate the prevalence of cyclotides in this genus. In addition, the structural diversity of the cyclotides was related to specific features of the sequences of their precursor proteins, their evolutionary selection and expression levels. A number of studies have suggested that the biological activities of the cyclotides are due to their ability to interact with and disrupt biological membranes. To better explain this behavior, quantitative structure-activity relationship (QSAR) models were developed to link the cyclotides’ biological activities to the membrane-interactive physicochemical properties of their molecular surfaces. Both scalar quantities (such as molecular surface areas) and moments (such as the distributions of specific properties over the molecular surface) were systematically taken into account in the development of these models. This approach allows the physicochemical properties of cyclotides to be geometrically interpreted, facilitating the development of guidelines for drug design using cyclotide scaffolds. Finally, an optimized microwave-assisted Fmoc-SPSS procedure for the total synthesis of cyclotides was developed. Microwave irradiation is used to accelerate and improve all the key steps in cyclotide synthesis, including the assembly of the peptide backbone by Fmoc-SPPS, the cleavage of the protected peptide, and the introduction of a thioester at the C-terminal carboxylic acid to obtain the head-to-tail cyclized cyclotide backbone by native chemical ligation. Keywords: cyclotide, cyclic cystine knot, evolution, peptide synthesis, chemical ligation, QSAR, Viola, Violaceae, phylogeny Sungkyu Park, Department of Medicinal Chemistry, Division of Pharmacognosy, Box 574, Uppsala University, SE-75123 Uppsala, Sweden. © Sungkyu Park 2016 ISSN 1651-6192 ISBN 978-91-554-9604-3 urn:nbn:se:uu:diva-292668 (http://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-292668) Creativity is Just Connecting Things Steve Jobs (1955- 2011) Dedicated to numerous occasions in our history! List of Papers This thesis is based on the following papers, which are referred to in the text by their Roman numerals. I Sungkyu Park, Ki-Oug Yoo, Erik Jacobsson, Pravech Aja- watanawong, Anders Backlund, Johan Rosengren, Inseok Doo, Ulf Göransson. (2016) Insight into cyclotide evolution from tran- scriptomic analyses and studies on their distribution in violets. Manuscript II Sungkyu Park, Adam Strömstedt, Ulf Göransson. (2014) Cyclo- tide structure-activity relationships: Qualitative and quantitative approaches linking cytotoxicity and anthelmintic activity to the clustering of physicochemical forces. PloS One. 9(3):e91430 III Adam Strömstedt, Sungkyu Park, Robert Burman, Ulf Görans- son. (2016) Exposing the true bacterial potency of cyclotides: ex- plained by lipid selectivity, structural characteristics and corre- lating antimicrobial activities. Manuscript IV Sungkyu Park, Gunasekera Sunithi, Teshome Aboye, Ulf Göransson. (2010) An efficient approach for the total synthesis of cyclotides by microwave assisted Fmoc-SPPS. International Journal of Peptide Research and Therapeutics, 16(3):167-176 Reprints were made with permission from the respective publishers. Contents 1. Introduction ............................................................................................... 11 1.1. The cyclic cystine knot (CCK): a unique structural motif ................ 11 1.2. All living organisms produce proteins, but what about proteins with CCK? ................................................................................................ 11 1.3. Cyclotide precursors in flowering plants are very diverse ................ 13 1.4. Cyclotides are classified on the basis of their cyclotide domain sequences .................................................................................................. 14 1.5. Cyclotides have diverse biological activities .................................... 16 1.6. Pharmacognostic approach in cyclotide research .............................. 16 2. Research aims ........................................................................................... 18 3. Evolution and distribution of cyclotides in Violets (Paper I) ................... 19 3.1. Phylogenetic studies on the family Violaceae ................................... 19 3.2. Previous studies of cyclotides on family Violaceae .......................... 21 3.3. Morphological diversity of Violets ................................................... 23 3.4. Discovery of new cyclotide precursor sequences .............................. 27 3.5. Nomenclature of cyclotides and precursors ...................................... 27 3.6. Classification of cyclotide precursors using their sequence signatures .................................................................................................. 28 3.7. Distribution of cyclotides in Violets ................................................. 33 4. Structure-activity relationships of cyclotides (Paper II and III) ................ 35 4.1 Physicochemical properties and molecular descriptors ...................... 35 4.2. Physicochemical properties as scalars and moments ........................ 36 4.3. Lipophilic index values can be computed for unnatural amino acids. ......................................................................................................... 37 4.4. The exposed surface ratio measures the extent to which a residue’s physicochemical properties affect those of the peptide as a whole. ......... 38 4.5. Procedure for computing the electrostatic moment. .......................... 41 4.6. Use of QSAR to analyze membrane activity and selectivity............. 44 5. Microwave-assisted total synthesis of cyclotides (Paper IV) ................... 47 6. Concluding remarks and future perspectives ............................................ 50 7. Popular scientific summary ....................................................................... 54 8. Acknowledgements ................................................................................... 57 9. References ................................................................................................. 62 Appendix I .................................................................................................... 70 Abbreviations CCK cyclic cystine knot CD cyclotide domain cyO2 cycloviolacin O2 CTR C-terminal repeat DCM dichloromethane DMF N,N-dimethylformamide TFA trifluoroacetic acid ER endoplasmic reticulum Fmoc 9-fluorenylmethoxycarbonyl kB1 kalata B1 MS mass spectrometry NMR nuclear magnetic resonance NTPD N-terminal prodomain NTPP N-terminal propeptide NTR N-terminal repeat PDB protein data bank PE phosphatidylethanolamine PC phosphatidylchloline QSAR quantitative structure-activity relation- ship SASA solvent-accessible surface area SPPS solid phase peptide synthesis EM electrostatic moment/ HBD amphi- pathic moment ES positively charge surface area LM lipophilic moment LS lipophilic surface area + LS the exclusive lipophilicity Side chains of amino acids and their physicochemical properties The 20 naturally occurring amino acids are classified into five categories according to the physicochemical properties of their side chains: hydrophilic (~), hydrophobic ($), flexible (G), rigid (P), and disulfide-forming (C). The hydrophilic residues are further divided into positively charged (+), negatively charged (=) and uncharged (*) groups. Similarly, the hydrophobic residues ($) are divided into aromatic (#) and al- kyl (<) groups. 1. Introduction 1.1. The cyclic cystine knot (CCK): a unique structural motif The cyclotides
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