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Identification of a Novel Vasodilatory Octapeptide from the Skin Secretion of the African Hyperoliid Frog, Kassina Senegalensis

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Identification of a Novel Vasodilatory Octapeptide from the Skin Secretion of the African Hyperoliid Frog, Kassina Senegalensis View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Queen's University Research Portal Identification of a Novel Vasodilatory Octapeptide from the Skin Secretion of the African Hyperoliid Frog, Kassina senegalensis Du, Q., Wang, H., Ma, C., Wu, Y., Xi, X., Zhou, M., ... Wang, L. (2017). Identification of a Novel Vasodilatory Octapeptide from the Skin Secretion of the African Hyperoliid Frog, Kassina senegalensis. Molecules, 22, [1215]. DOI: 10.3390/molecules22071215 Published in: Molecules Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights © 2017 The Authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:06. Nov. 2017 molecules Article Identification of a Novel Vasodilatory Octapeptide from the Skin Secretion of the African Hyperoliid Frog, Kassina senegalensis Qiang Du 1,†, Hui Wang 1,*,†, Chengbang Ma 2, Yue Wu 2, Xinping Xi 2,*, Mei Zhou 2 ID , Tianbao Chen 2 ID , Chris Shaw 2 and Lei Wang 2 1 School of Pharmacy, China Medical University, Shenyang 110001, Liaoning, China; [email protected] 2 Natural Drug Discovery Group, School of Pharmacy, Queen’s University, Belfast BT9 7BL, Northern Ireland, UK; [email protected] (C.M.); [email protected] (Y.W.); [email protected] (M.Z.); [email protected] (T.C.); [email protected] (C.S.); [email protected] (L.W.) * Correspondence: [email protected] (H.W.); [email protected] (X.X.); Tel.: +86-24-2325-6666 (H.W.); +44-28-9097-2200 (X.X.); Fax: +86-2325-5471 (H.W.); +44-28-9094-7794 (X.X.) † These authors contributed equally to this work. Received: 5 July 2017; Accepted: 19 July 2017; Published: 19 July 2017 Abstract: The defensive skin secretions of amphibians continue to be an excellent source of novel biologically-active peptides. Here we report the identification and pharmacological activity of a novel C-terminally amided myotropic octapeptide from the skin secretion of the African hyperoliid frog, Kassina senegalensis. The 8-amino acid peptide has the following primary structure: WMSLGWSL-amide and has a molecular mass of 978 Da. The primary structure and organisation of the biosynthetic precursor of WL-8 amide was successfully deduced from cloned skin secretion-derived cDNA. The open-reading frame encoded a single copy of WL-8, located at the C-terminus. Synthetic WL-8 amide was found to cause relaxation of rat tail artery smooth muscle with an EC50 of 25.98 nM. This peptide is unique in terms of its primary structure and is unlike any other peptide previously isolated from an amphibian source which has been archived in the NCBI database. WL-8 amide thus represents the prototype of a novel family of myotropic peptide from amphibian defensive skin secretions. Keywords: amphibian; skin secretion; peptide; smooth muscle 1. Introduction The skin secretions of anurans (frogs and toads) have long been established as an excellent source of structurally-unique peptides which can be used as lead compounds in research into novel therapeutic agents [1,2]. These peptides have been honed through natural selection and physiological adaptations to aid the survival of the organism over millions of years [3]. A wide range of pharmacologically-active peptides are present in skin secretions. These peptides may exert some biological effect or even be highly toxic to would-be predators [3]. An example which demonstrates the physiological effects these peptides can have on predators has been reported in a study of the garter snake. The defensive secretions produced by Xenopus can cause oral dyskinesias in the snake, such that it cannot physically close its mouth [4]. This effect, if reproduced on similar predators in Nature, would certainly permit the frog to escape. Many of the peptides isolated from amphibians exert their pharmacological functions by acting on specific targets within the body, for instance at G protein-linked receptors. This targeting ability of peptides makes them very interesting molecules in the search for potential drug candidates. The pharmacologically-active peptides found in the skin secretions of amphibians are often found to Molecules 2017, 22, 1215; doi:10.3390/molecules22071215 www.mdpi.com/journal/molecules Molecules 2017, 22, 1215 2 of 9 Molecules 2017, 22, 1215 2 of 8 befunctions analogues in humans of the naturally-occurring and in other vertebrates. regulatory Some are or neuropeptideseven identical to which their endogenous carry out physiological mammalian functionscounterparts in humans such as and thyrotropin-releasing in other vertebrates. hormon Some aree (TRH) even identical[5] and the to theircanonical endogenous bradykinin mammalian peptide, counterpartsbut most are suchnot identical as thyrotropin-releasing though they do hormonehave highly-conserved, (TRH) [5] and thebiologically-active canonical bradykinin regions peptide, within buttheir most structures are not [6]. identical This latter though group they includes do have highly-conserved,bombesin, which is biologically-active an analogue of gastrin-releasing regions within theirpeptide structures in humans [6]. and This also latter the group caeruleins, includes which bombesin, are similar which to gastrin is an analogue and cholecystokinin of gastrin-releasing found in peptidehumans in [7]. humans and also the caeruleins, which are similar to gastrin and cholecystokinin found in humansFrog [7 ].skin secretion is a complex mixture of proteins and peptides which have a variety of pharmacologicalFrog skin secretion effects such is a as complex neurotoxicity mixture and of myotoxicity. proteins and Many peptides proteins which and havepolypeptides a variety have of pharmacologicalbeen isolated from effects amphibian such asskin neurotoxicity which exhibit and a myotoxicity.contractile effect Many on proteinsrat bladder and smooth polypeptides muscle. haveHowever, been the isolated effects fromof low amphibian molecular-weight skin which peptides exhibit on such a contractile smooth muscles effect onare ratnot bladderfully understood. smooth muscle.Here, However, the discovery the effects of a prototype of low molecular-weight low molecular mass peptides peptide on suchfrom smooththe skin muscles secretion are of notthe fullyAfrican understood. hyperoliid frog, Kassina senegalensis, is reported. This peptide represents an entirely novel structuralHere, class the discovery of amphibian of a prototypeskin peptide low and molecular was found mass to display peptide a fromunique the relaxation skin secretion of rat ofartery the Africansmooth hyperoliidmuscle. The frog, peptideKassina was senegalensis named, WL-8, is reported. amide (978 This Da) peptide in accordance represents with an its entirely chain length novel structuraland first and class last of amino amphibian acid skinresidues. peptide We andfurther was de foundscribe to the display structure a unique of its relaxationbiosynthetic of ratprecursor artery smoothidentified muscle. through The peptidemolecular was cloning named, of WL-8 its amideencoding (978 Da)cDNA in accordancefrom a skin with secretion-derived its chain length andcDNA first library. and last amino acid residues. We further describe the structure of its biosynthetic precursor identified through molecular cloning of its encoding cDNA from a skin secretion-derived cDNA library. 2. Results 2. Results Each specimen of K. senegalensis yielded on average 30–35 mg dry weight of skin secretion K. senegalensis followingEach manual specimen stimulation. of Five mg ofyielded lyophilised on average skin secretion 30–35 was mg subjec dry weightted to reverse-phase of skin secretion high followingperformance manual liquid stimulation. chromatography Five mg(RP-HPLC) of lyophilised fractionation skin secretion that produced was subjected a complex to reverse-phasechromatogram high(Figure performance 1). liquid chromatography (RP-HPLC) fractionation that produced a complex chromatogram (Figure1). 1484 1081 678 WL-8 amide Absorbance [mA] Absorbance 275 -128 83:30 91:58 100:25 108:53 117:20 125:48 Time [mm:ss] FigureFigure 1.1. Region of reverse-phase high high performance performance liqu liquidid chromatography chromatography (RP-HPLC) (RP-HPLC) chromatogram chromatogram of oflyophilised lyophilised KassinaKassina senegalensis senegalensis skinskin secretion. secretion. The Theretention retention time timeof the of WL-8 the WL-8 peptide peptide is 97 min is 97 (32.3% min (32.3%acetonitrile) acetonitrile) and indicated and indicated by an arrow. by an arrow. Chromatographic fractions were screened using the smooth
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