Abstract
In recent decades, various types of bioactive substances have been identified from amphibian skin and its secretions. Bradykinin-related peptides (BRPs) are among these compounds that make up the host defence system of amphibians. In the present study, we identified six novel BRPs, amolopkinin-GN1, amolopkinin-RK1, amolopkinin-TR1, amolopkinin-LF1, ranakinin-MS1, and ranakinin-MS2, from five East Asian amphibians, Amolops granulosus, Amolops ricketti, Amolops torrentis, Amolops lifanensis, and Hylarana maosonensis. This is the first report on BRPs in the skin of these species. Physiological assays reveal that these peptides have a contractive effect on the smooth muscle of rat ileum.
Similar content being viewed by others
References
Conlon JM, Mechkarska M, Lukic ML, Flatt PR (2014) Potential therapeutic applications of multifunctional host-defense peptides from frog skin as anti-cancer, anti-viral, immunomodulatory, and anti-diabetic agents. Peptides 57:67–77
Wang X, Ren S, Guo C, Zhang W, Zhang X, Zhang B, Li S et al (2017) Identification and functional analyses of novel antioxidant peptides and antimicrobial peptides from skin secretions of four East Asian frog species. Acta Biochim Biophys Sin 49:550–559
McCrudden CM, Zhou M, Chen T, O’Rourke M, Walker B, Hirst D, Shaw C (2007) The complex array of bradykinin-related peptides (BRPs) in the peptidome of pickerel frog (Rana palustris) skin secretion is the product of transcriptional economy. Peptides 28:1275–1281
Gordon JL, Martin W (1983) Endothelium-dependent relaxation of the pig aorta: relationship to stimulation of 86Rb efflux from isolated endothelial cells. Br J Pharmacol 79:531–541
Fuller RW, Dixon CM, Cuss FM, Barnes PJ (1987) Bradykinin-induced bronchoconstriction in humans. Mode of action. Am Rev Respir Dis 135:176–180
Calixto JB, Nicolau M, Yunes RA (1988) Antagonistic effect of Mandevilla velutina extract on kinin-induced contractions of guinea-pig and cat ileum longitudinal smooth muscle. Gen Pharmacol 19:595–599
Steranka LR, Manning DC, DeHaas CJ, Ferkany JW, Borosky SA, Connor JR, Vavrek RJ et al (1988) Bradykinin as a pain mediator: receptors are localized to sensory neurons, and antagonists have analgesic actions. Proc Natl Acad Sci USA 85:3245–3249
Moreau ME, Garbacki N, Molinaro G, Brown NJ, Marceau F, Adam A (2005) The kallikrein-kinin system: current and future pharmacological targets. J Pharmacol Sci 99:6–38
Riccio MM, Proud D (1996) Evidence that enhanced nasal reactivity to bradykinin in patients with symptomatic allergy is mediated by neural reflexes. J Allergy Clin Immunol 97:1252–1263
Thompson AH, Bjourson AJ, Shaw C, McClean S (2006) Bradykinin-related peptides from Phyllomedusa hypochondrialis azurea: mass spectrometric structural characterisation and cloning of precursor cDNAs. Rapid Commun Mass Spectrom 20:3780–3788
Xi X, Li B, Chen T, Kwok HF (2015) A review on bradykinin-related peptides isolated from amphibian skin secretion. Toxins 7:951–970
Wang H, Yu Z, Hu Y, Yu H, Ran R, Xia J, Wang D et al (2012) Molecular cloning and characterization of antimicrobial peptides from skin of the broad-folded frog, Hylarana latouchii. Biochimie 94:1317–1326
Yang X, Hu Y, Xu S, Hu Y, Meng H, Guo C, Liu Y et al (2013) Identification of multiple antimicrobial peptides from the skin of fine-spined frog, Hylarana spinulosa (Ranidae). Biochimie 95:2429–2436
Liang J, Han Y, Li J, Xu X, Rees HH, Lai R (2006) A novel bradykinin-like peptide from skin secretions of rufous-spotted torrent frog, Amolops loloensis. Peptides 27:2683–2687
Zhou J, Bjourson AJ, Coulter DJ, Chen T, Shaw C, O’Rourke M, Hirst DG et al (2007) Bradykinin-related peptides, including a novel structural variant, (Val1)-bradykinin, from the skin secretion of Guenther’s frog, Hylarana guentheri and their molecular precursors. Peptides 28:781–789
Guo C, Hu Y, Li J, Liu Y, Li S, Yan K, Wang X et al (2014) Identification of multiple peptides with antioxidant and antimicrobial activities from skin and its secretions of Hylarana taipehensis, Amolops lifanensis, and Amolops granulosus. Biochimie 105:192–201
Saitou N (1988) Property and efficiency of the maximum likelihood method for molecular phylogeny. J Mol Evol 27:261–273
Takagaki Y, Kitamura N, Nakanishi S (1985) Cloning and sequence analysis of cDNAs for human high molecular weight and low molecular weight prekininogens. Primary structures of two human prekininogens. J Biol Chem 14:8601–8609
Xiang J, Wang H, Ma C, Zhou M, Wu Y, Wang L, Guo S et al (2016) Ex vivo smooth muscle pharmacological effects of a novel bradykinin-related peptide, and its analogue, from Chinese large odorous frog, Odorrana livida skin secretions. Toxins 8(10):283
Liu X, You D, Chen L, Wang X, Zhang K, Lai R (2008) A novel bradykinin-like peptide from skin secretions of the frog, Rana nigrovittata. J Pept Sci 14:626–630
Li J, Xu X, Xu C, Zhou W, Zhang K, Yu H, Zhang Y et al (2007) Anti-infection peptidomics of amphibian skin. Mol Cell Proteom 6:882–894
Conlon JM (1999) Bradykinin and its receptors in non-mammalian vertebrates. Regul Pept 79:71–81
Sin Y, Zhou M, Chen W, Wang L, Chen T, Walker B, Shaw C (2008) Skin bradykinin-related peptides (BRPs) and their biosynthetic precursors (kininogens): comparisons between various taxa of Chinese and North American ranid frogs. Peptides 29:393–403
Conlon JM, Aronsson U (1997) Multiple bradykinin-related peptides from the skin of the frog, Rana temporaria. Peptides 18:361–365
Chen M, Che Q, Wang X, Li J, Yang H, Li D, Zhang K et al (2010) Cloning and characterization of the first amphibian bradykinin gene. Biochimie 92:226–231
Li L, Bjourson AJ, He J, Cai G, Rao P, Shaw C (2003) Bradykinins and their cDNA from piebald odorous frog, Odorrana schmackeri, skin. Peptides 24:863–872
Jiang Y, Xi X, Ge L, Yang N, Hou X, Ma J, Ma C et al (2014) Bradykinin-related peptides (BRPs) from skin secretions of three genera of phyllomedusine leaf frogs and their comparative pharmacological effects on mammalian smooth muscles. Peptides 52:122–133
Zhou X, Wang L, Zhou M, Chen T, Ding A, Rao P, Walker B et al (2009) Amolopkinins W1 and W2–novel bradykinin-related peptides (BRPs) from the skin of the Chinese torrent frog, Amolops wuyiensis: antagonists of bradykinin-induced smooth muscle contraction of the rat ileum. Peptides 30:893–900
Funding
The study was supported by the Natural Science Foundation of Educational Committee of Hebei Province of China (Nos. QN2016129), Natural Science Foundation of Hebei Province of China (Nos. C2016205244), and National Natural Science Foundation of China (Nos. 31200309).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
All authors declare that they have no conflicts of interest.
Ethical Approval
This article does not contain any studies with human participants performed by any of the authors.
Rights and permissions
About this article
Cite this article
Zhang, B., Zhang, X., Yang, Y. et al. Identification and Functional Analysis of Novel Bradykinin-Related Peptides (BRPs) from Skin Secretions of Five Asian Frogs. Protein J 37, 324–332 (2018). https://doi.org/10.1007/s10930-018-9783-9
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10930-018-9783-9