Abstract
Bombesin mediates several biological activities in the gastrointestinal (GI) tract and central nervous system in mammals, including smooth muscle contraction, secretion of GI hormones and regulation of homeostatic mechanisms. Here, we report a novel bombesin-like peptide isolated from Boana raniceps. Its amino acid sequence, GGNQWAIGHFM-NH2, was identified and structurally confirmed by HPLC, MS/MS and 454-pyrosequencing; the peptide was named BR-bombesin. The effect of BR-bombesin on smooth muscle contraction was assessed in ileum and esophagus, and its anti-secretory activity was investigated in the stomach. BR-bombesin exerted significant contractile activity with a concentration–response curve similar to that of commercially available bombesin in ileum strips of Wistar rats. In esophageal strips, BR-bombesin acted as an agonist, as many other bombesin-related peptides act, although with different behavior compared to the muscarinic agonist carbachol. Moreover, BR-bombesin inhibited stomach secretion by approximately 50% compared to the untreated control group. This novel peptide has 80% and 70% similarity with the 10-residue C-terminal domain of human neuromedin B (NMB) and human gastrin releasing peptide (GRP10), respectively. Molecular docking analysis revealed that the GRP receptor had a binding energy equal to − 7.3 kcal.mol−1 and − 8.5 kcal.mol−1 when interacting with bombesin and BR-bombesin, respectively. Taken together, our data open an avenue to investigate BR-bombesin in disorders that involve gastrointestinal tract motility and acid gastric secretion.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akeson M, Sainz E, Mantey SA, Jensen RT, Battey JF (1997) Identification of four amino acids in the gastrin-releasing peptide C receptor that are required for high affinity agonist binding. J Biol Chem 272:17405–17409
Anastasi A, Erspamer V, Bucci M (1971) Isolation and structure of bombesin and alytesin, 2 analogous active peptides from the skin of the European amphibians Bombina and Alytes. Experientia 27(2):166–167. https://doi.org/10.1007/BF02145873
Anastasi A, Erspamer V, Endean R (1975) Aminoacid composition and sequence of litorin, a bombesin-like nonapeptide from the skin of the Australian leptodactylid frog Litoria aurea. Experientia 31(5):510–511. https://doi.org/10.1007/BF01932427
Andrade EB, Leite-Junior JMA, Silva-Leite RR, Vieira DL, Santos RC, Silva VG, Barbosa EA, Souza VV, Leite JRSA (2012) Anuran diversity on the Ilha do Caju, Parnaíba Delta River, Maranhão state Northeastern Brazil. Rev Bioci (taubaté) 18:14–21
Andrade EB, Leite JRSA, Andrade GV (2014) Anurans from the municipality of Ilha Grande, Parnaíba River Delta, Piauí, northeastern Brazil. Herpetol Notes 7:219–226
Apostolopoulos V, Bojarska J, Chai TT, Elnagdy S, Kaczmarek K, Matsoukas J, New R, Parang K, Lopez OP, Parhiz H, Perera CO, Pickholz M, Remko M, Saviano M, Skwarczynski M, Tang Y, Wolf WM, Yoshiya T, Zabrocki J, Zielenkiewicz P, AlKhazindar M, Barriga V, Kelaidonis K, Sarasia EM, Toth I (2021) A Global Review on short peptides: frontiers and perspectives. Molecules 26(2):430. https://doi.org/10.3390/molecules26020430
Arzabe C (1999) Reproductive activity patterns of anurans in two different altitudinal sites within the Brazilian Caatinga. Rev Brasil Zool 16(3):851–864
Ayalon A, Devitt PG, Rayford PL, Thompson JC (1981) Electrochemical response patterns to histamine, bombesin, and pentagastrin in isolated bullfrog gastric mucosa. Biochem Biophys Res Commun 103(4):1186–1193. https://doi.org/10.1016/0006-291x(81)90248-5
Bagnara JT, Taylor JD, Hadley ME (1968) The dermal chromatophore unit. J Cell Biol 38(1):67–79. https://doi.org/10.1083/jcb.38.1.67
Barashkova GM, Klimov PK, Kuranova VL, Kalikhevich VN, Ardemasova ZA, Reznik LV, Churkina SI (1992) The effect of regulatory peptides on water absorption in the large intestine of the frog. Fiziol Zh 38(1):57–63
Barbosa EA, Oliveira A, Plácido A, Socodato R, Portugal CC, Mafud AC, Ombredane AS, Moreira DC, Vale N, Bessa LJ, Joanitti GA, Alves C, Gomes P, Delerue-Matos C, Mascarenhas YP, Marani MM, Relvas JB, Pintado M, Leite JRSA (2018) Structure and function of a novel antioxidant peptide from the skin of tropical frogs. Free Radical Biol Med 115:68–79. https://doi.org/10.1016/j.freeradbiomed.2017.11.001
Barra D, Erspamer GF, Simmaco M, Bossa F, Melchiorri P, Erspamer V (1985) Rohdei-litorin: a new peptide from the skin of Phyllomedusa rohdei. Comparative Study FEBS Lett 182(1):53–56. https://doi.org/10.1016/0014-5793(85)81152-2
Barros RO, Junior FLCC, Pereira WS, Oliveira NMN, Ramos RM (2020) Interaction of drug candidates with various SARS-CoV-2 receptors: an in silico study to combat COVID-19. J Proteome Res 19(11):4567–4575. https://doi.org/10.1021/acs.jproteome.0c00327
Brand GD, Krause FC, Silva LP, Leite JR, Melo JA, Prates MV, Pesquero JB, Santos EL, Nakaie CR, Costa-Neto CM, Bloch C Jr (2006) Bradykinin-related peptides from Phyllomedusa hypochondrialis. Peptides 27(9):2137–2146. https://doi.org/10.1016/j.peptides.2006.04.020
Brunetti AE, Marani MM, Soldi RA, Mendonça JN, Faivovich J, Cabrera GM, Lopes NP (2018) Cleavage of peptides from amphibian skin revealed by combining analysis of gland secretion and in situ MALDI imaging mass spectrometry. ACS Omega 3(5):5426–5434. https://doi.org/10.1021/acsomega.7b02029
Buchan AM, Meloche AM (1994) Signal transduction events involved in Bombesin-stimulated gastrin release from human G cells in culture. Can J Physiol Pharmacol 72(9):1060–1065. https://doi.org/10.1139/y94-148
Campos RV, Buchan AM, Meloche RM, Pederson RA, Kwok YN, Coy DH (1990) Gastrin secretion from human antral G cells in culture. Gastroenterology 99(1):36–44. https://doi.org/10.1016/0016-5085(90)91226-v
Cancelarich L, Wilke N, Fanani ML, Moreira DC, Pérez LO, Barbosa EA, Plácido A, Socodato R, Portugal CC, Relvas JB, de la Torre BG, Albericio F, Basso NG, Leite JRSA, Marani MM (2020) Somuncurins: bioactive peptides from the skin of the endangered endemic Patagonian frog Pleurodema somuncurense. J Nat Prod 83(4):972–984. https://doi.org/10.1021/acs.jnatprod.9b00906
Chan WC, White PD (2000) Fmoc solid phase peptide synthesis. A practical approach. Oxford University Press, Oxford
Conlon JM, O’Harte F, Vaudry H (1991) Primary structures of the bombesin-like neuropeptides in frog brain show that bombesin is not the amphibian gastrin-releasing peptide. Biochem Biophys Res Commun 178(2):526–550. https://doi.org/10.1016/0006-291x(91)90139-x
Conlon JM, Al-Ghaferi N, Abraham B, Jiansheng H, Cosette P, Leprince J, Jouenne T, Vaudry H (2006) Antimicrobial peptides from diverse families isolated from the skin of the Asian frog. Rana Grahami Peptides 27(9):2111–2117. https://doi.org/10.1016/j.peptides.2006.03.002
Conlon JM, Meetani MA, Coquet L, Jouenne T, Leprince J, Vaudry H, Kolodziejek J, Nowotny N, King JD (2009) Antimicrobial peptides from the skin secretions of the New World frogs Lithobates capito and Lithobates warszewitschii (Ranidae). Peptides 30(10):1775–1781. https://doi.org/10.1016/j.peptides.2009.07.011
Cowan A, Khunawat P, Zhu XZ, Gmerek DE (1985) Effects of bombesin on behavior. Life Sci 37(2):135–145. https://doi.org/10.1016/0024-3205(85)90416-3
Dubois A (2017) The nomenclatural status of Hysaplesia, Hylaplesia, Dendrobates and related nomina (Amphibia, Anura), with general comments on zoological nomenclature and its governance, as well as on taxonomic databases and websites. Bionomina 11:1–48. https://doi.org/10.11646/bionomina.11.1.1
Erspamer V, Erspamer GF, Inselvini M, Negri L (1972a) Occurrence of bombesin and alytesin in extracts of the skin of three European discoglossid frogs and pharmacological actions of bombesin on extravascular smooth muscle. Br J Pharmacol 45(2):333–348. https://doi.org/10.1111/j.1476-5381.1972.tb08087.x
Erspamer V, Melchiorri P, Sopranzi N (1972b) The action of bombesin on the systemic arterial blood pressure of some experimental animals. Br J Pharmacol 45(3):442–450. https://doi.org/10.1111/j.1476-5381.1972.tb08100.x
Faivovich J, Haddad CFB, de Garcia PCA, Frost DR, Campbell JA, Wheeler WC (2005) Systematic review of the frog family Hylidae, with special reference to Hylinae: a phylogenetic analysis and taxonomic revision. Bull Am Mus Nat Hist 294:1–240
Gaudino G, Fasolo A, Merlo G, Lazarus LH, Renda T, D’Este L, Vandesande F (1985) Active peptides from amphibian skin are also amphibian neuropeptides. Peptides 6(3):209–213. https://doi.org/10.1016/0196-9781(85)90376-6
Gebhard LG, Carrizo FU, Stern AL, Burgardt NI, Faivovich J, Lavilla E, Ermácora MR (2004) A Kazal prolyl endopeptidase inhibitor isolated from the skin of Phyllomedusa sauvagii. Eur J Biochem 271(11):2117–2126. https://doi.org/10.1111/j.1432-1033.2004.04127.x
Gonzalez N, Moody TW, Igarashi H, Ito T, Jensen RT (2008) Bombesin-related peptides and their receptors: recent advances in their role in physiology and disease states. Curr Opin Endocrinol 15:58–64
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Heimbrook DC, Boyer ME, Garsky VM, Balishin NL, Kiefer DM, Oliff A, Riemen MW (1988) Minimal ligand analysis of gastrin-releasing peptide receptor. Receptor binding and mitogenesis. J Biol Chem 263:7016–7019
Jessen H, Aspmo SI (2008) Serum stability of peptides. In: Otvos L (eds) From: methods in molecular biology. Peptide based drug design, pp 494:177–186, https://doi.org/10.1007/978-1-59745-419-3 10.
Jha PK, Foppen E, Challet E, Kalsbeek A (2015) Effects of central gastrin-releasing peptide on glucose metabolism. Brain Res 1625:135–141. https://doi.org/10.1016/j.brainres.2015.08.040
Kang M, Maguma HT, Smith TH, Ross GR, Dewey WL, Akbarali HI (2012) The Role of β-Arrestin2 in the mechanism of morphine tolerance in the mouse and guinea pig gastrointestinal tract. J Pharmacol Exp Ther 340(3):567–576. https://doi.org/10.1124/jpet.111.186320
Kim JB, Johansson A, Holmgren S, Conlon JM (2001) Gastrin-releasing peptides from Xenopus laevis: purification, characterization, and myotropic activity. Am J Physiol Regul Integr Comp Physiol 281(3):R902-908. https://doi.org/10.1152/ajpregu.2001.281.3.R902
Krane IM, Naylor SL, Helin-Davis D, Chin WW, Spindel ER (1988) Molecular cloning of cDNAs encoding the human bombesin-like peptide neurometin B. Chromosomal localization and comparison to cDNAs encoding its amphibian homolog ranatensin. J Biol Chem 263(26):13317–13323
Ladram A, Nicolas P (2016) Antimicrobial peptides from frog skin: biodiversity and therapeutic promises. Fron Biosci 21:1341–1371. https://doi.org/10.2741/4461
LaPelusa A, Jan A (2020) Biochemistry, Bombesin StatPearls (internet). StatPearls Publishing, Treasure Island
Leger JP, Mathieson WB (1997) Effects of bombesin on behavioral thermoregulation in the bullfrog. Brain Behav Evolut 50(5):304–312. https://doi.org/10.1159/000113343
Li J, Yu H, Xu X, Wang X, Liu D, Lai R (2007) Multiple bombesin-like peptides with opposite functions from skin of Odorrana grahami. Genomics 89:413–418
Lin JT, Coy DH, Mantey SA, Jesen RT (1995) Comparison of the peptide structural requirements for high affinity interaction with bombesin receptors. Eur J Pharmacol 294(1):55–69. https://doi.org/10.1016/0014-2999(95)00510-2
Lin Y, Chen T, Zhou M, Wang L, Su S, Shaw C (2017) Ranatensin-HL: A bombesin-related tridecapeptide from the skin secretion of the broad-folded frog, Hylarana latouchii. Molecules 22(7):1110. https://doi.org/10.3390/molecules22071110
Lu CX, Nan KJ, Lei Y (2008) Agents for amphibians with anticancer properties. Anticancer Drugs 19(10):931–939. https://doi.org/10.1097/CAD.0b013e3283139100
Magalhães BS, Melo JAT, Leite JRSA, Silva LP, Prates MV, Vinecky F, Barbosa EA, Verly RM, Mehta A, Nicoli JR (2008) Post-secretory events alter the peptide content of the skin secretion of Hypsiboas raniceps. Biochem Bioph Res Co 377:1057–1061
Mahlapuu M, Håkansson J, Ringstad L, Björn C (2016) Antimicrobial peptides: an emerging category of therapeutic agents. Front Cell Infect Microbiol 6:194. https://doi.org/10.3389/fcimb.2016.00194
Mangoni ML, Casciaro B (2020) Development of antimicrobial peptides from amphibians. Antibiotics (basel) 9(11):772. https://doi.org/10.3390/antibiotics9110772
Marani MM, Dourado F, Quelemes P, Freitas A, Perfeito M, Barbosa E, Costa Veraz L, Coelho A, Barroso Andrade E, Eaton P, Longo JP, Azevedo RB, Delerue Matos C, Leite JRSA (2015) Characterization and biological activities of ocellatin peptides from the skin secretion of the frog Leptodactylus pustulatus (Leptodactylidae; Amphibian). J Nat Prod 78(7):1495–1504. https://doi.org/10.1021/np500907t
Melchiorri P, Sopranzi N, Erspamer V (1971) On the action of bombesin on the kidney of the rat and the dog. J Pharm Pharmacol 23(12):981–982. https://doi.org/10.1111/j.2042-7158.1971.tb09911.x
Miao Y, Li W, Duan L, Xiao Y (2010) A bombesin-like peptide from skin of Sanguirana varians. Comp Biochem Physiol B Biochem Mol Biol 155(2):106–109. https://doi.org/10.1016/j.cbpb.2009.10.007
Morris GM, Huey R, Lindstrom W, Sanner MF, Belew RK, Goodsell DS, Olson AJ (2009) AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J Comput Chem 30:2785–2791
Nagalla SR, Barry BJ, Spindel ER (1994) Cloning of complementary DNAs encoding the amphibian bombesin-like peptides Phe8 and Leu8 phyllolitorin from Phyllomedusa sauvagei: potential role of U to C RNA editing in generating neuropeptide diversity. Mol Endocrinol 8(8):943–951. https://doi.org/10.1210/mend.8.8.7997236
Nagalla SR, Barry BJ, Creswick KC, Eden P, Taylor JT, Spindel ER (1995) Cloning of a receptor for amphibian [Phe13]Bombesin distinct from the receptor for gastrin-releasing peptide: identification of a fourth Bombesin Receptor Subtype (BB4). Proc Natl Acad Sci USA 92:6205–6209
Nakajima T, Tanimura T, Pisano JJ (1970) Isolation and structure of a new vasoactive peptide. Fed Proc Fed Am Soc Exp Biol (abstract) 29:282
Nakajima T, Yasuhara T, Erspamer V, Erspamer GF, Negri L, Endean R (1980) Physalaemin- and bombesin-like peptides in the skin of the Australian leptodactylid frog Uperoleia rugosa. Chem Pharm Bull (tokyo) 28(3):689–695. https://doi.org/10.1248/cpb.28.689
Negri L, Erspamer GF, Severini C, Potenza RL, Melchiorri P, Erspamer V (1992) Dermorphin-related peptides from the skin of Phyllomedusa bicolor and their amidated analogs activate two mu opioid receptor subtypes that modulate antinociception and catalepsy in the rat. Proc Natl Acad Sci USA 89(15):7203–7207. https://doi.org/10.1073/pnas.89.15.7203
Ohki-Hamazaki H, Watase K, Yamamoto K, Ogura H, Yamano M, Yamada K, Maeno H (1997) Imaki Mice lacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature 390(6656):165–169. https://doi.org/10.1038/36568
Orly R, Haines DE (2003) Give a kiss to a frog and it will turn into… a neuropeptide: the genealogy of the Bombesin-Like Family. J His Neurosci. 12(4):411–412. https://doi.org/10.1076/jhin.12.4.411.27918
Pendharkar SA, Drury M, Walia M, Korc M, Petrov MS (2017) Gastrin-releasing peptide and glucose metabolism following pancreatitis. Gastroenterol Res 10(4):224–234. https://doi.org/10.14740/gr890w
Popov CSFC, Magalhães BS, Goodfellow BJ, Bocca AL, Pereira DM, Andrade PB, Valentão P, Pereira PJB, Rodrigues JE, de Holanda Veloso PH Jr, Rezende TMB (2019) Host-defense peptides AC12, DK16 and RC11 with immunomodulatory activity isolated from Hypsiboas raniceps skin secretion. Peptides 113:11–21. https://doi.org/10.1016/j.peptides.2018.12.007
Prates MV, Sforca ML, Regis WCB, Leite JRSA, Silva LP, Pertinhez TA, Araújo ALT, Azevedo RB, Spisni A, Bloch C Jr (2004) The NMR-derived solution structure of a new cationic antimicrobial peptide from the skin secretion of the Anuran Hyla punctate. J Biol Chem 279(13):13018–13026. https://doi.org/10.1074/jbc.M310838200
Ramos-Álvarez I, Moreno P, Mantey SA, Nakamura T, Nuche-Berenguer B, Moody TW, Coy DH, Jensen RT (2015) Insights into Bombesin receptors and ligands: highlighting recent advances. Peptides 72:128–144. https://doi.org/10.1016/j.peptides.2015.04.026
Rocha JA, Rego NCS, Carvalho BTS, Silva FI, Sousa JÁ, Ramos RM (2018) Computational quantum chemistry, molecular docking, and ADMET predictions of imidazole alkaloids of Pilocarpus microphyllus with schistosomicidal properties. PLoS ONE 13:e0198476
Santana CJ, Magalhães ACM, dos Santos Júnior ACM, Ricart CAO, Lima BD, Álvares ACM, Freitas SM, Pires Jr OR, Fontes W, Castro MS (2020a) Figainin 1, a novel amphibian skin peptide with antimicrobial and antiproliferative properties. Antibiotics 9(9):625. https://doi.org/10.3390/antibiotics9090625
Santana CJ, Magalhães ACM, Prías-Márquez CA, Falico DA, dos Santos Júnior ACM, Lima BD, Ricart CAO, Pilger DRB, Bonotto RM, Moraes CB, Freitas-Júnior LH, Álvares ACM, Freitas SM, Luz IS, Pires Jr OR, Fontes W, Castro MS (2020b) Biological properties of a novel multifunctional host defense peptide from the skin secretion of the chaco tree frog, Boana raniceps. Biomolecules 10:790. https://doi.org/10.3390/biom10050790
Severi C, Jensen RT, Erspamer V, D’Arpino L, Coy DH, Torsoli A, Delle FG (1991) Different receptors mediate the action of bombesin-related peptides on gastric smooth muscle cells. Am J Physiol 260(5):G683–G690. https://doi.org/10.1152/ajpgi.1991.260.5.G683
Shay H (1945) A simple method for the uniform production of gastric ulceration in the rat. Gastroenterology 5:43–61
Sousa JC, Berto RF, Gois EA, Fontenele-Cardi NC, Honório JE Jr, Konno K, Richardson M, Rocha MF, Camargo AA, Pimenta DC, Cardi BA, Carvalho KM (2009) Leptoglycin: a new Glycine/Leucine-rich antimicrobial peptide isolated from the skin secretion of the South American frog Leptodactylus pentadactylus (Leptodactylidae). Toxicon 54(1):23–32. https://doi.org/10.1016/j.toxicon.2009.03.011
Sousa NA, Oliveira GAL, de Oliveira AP, Lopes ALF, Iles B, Nogueira KM, Araújo TSL, Souza LKM, Araújo AR, Ramos-Jesus J, Plácido A, Amaral C, Campelo YDM, Barbosa EA, Portugal CC, Socodato R, Lobo A, Relvas J, Bemquerer M, Eaton P, Leite JRSA, Medeiros JVR (2020) Novel ocellatin peptides mitigate LPS-induced ROS formation and NF-kB activation in microglia and hippocampal neurons. Sci Rep 10(1):2696. https://doi.org/10.1038/s41598-020-59665-1
Spindel (2013) Bombesin peptides. In: Handbook of biologically active peptides. (Second Edition). Academic Press, pp 326–330. https://doi.org/10.1016/B978-0-12-385095-9.00046-4.
Subirós-Funosas R, Prohens R, Barbas R, El-Faham A, Albericio F (2009) Oxyma: an efficient additive for peptide synthesis to replace the benzotriazole-based HOBt and HOAt with a lower risk of explosion. Chem A Eur J 15(37):9394–9403
Taboada C, Brunetti AE, Pedron FN, Carnevale Neto F, Estrin DA, Bari SE, Chemes LB, Peporine Lopes N, Lagorio MG, Faivovich J (2017) Naturally occurring fluorescence in frogs. Proc Natl Acad Sci USA 114(14):3672–3677. https://doi.org/10.1073/pnas.1701053114
Toledo RC, Jared C (1995) Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol 111A(1):1–29. https://doi.org/10.1016/0300-9629(95)98515-I
Trott O, Olson AJ (2009) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, eficiente optimization, and multithreading. J Comput Chem 31:455–461
Wang H, Bian J, Chen Z, Miao Y, Li W (2011) A novel bombesin-like peptide from skin of Rana shuchinae. Mol Biol Rep 38:3599–3603. https://doi.org/10.1007/s11033-010-0471-x
Wang G, Li X, Wang Z (2016) APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res 44:D1087–D1093
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:W296–W303
Wechselberger C, Kreil G, Richter K (1992) Isolation and sequence of a cDNA encoding the precursor of a bombesinlike peptide from brain and early embryos of Xenopus laevis. Proc Natl Acad Sci USA 89(20):9819–9822. https://doi.org/10.1073/pnas.89.20.9819
Yasuhara T, Nakajima T, Nokihara K, Yanaihara C, Yanaihara N, Erspamer V, Erspamer GF (1983) Two new frog skin peptides, phyllolitorins of the bombesin-ranatensin family from Phyllomedusa sauvagei. Biomed Res 4:407–412
Zhou X, Ma C, Zhou M, Zhang Y, Xi X, Zhong R, Chen T, Shaw C, Wang L (2017) pharmacological effects of two novel bombesin-like peptides from the skin secretions of chinese piebald odorous frog (Odorrana schmackeri) and European Edible Frog (Pelophylax kl. esculentus) on smooth muscle. Molecules 22(10):1798. https://doi.org/10.3390/molecules22101798
Acknowledgements
M.M. is a researcher at CONICET. A.P. is a recipient of a post-doctoral grant from the project No. PTDC/BII-BIO/31158/2017 of the Fundação para a Ciência e a Tecnologia (FCT). The authors would like to thank EMBRAPA CENARGEN for the use of the mass spectrometer.
Funding
This work was financed by national funds through the Fundação para a Ciência e a Tecnologia (FCT), I.P., under the project No. PTDC/BII-BIO/31158/2017. J.R.L. and P.E. received funding from CNPq/PVE (grant number 400398/2014–1). A.G.V. received funding from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES, Brazil (Project number 1713871).
Author information
Authors and Affiliations
Contributions
Conceptualization: NAS, LV, DCM, AP, PE, LN, JVRM, JRSAL; Data curation: NAS, DCM, KKLG, PJCM, AP, PE, LN, JVRM, JRSAL; Formal analysis: NAS, MMM, ALFL, EMS, EAB, AGV, FTBK, SSL, KPG, DC, MB, PQ, LV, DCM, KKLG, PJCM, AP, PE, LN, JVRM, JRSAL; Funding acquisition: DCM, PJCM, AP, PE, LN, JVRM, JRSAL; Investigation: NAS, ALFL, EMS, EAB, AGV, FTBK, SSL, KPG, DC, MB, PQ, LV, DCM, KKLG, PJCM, AP, PE, LN, JVRM, LHS, JRSAL; Methodology: NAS, ALFL, LHS, EMS, EAB, AGV, FTBK, SSL, KPG, DC, MB, PQ, LV, DCM, KKLG, PJCM, AP, PE, LN, JVRM, JRSAL; Project administration: AP, PE, LN, JVRM, MMM, JRSAL; Resources: AP, PE, LN, JVRM, JRSAL; Supervision: AP, PE, LN, JVRM, JRSAL; Roles/Writing—original draft: NAS, MMM, DCM, KKLG, PJCM, AP, PE, LN, JVRM, JRSAL; Writing—review & editing: NAS, MMM, DCM, KKLG, PJCM, AP, PE, LN, JVRM, JRSAL.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Ethical approval
The paper has been submitted with full responsibility, following due ethical procedure, and there is no duplicate publication, fraud, plagiarism, or concerns about animal experimentation.
Research involving human participants and/or animals
Animals. The gastrointestinal experiments carried out in this study had their animal manipulation procedures approved by the Animal Ethics Committee of the Universidade Federal de Goiás (UFG/CEUA) under process number 25/12 (Resolution 01, of Law 11794/08). Human. For hemolysis tests. Volunteers signed an informed consent form and the protocol was registered with the Human Research Ethics Committee at Universidade Federal do Piaui (UFPI) (04/2014).
Informed consent
Does not apply to this manuscript.
Additional information
Handling editor: S. Beninati.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Sousa, N.A., Marani, M.M., Lopes, A.L.F. et al. BR-bombesin: a novel bombesin-related peptide from the skin secretion of the Chaco tree frog (Boana raniceps) with physiological gastric effects. Amino Acids 54, 733–747 (2022). https://doi.org/10.1007/s00726-021-03114-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-021-03114-4