Antimicrobial peptidomes of Bothrops atrox and Bothrops jararacussu snake venoms.
Animals
Anti-Bacterial Agents
/ chemistry
Anti-Infective Agents
/ chemistry
Antimalarials
/ chemistry
Bothrops
Crotalid Venoms
/ chemistry
Hemolytic Agents
/ chemistry
Humans
Leishmania
/ drug effects
Microbial Sensitivity Tests
Peptides
/ chemistry
Plasmodium falciparum
/ drug effects
Pseudomonas aeruginosa
/ drug effects
Spectrometry, Mass, Electrospray Ionization
Staphylococcus aureus
/ drug effects
Antimicrobial peptide
Bothrops atrox
Bothrops jararacussu
Peptidomics
Snake venom peptidome
Journal
Amino acids
ISSN: 1438-2199
Titre abrégé: Amino Acids
Pays: Austria
ID NLM: 9200312
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
received:
06
08
2020
accepted:
11
07
2021
pubmed:
6
9
2021
medline:
5
2
2022
entrez:
5
9
2021
Statut:
ppublish
Résumé
The worrisome emergence of pathogens resistant to conventional drugs has stimulated the search for new classes of antimicrobial and antiparasitic agents from natural sources. Antimicrobial peptides (AMPs), acting through mechanisms that do not rely on the interaction with a specific receptor, provide new possibilities for the development of drugs against resistant organisms. This study sought to purify and proteomically characterize the antimicrobial and antiparasitic peptidomes of B. atrox and B. jararacussu snake venoms against Gram-positive (Staphylococcus aureus, Methicillin-resistant Staphylococcus aureus-MRSA), Gram-negative (Escherichia coli, Pseudomonas aeruginosa, Klebsiella pneumoniae) bacteria, and the protozoan parasites Leishmania amazonensis and Plasmodium falciparum (clone W2, resistant to chloroquine). To this end, B. atrox and B. jararacussu venom peptides were purified by combination of 3 kDa cut-off Amicon
Identifiants
pubmed: 34482475
doi: 10.1007/s00726-021-03055-y
pii: 10.1007/s00726-021-03055-y
doi:
Substances chimiques
Anti-Bacterial Agents
0
Anti-Infective Agents
0
Antimalarials
0
Crotalid Venoms
0
Hemolytic Agents
0
Peptides
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1635-1648Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : # 406385/2018
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 303792/2016-1
Organisme : Universidad de Buenos Aires
ID : # 01.12.0450.0
Organisme : Financiadora de Estudos e Projetos
ID : 01.09.0278.04
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Akef HM (2018) Anticancer, antimicrobial, and analgesic activities of spider venoms. Toxicol Res 7:381–395. https://doi.org/10.1039/c8tx00022k
doi: 10.1039/c8tx00022k
Almeida JR, Resende LM, Watanabe RK et al (2016) Snake venom peptides and low mass proteins: molecular tools and therapeutic agents. Curr Med Chem 23:1–29. https://doi.org/10.2174/0929867323666161028155611
doi: 10.2174/0929867323666161028155611
Aminov RI (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 1:134. https://doi.org/10.3389/fmicb.2010.00134
doi: 10.3389/fmicb.2010.00134
pubmed: 21687759
pmcid: 3109405
Ashour DS, Othman AA (2020) Parasite–bacteria interrelationship. Parasitol Res 119:3145–3164. https://doi.org/10.1007/s00436-020-06804-2
doi: 10.1007/s00436-020-06804-2
pubmed: 32748037
Banbula A, Potempa J, Travis J et al (1998) Amino-acid sequence and three-dimensional structure of the Staphylococcus aureus metalloproteinase at 1.72 å resolution. Structure 6:1185–1193. https://doi.org/10.1016/S0969-2126(98)00118-X
doi: 10.1016/S0969-2126(98)00118-X
pubmed: 9753696
Betts JW, Hornsey M, La Ragione RM (2018) Novel antibacterials: alternatives to traditional antibiotics. Adv Microb Physiol 73:123–169. https://doi.org/10.1016/BS.AMPBS.2018.06.001
doi: 10.1016/BS.AMPBS.2018.06.001
pubmed: 30262108
Boman HG (2003) Antibacterial peptides: basic facts and emerging concepts. J Intern Med 254:197–215. https://doi.org/10.1046/j.1365-2796.2003.01228.x
doi: 10.1046/j.1365-2796.2003.01228.x
pubmed: 12930229
Boni MF, Feldman MW (2005) Evolution of antibiotic resistance by human and bacterial niche construction. Int J Organ Evol 59:477–491
Calvete JJ (2017) Venomics: integrative venom proteomics and beyond. Biochem J 474:611–634. https://doi.org/10.1042/BCJ20160577
doi: 10.1042/BCJ20160577
pubmed: 28219972
Carballar-Lejarazú R, Rodríguez MH, De La Cruz H-H et al (2008) Recombinant scorpine: a multifunctional antimicrobial peptide with activity against different pathogens. Cell Mol Life Sci 65:3081–3092. https://doi.org/10.1007/s00018-008-8250-8
doi: 10.1007/s00018-008-8250-8
pubmed: 18726072
Cassini A, Högberg LD, Plachouras D et al (2019) Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis 19:56–66. https://doi.org/10.1016/S1473-3099(18)30605-4
doi: 10.1016/S1473-3099(18)30605-4
pubmed: 30409683
pmcid: 6300481
Cendron LH, Bertol CD, Fuentefria DB et al (2014) Broad antibacterial activity of Bothrops jararaca venom against bacterial clinical isolates. Adv Microbiol 4:1174–1187
doi: 10.4236/aim.2014.416127
Centers for Disease Control U (2019) Antibiotic resistance threats in the United States, 2019. pp 1–150. https://doi.org/10.15620/cdc:82532
Chen LF, Chopra T (2009) Pathogens resistant to antibacterial agents. Infect Dis Clin North Am 23:817–845
doi: 10.1016/j.idc.2009.06.002
Chokshi A, Sifri Z, Cennimo D, Horng H (2019) Global contributors to antibiotic resistance. J Glob Infect Dis 11:36–42. https://doi.org/10.4103/jgid.jgid_110_18
doi: 10.4103/jgid.jgid_110_18
pubmed: 30814834
pmcid: 6380099
Chou T-L, Wu C-H, Huang K-F, Wang AH-J (2013) Crystal structure of a crystal structure of a Trimeresurus mucrosquamatus venom metalloproteinase providing new insights into the inhibition by endogenous tripeptide inhibitors. Toxicon 71:140–146. https://doi.org/10.1016/J.TOXICON.2013.05.009
doi: 10.1016/J.TOXICON.2013.05.009
pubmed: 23732127
CLSI (2018) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 11th edn. Clinical and Laboratory Standards Institute, Pennsylvania
Coutinho-Neto A, Caldeira CAS, Souza GHMF et al (2013) ESI-MS/MS identification of a bradykinin-potentiating peptide from Amazon Bothrops atrox snake venom using a hybrid Qq-oaTOF mass spectrometer. Toxins 5:327–335. https://doi.org/10.3390/toxins5020327
doi: 10.3390/toxins5020327
pubmed: 23430539
pmcid: 3640538
Culp EJ, Yim G, Waglechner N et al (2019) Hidden antibiotics in actinomycetes can be identified by inactivation of gene clusters for common antibiotics. Nat Biotechnol 37:1149–1154
doi: 10.1038/s41587-019-0241-9
Dadgostar P (2019) Antimicrobial resistance: implications and costs. Infect Drug Resist 3903–3910. https://doi.org/10.2147/IDR.S234610
Dal Mas C, Pinheiro DA, Campeiro JD et al (2017) Biophysical and biological properties of small linear peptides derived from crotamine, a cationic antimicrobial/antitumoral toxin with cell penetrating and cargo delivery abilities. Biochimica Et Biophysica Acta (BBA) Biomembranes 1859:2340–2349. https://doi.org/10.1016/J.BBAMEM.2017.09.006
doi: 10.1016/J.BBAMEM.2017.09.006
David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23:616–687. https://doi.org/10.1128/CMR.00081-09
doi: 10.1128/CMR.00081-09
pubmed: 20610826
pmcid: 2901661
Doron S, Davidson LE (2011) Antimicrobial stewardship. Mayo Clin Proc 86:1113–1123. https://doi.org/10.4065/mcp.2011.0358
doi: 10.4065/mcp.2011.0358
pubmed: 22033257
pmcid: 3203003
Eckmann C, Rojas LJ, Lyon S (2018) Know your enemy: managing resistant Gram-negative infections. Future Microbiol 13:1457–1460. https://doi.org/10.2217/fmb-2018-0202
doi: 10.2217/fmb-2018-0202
pubmed: 30311790
European Centre for Disease Prevention and Control (2018) 33000 people die every year due to infections with antibiotic-resistant bacteria. https://www.ecdc.europa.eu/en/news-events/33000-people-die-every-year-due-infections-antibiotic-resistant-bacteria
Ferreira SH, Bartelt DC, Greene LJ (1970) Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 9:2583–2593
doi: 10.1021/bi00815a005
Ferreira BL, Santos DO, Dos Santos AL et al (2011) Comparative analysis of viperidae venoms antibacterial profile: a short communication for proteomics. Evid-Based Complement Altern Med eCAM 2011:960267. https://doi.org/10.1093/ecam/nen052
doi: 10.1093/ecam/nen052
Freire-Moran L, Aronsson B, Manz C et al (2011) Critical shortage of new antibiotics in development against multidrug-resistant bacteria-time to react is now. Drug Resist Updates 14:118–124. https://doi.org/10.1016/J.DRUP.2011.02.003
doi: 10.1016/J.DRUP.2011.02.003
Fry BG, Roelants K, Champagne DE et al (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10:485–511. https://doi.org/10.1146/annurev.genom.9.081307.164356
doi: 10.1146/annurev.genom.9.081307.164356
Gomes VM, Carvalho AO, Da Cunha M et al (2005) Purification and characterization of a novel peptide with antifungal activity from Bothrops jararaca venom. Toxicon 45:817–827. https://doi.org/10.1016/j.toxicon.2004.12.011
doi: 10.1016/j.toxicon.2004.12.011
pubmed: 15904677
Gonçalves JM, Polson A (1947) The electrophoretic analysis of snake venoms. Arch Biochem 13:253–259
pubmed: 20240452
Greene LJ, Camargo AC, Krieger EM et al (1972) Inhibition of the conversion of angiotensin I to II and potentiation of bradykinin by small peptides present in Bothrops jararaca venom. Circ Res 31(Suppl 2):62–71
Gutiérrez JM, Calvete JJ, Habib AG et al (2017) Snakebite envenoming. Nat Rev Dis Primers 3:17063. https://doi.org/10.1038/nrdp.2017.63
doi: 10.1038/nrdp.2017.63
pubmed: 28905944
Huang K-F, Hung C-C, Wu S-H, Chiou S-H (1998) Characterization of three endogenous peptide inhibitors for multiple metalloproteinases with fibrinogenolytic activity from the venom of Taiwan habu Trimeresurus mucrosquamatus. Biochem Biophys Res Commun 248:562–568. https://doi.org/10.1006/bbrc.1998.9017
doi: 10.1006/bbrc.1998.9017
pubmed: 9703966
Hwang AY, Gums JG (2016) The emergence and evolution of antimicrobial resistance: impact on a global scale. Bioorg Med Chem 24:6440–6445
doi: 10.1016/j.bmc.2016.04.027
Ioset J, Brun R, Wenzler T et al (2009) Drug screening for kinetoplastid diseases: a training manual for screening in neglected diseases. In: DNDi and Pan-Asian Screening Network, p 74
Jenner RA, Undheim E (2017) Venom: the secrets of nature’s deadliest weapon, 1a. Natural History Museum, London
Keith JW, Pamer EG (2019) Enlisting commensal microbes to resist antibiotic-resistant pathogens. J Exp Med 216:10–19. https://doi.org/10.1084/jem.20180399
doi: 10.1084/jem.20180399
pubmed: 30309968
pmcid: 6314519
Kerkis I, Silva FDS, Pereira A et al (2010) Biological versatility of crotamine—a cationic peptide from the venom of a South American rattlesnake. Expert Opin Investig Drugs 19:1515–1525. https://doi.org/10.1517/13543784.2010.534457
doi: 10.1517/13543784.2010.534457
pubmed: 21062230
King GF (ed) (2015) Venoms to drugs. Royal Society of Chemistry, Cambridge
Kumar V, Kumar R, Agrawal P et al (2020) A method for predicting hemolytic potency of chemically modified peptides from its structure. Front Pharmacol 11:1–8. https://doi.org/10.3389/fphar.2020.00054
doi: 10.3389/fphar.2020.00054
Laarman AJ, Ruyken M, Malone CL et al (2011) Staphylococcus aureus metalloprotease aureolysin cleaves complement C3 to mediate immune evasion. J Immunol (baltimore, MD: 1950) 186:6445–6453. https://doi.org/10.4049/jimmunol.1002948
doi: 10.4049/jimmunol.1002948
Lambros C, Vanderberg JP (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65:418–420
doi: 10.2307/3280287
Luft FC (2008) The Bothrops legacy: vasoactive peptides from Brazil. Renin Acad Online. https://doi.org/10.3317/jraas.2008.009
doi: 10.3317/jraas.2008.009
Macedo SRA, de Barros NB, Ferreira AS et al (2015) Biodegradable microparticles containing crotamine isolated from Crotalus durissus terrificus display antileishmanial activity in vitro. Pharmacology 95:78–86. https://doi.org/10.1159/000371391
doi: 10.1159/000371391
pubmed: 25633844
Mancin AC, Soares AM, Andrião-Escarso SH et al (1998) The analgesic activity of crotamine, a neurotoxin from Crotalus durissus terrificus (South American Rattlesnake) venom: a biochemical and pharmacological study. Toxicon 36:1927–1937
doi: 10.1016/S0041-0101(98)00117-2
Marques-Porto R, Lebrun I, Pimenta DC (2008) Self-proteolysis regulation in the Bothrops jararaca venom: the metallopeptidases and their intrinsic peptidic inhibitor. Comp Biochem Physiol C Toxicol Pharmacol 147:424–433. https://doi.org/10.1016/j.cbpc.2008.01.011
doi: 10.1016/j.cbpc.2008.01.011
pubmed: 18325841
Morse SS (1995) Factors in the emergence of infectious diseases. Emerg Infect Dis 1:7–15
doi: 10.3201/eid0101.950102
Munekiyo SM, Mackessy SP (2005) Presence of peptide inhibitors in rattlesnake venoms and their effects on endogenous metalloproteases. Toxicon 45:255–263. https://doi.org/10.1016/j.toxicon.2004.10.009
doi: 10.1016/j.toxicon.2004.10.009
pubmed: 15683863
Oguiura N, Boni-Mitake M, Rádis-Baptista G (2005) New view on crotamine, a small basic polypeptide myotoxin from South American rattlesnake venom. Toxicon 46:363–370
doi: 10.1016/j.toxicon.2005.06.009
Ostrowsky B, Banerjee R, Bonomo RA et al (2018) Infectious diseases physicians: leading the way in antimicrobial stewardship. Clin Infect Dis 66:995–1003. https://doi.org/10.1093/cid/cix1093
doi: 10.1093/cid/cix1093
pubmed: 29444247
Palmer ME, Feldman MW (2012) Survivability is more fundamental than evolvability. PLoS ONE 7:38025
doi: 10.1371/journal.pone.0038025
Penna-Coutinho J, Cortopassi WA, Oliveira AA et al (2011) Antimalarial activity of potential inhibitors of Plasmodium falciparum lactate dehydrogenase enzyme selected by docking studies. PLoS ONE 6:e21237. https://doi.org/10.1371/journal.pone.0021237
doi: 10.1371/journal.pone.0021237
pubmed: 21779323
pmcid: 3136448
Pennington MW, Czerwinski A, Norton RS (2018) Peptide therapeutics from venom: current status and potential. Bioorg Med Chem 26:2738–2758. https://doi.org/10.1016/J.BMC.2017.09.029
doi: 10.1016/J.BMC.2017.09.029
pubmed: 28988749
Rádis-Baptista G, Kerkis I (2011) Crotamine, a small basic polypeptide myotoxin from rattlesnake venom with cell-penetrating properties. Curr Pharm Des 17:4351–4361
doi: 10.2174/138161211798999429
Radzicka A, Wolfenden R (1988) Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry 27:1664–1670. https://doi.org/10.1021/bi00405a042
doi: 10.1021/bi00405a042
Rodrigues M, Santos A, de la Torre BG et al (2012) Molecular characterization of the interaction of crotamine-derived nucleolar targeting peptides with lipid membranes. Biochem Biophys Acta 1818:2707–2717. https://doi.org/10.1016/j.bbamem.2012.06.014
doi: 10.1016/j.bbamem.2012.06.014
pubmed: 22749950
Rosas NSC (2013) Efeitos de veneno totais de serpentes brasileiras sobre Leishmania chagasi e Trypanosoma cruzi. Universidade Estadual do Ceará
Ruiz J, Calderon J, Rondón-Villarreal P, Torres R (2014) Analysis of structure and hemolytic activity relationships of antimicrobial peptides (AMPs). Advances in intelligent systems and computing. Springer, pp 253–258
Sala A, Cabassi CS, Santospirito D et al (2018) Novel Naja atra cardiotoxin 1 (CTX-1) derived antimicrobial peptides with broad spectrum activity. PLoS ONE 13:e0190778. https://doi.org/10.1371/journal.pone.0190778
doi: 10.1371/journal.pone.0190778
pubmed: 29364903
pmcid: 5783354
Samy R, Manikandan J, Sethi G et al (2014) Snake Venom proteins: development into antimicrobial and wound healing agents. Mini-Rev Org Chem 11:4–14. https://doi.org/10.2174/1570193X1101140402100131
doi: 10.2174/1570193X1101140402100131
Sciani JM, Pimenta DC (2017) The modular nature of bradykinin-potentiating peptides isolated from snake venoms. J Venom Anim Toxins Incl Trop Dis 23:45. https://doi.org/10.1186/s40409-017-0134-7
doi: 10.1186/s40409-017-0134-7
pubmed: 29090005
pmcid: 5657115
Sciani JM, Vigerelli H, Costa AS et al (2017) An unexpected cell-penetrating peptide from Bothrops jararaca venom identified through a novel size exclusion chromatography screening. J Pept Sci 23:68–76. https://doi.org/10.1002/psc.2965
doi: 10.1002/psc.2965
pubmed: 28054409
Smilkstein M, Sriwilaijaroen N, Kelly JX et al (2004) Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob Agents Chemother 48:1803–1806. https://doi.org/10.1128/aac.48.5.1803-1806.2004
doi: 10.1128/aac.48.5.1803-1806.2004
pubmed: 15105138
pmcid: 400546
Stark M, Liu L-P, Deber CM (2002) Cationic hydrophobic peptides with antimicrobial activity. Antimicrob Agents Chemother 46:3585–3590. https://doi.org/10.1128/AAC.46.11.3585-3590.2002
doi: 10.1128/AAC.46.11.3585-3590.2002
pubmed: 12384369
pmcid: 128737
Trager W, Jensen JB (1976) Human malaria parasites in continuous culture. Science 193:673–675. https://doi.org/10.1126/science.781840
doi: 10.1126/science.781840
pubmed: 781840
Villalta-Romero F, Gortat A, Herrera AE et al (2012) Identification of new snake venom metalloproteinase inhibitors using compound screening and rational peptide design. ACS Med Chem Lett 3:540–543. https://doi.org/10.1021/ml300068r
doi: 10.1021/ml300068r
pubmed: 24900507
pmcid: 4025828
Villalta-Romero F, Borro L, Mandic B et al (2017) Discovery of small molecule inhibitors for the snake venom metalloprotease BaP1 using in silico and in vitro tests. Bioorg Med Chem Lett 27:2018–2022. https://doi.org/10.1016/j.bmcl.2017.03.007
doi: 10.1016/j.bmcl.2017.03.007
pubmed: 28347665
Villar-Briones A, Aird SD (2018) Organic and peptidyl constituents of snake venoms: the picture is vastly more complex than we imagined. Toxins. https://doi.org/10.3390/toxins10100392
doi: 10.3390/toxins10100392
pubmed: 30261630
pmcid: 6215107
Wagstaff SC, Favreau P, Cheneval O et al (2008) Molecular characterisation of endogenous snake venom metalloproteinase inhibitors. Biochem Biophys Res Commun 365:650–656. https://doi.org/10.1016/j.bbrc.2007.11.027
doi: 10.1016/j.bbrc.2007.11.027
pubmed: 18029259
Wang Z, Wang G (2019) The Antimicrobial Peptide Database (APD). In: 2014. http://aps.unmc.edu/AP/about.php
Wang G, Li X, Wang Z (2009) APD2: the updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Res 37:933–937. https://doi.org/10.1093/nar/gkn823
doi: 10.1093/nar/gkn823
Weiner LM, Webb AK, Limbago B et al (2016) Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the national healthcare safety network at the centers for disease control and prevention, 2011–2014. Infect Control Hosp Epidemiol 37:1288–1301. https://doi.org/10.1017/ice.2016.174
doi: 10.1017/ice.2016.174
pubmed: 27573805
pmcid: 6857725
WHO WHO (2014) Antimicrobial resistance: global report on surveillance. World Health Organization, p 232
WHO WHO (2018) Antimicrobial resistance. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance
Wielinga PR, Schlundt J (2012) Food safety: at the center of a one health approach for combating zoonoses. In: Current topics in microbiology and immunology, pp 3–17
Yamane ES, Bizerra FC, Oliveira EB et al (2013) Unraveling the antifungal activity of a South American rattlesnake toxin crotamine. Biochimie 95:231–240. https://doi.org/10.1016/j.biochi.2012.09.019
doi: 10.1016/j.biochi.2012.09.019
pubmed: 23022146
Zhang J, Xin L, Shan B et al (2012) PEAKS DB: de novo sequencing assisted database search for sensitive and accurate peptide identification. Mol Cell Proteomics 11:M111.010587. https://doi.org/10.1074/mcp.M111.010587
doi: 10.1074/mcp.M111.010587
pubmed: 22186715
Zhao F, Lan X-Q, Du Y et al (2018) King cobra peptide OH-CATH30 as a potential candidate drug through clinic drug-resistant isolates. Zool Res 39:87. https://doi.org/10.24272/J.ISSN.2095-8137.2018.025
doi: 10.24272/J.ISSN.2095-8137.2018.025
pubmed: 29515090
pmcid: 5885386