Effects of the Natural Peptide Crotamine from a South American Rattlesnake on Candida auris, an Emergent Multidrug Antifungal Resistant Human Pathogen
Abstract
:1. Introduction
2. Materials and Methods
2.1. Crotamine
2.2. Microorganisms
2.3. Identification of Candida spp. by Sequencing of the ITS Region of rDNA
2.4. Assays for Checking In Vitro Susceptibility of Candida spp. against Antifungal Drugs
2.5. Assays for Checking In Vitro Susceptibility of Candida spp. for Natural Peptides Including Crotamine
2.6. Statistical Analysis
3. Results
Susceptibility Tests
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Colombo, A.L.; de Almeida Junior, J.N., Jr.; Slavin, M.A.; Chen, S.C.; Sorrell, T.C. Candida and invasive mould diseases in non-neutropenic critically ill patients and patients with haematological cancer. Lancet Infect. Dis. 2017, 17, e344–e356. [Google Scholar] [CrossRef]
- Colombo, A.L.; Junior, J.N.A.; Guinea, J. Emerging multidrug-resistant Candida species. Curr. Opin. Infect. Dis. 2017, 30, 528–538. [Google Scholar] [CrossRef] [PubMed]
- Chowdhary, A.; Sharma, C.; Meis, J.F. Candida auris: A rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally. PLoS Pathog. 2017, 13, e1006290. [Google Scholar] [CrossRef]
- Saris, K.; Meis, J.F.; Voss, A. Candida auris. Curr. Opin. Infect. Dis. 2018, 31, 334–340. [Google Scholar] [CrossRef] [PubMed]
- Rossato, L.; Colombo, A.L. Candida auris: What have we learned about its mechanisms of pathogenicity? Front. Microbiol. 2018, 9, 3081. [Google Scholar] [CrossRef]
- Lockhart, S.R.; Etienne, K.A.; Vallabhaneni, S.; Farooqi, J.; Chowdhary, A.; Govender, N.P.; Colombo, A.L.; Calvo, B.; Cuomo, C.A.; Desjardins, C.A.; et al. Simultaneous emergence of multidrug-resistant Candida auris on 3 continents confirmed by whole-genome sequencing and epidemiological analyses. Clin. Infect. Dis. 2017, 64, 134–140. [Google Scholar] [CrossRef]
- Kordalewska, M.; Lee, A.; Park, S.; Berrio, I.; Chowdhary, A.; Zhao, Y.; Perlin, D.S. Understanding echinocandin resistance in the emerging pathogen Candida auris. Antimicrob. Agents Chemother. 2018, 62, e00238-18. [Google Scholar] [CrossRef] [PubMed]
- Hayashi, M.A.; Bizerra, F.C.; Da Silva, P.I., Jr. Antimicrobial compounds from natural sources. Front. Microbiol. 2013, 4, 195. [Google Scholar] [CrossRef] [Green Version]
- Hayashi, M.A.; Oliveira, E.B.; Kerkis, I.; Karpel, R.L. Crotamine: A novel cell-penetrating polypeptide nanocarrier with potential anti-cancer and biotechnological applications. Methods Mol. Biol. 2012, 906, 337–352. [Google Scholar]
- Schenberg, S. Geographical pattern of crotamine distribution in the same rattlesnake subspecies. Science 1959, 129, 1361–1363. [Google Scholar] [CrossRef]
- Lima, S.C.; Porta, L.C.; Lima, Á.D.C.; Campeiro, J.D.; Meurer, Y.; Teixeira, N.B.; Duarte, T.; Oliveira, E.B.; Picolo, G.; Godinho, R.O.; et al. Pharmacological characterization of crotamine effects on mice hind limb paralysis employing both ex vivo and in vivo assays: Insights into the involvement of voltage-gated ion channels in the crotamine action on skeletal muscles. PLoS Negl. Trop. Dis. 2018, 12, e0006700. [Google Scholar] [CrossRef]
- Nascimento, F.D.; Hayashi, M.A.; Kerkis, A.; Oliveira, V.; Oliveira, E.B.; Rádis-Baptista, G.; Nader, H.B.; Yamane, T.; Tersariol, I.L.; Kerkis, I. Crotamine mediates gene delivery into cells through the binding to heparan sulfate proteoglycans. J. Biol. Chem. 2007, 282, 21349–21360. [Google Scholar] [CrossRef]
- Nascimento, F.D.; Sancey, L.; Pereira, A.; Rome, C.; Oliveira, V.; Oliveira, E.B.; Nader, H.B.; Yamane, T.; Kerkis, I.; Tersariol, I.L.; et al. The natural cell-penetrating peptide crotamine targets tumor tissue in vivo and triggers a lethal calcium-dependent pathway in cultured cells. Mol. Pharm. 2012, 9, 211–221. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.; Yang, Y.L.; Jang, S.H.; Jang, Y.S. Human β-defensin 2 plays a regulatory role in innate antiviral immunity and is capable of potentiating the induction of antigen-specific immunity. Virol. J. 2018, 15, 124. [Google Scholar] [CrossRef]
- Yamane, E.S.; Bizerra, F.C.; Oliveira, E.B.; Moreira, J.T.; Rajabi, M.; Nunes, G.L.; de Souza, A.O.; da Silva, I.D.; Yamane, T.; Karpel, R.L.; et al. Unraveling the antifungal activity of a South American rattlesnake toxin crotamine. Biochimie 2013, 95, 231–240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jung, S.W.; Lee, J.; Cho, A.E. Elucidating the bacterial membrane disruption mechanism of human α-defensin 5: A theoretical study. J. Phys. Chem. B 2017, 121, 741–748. [Google Scholar] [CrossRef] [PubMed]
- Mathew, B.; Nagaraj, R. Variations in the interaction of human defensins with Escherichia coli: Possible implications in bacterial killing. PLoS ONE 2017, 12, e0175858. [Google Scholar] [CrossRef] [PubMed]
- Awang, T.; Pongprayoon, P. The adsorption of human defensin 5 on bacterial membranes: Simulation studies. J. Mol. Model. 2018, 24, 273. [Google Scholar] [CrossRef]
- Costa, B.A.; Sanches, L.; Gomide, A.B.; Bizerra, F.; Dal Mas, C.; Oliveira, E.B.; Perez, K.R.; Itri, R.; Oguiura, N.; Hayashi, M.A. Interaction of the rattlesnake toxin crotamine with model membranes. J. Phys. Chem. B 2014, 118, 5471–5479. [Google Scholar] [CrossRef]
- Feng, J.; Xie, Z.; Yang, W.; Zhao, Y.; Xiang, F.; Cao, Z.; Li, W.; Chen, Z.; Wu, Y. Human beta-defensin 1, a new animal toxin-like blocker of potassium channel. Toxicon 2016, 113, 1–6. [Google Scholar] [CrossRef]
- Zhao, Y.; Xie, Z.; Feng, J.; Li, W.; Cao, Z.; Wu, Y. Pharmacological characterization of human beta-defensins 3 and 4 on potassium channels: Evidence of diversity in beta-defensin-potassium channel interactions. Peptides 2018, 108, 14–18. [Google Scholar] [CrossRef]
- Yount, N.Y.; Kupferwasser, D.; Spisni, A.; Dutz, S.M.; Ramjan, Z.H.; Sharma, S.; Waring, A.J.; Yeaman, M.R. Selective reciprocity in antimicrobial activity versus cytotoxicity of hBD-2 and crotamine. Proc. Natl. Acad. Sci. USA 2009, 106, 14972–14977. [Google Scholar] [CrossRef] [Green Version]
- Peigneur, S.; Orts, D.J.; Prieto da Silva, A.R.; Oguiura, N.; Boni-Mitake, M.; de Oliveira, E.B.; Zaharenko, A.J.; de Freitas, J.C.; Tytgat, J. Crotamine pharmacology revisited: Novel insights based on the inhibition of KV channels. Mol. Pharmacol. 2012, 82, 90–96. [Google Scholar] [CrossRef] [PubMed]
- Pachón-Ibáñez, M.E.; Smani, Y.; Pachón, J.; Sánchez-Céspedes, J. Perspectives for clinical use of engineered human host defense antimicrobial peptides. FEMS Microbiol. Rev. 2017, 41, 323–342. [Google Scholar] [CrossRef]
- Candido-Ferreira, I.L.; Kronenberger, T.; Sayegh, R.S.; Batista, I.F.; da Silva Junior, P.I. Evidence of an antimicrobial peptide signature encrypted in HECT E3 ubiquitin ligases. Front. Immunol. 2017, 7, 664. [Google Scholar] [CrossRef]
- Calvo, B.; Melo, A.S.; Perozo-Mena, A.; Hernandez, M.; Francisco, E.C.; Hagen, F.; Meisand, J.F.; Colombo, A.L. First report of Candida auris in America: Clinical and microbiological aspects of 18 episodes of candidemia. J. Infect. 2016, 73, 369–374. [Google Scholar] [CrossRef]
- Mohsin, J.; Hagen, F.; Al-Balushi, Z.A.M.; de Hoog, G.S.; Chowdhary, A.; Meis, J.F.; Al-Hatmi, A.M.S. The first cases of Candida auris candidaemia in Oman. Mycoses 2017, 60, 569–575. [Google Scholar] [CrossRef]
- Satoh, K.; Makimura, K.; Hasumi, Y.; Nishiyama, Y.; Uchida, K.; Yamaguchi, H. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol. Immunol. 2009, 53, 41–44. [Google Scholar] [CrossRef]
- Merseguel, K.B.; Nishikaku, A.S.; Rodrigues, A.M.; Padovan, A.C.; e Ferreira, R.C.; de Azevedo Melo, A.S.; da Silva Briones, M.R.; Colombo, A.L. Genetic diversity of medically important and emerging Candida species causing invasive infection. BMC Infect. Dis. 2015, 15, 57. [Google Scholar] [CrossRef]
- Prakash, A.; Sharma, C.; Singh, A.; Singh, P.K.; Kumar, A.; Hagen, F.; Govender, N.P.; Colombo, A.L.; Meis, J.F.; Chowdhary, A. Evidence of genotypic diversity among Candida auris isolates by multilocus sequence typing, matrix-assisted laser desorption ionization timeof-flight mass spectrometry and amplified fragment length polymorphism. Clin. Microbiol. Infect. 2016, 22, 277.e1. [Google Scholar] [CrossRef]
- Clinical and Laboratory Standards Institute. Performance Standards for Antifungal Susceptibility Testing of Yeasts; approved standard. In CLSI Document M60, 1st ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2017. [Google Scholar]
- Ehret-Sabatier, L.; Loew, D.; Goyffon, M.; Fehlbaum, P.; Hoffmann, J.A.; van Dorsselaer, A.; Bulet, P. Characterization of novel cysteine-rich antimicrobial peptides from scorpion blood. J. Biol. Chem. 1996, 271, 29537–29544. [Google Scholar] [CrossRef] [PubMed]
- Centers for Disease Control and Prevention. Antifungal Susceptibility Testing and Interpretation. Available online: https://www.cdc.gov/fungal/candida-auris/c-auris-antifungal.html (accessed on 10 January 2019).
- Fakhim, H.; Chowdhary, A.; Prakash, A.; Vaezi, A.; Dannaoui, E.; Meis, J.F.; Badali, H. In vitro interactions of echinocandins with triazoles against multidrug-resistant Candida auris. Antimicrob. Agents Chemother. 2017, 61, e01056-17. [Google Scholar] [CrossRef] [PubMed]
- Eldesouky, H.E.; Li, X.; Abutaleb, N.S.; Mohammad, H.; Seleem, M.N. Synergistic interactions of sulfamethoxazole and azole antifungal drugs against emerging multidrug-resistant Candida auris. Int. J. Antimicrob. Agents 2018, 52, 754–761. [Google Scholar] [CrossRef]
- Wall, G.; Chaturvedi, A.K.; Wormley, F.L., Jr.; Wiederhold, N.P.; Patterson, H.P.; Patterson, T.F.; Lopez-Ribot, J.L. Screening a repurposing library for inhibitors of multidrug-resistant Candida auris identifies ebselen as a repositionable candidate for antifungal drug development. Antimicrob. Agents Chemother. 2018, 62, e01084-18. [Google Scholar] [CrossRef]
- Marinovic, M.P.; Dal Mas, C.; Monte, G.G.; Felix, D.; Campeiro, J.D.; Hayashi, M.A.F. Crotamine: Function diversity and potential applications. In Snake Venoms; Gopalakrishnakone, P., Inagaki, H., Vogel, C.W., Mukherjee, A., Rahmy, T., Eds.; Springer: Dordrecht, The Netherlands, 2017; pp. 265–293. [Google Scholar]
- Dal Mas, C.; Pinheiro, D.A.; Campeiro, J.D.; Mattei, B.; Oliveira, V.; Oliveira, E.B.; Miranda, A.; Perez, K.R.; Hayashi, M.A. Biophysical and biological properties of small linear peptides derived from crotamine, a cationic antimicrobial/antitumoral toxin with cell penetrating and cargo delivery abilities. Biochim. Biophys. Acta Biomembr. 2017, 1859, 2340–2349. [Google Scholar] [CrossRef]
- da Silva, C.R.; de Andrade Neto, J.B.; de Sousa Campos, R.; Figueiredo, N.S.; Sampaio, L.S.; Magalhães, H.I.; Cavalcanti, B.C.; Gaspar, D.M.; de Andrade, G.M.; Lima, I.S.; et al. Synergistic effect of the flavonoid catechin, quercetin, or epigallocatechin gallate with fluconazole induces apoptosis in Candida tropicalis resistant to fluconazole. Antimicrob. Agents Chemother. 2014, 58, 1468–1478. [Google Scholar] [CrossRef] [PubMed]
Strains | AMB | FLC | MIC |
---|---|---|---|
C. auris CBS 10913 | 0.5/0.5 (S) | 2/2 (S) | 0.03/0.06 (S) |
C. auris 470/2015 | 2/2 (R) | >64/>64 (R) | 0.06/0.12 (S) |
C. auris 484/2015 | 4/4 (R) | >64/>64 (R) | 0.06/0.12 (S) |
C. auris 467/2015 | 2/4 (R) | >64/>64 (R) | 0.06/0.12 (S) |
C. auris CBS 14916 | 2/2 (R) | >64/>64 (R) | 0.12/0.12 (S) |
C. haemulonii 9873/2014 | 1/>16 (R) | 8/16 (R) | 0.03/0.06 (S) |
C. haemulonii 1112/2016 | 1/>16 (R) | 8/16 (R) | 0.03/0.06 (S) |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dal Mas, C.; Rossato, L.; Shimizu, T.; Oliveira, E.B.; da Silva Junior, P.I.; Meis, J.F.; Colombo, A.L.; Hayashi, M.A.F. Effects of the Natural Peptide Crotamine from a South American Rattlesnake on Candida auris, an Emergent Multidrug Antifungal Resistant Human Pathogen. Biomolecules 2019, 9, 205. https://doi.org/10.3390/biom9060205
Dal Mas C, Rossato L, Shimizu T, Oliveira EB, da Silva Junior PI, Meis JF, Colombo AL, Hayashi MAF. Effects of the Natural Peptide Crotamine from a South American Rattlesnake on Candida auris, an Emergent Multidrug Antifungal Resistant Human Pathogen. Biomolecules. 2019; 9(6):205. https://doi.org/10.3390/biom9060205
Chicago/Turabian StyleDal Mas, Caroline, Luana Rossato, Thaís Shimizu, Eduardo B. Oliveira, Pedro I. da Silva Junior, Jacques F. Meis, Arnaldo Lopes Colombo, and Mirian A. F. Hayashi. 2019. "Effects of the Natural Peptide Crotamine from a South American Rattlesnake on Candida auris, an Emergent Multidrug Antifungal Resistant Human Pathogen" Biomolecules 9, no. 6: 205. https://doi.org/10.3390/biom9060205