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BioMed Research International
Volume 2014, Article ID 675985, 9 pages
http://dx.doi.org/10.1155/2014/675985
Review Article

State of the Art in the Studies on Crotamine, a Cell Penetrating Peptide from South American Rattlesnake

1Laboratório de Genética, Instituto Butantan, Av. Vital Brasil, 1500 05503-900 São Paulo, SP, Brazil
2Departamento de Farmacologia, Universidade Federal de São Paulo (UNIFESP), São Paulo, SP, Brazil
3Labomar-Instituto de Ciências do Mar, Universidade Federal do Ceará, Fortaleza, CE, Brazil
4Universidade Estadual da Amazônia (UEA) e Laboratório de Bioquímica e Biologia Molecular, Centro de Biotecnologia da Amazônia (CBA), Manaus, AM, Brazil

Received 15 March 2013; Revised 5 August 2013; Accepted 8 August 2013; Published 15 January 2014

Academic Editor: Marcelo Palma Sircili

Copyright © 2014 Irina Kerkis et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Nicastro, L. Franzoni, C. De Chiara, A. C. Mancin, J. R. Giglio, and A. Spisni, “Solution structure of crotamine, a Na+ channel affecting toxin from Crotalus durissus terrificus venom,” European Journal of Biochemistry, vol. 270, no. 9, pp. 1969–1979, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. V. Fadel, P. Bettendorff, T. Herrmann et al., “Automated NMR structure determination and disulfide bond identification of the myotoxin crotamine from Crotalus durissus terrificus,” Toxicon, vol. 46, no. 7, pp. 759–767, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. A. M. Siqueira, N. F. Martins, M. E. De Lima et al., “A proposed 3D structure for crotamine based on homology building, molecular simulations and circular dichroism,” Journal of Molecular Graphics and Modelling, vol. 20, no. 5, pp. 389–398, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. M. A. Coronado, A. Gabdulkhakov, D. Georgieva et al., “Structure of the polypeptide crotamine from the Brazilian rattlesnake Crotalus durissus terrificus,” Acta Crystallographica D, vol. 69, pp. 1958–1964, 2013. View at Google Scholar
  5. G. Rádis-Baptista, B. G. de la Torre, and D. Andreu, “Insights into the uptake mechanism of NrTP, a cell-penetrating peptide preferentially targeting the nucleolus of tumour cells,” Chemical Biology and Drug Design, vol. 79, no. 6, pp. 907–915, 2012. View at Publisher · View at Google Scholar · View at Scopus
  6. Crotalus durissus terrificus (Laurenti, 1768) Taxonomy ID: 8732.
  7. W. Beçak, M. L. Beçak, H. R. S. Nazareth, and S. Ohno, “Close karyological kinship between the reptilian suborder serpentes and the class aves,” Chromosoma, vol. 15, no. 5, pp. 606–617, 1964. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Rádis-Baptista, T. Kubo, N. Oguiura et al., “Structure and chromosomal localization of the gene for crotamine, a toxin from the South American rattlesnake, Crotalus durissus terrificus,” Toxicon, vol. 42, no. 7, pp. 747–752, 2003. View at Publisher · View at Google Scholar · View at Scopus
  9. J. M. Gonçalves and E. G. Arantes, “Estudos sobre venenos de serpentes Brasileiras. III-determinação quantitativa de crotamina no veneno de cascavel Brasileira,” Anais da Academia Brasileira de Ciências, vol. 28, pp. 369–371, 1956. View at Google Scholar
  10. N. Oguiura, M. E. Camargo, A. R. P. Da Silva, and D. S. P. Q. Horton, “Quantification of crotamine, a small basic myotoxin, in South American rattlesnake (Crotalus durissus terrificus) venom by enzyme-linked immunosorbent assay with parallel-lines analysis,” Toxicon, vol. 38, no. 3, pp. 443–448, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. D. L. Cameron and A. T. Tu, “Chemical and functional homology of myotoxin a from prairie rattlesnake venom and crotamine from South American rattlesnake venom,” Biochimica et Biophysica Acta, vol. 532, no. 1, pp. 147–154, 1978. View at Google Scholar · View at Scopus
  12. A. Kerkis, I. Kerkis, G. Rádis-Baptista et al., “Crotamine is a novel cell-penetrating protein from the venom of rattlesnake Crotalus durissus terrificus,” FASEB Journal, vol. 18, no. 12, pp. 1407–1409, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. I. Kerkis, M. A. F. Hayashi, N. F. Lizier et al., “Pluripotent stem cells as an in vitro model of neuronal differentiation,” in Embryonic Stem Cells-Differentiation and Pluripotent Alternatives, Kallos, Ed., pp. 81–98, InTech, Rijeka, Croatia, 2011. View at Google Scholar
  14. P. C. Chen, M. A. Hayashi, E. B. Oliveira et al., “DNA-interactive properties of crotamine, a cell-penetrating polypeptide and a potential drug carrier,” PLoS ONE, vol. 7, no. 11, Article ID e48913, pp. 1–11, 2012. View at Google Scholar
  15. G. Rádis-Baptista and I. Kerkis, “Crotamine, a small basic polypeptide myotoxin from rattlesnake venom with cell-penetrating properties,” Current Pharmaceutical Design, vol. 17, no. 38, pp. 4351–4361, 2011. View at Google Scholar
  16. M. A. Hayashi, F. D. Nascimento, A. Kerkis et al., “Cytotoxic effects of crotamine are mediated through lysosomal membrane permeabilization,” Toxicon, vol. 52, no. 3, pp. 508–517, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Boni-Mitake, H. Costa, V. S. Vassilieff, and J. R. Rogero, “Distribution of 125I-labeled crotamine in mice tissues,” Toxicon, vol. 48, no. 5, pp. 550–555, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. J. P. Blumling III and G. A. Silva, “Targeting the brain: advances in drug delivery,” Current Pharmaceutical Biotechnology, vol. 13, no. 12, pp. 2417–2426, 2012. View at Publisher · View at Google Scholar
  19. E. C. de Lange, “The physiological characteristics and transcytosis mechanisms of the blood-brain barrier (BBB),” Current Pharmaceutical Biotechnology, vol. 13, no. 12, pp. 2319–2327, 2012. View at Publisher · View at Google Scholar
  20. F. D. Nascimento, M. A. F. Hayashi, A. Kerkis et al., “Crotamine mediates gene delivery into cells through the binding to heparan sulfate proteoglycans,” Journal of Biological Chemistry, vol. 282, no. 29, pp. 21349–21360, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. D. Sarko, B. Beijer, R. G. Boy et al., “The pharmacokinetics of cell-penetrating peptides,” Molecular Pharmaceutics, vol. 7, no. 6, pp. 2224–2231, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Gehl, “Electroporation: theory and methods, perspectives for drug delivery, gene therapy and research,” Acta Physiologica Scandinavica, vol. 177, no. 4, pp. 437–447, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. G. M. Poon and J. Gariépy, “Cell-surface proteoglycans as molecular portals for cationic peptide and polymer entry into cells,” Biochemical Society Transactions, vol. 35, no. 4, pp. 788–793, 2007. View at Google Scholar · View at Scopus
  24. D. Jha, R. Mishra, S. Gottschalk et al., “CyLoP-1: a novel cysteine-rich cell-penetrating peptide for cytosolic delivery of cargoes,” Bioconjugate Chemistry, vol. 22, no. 3, pp. 319–328, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Schweizer, “Cationic amphiphilic peptides with cancer-selective toxicity,” European Journal of Pharmacology, vol. 625, no. 1–3, pp. 190–194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. N. Boulanger, C. Lowenberger, P. Volf et al., “Characterization of a defensin from the sand fly Phlebotomus duboscqi induced by challenge with bacteria or the protozoan parasite Leishmania major,” Infection and Immunity, vol. 72, no. 12, pp. 7140–7146, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. G. Maróti Gergely, A. Kereszt, É. Kondorosi, and P. Mergaert, “Natural roles of antimicrobial peptides in microbes, plants and animals,” Research in Microbiology, vol. 162, no. 4, pp. 363–374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. Y. Park, S. N. Park, S. Park et al., “Synergism of Leu-Lys rich antimicrobial peptides and chloramphenicol against bacterial cells,” Biochimica et Biophysica Acta, vol. 1764, no. 1, pp. 24–32, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Bulet, R. Stöcklin, and L. Menin, “Anti-microbial peptides: from invertebrates to vertebrates,” Immunological Reviews, vol. 198, pp. 169–184, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. K. A. Brogden, “Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria?” Nature Reviews Microbiology, vol. 3, no. 3, pp. 238–250, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. M. L. Crouch, L. A. Becker, I. S. Bang, H. Tanabe, A. J. Ouellette, and F. C. Fang, “The alternative sigma factor σE is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides,” Molecular Microbiology, vol. 56, no. 3, pp. 789–799, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. A. M. S. Mayer, A. D. Rodríguez, R. G. S. Berlinck, and N. Fusetani, “Marine pharmacology in 2007-8: marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; Affecting the immune and nervous system, and other miscellaneous mechanisms of action,” Comparative Biochemistry and Physiology C, vol. 153, no. 2, pp. 191–222, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. N. Y. Yount, D. Kupferwasser, A. Spisni et al., “Selective reciprocity in antimicrobial activity versus cytotoxicity of hBD-2 and crotamine,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 35, pp. 14972–14977, 2009. View at Google Scholar
  34. G. Rádis-Baptista, N. Oguiura, M. A. F. Hayashi et al., “Nucleotide sequence of crotamine isoform precursors from a single South American rattlesnake (Crotalus durissus terrificus),” Toxicon, vol. 37, no. 7, pp. 973–984, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Maróti Gergely, A. Kereszt, É. Kondorosi, and P. Mergaert, “Natural roles of antimicrobial peptides in microbes, plants and animals,” Research in Microbiology, vol. 162, no. 4, pp. 363–374, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. E. S. Yamane, F. C. Bizerra, E. B. Oliveira et al., “Unraveling the antifungal activity of a South American rattlesnake toxin crotamine,” Biochimie, vol. 95, no. 2, pp. 231–240, 2013. View at Publisher · View at Google Scholar
  37. T. Calandra and O. Marchetti, “Clinical trials of antifungal prophylaxis among patients undergoing surgery,” Clinical Infectious Diseases, vol. 39, supplement 4, pp. S185–S192, 2004. View at Publisher · View at Google Scholar · View at Scopus
  38. G. Kragol, L. Otvos Jr., J. Feng, W. Gerhard, and J. D. Wade, “Synthesis of a disulfide-linked octameric peptide construct carrying three different antigenic determinants,” Bioorganic and Medicinal Chemistry Letters, vol. 11, no. 11, pp. 1417–1420, 2001. View at Publisher · View at Google Scholar · View at Scopus
  39. F. D. Nascimento, L. Sancey, A. Pereira et al., “The natural cell-penetrating peptide crotamine targets tumor tissue in vivo and triggers a lethal calcium-dependent pathway in cultured cells,” Molecular Pharmaceutics, vol. 9, no. 2, pp. 211–221, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. Y. Lan, Y. Ye, J. Kozlowska, J. K. W. Lam, A. F. Drake, and A. J. Mason, “Structural contributions to the intracellular targeting strategies of antimicrobial peptides,” Biochimica et Biophysica Acta, vol. 1798, no. 10, pp. 1934–1943, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. D. W. Hoskin and A. Ramamoorthy, “Studies on anticancer activities of antimicrobial peptides,” Biochimica et Biophysica Acta, vol. 1778, no. 2, pp. 357–375, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. A. R. Lizzi, V. Carnicelli, M. M. Clarkson, A. Di Giulio, and A. Oratore, “Lactoferrin derived peptides: mechanisms of action and their perspectives as antimicrobial and antitumoral agents,” Mini-Reviews in Medicinal Chemistry, vol. 9, no. 6, pp. 687–695, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. B. Findlay, G. G. Zhanel, and F. Schweizer, “Cationic amphiphiles, a new generation of antimicrobials inspired by the natural antimicrobial peptide scaffold,” Antimicrobial Agents and Chemotherapy, vol. 54, no. 10, pp. 4049–4058, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Papo and Y. Shai, “Host defense peptides as new weapons in cancer treatment,” Cellular and Molecular Life Sciences, vol. 62, no. 7-8, pp. 784–790, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Pereira, A. Kerkis, M. A. Hayashi et al., “Crotamine toxicity and efficacy in mouse models of melanoma,” Expert Opinion on Investigational Drugs, vol. 20, no. 9, pp. 1189–1200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. G. León, L. Sánchez, A. Hernández et al., “Immune response towards snake venoms,” Inflammation and Allergy-Drug Targetsno, vol. 10, no. 5, pp. 381–398, 2011. View at Publisher · View at Google Scholar
  47. K. A. Marr, “The changing spectrum of candidemia in oncology patients: therapeutic implications,” Current Opinion in Infectious Diseases, vol. 13, no. 6, pp. 615–620, 2000. View at Google Scholar · View at Scopus
  48. C. Zhao, T. Nguyen, L. Liu, R. E. Sacco, K. A. Brogden, and R. I. Lehrer, “Gallinacin-3, an inducible epithelial β-defensin in the chicken,” Infection and Immunity, vol. 69, no. 4, pp. 2684–2691, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. B. G. Fry, “From genome to “venome”: molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins,” Genome Research, vol. 15, no. 3, pp. 403–420, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Wanke, A. J. Zaharenko, E. Redaelli, and E. Schiavon, “Actions of sea anemone type 1 neurotoxins on voltage-gated sodium channel isoforms,” Toxicon, vol. 54, no. 8, pp. 1102–1111, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Diochot, A. Baron, L. D. Rash et al., “A new sea anemone peptide, APETx2, inhibits ASIC3, a major acid-sensitive channel in sensory neurons,” EMBO Journal, vol. 23, no. 7, pp. 1516–1525, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Diochot and M. Lazdunski, “Sea anemone toxins affecting potassium channels,” Progress in molecular and subcellular biology, vol. 46, pp. 99–122, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Peigneur, D. J. Orts, A. R. Prieto da Silva et al., “Crotamine pharmacology revisited: novel insights based on the inhibition of KV channels,” Molecular Pharmacologyno, vol. 82, no. 1, pp. 90–96, 2012. View at Google Scholar
  54. C. T. Rizzi, J. L. Carvalho-de-Souza, E. Schiavon, A. C. Cassola, E. Wanke, and L. R. P. Troncone, “Crotamine inhibits preferentially fast-twitching muscles but is inactive on sodium channels,” Toxicon, vol. 50, no. 4, pp. 553–562, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Rodrigues, A. Santos, B. G. de la Torre et al., “Molecular characterization of the interaction of crotamine-derived nucleolar targeting peptides with lipid membranes,” Biochimica et Biophysica Actano, vol. 818, no. 11, pp. 2707–2717, 2012. View at Google Scholar