Proteomics of the neurotoxic fraction from the sea anemone Bunodosoma cangicum venom: Novel peptides belonging to new classes of toxins

Comparative Biochemistry and Physiology - Part D: Genomics and Proteomics

Volumn 3, Issue 3, 2008, Pages 219-225

  Zaharenko, André Junqueira ^a   Ferreira Jr , Wilson Alves ^a   Oliveira, Joacir Stolarz ^a   Richardson, Michael ^b   Pimenta, Daniel Carvalho ^c   Konno, Katsuhiro ^d   Portaro, Fernanda C V ^c   de Freitas, José Carlos ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FUNDAÇÃO EZEQUIEL DIAS   (Brazil)

^c INSTITUTO BUTANTAN   (Brazil)

^d UNIVERSITY OF TOYAMA   (Japan)

Author keywords

Bunodosoma cangicum; HPLC; Ion channels; Mass spectrometry; Neurotoxins; Peptide mass fingerprint; Sea anemone

Indexed keywords

NEUROTOXIN; POTASSIUM CHANNEL; SEA ANEMONE TOXIN; SODIUM CHANNEL;

ACTION POTENTIAL; AMINO ACID SEQUENCE; ARTICLE; BIOASSAY; BUNODOSOMA CANGICUM; CONTROLLED STUDY; CRAB; ELECTROSPRAY MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEA ANEMONE;

ACTINIARIA; ARANEAE; BUNODOSOMA CANGICUM; DECAPODA (CRUSTACEA); GASTROPODA; SCORPIONES; SERPENTES;

EID: 47849109030     PISSN: 1744117X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbd.2008.04.002     Document Type: Article

References (55)

1. Anderluh G., and Macek P. Cytolytic peptide and protein toxins from sea anemones (Anthozoa: Actiniaria). Toxicon 40 (2002) 111-124
2. Barhanin J., Hugues M., Schweitz H., Vincent J.P., and Lazdunski M. Structure-function relationships of sea anemone toxin II from Anemonia sulcata. J. Biol. Chem. 256 (1981) 5764-5769
3. Barona J., Batista C.V., Zamudio F.Z., Gomez-Lagunas F., Wanke E., Otero R., and Possani L.D. Proteomic analysis of the venom and characterization of toxins specific for Na+- and K+ -channels from the Colombian scorpion Tityus pachyurus. Biochim. Biophys. Acta. 1764 (2006) 76-84
4. Batista C.V., del Pozo L., Zamudio F.Z., Contreras S., Becerril B., Wanke E., and Possani L.D. Proteomics of the venom from the Amazonian scorpion Tityus cambridgei and the role of prolines on mass spectrometry analysis of toxins. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 803 (2004) 55-66
5. Batista C.V., D'Suze G., Gomez-Lagunas F., Zamudio F.Z., Encarnacion S., Sevcik C., and Possani L.D. Proteomic analysis of Tityus discrepans scorpion venom and amino acid sequence of novel toxins. Proteomics 6 (2006) 3718-3727
6. Belmonte G., Menestrina G., Pederzolli C., Krizaj I., Gubensek F., Turk T., and Macek P. Primary and secondary structure of a pore-forming toxin from the sea anemone, Actinia equina L., and its association with lipid vesicles. Biochim. Biophys. Acta. 1192 (1994) 197-204
7. Beress L., and Beress R. Purification of three polypeptides with neuro- and cardiotoxic activity from the sea anemone Anemonia sulcata. Toxicon 13 (1975) 359-367
8. Beress L., Wunderer G., and Wachter E. Amino acid sequence of toxin III from Anemonia sulcata. Hoppe-Seyler Z. Physiol. Chem. 358 (1977) 985-988
9. Bosmans F., Aneiros A., and Tytgat J. The sea anemone Bunodosoma granulifera contains surprisingly efficacious and potent insect-selective toxins. FEBS Lett. 532 (2002) 131-134
10. Bruhn T., Schaller C., Schulze C., Sanchez-Rodriguez J., Dannmeier C., Ravens U., Heubach J.F., Eckhardt K., Schmidtmayer J., Schmidt H., Aneiros A., Wachter E., and Beress L. Isolation and characterisation of five neurotoxic and cardiotoxic polypeptides from the sea anemone Anthopleura elegantissima. Toxicon 39 (2001) 693-702
11. Castañeda O., Sotolongo V., Amor A.M., Stocklin R., Anderson A.J., Harvey A.L., Engstrom A., Wernstedt C., and Karlsson E. Characterization of a potassium channel toxin from the Caribbean Sea anemone Stichodactyla helianthus. Toxicon 33 (1995) 603-613
12. Clauser K.R., Baker P., and Burlingame A.L. Role of accurate mass measurement (+/- 10 ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal. Chem. 71 (1999) 2871-2882
13. Cunha R.B., Santana A.N., Amaral P.C., Carvalho M.D., Carvalho D.M., Cavalheiro E.A., Maigret B., Ricart C.A., Cardi B.A., Sousa M.V., and Carvalho K.M. Primary structure, behavioral and electroencephalographic effects of an epileptogenic peptide from the sea anemone Bunodosoma cangicum. Toxicon 45 (2005) 207-217
14. de Oliveira J.S., Zaharenko A.J., Freitas J.C., Konno K., de Andrade S.A., Portaro F.C., Richardson M., Sant'anna O.A., and Tambourgi D.V. Caissarolysin I (Bcs I), a new hemolytic toxin from the Brazilian sea anemone Bunodosoma caissarum: purification and biological characterization. Biochim. Biophys. Acta 1760 (2006) 453-461
15. Diochot S., Schweitz H., Beress L., and Lazdunski M. Sea anemone peptides with a specific blocking activity against the fast inactivating potassium channel Kv3.4. J. Biol. Chem. 273 (1998) 6744-6749
16. Diochot S., Loret E., Bruhn T., Beress L., and Lazdunski M. APETx1, a new toxin from the sea anemone Anthopleura elegantissima, blocks voltage-gated human ether-a-go-go-related gene potassium channels. Mol. Pharmacol. 64 (2003) 59-69
17. Diochot S., Baron A., Rash L.D., Deval E., Escoubas P., Scarzello S., Salinas M., and Lazdunski M. A new sea anemone peptide, APETx2, inhibits ASIC3, a major acid-sensitive channel in sensory neurons. Embo J. 23 (2004) 1516-1525
18. Favreau P., Menin L., Michalet S., Perret F., Cheneval O., Stocklin M., Bulet P., and Stocklin R. Mass spectrometry strategies for venom mapping and peptide sequencing from crude venoms: case applications with single arthropod specimen. Toxicon 47 (2006) 676-687
19. Fox J.W., Ma L., Nelson K., Sherman N.E., and Serrano S.M. Comparison of indirect and direct approaches using ion-trap and Fourier transform ion cyclotron resonance mass spectrometry for exploring viperid venom proteomes. Toxicon 47 (2006) 700-714
20. Goudet C., Ferrer T., Galan L., Artiles A., Batista C.F., Possani L.D., Alvarez J., Aneiros A., and Tytgat J. Characterization of two Bunodosoma granulifera toxins active on cardiac sodium channels. Br. J. Pharmacol. 134 (2001) 1195-1206
21. Grotendorst G.R., and Hessinger D.A. Enzymatic characterization of the major phospholipase A2 component of sea anemone (Aiptasia pallida) nematocyst venom. Toxicon 38 (2000) 931-943
22. Guette C., Legros C., Tournois G., Goyffon M., and Celerier M.L. Peptide profiling by matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry of the Lasiodora parahybana tarantula venom gland. Toxicon 47 (2006) 640-649
23. Hanck D.A., and Sheets M.F. Site-3 toxins and cardiac sodium channels. Toxicon 49 (2007) 181-193
24. Honma T., Iso T., Ishida M., Nagashima Y., and Shiomi K. Occurrence of type 3 sodium channel peptide toxins in two species of sea anemones (Dofleinia armata and Entacmaea ramsayi). Toxicon 41 (2003) 637-639
25. Honma T., Hasegawa Y., Ishida M., Nagai H., Nagashima Y., and Shiomi K. Isolation and molecular cloning of novel peptide toxins from the sea anemone Antheopsis maculata. Toxicon 45 (2005) 33-41
26. Honma T., Minagawa S., Nagai H., Ishida M., Nagashima Y., and Shiomi K. Novel peptide toxins from acrorhagi, aggressive organs of the sea anemone Actinia equina. Toxicon 46 (2005) 768-774
27. Jakubowski J.A., Kelley W.P., and Sweedler J.V. Screening for post-translational modifications in conotoxins using liquid chromatography/mass spectrometry: an important component of conotoxin discovery. Toxicon 47 (2006) 688-699
28. Kawai N., Miwa A., Shimazaki K., Sahara Y., Robinson H.P., and Nakajima T. Spider toxin and the glutamate receptors. Comp. Biochem. Physiol. C 98 (1991) 87-95
29. Lagos P., Duran R., Cervenansky C., Freitas J.C., and Silveira R. Identification of hemolytic and neuroactive fractions in the venom of the sea anemone Bunodosoma cangicum. Braz. J. Med. Biol. Res. 34 (2001) 895-902
30. Lewis R.J., and Garcia M.L. Therapeutic potential of venom peptides. Nat. Rev. Drug Discov. 2 (2003) 790-802
31. Li S., Wang J., Zhang X., Ren Y., Wang N., Zhao K., Chen X., Zhao C., Li X., Shao J., Yin J., West M.B., Xu N., and Liu S. Proteomic characterization of two snake venoms: Naja naja atra and Agkistrodon halys. Biochem. J. 384 (2004) 119-127
32. Machado L.F., Laugesen S., Botelho E.D., Ricart C.A., Fontes W., Barbaro K.C., Roepstorff P., and Sousa M.V. Proteome analysis of brown spider venom: identification of loxnecrogin isoforms in Loxosceles gaucho venom. Proteomics 5 (2005) 2167-2176
33. Malpezzi E.L., Freitas J.C., Muramoto K., and Kamiya H. Characterization of peptides in sea anemone venom collected by a novel procedure. Toxicon 31 (1993) 853-864
34. Nascimento D.G., Rates B., Santos D.M., Verano-Braga T., Barbosa-Silva A., Dutra A.A., Biondi I., Martin-Eauclaire M.F., De Lima M.E., and Pimenta A.M. Moving pieces in a taxonomic puzzle: venom 2D-LC/MS and data clustering analyses to infer phylogenetic relationships in some scorpions from the Buthidae family (Scorpiones). Toxicon 47 (2006) 628-639
35. Nawarak J., Sinchaikul S., Wu C.Y., Liau M.Y., Phutrakul S., and Chen S.T. Proteomics of snake venoms from Elapidae and Viperidae families by multidimensional chromatographic methods. Electrophoresis 24 (2003) 2838-2854
36. Nevalainen T.J., Peuravuori H.J., Quinn R.J., Llewellyn L.E., Benzie J.A., Fenner P.J., and Winkel K.D. Phospholipase A2 in cnidaria. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 139 (2004) 731-735
37. Norton R.S. Structure and structure-function relationships of sea anemone proteins that interact with the sodium channel. Toxicon 29 (1991) 1051-1084
38. Oliveira J.S., Redaelli E., Zaharenko A.J., Cassulini R.R., Konno K., Pimenta D.C., Freitas J.C., Clare J.J., and Wanke E. Binding specificity of sea anemone toxins to Nav 1.1-1.6 sodium channels: unexpected contributions from differences in the IV/S3-S4 outer loop. J. Biol. Chem. 279 (2004) 33323-33335
39. Oliveira J.S., Zaharenko A.J., Ferreira Jr. W.A., Konno K., Shida C.S., Richardson M., Lucio A.D., Beirao P.S., and Freitas J.C. BcIV, a new paralyzing peptide obtained from the venom of the sea anemone Bunodosoma caissarum. A comparison with the Na+ channel toxin BcIII. Biochim. Biophys. Acta 1764 (2006) 1592-1600
40. Pimenta A.M., De Marco Almeida F., de Lima M.E., Martin-Eauclaire M.F., and Bougis P.E. Individual variability in Tityus serrulatus (Scorpiones, Buthidae) venom elicited by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 17 (2003) 413-418
41. Pimenta A.M., Rates B., Bloch Jr. C., Gomes P.C., Santoro M.M., de Lima M.E., Richardson M., and Cordeiro Mdo N. Electrospray ionization quadrupole time-of-flight and matrix-assisted laser desorption/ionization tandem time-of-flight mass spectrometric analyses to solve micro-heterogeneity in post-translationally modified peptides from Phoneutria nigriventer (Aranea, Ctenidae) venom. Rapid Commun. Mass Spectrom. 19 (2005) 31-37
42. Quinton L., Le Caer J.P., Vinh J., Gilles N., and Chamot-Rooke J. Fourier transform mass spectrometry: a powerful tool for toxin analysis. Toxicon 47 (2006) 715-726
43. Rogers J.C., Qu J., Tanada T.N., Scheuer T., and Catterall W.A. Molecular determinants of high affinity binding of alpha-scorpion toxin and sea anemone toxin in the S3-S4 extracellular loop in domain IV of the Na+ channel alpha subunit. J. Biol. Chem. 271 (1996) 15950-15962
44. Salceda E., Garateix A., and Soto E. The sea anemone toxins BgII and BgIII prolong the inactivation time course of the tetrodotoxin-sensitive sodium current in rat dorsal root ganglion neurons. J. Pharmacol. Exp. Ther. 303 (2002) 1067-1074
45. Schweitz H., Bruhn T., Guillemare E., Moinier D., Lancelin J.M., Beress L., and Lazdunski M. Kalicludines and kaliseptine. Two different classes of sea anemone toxins for voltage sensitive K+ channels. J. Biol. Chem. 270 (1995) 25121-25126
46. Shiomi K., Qian W.H., Lin X.Y., Shimakura K., Nagashima Y., and Ishida M. Novel polypeptide toxins with crab lethality from the sea anemone Anemonia erythraea. Biochim. Biophys. Acta. 1335 (1997) 191-198
47. Shiomi K., Honma T., Ide M., Nagashima Y., Ishida M., and Chino M. An epidermal growth factor-like toxin and two sodium channel toxins from the sea anemone Stichodactyla gigantea. Toxicon 41 (2003) 229-236
48. Simpson R.J., Reid G.E., Moritz R.L., Morton C., and Norton R.S. Complete amino acid sequence of tenebrosin-C, a cardiac stimulatory and haemolytic protein from the sea anemone Actinia tenebrosa. Eur. J. Biochem. 190 (1990) 319-328
49. Sunahara S., Muramoto K., Tenma K., and Kamiya H. Amino acid sequence of two sea anemone toxins from Anthopleura fuscoviridis. Toxicon 25 (1987) 211-219
50. Taggi A.E., Meinwald J., and Schroeder F.C. A new approach to natural products discovery exemplified by the identification of sulfated nucleosides in spider venom. J. Am. Chem. Soc. 126 (2004) 10364-10369
51. Terlau H., and Olivera B.M. Conus venoms: a rich source of novel ion channel-targeted peptides. Physiol. Rev. 84 (2004) 41-68
52. Vianna Braga M.C., Konno K., Portaro F.C., Freitas J.C., Yamane T., Olivera B.M., and Pimenta D.C. Mass spectrometric and high performance liquid chromatography profiling of the venom of the Brazilian vermivorous mollusk Conus regius: feeding behavior and identification of one novel conotoxin. Toxicon 45 (2005) 113-122
53. Watters M.R., and Stommel E.W. Marine neurotoxins: envenomations and contact toxins. Curr. Treat Options Neurol. 6 (2004) 115-123
54. Wilson D., and Alewood P.F. Taxonomy of Australian Funnel-web spiders using rp-HPLC/ESI-MS profiling techniques. Toxicon 47 (2006) 614-627
55. Zaharenko, A.J., Ferreira, W.A. Jr., Oliveira, J.S., Konno, K., Richardson, M., Schiavon, E., Wanke, E., Freitas, J.C. in press Revisiting cangitoxin, a sea anemone peptide: purification and characterization of cangitoxins II and III from the venom of Bunodosoma cangicum. Toxicon.