Intraspecific variation of venom injected by fish-hunting Conus snails

Journal of Experimental Biology

Volumn 208, Issue 15, 2005, Pages 2873-2883

  Jakubowski, Jennifer A ^a   Kelley, Wayne P ^a,c   Sweedler, Jonathan V ^a   Gilly, William F ^b   Schulz, Joseph R ^b,d  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b STANFORD UNIVERSITY   (United States)

^c GLAXOSMITHKLINE   (United States)

^d OCCIDENTAL COLLEGE   (United States)

Author keywords

Conotoxin; Conus catus; Conus striatus; Duct venom; Injected venom; Intraspecific variation; Liquid chromatography; Mass spectrometry

Indexed keywords

CONOTOXIN; PEPTIDE;

ANIMAL; ARTICLE; CHEMISTRY; COMPARATIVE STUDY; CONUS SNAIL; ELECTROSPRAY MASS SPECTROMETRY; FRACTIONATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; SPECIES DIFFERENCE;

ANIMALS; CHEMICAL FRACTIONATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CONOTOXINS; CONUS SNAIL; PEPTIDES; SPECIES SPECIFICITY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ANIMALIA; CONUS CATUS; CONUS STRIATUS; CONUS TULIPA; GASTROPODA;

EID: 24644492990     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01713     Document Type: Article

References (50)

1. Binford, G. J. (2001). An analysis of geographic and intersexual chemical variation in venoms of the spider Tegenaria agrestis (Agelenidae). Toxicon 39, 955-968.
2. Bingham, J. P., Jones, A., Lewis, R. J., Andrew, P. R. and Alewood, P. F. (1996). Conus venom peptides (conopeptides): inter-species, intra-species and within individual variation revealed by ionspray mass spectrometry. In Biomedical Aspects of Marine Pharmacology (ed. E. Lazarovici, M. E. Spira and E. Zlotkin), pp. 13-27. Fort Collins, CO, USA: Alaken.
3. Bingham, J. P., Broxton, N. M., Livett, B. G., Down, J. G., Jones, A. and Moczydlowski, E. G. (2005). Optimizing the connectivity in disulfide-rich peptides: alpha-conotoxin SII as a case study. Anal. Biochem. 338, 48-61.
4. Bulaj, G., DeLaCruz, R., Azimi-Zonooz, A., West, P., Watkins, M., Yoshikami, D. and Olivera, B. M. (2001). Delta-conotoxin structure/function through a cladistic analysis. Biochemistry 40, 13201-13208.
5. Chippaux, J. P., Williams, V. and White, J. (1991). Snake venom variability: methods of study, results and interpretation. Toxicon 29, 1279-1303.
6. Chivian, E., Roberts, C. M. and Bernstein, A. S. (2003). The threat to cone snails. Science 302, 391.
7. Conticello, S. G., Gilad, Y., Avidan, N., Ben-Asher, E., Levy, Z. and Fainzilber, M. (2001). Mechanisms for evolving hypervariability: the case of conopeptides. Mol. Biol. Evol. 18, 120-131.
8. Craig, A. G., Fischer, W. H., Rivier, J. E., McIntosh, J. M. and Gray, W. R. (1995). MS based scanning methodologies applied to Conus venom. In Techniques in Protein Chemistry VI. Vol. VI (ed. J. W. Crabb), pp. 31-37. San Diego: Academic Press.
9. Craig, A. G., Zafaralla, G., Cruz, L. J., Santos, A. D., Hillyard, D. R., Dykert, J., Rivier, J. E., Gray, W. R., Imperial, J., Delacruz, R. G. et al. (1998). An O-glycosylated neuroexcitatory Conus peptide. Biochemistry 37, 16019-16025.
10. Creer, S., Malhotra, A., Thorpe, R. S., Stocklin, R., Favreau, P. and Chou, W. H. (2003). Genetic and ecological correlates of intraspecific variation in pitviper venom composition detected using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF-MS) and isoelectric focusing. J. Mol. Evol. 56, 317-329.
11. Cristina de Oliveira, K., Goncalves de Andrade, R. M., Giusti, A. L., Dias da Silva, W. and Tambourgi, D. V. (1999). Sex-linked variation of Loxosceles intermedia spider venoms. Toxicon 37, 217-221.
12. Daltry, J. C., Ponnudurai, G., Shin, C. K., Tan, N. H., Thorpe, R. S. and Wuster, W. (1996a). Electrophoretic profiles and biological activities: intraspecific variation in the venom of the Malayan pit viper (Calloselasma rhodostoma). Toxicon 34, 67-79.
13. Daltry, J. C., Wuster, W. and Thorpe, R. S. (1996b). Diet and snake venom evolution. Nature 379, 537-540.
14. Duda, T. F. and Palumbi, S. R. (1999). Molecular genetics of ecological diversification: duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc. Natl. Acad. Sci. USA 96, 6820-6823.
15. Duda, T. F. and Palumbi, S. R. (2000). Evolutionary diversification of multigene families: allelic selection of toxins in predatory cone snails. Mol. Biol. Evol. 17, 1286-1293.
16. Duda, T. F., Jr and Palumbi, S. R. (2004). Gene expression and feeding ecology: evolution of piscivory in the venomous gastropod genus Conus. Proc. R. Soc. Lond. B 271, 1165-1174.
17. Duda, T. F., Bingham, J. P., Livett, B. G., Kohn, A. J., Massilia, G. R., Schultz, J. R., Down, J., Sandall, D. and Sweedler, J. V. (2004). How much at risk are cone snails? Science 303, 955.
18. El Hafny, B., Chgoury, F., Adil, N., Cohen, N. and Hassar, M. (2002). Intraspecific variability and pharmacokinetic characteristics of Androctonus mauretanicus mauretanicus scorpion venom. Toxicon 40, 1609-1616.
19. Ellison, M. A. (2003). Novel natural and combinatorial alpha4,3 conotoxins as inhibitors of the alpha7 nicotinic acetylcholine receptor. PhD thesis, University of Utah, Salt Lake City, USA.
20. Escoubas, P., Corzo, G., Whiteley, B. J., Celerier, M. L. and Nakajima, T. (2002). Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry and high-performance liquid chromatography study of quantitative and qualitative variation in tarantula spider venoms. Rapid Commun. Mass Spectr. 16, 403-413.
21. Espiritu, D. J. D., Watkins, M., Dia-Monje, V., Cartier, G. E., Cruz, L. J. and Olivera, B. M. (2001). Venomous cone snails: molecular phylogeny and the generation of toxin diversity. Toxicon 39, 1899-1916.
22. Francischetti, I. M., Gombarovits, M. E., Valenzuela, J. G., Carlini, C. R. and Guimaraes, J. A. (2000). Intraspecific variation in the venoms of the South American rattlesnake (Crotalus durissus terrificus). Comp. Biochem. Physiol. 127C, 23-36.
23. Garrett, J. E., Buczek, O., Watkins, M., Olivera, B. M. and Bulaj, G. (2005). Biochemical and gene expression analyses of conotoxins in Conus textile venom ducts. Biochem. Biophys. Res. Commun. 328, 362-367.
24. Hopkins, C., Grilley, M., Miller, C., Shon, K. J., Cruz, L. J., Gray, W. R., Dykert, J., Rivier, J., Yoshikami, D. and Olivera, B. M. (1995). A new family of Conus peptides targeted to the nicotinic acetylcholine receptor. J. Biol. Chem. 270, 22361-22367.
25. Jakubowski, J. A. and Sweedler, J. V. (2004). Sequencing and mass profiling highly modified conotoxins using global reduction/alkylation followed by mass spectrometry. Anal. Chem. 76, 6541-6547.
26. Jimenez, E. C., Olivera, B. M., Gray, W. R. and Cruz, L. J. (1996). Contryphan is a D-tryptophan-containing Conus peptide. J. Biol. Chem. 271, 28002-28005.
27. Jimenez, E. C., Craig, A. G., Watkins, M., Hillyard, D. R., Gray, W. R., Gulyas, J., Rivier, J. E., Cruz, L. J. and Olivera, B. M. (1997). Bromocontryphan - post-translational bromination of tryptophan. Biochemistry 36, 989-994.
28. Jones, A., Bingham, J. P., Gehrmann, J., Bond, T., Loughnan, M., Atkins, A., Lewis, R. J. and Alewood, P. F. (1996). Isolation and characterization of conopeptides by high-performance liquid chromatography combined with mass spectrometry and tandem mass spectrometry. Rapid Commun. Mass Spectrom. 10, 138-143.
29. Kalapothakis, E. and Chavez-Olortegui, C. (1997). Venom variability among several Tityus serrulatus specimens. Toxicon 35, 1523-1529.
30. Kohn, A. J. (1956). Piscivorous gastropods of the genus Conus. Proc. Natl. Acad. Sci. USA 42, 168-172.
31. Lai, C. C. and Her, G. R. (2000). Analysis of phospholipase A(2) glycosylation patterns from venom of individual bees by capillary electrophoresis/electrospray ionization mass spectrometry using an ion trap mass spectrometer. Rapid Commun. Mass Spectr. 14, 2012-2018.
32. Lu, B. S., Yu, F., Zhao, D., Huang, P. T. and Huang, C. F. (1999). Conopeptides from Conus striatus and Conus textile by cDNA cloning. Peptides 20, 1139-1144.
33. MacKessy, S. P., Williams, K. and Ashon, K. G. (2003). Ontogenetic variation in venom composition and diet of Crotalus oreganus concolor: A case of venom paedomorphosis? Copeia 4, 769-782.
34. Marshall, J., Kelley, W. P., Rubakhin, S. S., Bingham, J. P., Sweedler, J. V. and Gilly, W. F. (2002). Anatomical correlates of venom production in Conus californicus. Biol. Bull. 203, 27-41.
35. Martinez, J. S., Olivera, B. M., Gray, W. R., Craig, A. G., Groebe, D. R., Abramson, S. N. and McIntosh, J. M. (1995). Alpha-conotoxin EI, a new nicotinic acetylcholine receptor antagonist with novel selectivity. Biochemistry 34, 14519-14526.
36. + channels. Biochem. Biophys. Res. Commun. 303, 238-246.
37. Monteiro, R. Q., Dutra, D. L. S., Machado, O. L. T., Carlini, C. R., Guimaraes, J. A., Bon, C. and Zingali, R. B. (1998a). Bothrops jararaca snakes produce several bothrojaracin isoforms following an individual pattern. Comp. Biochem. Physiol. 120B, 791-798.
38. Monteiro, R. Q., Yamanouye, N., Carlini, C. R., Guimaraes, J. A., Bon, C. and Zingali, R. B. (1998b). Variability of bothrojaracin isoforms and other venom principles in individual jararaca (Bothrops jararaca) snakes maintained under seasonally invariant conditions. Toxicon 36, 153-163.
39. Olivera, B. M. (1997). E. E. Just Lecture, 1996. Conus venom peptides, receptor and ion channel targets, and drug design - 50 million years of neuropharmacology. Mol. Biol. Cell 8, 2101-2109.
40. Pimenta, A. M. C., Almeida, F. D., de Lima, M. E., Martin-Eauclaire, M. F. and Bougis, P. E. (2003). Individual variability in Tityus serrulatus (Scorpiones, Buthidae) venom elicited by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectr. 17, 413-418.
41. Ramilo, C. A., Zafaralla, G. C., Nadasdi, L., Hammerland, L. G., Yoshikami, D., Gray, W. R., Kristipati, R., Ramachandran, J., Miljanich, G. and Olivera, B. M. (1992). Novel alpha- and omega-conotoxins from Conus striatus venom. Biochemistry 31, 9919-9926.
42. Santos, A. D., McIntosh, J. M., Hillyard, D. R., Cruz, L. J. and Olivera, B. M. (2004). The A-superfamily of conotoxins - structural and functional divergence. J. Biol. Chem. 279, 17596-17606.
43. Schulz, J. R., Norton, A. G. and Gilly, W. F. (2004). The projectile tooth of a fish-hunting cone snail: Conus catus injects venom into fish prey using a high-speed ballistic mechanism. Biol. Bull. 207, 77-79.
44. Shon, K. J., Grilley, M. M., Marsh, M., Yoshikami, D., Hall, A. R., Kurz, B., Gray, W. R., Imperial, J. S., Hillyard, D. R. and Olivera, B. M. (1995). Purification, characterization, synthesis, and cloning of the lockjaw peptide from Conus purpurascens venom. Biochemistry 34, 4913-4918.
45. Shon, K. J., Grilley, M., Jacobsen, R., Cartier, G. E., Hopkins, C., Gray, W. R., Watkins, M., Hillyard, D. R., Rivier, J., Torres, J. et al. (1997). A noncompetitive peptide inhibitor of the nicotinic acetylcholine receptor from Conus purpurascens venom. Biochemistry 36, 9581-9587.
46. Teichert, R. W., Rivier, J., Dykert, J., Cervini, L., Gulyas, J., Bulaj, G., Ellison, M. and Olivera, B. M. (2004). AlphaA-Conotoxin OIVA defines a new alphaA-conotoxin subfamily of nicotinic acetylcholine receptor inhibitors. Toxicon 44, 207-214.
47. Vianna Braga, M. C., Konno, K., Portaro, F. C., Carlos de Freitas, J., Yamane, T., Olivera, B. M. and Pimenta, D. C. (2005). 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, 113-122.
48. Walker, C. S., Steel, D., Jacobsen, R. B., Lirazan, M. B., Cruz, L. J., Hooper, D., Shetty, R., DelaCruz, R. C., Nielsen, J. S., Zhou, L. M. et al. (1999). The T-superfamily of conotoxins. J. Biol. Chem. 274, 30664-30671.
49. Watson, E. and Kenney, W. C. (1992). Multiple peak formation from reversed-phase liquid chromatography of recombinant human platelet-derived growth factor. J. Chromatogr. 606, 165-170.
50. Zafaralla, G. C., Ramilo, C., Gray, W. R., Karlstrom, R., Olivera, B. M. and Cruz, L. J. (1988). Phylogenetic specificity of cholinergic ligands: alpha-conotoxin SI. Biochemistry 27, 7102-7105.