Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones

Proceedings of the Royal Society B: Biological Sciences

Volumn 279, Issue 1732, 2012, Pages 1351-1358

  Moran, Yehu ^a,b   Genikhovich, Grigory ^b   Gordon, Dalia ^a   Wienkoop, Stefanie ^b   Zenkert, Claudia ^c   Özbek, Suat ^c   Technau, Ulrich ^b   Gurevitz, Michael ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Nematocyst; Neurotoxin; Sea anemone; Venom

Indexed keywords

CYTOLOGY; IMMUNOASSAY; INVERTEBRATE; LARVA; RECOMBINATION; SECRETION; TOXIN; VENOM;

ACTINIARIA; ANEMONE; ANEMONIA VIRIDIS; ANTHOPLEURA ELEGANTISSIMA; ANTHOZOA; CNIDARIA; CRUSTACEA; HYDRIDAE; NEMATOSTELLA VECTENSIS; SCYPHOZOA;

EID: 84857522821     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.1731     Document Type: Article

References (47)

1. Ruppert, E. E. & Barnes, R. D. 1994 The cnidarians. In Invertebrate zoology, pp. 103-154, 6th edn. Philadelphia, PA: Saunders College Publishing.
2. Tibballs, J. 2006 Australian venomous jellyfish, envenomation syndromes, toxins and therapy. Toxicon 48, 830-859. (doi:10.1016/j.toxicon.2006.07.020)
3. Kass-Simon, G. & Scappaticci Jr, A. A. 2002 The behavioral and developmental physiology of nematocysts. Can. J. Zool. 80, 1772-1794. (doi:10.1139/z02-135)
4. Özbek, S., Balasubramanian, P. G. & Holstein, T. W. 2009 Cnidocyst structure and the biomechanics of discharge. Toxicon 54, 1038-1045. (doi:10.1016/j.toxicon. 2009.03.006)
5. Nüchter, T., Benoit, M., Engel, U., Ozbek, S. & Holstein, T. W. 2006 Nanosecond-scale kinetics of nematocyst discharge. Curr. Biol. 16, R316-R318. (doi:10. 1016/j.cub.2006.03.089)
6. Grotendorst, G. R. & Hessinger, D. A. 1999 Purification and partial characterization of the phospholipase A2 and co-lytic factor from sea anemone (Aiptasia pallida) nematocyst venom. Toxicon 37, 1779-1796. (doi:10.1016/ S0041-0101(99)00120-8)
7. Carrette, T. & Seymour, J. 2004 A rapid and repeatable method for venom extraction from cubozoan nematocysts. Toxicon 44, 135-139. (doi:10.1016/j.toxicon.2004. 04.008)
8. Schlesinger, A., Zlotkin, E., Kramarsky-Winter, E. & Loya, Y. 2009 Cnidarian internal stinging mechanism. Proc. R. Soc. B 276, 1063-1067. (doi:10.1098/rspb. 2008.1586)
9. Lotan, A., Fishman, L., Loya, Y. & Zlotkin, E. 1995 Delivery of a nematocyst toxin. Nature 375, 456. (doi:10.1038/375456a0)
10. Basulto, A., Perez, V. M., Noa, Y., Varela, C., Otero, A. J.& Pico, M. C. 2006 Immunohistochemical targeting of sea anemone cytolysins on tentacles, mesenteric filaments and isolated nematocysts of Stichodactyla helianthus. J. Exp. Zool. A Comp. Exp. Biol. 305, 253-258. (doi:10. 1002/jez.a.256)
11. Ramasamy, S., Isbister, G. K., Seymour, J. E. & Hodgson, W. C. 2005 Pharmacologically distinct cardiovascular effects of box jellyfish (Chironex fleckeri) venom and a tentacle-only extract in rats. Toxicol. Lett. 155, 219-226. (doi:10.1016/j.toxlet.2004.09.018)
12. Xiao, L., He, Q., Guo, Y., Zhang, J., Nie, F., Li, Y., Ye, X. & Zhang, L. 2009 Cyanea capillata tentacle-only extract as a potential alternative of nematocyst venom: its cardiovascular toxicity and tolerance to isolation and purification procedures. Toxicon 53, 146-152. (doi:10. 1016/j.toxicon.2008.10.023)
13. Wanke, E., Zaharenko, A. J., Redaelli, E. & Schiavon, E. 2009 Actions of sea anemone type 1 neurotoxins on voltage-gated sodium channel isoforms. Toxicon 54, 1102-1111. (doi:10.1016/j.toxicon.2009.04.018)
14. Moran, Y., Gordon, D. & Gurevitz, M. 2009 Sea anemone toxins affecting voltage-gated sodium channels: molecular and evolutionary features. Toxicon 54, 1089-1101. (doi:10.1016/j.toxicon.2009.02.028)
15. Fritzenwanker, J. H. & Technau, U. 2002 Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa). Dev. Genes Evol. 212, 99-103. (doi:10.1007/ s00427-002-0214-7)
16. Darling, J. A., Reitzel, A. R., Burton, P. M., Mazza, M. E., Ryan, J. F., Sullivan, J. C. & Finnerty, J. R. 2005 Rising starlet: the starlet sea anemone, Nematostella vectensis. Bioessays 27, 211-221. (doi:10.1002/bies.20181)
17. Putnam, N. H. et al. 2007 Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317, 86-94. (doi:10.1126/science. 1139158)
18. Moran, Y., Weinberger, H., Sullivan, J. C., Reitzel, A. M., Finnerty, J. R. & Gurevitz, M. 2008 Concerted evolution of sea anemone neurotoxin genes is revealed through analysis of the Nematostella vectensis genome. Mol. Biol. Evol. 25, 737-747. (doi:10.1093/molbev/msn021)
19. Moran, Y., Weinberger, H., Reitzel, A. M., Sullivan, J. C., Kahn, R., Gordon, D., Finnerty, J. R.& Gurevitz, M. 2008 Intron retention as a posttranscriptional regulatory mechanism of neurotoxin expression at early life stages of the starlet anemone Nematostella vectensis. J. Mol. Biol. 380, 437-443. (doi:10.1016/j.jmb.2008.05.011)
20. Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D. & Martindale, M. Q. 2009 Anatomy and development of the nervous system of Nematostella vectensis, an anthozoan cnidarian. Dev. Neurobiol. 69, 235-254. (doi:10.1002/dneu.20698)
21. Westerfield, M. 1994 The zebrafish book: a guide for the laboratory use of zebrafish. Eugene, OR: University of Oregon Press.
22. Moran, Y., Kahn, R., Cohen, L., Gur, M., Karbat, I., Gordon, D. & Gurevitz, M. 2007 Molecular analysis of the sea anemone toxin Av3 reveals selectivity to insects and demonstrates the heterogeneity of receptor site-3 on voltage-gated Na-channels. Biochem. J. 406, 41-48. (doi:10.1042/BJ20070233)
23. David, C. N. 1972 Quantitative method for maceration of hydra tissue.Wilhelm Roux's Arch. Dev. Biol. 171, 259-263.
24. Renfer, E., Amon-Hassenzahl, A., Steinmetz, P. R. & Technau, U. 2010 A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc. Natl Acad. Sci. USA 107, 104-108. (doi:10.1073/pnas. 0909148107)
25. Adamczyk, P. et al. 2010 A non-sulfated chondroitin stabilizes membrane tubulation in cnidarian organelles. J. Biol. Chem. 285, 25 613-25 623. (doi:10.1074/jbc. M110.107904)
26. David, C. N., Ozbek, S., Adamczyk, P., Meier, S., Pauly, B., Chapman, J., Hwang, J. S., Gojobori, T. & Holstein, T. W. 2008 Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet. 24, 431-438. (doi:10.1016/j.tig.2008.07.001)
27. Zenkert, C., Takahashi, T., Diesner, M. O. & Özbek, S. 2011 Morphological and molecular analysis of the Nematostella vectensis cnidom. PLoS ONE 6, e22725. (doi:10.1371/journal.pone.0022725)
28. Frank, P. G. & Bleakney, J. S. 1976 Histology and sexual reproduction of the anemone Nematostella vectensis Stephenson. J. Nat. Hist. 10, 441-449. (doi:10.1080/ 00222937600770331)
29. Watson, G. M. & Mariscal, R. N. 1983 Comparative ultrastructure of catch tentacles and feeding tentacles in the sea anemone Haliplanella. Tissue Cell 15, 939-953. (doi:10.1016/0040-8166(83)90059-9)
30. Westfall, J. A. & Sayyar, K. L. 1997 Ultrastructure of neurons and synapses in the tentacle epidermis of the sea anemone Calliactis parasitica. J. Morphol. 232, 207-216. (doi:10.1002/(SICI)1097-4687(199705)232: 2,207::AID-JMOR5.3.0.CO;2-6)
31. Delgado, L. M., Couve, E. & Schmachtenberg, O. 2010 GABA and glutamate immunoreactivity in tentacles of the sea anemone Phymactis papillosa (Lesson 1830). J. Morphol. 271, 845-852. (doi:10.1002/ jmor.10838)
32. Daly, M., Chaudhuri, A., Gusmão, L. & Rodríguez, E. 2008 Phylogenetic relationships among sea anemones (Cnidaria: Anthozoa: Actiniaria). Mol. Phylogenet. Evol. 48, 292-301. (doi:10.1016/j.ympev.2008.02.022)
33. Thomason, J. C. 1991 Cnida discharge and mechanism of venom delivery in Anemonia viridis (Cnidaria, Actiniaria). Hydrobiologia 216/217, 649-654. (doi:10.1007/ BF00026526)
34. Klug, M., Weber, J. & Tardent, P. 1989 Hemolytic and toxic properties of Hydra attenuata nematocysts. Toxicon 27, 325-339. (doi:10.1016/0041-0101(89)90180-3)
35. Krayesky, S. L., Mahoney, J. L., Kinler, K. M., Peltier, S., Calais, W., Allaire, K.& Watson, G. M. 2010 Regulation of spirocyst discharge in the model sea anemone, Nematostella vectensis. Mar. Biol. 8, 183-193. (doi:10.1007/s00227- 009-1384-x)
36. Bruhn, T. et al. 2001 Isolation and characterisation of five neurotoxic and cardiotoxic polypeptides from the sea anemone Anthopleura elegantissima. Toxicon 39, 693-702. (doi:10.1016/S0041-0101(00)00199-9)
37. Moran, Y., Cohen, L., Kahn, R., Karbat, I., Gordon, D. & Gurevitz, M. 2006 Expression and mutagenesis of the sea anemone toxin Av2 reveals key amino acid residues important for activity on insect voltage-gated sodium channels. Biochemistry 45, 8864-8873. (doi:10.1021/ bi060386b)
38. Frank, P. G. & Bleakney, J. S. 1978 Asexual reproduction, diet, and anomalies of the anemone Nematostella vectensis in Nova Scotia. Can. Field Nat. 92, 259-263.
39. Sebens, K. P. 1981 The allometry of feeding, energetics, and body size in three sea anemone species. Biol. Bull. 161, 152-171. (doi:10.2307/1541115)
40. Van-Praët, M. 1985 Nutrition of sea anemones. Adv. Mar. Biol. 22, 65-99. (doi:10.1016/S0065-2881(08) 60050-4)
41. Chintiroglou, C. & Koukouras, A. 1992 The feeding habits of three Mediterranean sea anemone species, Anemonia viridis (Forskal), Actinia equina (Linnaeus) and Cereus pedunculatus (Pennant). Helgolander. Meeresunters 46, 53-68. (doi:10.1007/BF02366212)
42. Edmunds, M., Potts, G. W., Swinfen, R. C. & Waters, V. L. 1974 The feeding preferences of Aeolidia papillosa (L.) (Mollusca, Nudibranchia). J. Mar. Biol. Assoc. UK 54, 939-947. (doi:10.1017/S0025315400057660)
43. Barlow, A., Pook, C. E., Harrison, R. A. & Wüster, W. 2009 Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proc. R. Soc. B 276, 2443-2449. (doi:10. 1098/rspb.2009.0048)
44. Fry, B. G., Vidal, N., Van der Weerd, L., Kochva, E. & Renjifo, C. 2009 Evolution and diversification of the toxicofera reptile venom system. J. Proteomics 72, 127-136. (doi:10.1016/j.jprot.2009.01.009)
45. Honma, T., Nagai, H., Nagashima, Y. & Shiomi, K. 2003 Molecular cloning of an epidermal growth factor-like toxin and two sodium channel toxins from the sea anemone Stichodactyla gigantea. Biochim. Biophys. Acta 1652, 103-106. (doi:10.1016/j.bbapap.2003.08.007)
46. Nagai, H., Takuwa, K., Nakao, M., Sakamoto, B., Crow, G. L. & Nakajima, T. 2000 Isolation and characterization of a novel protein toxin from the Hawaiian box jellyfish (sea wasp) Carybdea alata. Biochem. Biophys. Res. Commun. 275, 589-594. (doi:10.1006/bbrc.2000.3352)
47. Bode, H. R. 1996 The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. J. Cell. Sci. 109, 1155-1164.