Hydrozoan nematocytes send and receive synaptic signals induced by mechano-chemical stimuli

Journal of Experimental Biology

Volumn 211, Issue 17, 2008, Pages 2876-2888

  Oliver, Dominik ^a,b   Brinkmann, Martin ^a,c   Sieger, Thiemo ^a,d   Thurm, Ulrich ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c Smiths Medical International ^*  (Germany)

^d Tyska Skolan   (Sweden)

Author keywords

Cnidocyte; Hair cell; Mechanoreception; Postsynaptic potential

Indexed keywords

ANIMAL; ARTICLE; CHEMORECEPTOR; COMPARATIVE STUDY; EVOKED RESPONSE; HYDROZOA; MECHANORECEPTOR; METABOLISM; NERVE TRACT; PATCH CLAMP; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ANIMALS; CHEMORECEPTORS; EVOKED POTENTIALS; HYDROZOA; MECHANORECEPTORS; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; SYNAPTIC TRANSMISSION;

HYDROIDA; HYDROZOA;

EID: 53949096316     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.018515     Document Type: Article

References (45)

1. Anderson, P. A. V. and McKay, M. C. (1987). The electrophysiology of cnidocytes. J. Exp. Biol. 133, 215-230.
2. Boudkkazi, S., Carlier, E., Ankri, N., Fronzaroli, L., Caillard, O. and Debanne, D. (2006). Synaptic timing at unitary synaptic contacts between layer 5 pyramidal neurons. FENS Abstr. vol. 3, A151.4.
3. Brinkmann, A. and Petersen, K. W. (1960). On some distinguishing characters of Dipurena reesi Vanucci 1956 and Cladonema radiatum Dujardin 1843. Publ. Stat. Napoli 31, 386-392.
4. Brinkmann, M. (1994). Das Rezeptor-Effektor-System der Nesselzellen eines Hydropolypen (Corynidae). Inaugural-Dissertation der Naturwissenschaftlichen Fakultät der Universität Münster, 1-115.
5. Brinkmann, M., Oliver, D. and Thurm, U. (1995). Interaction of mechano- and chemosensory signals within the same sensory cell. Pflügers Arch. Eur. J. Physiol. 429 (Suppl), R153.
6. Brinkmann, M., Oliver, D. and Thurm, U. (1996). Mechanoelectric transduction in nematocytes of a hydropolyp (Corynidae). J. Comp. Physiol. A 178, 125-138.
7. Dunlap, K., Takeda, K. and Brehm, P. (1987). Activation of a calcium-dependent photoprotein by chemical signalling through gap junctions. Nature 325, 60-62.
8. Fuchs, P. A. (1996). Synaptic transmission at vertebrate hair cells. Curr. Opin. Neurobiol. 13, 514-519.
9. Fuchs, P. A., Glowatzki, E. and Moser, T. (2003). The afferent synapse of cochlear hair cells. Curr. Opin. Neurobiol. 13, 452-458.
10. Germain, G. and Anctil, M. (1996). Evidence for intercellular coupling and connexin-like protein in the luminescent endoderm of Renilla koellikeri (Cnidaria, Anthozoa). Biol. Bull. 191, 353-366.
11. Gitter, A. H. and Thurm, U. (1996). Rapid exocytosis of stenotele nematocysts in Hyd ra vulgaris. J. Comp, Physiol. A 178, 117-124.
12. Gitter, A. H., Oliver, D. and Thurm, U. (1994). Calcium- and voltage-dependence of nematocyst discharge in Hydra vulgaris. J. Comp. Physiol. A 175, 115-122.
13. Golz, R. (1994). The apical surface of hydrozoan nematocytes: Structural adaptations to mechanosensory and exocytotic functions. J. Morphol. 222, 49-59.
14. Golz, R. and Thurm, U. (1991). Cytoskeleton-membrane interactions in the cnidocil complex of hydrozoan nematocytes. Cell Tissue Res. 263, 573-583.
15. Holtmann, M. and Thurm, U. (2001a). Mono- and oligo-vesicular synapses and their connectivity in a cnidarian sensory epithelium (Coryne tubulosa). J. Comp. Neurol. 432, 537-549.
16. Holtmann, M. and Thurm, U. (2001b). Variations of concentric hair cells in a cnidarian sensory epithelium (Coryne tubulosa). J. Comp. Neurol. 432, 550-563.
17. Johnston, D. and Wu, S. M.-S. (1995). Foundations of Cellular Neurophysiology, pp. 369, 392-395. London: MIT Press.
18. Kass-Simon, G. and Pierobon, P. (2007). Cnidarian chemical neurotransmission, an updated overview. Comp. Biochem. Physiol. A 146, 9-25.
19. Kass-Simon, G. and Scappaticci, A. A., Jr (2004). Glutamatergic and GABAnergic control in the tentacle effector systems of Hydra vulgaris. Hydrobiologia 530/531, 67-71.
20. Katz, B. and Miledi, R. (1967). The timing of calcium action during neuromuscular transmission. J. Physiol. 189, 535-544.
21. Kerfoot, P. A. H., Mackie, G. O., Meech, R. W., Roberts, A. and Singla, C. L. (1985). Neuromuscular transmission in the jellyfish Aglantha digitale. J. Exp. Biol. 116, 1-25.
22. Lawonn, P. (1999). Die rezeptorischen und effektorischen Funktionen der Nesselzellen von Hydra vulgaris und ihre sensorische und synaptische Modulation. Inaugural-Dissertation. Naturwissenschaftliche Fakultät der Universität Münster 1-187.
23. Mackie, G. O. (2004). Epithelial conduction: recent findings, old questions, and where do we go from here? Hydrobiologia 530/531, 73-80.
24. Mire, P., Nasse, J. and Venable-Thibodeaux, S. (2000). Gap junctional communication in the vibration-sensitive response of sea anemones. Hear. Res. 144, 109-123.
25. Murphey, A. D., Hadley, R. D. and Kater, S. B. (1983). Axotomy-induced parallel increases in electrical and dye coupling between identified neurons of Heliosoma. J. Neurosci. 3, 1422-1429.
26. Neher, E. (1993). Secretion without full fusion. Nature 363, 497-498.
27. Nüchter, T., Benoit, M., Engel, U., Özbek, S. and Holstein, T. W. (2006). Nanosecond-scale kinetics of nematocyst discharge. Curr. Biol. 16, R316-R318.
28. Pantin, C. F. A. (1942). The excitation of nematocysts. J. Exp. Biol. 19, 294-310.
29. Parker, G. H. (1916). The effector systems of actinians. J. Exp. Zool. 21, 461-484.
30. Price, R. B. and Anderson, P. A. V. (2006). Chemosensory pathways in the capitate tentacles of the hydroid Cladonema. Invert. Neurosci. 6, 23-32.
31. Purcell, J. E. and Anderson, P. A. V. (1995). Electrical responses to water-soluble components of fish mucus recorded from the nematocytes of a fish predator, Physalia physalis. Mar. Fresh. Behav. Physiol. 26, 149-162.
32. Shibayama, J., Paznekas, W., Seki, A., Taffet, S., Jabs, E. W., Delmar, M. and Musa, H. (2005). Functional characterization of connexin43 mutations found in patients with oculodentodigital dysplasia. Circ. Res. 96, e83-e91.
33. Sieger, T. and Thurm, U. (1997). Glutamatergic properties of synaptic transmission of the hair-cell-analog nematocytes of Corynidae polyps and their modulation by choline-derivatives. Göttingen Neurobiol. Report 1997, 736.
34. Slautterback, D. B. (1967). The cnidoblast-musculoepithelial cell complex in the tentacles of Hydra. Z. Zellforschg. 79, 296-318.
35. Spencer, A. N. (1982). The physiology of a coelenterate neuromuscular synapse. J. Comp. Physiol. 148, 353-363.
36. Tardent, P. (1995). The cnidarian cnidocyte, a high-tech cellular weaponry. BioEssays 17, 351-362.
37. Thurm, U. and Lawonn, P. (1990). Die sensorischen Eigenschaften des Cnidocil-Apparates als Grundlage des Beutefangs der Hydropolypen. Verh. Dtsch. Zool. Ges. 83, 431.
38. Thurm, U., Brinkmann, M., Golz, R., Lawonn, P. and Oliver, D. (1998a). The supramolecular basis of mechanoelectric transduction studied in concentric hair bundles of invertebrates. In From Structure to Information in Sensory Systems (ed. C. Taddei-Ferretti, and C. Musio), pp. 228-236. Singapore, New Jersey, London. Hong Kong: World Scientific Publishing.
39. Thurm, U., Brinkmann, M., Holtmann, M., Lawonn, P., Oliver, D. and Sieger, T. (1998b). Modulation of the output of a mechanosensory cell by chemosensory and synaptic inputs. In From Structure to Information in Sensory Systems (ed. C. Taddei-Ferretti and C. Musio), pp. 237-253. London: World Scientific Publishing.
40. Thurm, U., Brinkmann, M., Golz, R., Holtmann, M., Oliver, D. and Sieger, T. (2004). Mechanoreception and synaptic transmission of hydrozoan nematocytes. Hydrobiologia 530/531, 97-105.
41. Vyshedskiy, A. and Lin, J.-W. (1998). Change of transmitter release kinetics during facilitation revealed by prolonged test pulses at the inhibitor of the crayfish opener muscle. J. Neurophysiol. 78, 1791-1799.
42. Vyshedskiy, A., Delaney, K. R. and Lin, J.-W. (1998). Neuromodulators enhance transmitter release by two separate mechanisms at the inhibitor of crayfish opener muscle. J. Neurosci. 18, 5160-5169.
43. Waldeck, R. F., Pereda, A. and Faber, D. S. (2000). Properties and plasticity of paired-pulse depression at a central synapse. J. Neurosci. 20, 5312-5320.
44. Watson, G. M. and Hessinger, D. A. (1989). Cnidocytes and adjacent supporting cells form receptor-effector complexes in anemone tentacles. Tissue Cell 21, 17-24.
45. Westfall, J. A. (1996). Synapses in the first-evolved nervous systems. J. Neurocytol. 25, 735-746.