Identification and localization of a [Met5]-enkephalin-like peptide in the mollusc, Lymnaea stagnalis

Brain Research

Volumn 737, Issue 1-2, 1996, Pages 1-15

  Ewadinger, N M ^a   Ridgway, R L ^b   Syed, N I ^a   Lukowiak, K ^a   Bulloch, A G M ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b SEATTLE PACIFIC UNIVERSITY   (United States)

Author keywords

Gastropod; Heart; High performance liquid chromatography; Identified neuron; Immunocytochemistry; Neuronal map; Opioid peptide; Radioimmunoassay

Indexed keywords

ENKEPHALIN; NEUROPEPTIDE; OPIATE PEPTIDE; METENKEPHALIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOCYTOCHEMISTRY; MOLLUSC; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; ANIMAL; ANTIBODY SPECIFICITY; CHEMISTRY; CROSS REACTION; FLUORESCENT ANTIBODY TECHNIQUE; HEART ATRIUM; HEART MUSCLE; IMMUNOBLOTTING; IMMUNOLOGY; LYMNAEA; PHYSIOLOGY;

ANIMALS; ANTIBODY SPECIFICITY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROSS REACTIONS; ELECTROPHYSIOLOGY; ENKEPHALIN, METHIONINE; FLUORESCENT ANTIBODY TECHNIQUE; HEART ATRIA; IMMUNOBLOTTING; LYMNAEA; MYOCARDIUM; NEURONS; OPIOID PEPTIDES; RADIOIMMUNOASSAY;

EID: 0030597065     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-8993(96)00649-X     Document Type: Article

References (76)

1. [1] Benjamin, P.R. and Rose, R.M., Central generation of bursting in the feeding system of the snail Lymnaea stagnalis, J. Exp. Biol., 80 (1979) 93-118.
2. [2] Benjamin, P.R. and Pilkington, J.B., The electrotonic location of low-resistance intercellular junctions between a pair of giant neurons in the snail Lymnaea, J. Physiol., 370 (1986) 111-126.
3. [3] Benjamin, P.R., Rose, R.M., Slade, C.T. and Lacy, M.G., Morphology of identified neurones in the buccal ganglia of Lymnaea stagnalis, J. Exp. Biol., 80 (1979) 119-135.
4. [4] Benjamin, P.R., Elliott, C.J. and Ferguson, G.P., Neural network analysis in the snail brain. In A. Selverston (Ed.), Model Neural Networks and Behaviour, Plenum Press, New York, 1985, pp. 87-108.
5. [5] Boer, H.H., Van Minnen, J., Stefano, G.B. and Leung, M.K., Opioid peptides in CNS of Lymnaea stagnalis. In H.H. Boer, W.P.M. Geraerts and J. Joosse (Eds.), Molluscan Models, Proceedings of the Second Symposium on Molluscan Neurobiology, North Holland Publishing/Elsevier, Amsterdam, 1987, pp. 68-72.
6. [6] Bogerd, J., Geraerts, W.P.M., Van Heerikhuizen, H., Kerkhoven, R.M. and Joosse, J., Characterization and evolutionary aspects of a transcript encoding a neuropeptide precursor of Lymnaea neurons, VD1 and RPD2, Mol. Brain Res., 11 (1991) 47-54.
7. [7] Bogerd, J., Van Kesteren, R.E., Van Heerikhuizen, H., Geraerts, W.P.M., Veenstra, J., Smit, A.B. and Joosse, J., Alternative splicing generates diversity of VD1/RPD2 α-peptides in the central nervous system of Lymnaea stagnalis, Cell. Mol. Neurobiol., 13 (1993) 123-136.
8. [8] Bogerd, J., Li, K.W., Jiménez, C.R., Van der Schors, R.C., Ebberink, R.H.M. and Geraerts, W.P.M., Processing, axonal transport and cardioregulatory functions of peptides derived from two related prohormones generated by alternative splicing of a single gene in identified neurons VD1 and RPD2 of Lymnaea, Mol. Brain Res., 23 (1994) 66-72.
9. [9] Buckett, K.J., Dockray, G.J., Osborne, N.N. and Benjamin, P.R., Pharmacology of the myogenic heart of the pond snail Lymnaea stagnalis, J. Neurophysiol., 63 (1990) 1413-1425.
10. [10] Buckett, K.J., Peters, M. and Benjamin, P.R., Excitation and inhibition of the heart of the snail, Lymnaea, by non-FMRFamidergic motoneurons, J. Neurophysiol., 63 (1990) 1436-1447.
11. [11] Buckett, K.J., Peters, M., Dockray, G.J., Van Minnen, J. and Benjamin, P.R., Regulation of heartbeat in Lymnaea by motoneurons containing FMRFamide-like peptides, J. Neurophysiol., 63 (1990) 1426-1435.
12. [12] Bulloch, A.G.M. and Ridgway, R.L., Comparative aspects of gastropod neurobiology. In O. Breicbach and W. Kutsch (Eds.), The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach, Birkhauser Verlag, Basel, 1994, pp. 89-113.
13. [13] Chard, T., In T.S. Work and E. Work (Eds.), An Introduction to Radioimmunoassay and Related Techniques, Elsevier Biomedical Press, New York, 1982.
14. [14] Cook, A., The withdrawal response of a freshwater snail (Lymnaea stagnalis L.), J. Exp. Biol., 62 (1975) 783-796.
15. [15] Coons, A.H., Fluorescent antibody methods. In J.F. Danielli (Ed.), General Cytochemical Methods, Academic Press, New York, 1958, pp. 399-422.
16. [16] Croll, R.P. and Chiasson, B.J., Postembryonic development of serotonin-like immunoreactivity in the central nervous system of the snail, Lymnaea stagnalis, J. Comp. Neurol., 280 (1989) 122-142.
17. -16 mole level, J. Neuroimmunol., 8 (1985) 57-67.
18. [18] Dyakonova, T.L., Moroz, L.L. and Winlow, W., Facilitation of electrical coupling between identified central neurones by met-enkephalin in Helix and Lymnaea, J. Physiol., 438 (1991) 283P.
19. [19] Elekes, K., Stefano, G.B. and Carpenter, D.O., Enkephalin-like immunoreactive neurons in the central nervous system of gastropods (Helix pomatia, Lymnaea stagnalis, Aplysia californica): a comparative immunocytochemical study, Cell Tissue Res., 272 (1993) 329-341.
20. [20] Elliot, C.J. and Benjamin, P.R., Interactions of pattern generating interneurones controlling feeding in Lymnaea stagnalis, J. Neurophysiol., 54 (1985) 1396-1411.
21. [21] Ewadinger, N.M., Syed, N.I., Ridgway, R.L., Bulloch, A.G.M. and Lukowiak, K., Putative cardiovascular role for met-enkephalin and α-peptide in Lymnaea stagnalis, Soc. Neurosci. Abstr., 18(1) (1992) 469.
22. [22] Ewadinger, N.M., Syed, N.I., Lukowiak, K. and Bulloch, A.G.M., Differential tracer coupling between pairs of identified neurones of the mollusc Lymnaea stagnalis, J. Exp. Biol., 192 (1994) 291-297.
23. [23] Ferguson, G.P. and Benjamin, P.R., The whole-body withdrawal response of Lymnaea stagnalis, J. Exp. Biol., 158 (1991) 63-95.
24. [24] Geraerts, W.P.M., Ter Maat, A. and Vreugdenhill, E., The peptidergic neuroendocrine control of egg laying behaviour in Aplysia and Lymnaea. In H. Laufer and R. Downer (Eds.). Invertebrate endocrinology. Vol. 2. Endocrinology of selected invertebrate types, Alan R. Liss, New York, 1988, pp. 144-231.
25. [25] Gesser, B.P. and Larsson, L.I., Changes from enkephalin-like to gastrin/cholecystokinin-like immunoreactivity in snail neurons, J. Neurosci., 5 (1985) 1412-1417.
26. [26] Gutiérrez, R. and Asai, M., IR-met and IR-leu-enkephalin content in the perioesophageal ganglia of Helix aspersa seasonal variations, Comp. Biochem. Physiol., 100C (1991) 609-613.
27. [27] Harrison, L.M., Kastin, A.J., Weber, J.T., Banks, W.A., Hurley, D.L. and Zadina, J.E., The opiate system in invertebrates, Peptides, 15 (1994) 1309-1329.
28. [28] Hawkes, R., The dot immunobinding assay, Meth. Enzymol., 121 (1986) 484-491.
29. [29] Hawkes, R., Niday, E. and Gordon, J., A dot-immunobinding asssay for monoclonal and other antibodies, Anal. Biochem., 119 (1982) 142-147.
30. [30] Hughes, J., Search for the endogenous ligand of the opiate receptor, Neurosci. Res. Prog. Bull., 13 (1975) 55-58.
31. [31] Hughes, J., Isolation of a endogenous compound from the brain with pharmacological properties similar to morphine, Brain Res., 88 (1975) 295-308.
32. [32] Hughes, J., Smith, T.W., Kosterlitz, H.W., Fothergill, L.A., Morgan, B.A. and Morris, H.R., Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature, 258 (1975) 577-579.
33. [33] Jaffe, J.H. and Martin, W.R., Opioid analgesics and antagonists. In L. Goodman and A. Gilman (Eds.). The Pharmacological Basis of Therapeutics, Pergamon Press, New York, 1990, pp. 485-521.
34. [34] Janse, C., Van der Wilt, G.J., Van der Plas, J. and Van der Proest, M., Central and peripheral neurons involved in oxygen perception in the pulmonate snail Lymnaea stagnalis (Mollusca, Gastropoda), Comp. Biochem. Physiol., 82A (1985) 459-469.
35. [35] Jaros, P.P., Enkephalins, biologically active neuropeptidcs in invertebrates with special reference to crustaceans. In K. Wiese, W.D. Krenz, J. Tautz, H. Reichert and B. Mullony (Eds.), Frontiers in Crustacean Neurobiology, Birhäuser, Basel, 1990, pp. 471-482.
36. [36] Kemenes, G., Rózsa, K.S., Stefano, G.B. and Carpenter, D.O., Distinct receptors for leu- and met-enkephalin on the metacerebral giant cell of Aplysia, Cell. Mol. Neurobiol., 12 (1992) 107-119.
37. [37] Kerkhoven, R.M., Croll, R.P., Van Minnen, J., Bogerd, J., Ramkema, M.D., Lodder, H. and Boer, H.H., Axonal mapping of the giant peptidergic neurons VD1 and RPD2 located in the CNS of the pond snail Lymnaea stagnalis, with particular reference to the innervation of the auricle of the heart, Brain Res., 565 (1991) 8-16.
38. [38] Kerkhoven, R.M., Croll, R.P., Ramkema, M.D., Van Minnen, J., Bogerd, J. and Boer, H.H., The VD1/RPD2 neuronal system in the central nervous system of the pond snail Lymnaea stagnalis studied by in situ hybridization and immunocytochemistry, Cell Tissue Res., 267 (1992) 551-559.
39. [39] Leung, M. and Stefano, G.B., Isolation of molluscan opioid peptides, Life Sci., 33 (1983) 77-80.
40. [40] Leung, M.K. and Stefano, G.B., Isolation and identification of enkephalins in pedal ganglia of Mytilus edulis (mollusca), Proc. Natl. Acad. Sci. USA. 81 (1984) 955-958.
41. [41] Leung, M.K. and Stefano, G.B., Comparative neurobiology of opioids in invertebrates with special attention to senescent alterations, Prog. Neurobiol., 28 (1987) 131-159.
42. [42] Leung, M.K., Boer, H.H., Van Minnen, J., Lundy, J. and Stefano, G.B., Evidence for an enkephalinergic system in the nervous system of the pond snail, Lymnaea stagnalis, Brain Res., 531 (1990) 66-71.
43. [43] Leung, M.K., Le, S., Houston, S. and Stefano, G.B., Degradation of met-enkephalin by hemolymph peptidases in Mytilus edulis, Cell. Mol. Neurobiol., 5 (1992) 367-378.
44. [44] Lewis, R.V., Stern, A.S., Kimura, S., Rossier, J., Stein, S. and Udenfriend, S., An about 50,000-dalton protein in adrenal medulla: a common precursor of [met]- and [leu]-enkephalin, Science, 208 (1980) 1459-1461.
45. [45] Li, K.W. and Geraerts, W.P.M., Molecular characterization, biosynthesis and release of molluscan insulin-related peptides of Lymnaea stagnalis. In K.S. Kits, H.H. Boer and J. Joosse (Eds.), Molluscan Neurobiology, North-Holland Publishing/Elsevier, Amsterdam, 1991, pp. 322-327.
46. 2 (FMRFamide) and novel related peptides are encoded by multiple copies by a single gene in the snail Lymnaea stagnalis, J. Neurosci., 10 (1990) 412-419.
47. [47] Lukowiak, K., Thornhill, J.A. and Edstrom, J.P., Methionine enkephalin increases CNS suppressive control exerted over gill reflex behaviors and associated neural activity in Aplysia californica, Reg. Peptides, 3 (1982) 303-310.
48. [48] Luo, D., Stell, W.K. and Cupo, A., Synthesis and post-translational processing of proenkephalin in light- and dark-adapted chicken retinas, Neurochem. Int., 19 (1991) 483-494.
49. [49] Lüschen, W., Buck, F., Willig, A. and Jaros, P.P., Isolation, sequence analysis and physiological properties of enkephalins in the nervous tissue of the shore crab Carcinus meanas L., Proc. Natl. Acad. Sci. USA, 88 (1991) 8671-8675.
50. [50] Magoski, N.M., Sycd, N.I. and Bulloch, A.G.M., A neuronal network from the mollusc Lymnaea stagnalis, Brain Res., 645 (1994) 201-214.
51. B: immunolabeling of neurons in diverse invertebrates, J. Comp. Neurol., 273 (1988) 500-512.
52. [52] Murphy, A.D. and Lukowiak, K., Identified small cardioactive peptide B immunoreactive neurons and patterned motor activity in the buccal ganglia of Helisoma. In H.H. Boer, W.P.M. Geraerts and J. Joosse (Eds.), Neurobiology: Molluscan Models, North-Holland Publishing/Elsevier, Amsterdam, 1987, pp. 124-126.
53. [53] Nezlin, L., Moroz, L., Elofsson, R. and Sakharov, D., Immunolabeled neuroactive substances in the osphradium of the pond snail Lymnaea stagnalis, Cell Tissue Res., 275 (1994) 269-275.
54. [54] Ortiz, T., Piñero, J. and Coveñas, R., Met-enkephalin-like immunoreactivity in the nervous system of Helix aspersa, Zool. Sci., 4 (1987) 743-746.
55. [55] Sakharov, D., Nezlin, L., Moroz, L. and Elofsson, R., Patterns of enkephalin immunolabeling in the pulmonate snail Cepaea nemoralis and related molluscs, Brain Res., 620 (1993) 114-121.
56. [56] Santama, N, Brierley, M., Burke, J.F. and Benjamin, P.R., Neural network controlling feeding in Lymnaea stagnalis: immunocytochemical localization of myomodulin, small cardioactive peptide, buccalin and FMRFamide-related peptides, J. Comp. Neurol., 342 (1994) 352-365.
57. [57] Schot, L.P.C., Boer, H.H., Swaab, D.F. and Van Noorden, S., Immunocytochemical demonstration of peptidergic neurons in the central nervous system of the pond snail Lymnaea stagnalis with antisera raised to biologically active peptides of vertebrates, Cell Tissue Res., 216 (1981) 273-291.
58. [58] Skelton, M., Alevizos, A. and Koester, J., Control of the cardiovascular system of Aplysia by identified neurons, Experentia, 48 (1992) 809-817.
59. [59] Smit, A.B., Jiménez, C.R., Dirks, R.W., Croll, R.P. and Geraerts, W.P.M., Characterization of a cDNA clone encoding multiple copies of the neuropeptide APGWamide in the mollusk Lymnaea stagnalis, J. Neurosci., 12 (1992) 1709-1715.
60. [60] Soffe, S.R. and Benjamin, P.R., Morphology of two electrotonically-coupled giant neurosecretory neurons in the snail, Lymnaea stagnalis, Comp. Biochem. Physiol., 67A (1980) 35-46.
61. [61] Stefano, G.B., In CRC Handbook of Comparative Opioid and Related Neuropeptide Mechanisms, CRC Press, Boca Raton, 1986.
62. [62] Stefano, G.B. and Catapane, E.J., Enkephalins increase dopamine levels in the CNS of a marine mollusc, Life Sci., 24 (1979) 1617-1622.
63. [63] Stefano, G.B., Kream, R.M. and Zukin, R.S., Demonstration of stereospecific opiate binding in the nervous tissue of the marine mollusc Mytilus edulis, Brain Res., 181 (1980) 440-445.
64. [64] Stefano, G.B., Hall, B., Makman, M.H. and Dvorkin, B., Opioid inhibition of dopamine release from nervous tissue of Mytilus edulis and Octopus bimaculatus, Science, 213 (1981) 928-930.
65. [65] Sternberger, L.A., The unlabeled antibody peroxidase-antiperoxidase (PAP) method. In L.A. Sternberger (Ed.), Immunocytochemistry, Wiley, New York, 1979, pp. 104-169.
66. [66] Syed, N.I. and Winlow, W., Coordination of locomotor and cardiorespiratory networks of Lymnaea stagnalis by a pair of identified interneurones, J. Exp. Biol., 158 (1991) 37-62.
67. [67] Syed, N.I. and Winlow, W., Respiratory behavior in the pond snail Lymnaea stagnalis II. neural elements of the central pattern generator (CPG), J. Comp. Physiol., 169A (1991) 557-768.
68. [68] Syed, N.I., Harrison, D. and Winlow, W., Locomotion in Lymnaea: role of serotonergic A cluster neurones, Symp. Biol. Hung., 36 (1988) 387-402.
69. [69] Ter Maat, A., Jansen, R.F. and Bos, N.P.A., The effects of met-enkephalin and FMRFamide on the excitability of the neurosecretory caudodorsal cells of the pond snail. In G.B. Stefano (Ed.), CRC Handbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol.2, CRC Press, Boca Raton, FL, 1986, pp. 145-157.
70. [70] Truman, J.W. and Taghert, P.H., Insect Neuropeptides. In D.T. Krieger, M.J. Brownstein and J.B. Martin (Eds.), Brain Peptides, John Wiley, New York, 1983, pp. 165-181.
71. [71] Van der Wilt, G., Van der Roest, M. and Janse, C., The role of two peptidergic giant neurons in modulation of respiratory behaviour in the pond snail, Lymnaea stagnalis, Symp. Biol. Hung., 36 (1988) 377-386.
72. [72] Van Duivenboden, Y.A. and Ter Maat, A., Masculinity and receptivity in the hermaphrodite pond snail, Lymnaea stagnalis, Anim. Behav., 33 (1985) 885-891.
73. [73] Van Duivenboden, Y.A. and Ter Maat, A., Mating behavior of Lymnaea stagnalis, Malacologia, 28 (1988) 53-64.
74. [74] Vreugdenhil, E., Jackson, J.F., Bouwmeester, T., Smit, A.B., Van Minnen, J., Van Heerikhuizen, H., Klootwijk, J. and Joosse, J., Isolation, characterization and evolutionary aspects of a cDNA clone encoding multiple neuropeptides involved in the stereotyped egg-laying behavior of the freshwater snail Lymnaea stagnalis, J. Neurosci., 8 (1988) 4184-4191.
75. [75] Williamson, M.E. and Emson, P.C., Peptides in the brain of the common snail, Helix aspersa, Biochem. Soc. Trans., 10 (1982) 384-385.
76. [76] Zamboni, L. and De Martino, C., Buffered picric acid-formaldehyde: a new, rapid fixative for electron microscopy, J. Cell Biol., 35 (1967) 148A.