Peptide signaling in Hydra

International Journal of Developmental Biology

Volumn 56, Issue 6-8, 2012, Pages 543-550

  Fujisawa, Toshitaka ^a   Hayakawa, Eisuke ^a,b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Evolution; GPCR; Hydra; Signaling pathway; Signaling peptides

Indexed keywords

ARGINYLPHENYLALANINAMIDE; EPITHELIOPEPTIDE; HYM 1071; HYM 176; HYM 248; HYM 249; HYM 331; HYM 338; HYM 357; HYM 370; HYM 53; HYM 54; HYM 690; KAMIDE; METAMORPHOSISN A; NEUROPEPTIDE; PEPTIDE; RFAMIDE II; RFAMIDE III; RIAMIDE I; RNAMIDE I; RNAMIDE II; RPAMIDE I; RPAMIDE II; RPAMIDE III; RPAMIDE IV; RPAMIDE V; RWAMIDE; RWAMIDE I; RWAMIDE II; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; CNIDARIA; GENE IDENTIFICATION; HYDRA; HYDRA MAGNIPAPILLATA; MOLECULAR EVOLUTION; NONHUMAN; PEPTIDE SIGNALING; PEPTIDE SYNTHESIS; PEPTIDOMICS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PROCESSING; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; HYDRA; INSULIN; PEPTIDES; PROTEIN SORTING SIGNALS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; SODIUM CHANNELS;

CNIDARIA; HYDRA; HYDRA MAGNIPAPILLATA; METAZOA;

EID: 84864472835     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.113477tf     Document Type: Article

References (71)

1. AUGUSTIN, R. and BOSCH, T.C.G. (2010). Cnidarian immunity: a tale of two barriers. Adv Exp Med Biol. 708:1-16.
2. BÖTTGER, A., STRASSER, D., ALEXANDROVA, O., LEVIN, A., FISCHER, S., LASI, M., RUDD, S. and DAVID, C.N. (2006). Genetic screen for signal peptides in Hydra reveals novel secreted proteins and evidence for non-classical protein secretion. Eur J Cell Biol 85: 1107-1117.
3. BRUMWELL, G.B. and MARTIN, V.J. (1996). Ultrastructural localization of RFamide-like peptides in neuronal dense-cored vesicles of a cnidarian planula larva. Invertebr Biol 115: 13-19.
4. CARSTENSEN, K., RINEHART, K.L., MCFARLANE, I.D. and GRIMMELIKHUIJZEN, C.J.P. (1992). Isolation of Leu-Pro-Pro-Gly-Pro-Leu-Pro-Arg-Pro-NH2 (Antho-RPamide), an N-terminally protected, biologically active neuropeptide from sea anemones. Peptides (Tarryt.), 13: 851-857.
5. CARSTENSEN, K., MCFARLANE, I. D, RINEHARD, K. L, HUDMAN, D., SUN, F. and GRIMMELIKHUIJZEN, C.J.P. (1993). Isolation of
6. CHAPMAN, J.A., KIRKNESS, E.F., SIMAKOV, O., HAMPSON, S.E., MITROS, T., WEINMAIER, T. RATTEI, T., BALASUBRAMANIAN, P.G., BORMAN, J., BUSAM, D. et al. (2010). The dynamic genome of Hydra. Nature 464: 592-596.
7. CHERA, S., KALOULIS, K. and GALLIOT, B. (2007). The cAMP response element binding protein (CREB) as an integrative HUB selector in metazoans: clues from the hydra model system. Bio Systems 87:191-203.
8. CHERA, S., GHILA, L., WENGER, Y. and GALLIOT, B. (2011). Injury-induced activation of the MAPK/CREB pathway triggers apoptosis-induced compensatory proliferation in hydra head regeneration. Dev Growth Differ 53:186-201.
9. COTTRELL, G.A., GREEN, K.A. and DAVIES, N.W. (1990). The neuropeptide Phe-Met-Arg-Phe-NH2 (FMRFamide) can activate a ligand-gated ion channel in Helix neurones. Pflugers Arch 416: 612-614.
10. DÜRRNAGEL, S., KUHN, A., TSIAIRIS, C.D., WILLIAMSON, M., KALBACHER, H., GRIMMELIKHUIJZEN, C.J.P., HOLSTEIN, T.W. and GRÜNDER, S. (2010). Three homologous subunits form a high affinity peptide-gated ion channel in Hydra. J Biol Chem 285: 11958-11965.
11. FREDRIKSSON, R. and SCHOETH, H.B. (2005). The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol Pharmacol 67: 1414-1425.
12. FRICKER, L.D. (2010). Analysis of mouse brain peptides using mass spectrometry-based peptidomics: Implications for novel functions ranging from non-classical neuropeptides to microproteins. Mol Biosyst 6: 1355-1365.
13. FUJISAWA, T. (2003). Hydra regeneration and epitheliopeptides. Dev Dyn 226: 182-189.
14. FUJISAWA, T. (2008). Hydra peptide project 1993-2007. Dev Growth Differ 50 Suppl 1: 257-268.
15. GALLIOT, B., WELSCHOF, M., SCHUCKERT, O., HOFFMEISTER, S. and SCHALLER, H. (1995). The cAMP response element binding protein is involved in hydra regeneration. Development 121: 1205-1216.
16. GOLUBOVIC, A., KUHN, A., WILLIAMSON, M., KALBACHER, H., HOLSTEIN, T.W., GRIMMELIKHUIJZEN, C.J.P. and GRÜNDER, S.(2007). A peptide-gated ion channel from the freshwater polyp Hydra. J Biol Chem 282: 35098-35103.
17. GRAFF, D. and GRIMMELIKHUIJZEN, C.J.P. (1988a). Isolation of
18. GRAFF, D. and GRIMMELIKHUIJZEN, C.J.P. (1988b). Isolation of
19. GRENS, A., SHIMIZU, H., HOFFMEISTER, S., BODE, H.R. and FUJISAWA, T. (1999). Pedibin/Hym-346 lowers positional value thereby enhancing foot formation in Hydra. Development 126: 517-524.
20. GRIMMELIKHUIJZEN, C.J.P. and GRAFF, D. (1986). Isolation of
21. GRIMMELIKHUIJZEN, C.J.P. and GROEGER, A. (1987). Isolation of the neuropeptide pGlu-Gly-Arg-Phe-amide from the pennatulid Renilla köllikeri. FEBS Lett 211: 105-108.
22. GRIMMELIKHUIJZEN, C.J.P., HAHN, M., RINEHART, K.L. and SPENCER, A.N. (1988). Isolation of
23. GRIMMELIKHUIJZEN, C.J.P., RINEHART, K.L., JACOB, E., GRAFF, D., REINSCHEID, R.K., NOTHACKER, H.-P. and STALEY, A.L. (1990). Isolation of L-3-phenyllactyl-Leu-Arg-Asn-NH2 (Antho-RNamide), a sea anemone neuropeptide containing an unusual amino-terminal blocking group. Proc Natl Acad Sci USA 87: 5410-5414.
24. GRIMMELIKHUIJZEN, C.J.P., DARMER, D., SCHMUZLER, C., CARSTENSEN, K., MOOSLER, A., NOTHACKER, H. P. REINSCHEID, R.K., VOLLERT, H., RINEHART, K.K. and MCFARLANE, I.D. (1992). The peptidergic nervous system of coelenterates. Prog Brain Res 92: 137-148.
25. GRIMMELIKHUIJZEN, C.J.P., WILLIAMSON, M. and HANSEN, G.N. (2002). Neuropeptides in cnidarians. Can J Zool 80: 1690-1702.
26. HARAFUJI, N., TAKAHASHI, T., HATTA, M., TEZUKA, H., MORISHITA, F., MATSUSHIMA, O. and FUJISAWA, T. (2001). Enhancement of foot formation in Hydra by a novel epitheliopeptide, Hym-323. Development 128: 437-446.
27. HAYAKAWA, E., TAKAHASHI, T., NISHIMIYA-FUJISAWA, C. and FUJISAWA, T. (2007). A novel neuropeptide (FRamide) family identified by a peptidomic approach in Hydra magnipapillata. FEBS J 274: 5438-5448.
28. HUSSON, S.J., CLYNEN, E., BAGGERMAN, G., DE LOOF, A. and SCHOOFS, L. (2005). Discovering neuropeptides in Caenorhabditis elegans by two dimensional liquid chromatography and mass spectrometry. Biochem Biophys Res Comm 335: 76-86.
29. HOFFMEISTER, S.A.H. (1996). Isolation and characterization of two new morphogenetically active peptides from Hydra vulgaris. Development 122: 1941-1948.
30. IWAO, K., FUJISAWA, T. and HATTA, M. (2002). A cnidarian neuropeptide of the GLWamide family induces metamorphosis of reef-building corals in the genus Acropora. Coral Reefs 21: 127-129.
31. KALOULIS, K., CHERA, S., HASSEL, M., GAUCHAT, D. and GALLIOT, B. (2004). Reactivation of developmental programs: the cAMP-response element-binding protein pathway is involved in hydra head regeneration. Proc Natl Acad Sci USA 101: 2363-2368.
32. KATSUKURA, Y., DAVID, C.N., GRIMMELIKHUIJZEN, C.J. and SUGIYAMA T. (2003). Inhibition of metamorphosis by RFamide neuropeptides in planula larvae of Hydractinia echinata. Dev Genes Evol 213: 579-586.
33. KELLENBERGER, S. and SCHILD, L. (2002). Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol Rev 82: 735-767
34. KOIZUMI, O., WILSON, J.D., GRIMMELIKHUIJZEN, C.J. and WESTFALL, J.A. (1989). Ultrastructural localization of RFamide-like peptides in neuronal dense-cored vesicles in the peduncle of Hydra. J Exp Zool 249: 17-22.
35. LAMPERT, T.J., COLEMAN, K.D. and HENNESSEY, T.M. (2011). Chemoattraction to lysophosphatidic acid does not require a change in membrane potential in Tetrahymena thermophila. Cell Biol Int 35: 519-528.
36. LEITZ, T., MORAND, K. and MANN, M. (1994). Metamorphosin A: a novel peptide controlling development of the lower metazoan Hydractinia echinata (Coelenterata, Hydrozoa). Dev Biol 163: 440-446.
37. LEITZ, T. and LAY, M. (1994). Metamorphosin A is a neuropeptide. Dev Gene Evol 204: 276-279
38. LINGUEGLIA, E. (2007). Acid sensing ion channels in sensory perception. J Biol Chem 282: 17325-17329.
39. LINGUEGLIA, E., CHAMPIGNY, G., LAZDUNSKI, M. and BARBRY, P. (1995). Cloning of the amiloride-sensitive FMRFamide peptide-gated sodium channel. Nature 378: 730-733.
40. LOHMANN, J.U. and BOSCH, T.C. (2000). The novel peptide HEADY specifies apical fate in a simple radially symmetric metazoan. Genes Dev 14: 2771-2777.
41. McFARLANE, I.D., GRAFF, D. and GRIMMELIKHUIJZEN, C.J.P. (1987). Excitatory actions of Antho-RFamide, an anthozoan neuropeptide, on muscles and conducting systems in the sea anemone Calliactis parasitica. J Exp Biol 133: 157-168.
42. McFARLANE, I.D. and GRIMMELIKHUIJZEN, C.J.P. (1991). Three anthozoan neuropeptides, Antho-RFamide and Antho-RWamides I and II, modulate spontaneous tentacle contractions in sea anemones. J Exp Biol 155: 669-673.
43. McFARLANE, I.D., REINSCHEID, R.K. and GRIMMELIKHUIJZEN, C.J.P. 1992. Opposite actions of the anthozoan neuropeptide Antho-RNamide on antagonistic muscle groups in sea anemones. J Exp Biol 164: 295-299.
44. McFARLANE, I.D., HUDMAN, D., NOTHACKER, H.P. and GRIMMELIKHUIJZEN, C.J.P. (1993). The expansion behaviour of sea anemones may be coordinated by two inhibitory neuropeptides, Antho-KAamide and Antho-RIamide. Proc Biol Sci 253: 183-188.
45. MILDE, S., HEMMRICH, G., ANTON-ERXLEBEN, F., KHALTURIN, K., WITTLIEB, J, and BOSCH, T, C. (2009). Characterization of taxonomically restricted genes in a phylum-restricted cell type. Genome Biol 10: R8.
46. MOOSLER, A., RINEHART, K.L. and GRIMMELIKHUIJZEN, C.J.P. (1996). Isolation of four novel neuropeptides, the Hydra-RFamides I-IV, from Hydra magnipapillata. Biochem Biophys Res Commun 229: 596-602.
47. MOOSLER, A., RINEHART, K.L. and GRIMMELIKHUIJZEN, C.J.P. (1997). Isolation of three novel neuropeptides, the Cyanea-RFamides I-III, from Scyphomedusae. Biochem Biophys Res Commun 236: 743-749.
48. NOTHACKER, H.-P., RINEHART, K.L. and GRIMMELIKHUIJZEN, C.J.P. (1991a). Isolation of L-3-phenyllactyl-Phe-Lys-Ala-NH2 (Antho-KAamide), a novel neuropeptide from sea anemones. Biochem Biophys Res Commun 179: 1205-1211.
49. NOTHACKER, H.-P., RINEHART, K.L., MCFARLANE, I.D., and GRIMMELIKHUIJZEN, C.J.P. (1991b). Isolation of two novel neuropeptides from sea anemones: the unusual, biologically active L-3-phenyllactyl-Tyr-Arg-Ile-NH2 and its des-phenyllactyl fragment Tyr-Arg-Ile-NH2. Peptides (Elmsford) 12: 1165-1173.
50. PIEROBON, P. (2012). Coordinated modulation of cellular signaling through ligand-gated ion channels in Hydra vulgaris (Cnidaria, Hydrozoa). Int J Dev Biol 56: 551-565.
51. PIOTROWICZ, R.S., MARTIN, J.L., DILLMAN, W.H. and LEVIN, E.G. (1997). The 27-kDa heat shock protein facilitates basic fibroblast growth factor release from endothelial cells. J Biol Chem 272: 7042-7047.
52. PRABHU, Y., MONDAL, S., EICHINGER, L. and NOEGEL, A.A. (2007). A GPCR involved in post aggregation events in Dictyostelium discoideum. Dev Biol 312: 29-43.
53. PRITCHARD, L.E. and WHITE, A. (2007). Neuropeptide processing and its impact on melanocortin pathways. Endocrinology 148: 4201-4207.
54. SCHALLER, H.C. and BODENMULLER, H. (1981). Isolation and amino acid sequence of a morphogenetic peptide from Hydra. Proc Natl Acad Sci USA 78: 7000-7004.
55. SHIMIZU, H. (2012). Transplantation analysis of developmental mechanisms in Hydra. Int J Dev Biol 56: 463-472.
56. SHIMIZU, H. and FUJISAWA, T. (2003). Peduncle of Hydra and the heart of higher organisms share a common ancestral origin. Genesis 36:182-186.
57. SRIVASTAVA, M., SIMAKOV, O., CHAPMAN, J., FAHEY, B., GAUTHIER, M.E., MITROS, T., RICHARDS, G.S., CONACO, C., DACRE, M., HELLSTEN, U. et al. (2010). The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466: 720-726.
58. STEELE, R.E. (2012). The Hydra genome: insights, puzzles, and opportunities for developmental biologists. Int J Dev Biol 56: 535-542.
59. STEELE, R. E., LIEU, P., MAI, N. H., SHENK, M. A., and SARRAS, M. P., Jr. (1996). Response to insulin and the expression pattern of a gene encoding an insulin receptor homologue suggest a role for an insulin-like molecule in regulating growth and development in Hydra. Dev Genes Evol 206: 247-259.
60. SUGA, H., SCHMID, V. and GEHRING, W.J. (2008). Evolution and functional diversity of jellyfish opsins. Curr Bio 18:51-55.
61. SUZUKI, Y., KOBAYASHI, M., MIYASHITA, H., OHTA, H., SONODA, H. and SATO, Y. (2010). Isolation of a small vasohibin-binding protein (SVBP) and its role in vasohibin secretion. J Cell Sci 123(Pt 18): 3094-3101.
62. TAGUCHI, A. and WHITE, M.F. (2008). Insulin-like signaling, nutrient homeostasis, and life span. Ann Rev Physiol 70: 191-212.
63. TAKAHASHI, T., MUNEOKA, Y., LOHMANN, J., DE HARO, L.M., SOLLEDER, G., BOSCH, T.C.G., DAVID, C.N., BODE, H.R., KOIZUMI, O., SHIMIZU, H., HATTA, M., FUJISAWA, T. and SUGIYAMA, T. (1997). Systematic isolation of peptide signal molecules regulating development in Hydra: LWamide and PW families. Proc Natl Acad Sci USA 94: 1241-1246.
64. TAKAHASHI, T., KOIZUMI, O., ARIURA, Y., ROMANOVITCH, A., BOSCH, T.C.G., KOBAYAKAWA, Y., MOHRI, S., BODE, H.R., YUM, S., HATTA, M. and FUJISAWA, T. (2000). A novel neuropeptide, Hym-355, positively regulates neuron differentiation in Hydra. Development 127: 997-1005.
65. TAKAHASHI, T., HATTA, M., YUM, S., KOIZUMI, O., KOBAYAKAWA, Y., GEE, L., OHTANI, M., FUJISAWA, T. and BODE, H.R. (2005). Hym-301, a novel peptide, regulates the number of tentacles formed in Hydra. Development 132: 2225-2234.
66. TAKAHASHI, T., KOIZUMI, O., HAYAKAWA, E., MINOBE, S., SUETSUGU, R., KOBAYAKAWA, Y., BOSCH, T. C, DAVID, C. N, and FUJISAWA, T. (2009). Further characterization of the PW peptide family that inhibits neuron differentiation in Hydra. Dev Genes Evol 219: 119-129.
67. WEST, D.L. (1978). The epitheliomuscular cell of Hydra: its fine structure, three-dimensional architecture and relation to morphogenesis. Tissue Cell 10: 629-646.
68. WESTFALL, J.A. and GRIMMELIKHUIJZEN, C.J.P. (1993). Antho-RFamide immunoreactivityin neuronal synaptic and nonsynaptic vesicles of sea anemones. Biol Bull 185: 109-114.
69. WESTFALL, J.A., SAYYAR, K.L., ELLIOTT, C.F. and GRIMMELIKHUIJZEN, C.J.P. (1995). Ultrastructural localization of Antho-RWamides I and II at neuromuscular synapses in the gastrodermis and oral sphincter muscle of the sea anemone Calliactis parasitica. Biol Bull 189: 280-287.
70. WOOD, R.L. (1979). The fine structure of the hypostome and mouth of Hydra. II. Transmission electron microscopy. Cell Tissue Res 199: 319-338.
71. YUM, S., TAKAHASHI, T., KOIZUMI, O., ARIURA, Y., KOBAYAKAWA, Y., MOHRI, S., and FUJISAWA, T. (1998). A novel neuropeptide, Hym-176, induces contraction of the ectodermal muscle in Hydra. Biochem Biophys Res Commun 248: 584-590.