Neuronal evolution: Analysis of regulatory genes in a first-evolved nervous system, the hydra nervous system

BioSystems

Volumn 76, Issue 1-3, 2004, Pages 75-87

  Miljkovic Licina, Marijana ^a   Gauchat, Dominique ^a   Galliot, Brigitte ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Budding and regeneration; Mechanoreceptor cells; Neurogenesis and patterning; Origin of neuronal cells

Indexed keywords

CELL NUCLEUS RECEPTOR; THROMBOSPONDIN;

NERVOUS SYSTEM;

ANIMAL CELL; CONFERENCE PAPER; GENE EXPRESSION; GENETIC REGULATION; HOMEOBOX; MECHANORECEPTOR; MOLECULAR EVOLUTION; MORPHOGENESIS; NERVE CELL; NERVE CELL NETWORK; NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POLYP; PROTEIN EXPRESSION; REGULATOR GENE; REGULATORY MECHANISM;

ANIMALIA; BILATERIA; CNIDARIA; HYDRA;

EID: 4444248476     PISSN: 03032647     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biosystems.2004.05.030     Document Type: Conference Paper

References (79)

1. Adams J.C., Tucker R.P. The thrombospondin type 1 repeat (Tsr) superfamily: diverse proteins with related roles in neuronal development. Dev. Dyn. 218:2000;280-299
2. Aerne B.L., Stidwill R.P., Tardent P. Nematocyte discharge in hydra does not require the presence of nerve cells. J. Exp. Zool. 258:1991;137-141
3. Anderson P.A. Physiology of a bidirectional, excitatory, chemical synapse. J. Neurophysiol. 53:1985;821-835
4. Anderson P.A., Spencer A.N. The importance of cnidarian synapses for neurobiology. J. Neurobiol. 20:1989;435-457
5. Anderson, P.A.V., 1989. Concluding remarks, In Anderson, P.A.V. (Ed.), Evolution of the First Nervous Systems, NATO Series, Serie A: Life Sciences, vol. 188, Plenum Press, New York, pp. 409-413.
6. Anderson P.A.V., McKay M.C. The electrophysiology of cnidocytes. J. Exp. Biol. 133:1987;215-230
7. Ayala F.J., Rzhetsky A. Origin of the metazoan phyla: Molecular clocks confirm paleontological estimates. Proc. Natl. Acad. Sci. USA. 95:1998;606-611
8. Bellis S.L., Grosvenor W., Kass-Simon G., Rhoads D.E. Chemoreception in Hydra vulgaris (attenuata): initial characterization of two distinct binding sites for L-glutamic acid. Biochem. Biophys. Acta. 1061:1991;89-94
9. Bode H.R. The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. J. Cell. Sci. 109:1996;1155-1164
10. Bouillon, J., 1994. Embranchement des cnidaires (cnidaria), In Grassé, P.P. (Ed.), Traité de zoologie. Cnidaires, cténaires, Masson, Paris, pp. 1-28.
11. Brinkmann M., Oliver D., Thurm U. Mechanoelectric transduction in nematocytes of a hydropolyp (corynidae). J. Comp. Physiol. A. 178:1996;125-138
12. Campbell, R.D., 1988. The nematocyte: an encapsulation of developmental processes, In Hessinger, D.A., Lenhoff, H.M. (Eds.), The Biology of Nematocysts, Academic Press, San Diego, pp. 115-121.
13. Campbell R.D., Marcum B.A. Nematocyte migration in hydra: evidence for contact guidance in vivo. J. Cell Sci. 41:1980;33-51
14. Colasanti M., Venturini G., Merante A., Musci G., Lauro G.M. Nitric oxide involvement in Hydra vulgaris very primitive olfactory-like system. J. Neurosci. 17:1997;493-499
15. Cooney A.J., Lee C.T., Lin S.C., Tsai S.Y., Tsai M.J. Physiological function of the orphans gcnf and COUP-TF. Trends Endocrinol. Metab. 12:2001;247-251
16. David C.N. A quantitative method for maceration of hydra tissue. Roux' Archiv. Dev. Biol. 171:1973;259-268
17. De Petrocellis L., Melck D., Bisogno T., Milone A., Di Marzo V. Finding of the endocannabinoid signalling system in hydra, a very primitive organism: possible role in the feeding response. Neuroscience. 92:1999;377-387
18. DeRobertis E.M., Sasai Y. A common plan for dorsoventral patterning in bilateria. Nature. 380:1996;37-40
19. Devine C., Hinman V.F., Degnan B.M. Evolution and developmental expression of nuclear receptor genes in the ascidian herdmania. Int. J. Dev. Biol. 46:2002;687-692
20. Engel U., Oezbek S., Engel R., Petri B., Lottspeich F., Holstein T.W. Nowa, a novel protein with minicollagen cys-rich domains, is involved in nematocyst formation in hydra. J. Cell Sci. 115:2002;3923-3934
21. Escriva H., Safi R., Hanni C., Langlois M.C., Saumitou-Laprade P., Stehelin D., Capron A., Pierce R., Laudet V. Ligand binding was acquired during evolution of nuclear receptors. Proc. Natl. Acad. Sci. USA. 94:1997;6803-6808
22. Fujisawa T. Hydra regeneration and epitheliopeptides. Dev. Dyn. 226:2003;182-189
23. Galliot B. Conserved and divergent genes in apex and axis development of cnidarians. Curr. Opin. Genet. Dev. 10:2000;629-637
24. Galliot B., de Vargas C., Miller D. Evolution of homeobox genes: Q50 paired-like genes founded the paired class. Dev. Genes Evol. 209:1999;186-197
25. Galliot B., Miller D. Origin of anterior patterning. How old is our head? Trends Genet. 16:2000;1-5
26. Galliot B., Schmid V. Cnidarians as a model system for understanding evolution and regeneration. Int. J. Dev. Biol. 46:2002;39-48
27. Gauchat, D., Escriva, H., Miljkovic-Licina, M., Chera, S., Langlois, M-C., Begue, A., Laudet, V., Galliot, B., in press. The orphan COUP-TF nuclear receptors are markers for neurogenesis from cnidarians to vertebrates. Dev. Biol.
28. Gauchat D., Kreger S., Holstein T., Galliot B. Prdl-a, a gene marker for hydra apical differentiation related to triploblastic paired-like head-specific genes. Development. 125:1998;1637-1645
29. Gauchat D., Mazet F., Berney C., Schummer M., Kreger S., Pawlowski J., Galliot B. Evolution of ANTP-class genes and differential expression of hydra hox/parahox genes in anterior patterning. Proc. Natl. Acad. Sci. USA. 97:2000;4493-4498
30. Gilbert, S.F., 2000. Developmental mechanisms of evolutionary change, In Gilbert, S.F. (Ed.), Developmental Biology, 6th ed., Sinauer, USA, pp. 679-709.
31. Grasso L.C., Hayward D.C., Trueman J.W., Hardie K.M., Janssens P.A., Ball E.E. The evolution of nuclear receptors: evidence from the coral acropora. Mol. Phylogenet. Evol. 21:2001;93-102
32. Grens, A., Mason, E., Marsh, J.L., Bode, H.R., 1995. Evolutionary conservation of a cell fate specification gene: the hydra achaete-scute homolog has proneural activity in Drosophila. Development 121, 4027-4035.
33. Grigoriev N.G., Spafford J.D., Spencer A.N. Modulation of jellyfish potassium channels by external potassium ions. J. Neurophysiol. 82:1999;1728-1739
34. Grimmelikhuijzen, C.J., Graff, D., Koizumi, O., Westfall, J.A., McFarlane, I.D., 1989. Neurons and their peptide transmitters in coelenterates, In: Anderson, P.A.V. (Ed.), Evolution of the First Nervous Systems, NATO Series, Serie A: Life Sciences, vol. 188, Plenum Press, New York, pp. 95-109.
35. Grimmelikhuijzen C.J., Westfall J.A. The nervous systems of cnidarians. Experiment. 72:1995;7-24
36. Hansen G.N., Williamson M., Grimmelikhuijzen C.J. Two-color double-labeling in situ hybridization of whole-mount hydra using RNA probes for five different hydra neuropeptide preprohormones: evidence for colocalization. Cell Tissue Res. 301:2000;245-253
37. Hansen G.N., Williamson M., Grimmelikhuijzen C.J. A new case of neuropeptide coexpression (RGamide and LWamides) in hydra, found by whole-mount, two-color double-labeling in situ hybridization. Cell Tissue Res. 308:2002;157-165
38. Hoffmann U., Kroiher M. A possible role for the cnidarian homologue of serum response factor in decision making by undifferentiated cells. Dev. Biol. 236:2001;304-315
39. Holstein, T., Hausmann, K., 1988. The cnidocil apparatus of hydrozoans: a progenitor of metazoan mechanoreceptors? In: Hessinger, D.A., Lenhoff, H.M. (Eds.), The Biology of Nematocysts, Academic Press, San Diego, pp. 53-73.
40. Holstein T.W., Hobmayer E., Technau U. Cnidarians: an evolutionarily conserved model system for regeneration? Dev. Dyn. 226:2003;257-267
41. Holtmann M., Thurm U. Mono- and oligo-vesicular synapses and their connectivity in a cnidarian sensory epithelium (coryne tubulosa). J. Comp. Neurol. 432:2001;537-549
42. Jeziorski M.C., Greenberg R.M., Anderson P.A. Cloning and expression of a jellyfish calcium channel beta subunit reveal functional conservation of the alpha1-beta interaction. Recept. Chann. 6:1999;375-386
43. Koch A.W., Holstein T.W., Mala C., Kurz E., Engel J., David C.N. Spinalin, a new glycine- and histidine-rich protein in spines of hydra nematocysts. J. Cell Sci. 111:1998;1545-1554
44. Koizumi O., Itazawa M., Mizumoto H., Minobe S., Javois L.C., Grimmelikhuijzen C.J., Bode H.R. Nerve ring of the hypostome in hydra. I. Its structure, development, and maintenance. J. Comp. Neurol. 326:1992;7-21
45. Koizumi O., Mizumoto H., Sugiyama T., Bode H.R. Nerve net formation in the primitive nervous system of hydra - an overview. Neurosci. Res. 13(Suppl):1990;S165-S170
46. Kung, C., 1989. Ion channels of unicellular microbes, In: Anderson, P.A.V. (Ed.), Evolution of the First Nervous Systems, NATO Series, Serie A: Life Sciences, vol. 188, Plenum Press, New York, pp. 203-214.
47. Langlois M.C., Vanacker J.M., Holland N.D., Escriva H., Queva C., Laudet V., Holland L.Z. AmphiCOUP-TF, a nuclear orphan receptor of the lancelet Branchiostoma floridae, is implicated in retinoic acid signalling pathways. Dev. Genes Evol. 210:2000;471-482
48. Lawn I.D., Mackie G.O., Silver G. Conduction system in a sponge. Science. 211:1981;1169-1171
49. Lenhoff, H.M., Heagy, W., Danner, J., 1982. Bioassay for, and characterization of, activators and inhibitors of the feeding response, In: Lenhoff, H.M. (Ed.), Hydra: Research Methods, Plenum Press, New York.
50. Leys S.P., Mackie G.O., Meech R.W. Impulse conduction in a sponge. J. Exp. Biol. 202:1999;1139-1150
51. Lindgens D., Holstein T.W., Technau U. Hyzic, the Hydra homolog of the zic/odd-paired gene, is involved in the early specification of the sensory nematocytes. Development. 131:2004;191-201
52. Longin A., Souchier C., Ffrench M., Bryon P.A. Comparison of anti-fading agents used in fluorescence microscopy: image analysis and laser confocal microscopy study. J. Histochem. Cytochem. 41:1993;1833-1840
53. Loomis W.F. Glutathione control of the specific feeding reactions of hydra. Ann. N.Y. Acad. Sci. 62:1955;209-228
54. Mackie G.O. Neuroid conduction and the evolution of conducting tissues. Q. Rev. Biol. 45:1970;319-332
55. MacWilliams H.K. Hydra transplantation phenomena and the mechanism of hydra head regeneration. Part II. Properties of the head activation. Dev. Biol. 96:1983;239-257
56. Mitgutsch C., Hauser F., Grimmelikhuijzen C.J. Expression and developmental regulation of the hydra-RFamide and hydra-LWamide preprohormone genes in hydra: evidence for transient phases of head formation. Dev. Biol. 207:1999;189-203
57. Nielsen, C., 1997. Phylum Cnidaria, Animal Evolution Interrelationships of the Living Phyla, Oxford University Press, Oxford, pp. 53-60.
58. Ostroumova T.V., Markova L.N. The effects of dopamine synthesis inhibitors and dopamine antagonists on regeneration in the hydra hydra attenuata. Neurosci. Behav. Physiol. 32:2002;293-298
59. Otto J.J., Campbell R.D. Budding in hydra attenuata: bud stages and fate map. J. Exp. Zool. 200:1977;417-428
60. Passano L.M., McCullough C.B. Co-ordinating systems and behaviour in hydra II. The rythmic potential system. J. Exp. Biol. 42:1965;205-231
61. Pereira F.A., Tsai M.J., Tsai S.Y. COUP-TF orphan nuclear receptors in development and differentiation. Cell Mol. Life Sci. 57:2000;1388-1398
62. Pierobon P., Minei R., Porcu P., Sogliano C., Tino A., Marino G., Biggio G., Concas A. Putative glycine receptors in hydra: A biochemical and behavioural study. Eur. J. Neurosci. 14:2001;1659-1666
63. Raff, R.A., 1996. Deep time and metazoan origins, In: Raff, R.A. (Ed.), The Shape of Life. Genes, Development and the Evolution of Animal Form, Chicago University Press, Chicago, pp. 63-102.
64. Schaller H.C., Hoffmeister S.A., Dubel S. Role of the neuropeptide head activator for growth and development in hydra and mammals. Development. 107:1989;99-107
65. Schummer M., Scheurlen I., Schaller C., Galliot B. HOM/HOX homeobox genes are present in hydra (Chlorohydra viridissima) and are differentially expressed during regeneration. EMBO J. 11:1992;1815-1823
66. Shankland M., Seaver E.C. Evolution of the bilaterian body plan: what have we learned from annelids? Proc. Natl. Acad. Sci. USA. 97:2000;4434-4437
67. Shimizu H. Feeding and wounding responses in hydra suggest functional and structural polarization of the tentacle nervous system. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 131:2002;669-674
68. Spemann H., Mangold H. Induction of embryonic primordia by implantation of organizers from a different species. 1923. Int. J. Dev. Biol. 45:2001;13-38
69. Spencer, A.N., 1989. Chemical and electrical synaptic transmission in the cnidarian, In: Anderson, P.A.V. (Ed.), Evolution of the First Nervous Systems, NATO Series, Serie A: Life Sciences, vol. 188, Plenum Press, New York, pp. 33-53.
70. Spring J., Yanze N., Josch C., Middel A.M., Winninger B., Schmid V. Conservation of brachyury, Mef2, and snail in the myogenic lineage of jellyfish: a connection to the mesoderm of bilateria. Dev. Biol. 244:2002;372-384
71. Stern C.D. Detection of multiple gene products simultaneously by in situ hybridization and immunohistochemistry in whole mounts of avian embryos. Curr. Top. Dev. Biol. 36:1998;223-243
72. Stern C.D. Initial patterning of the central nervous system: how many organizers? Nat. Rev. Neurosci. 2:2001;92-98
73. Takahashi T., Koizumi O., Ariura Y., Romanovitch A., Bosch T.C., Kobayakawa Y., Mohri S., Bode H.R., Yum S., Hatta M., Fujisawa T. A novel neuropeptide, Hym-355, positively regulates neuron differentiation in hydra. Development. 127:2000;997-1005
74. Tardent P. The cnidarian cnidocyte, a high-tech cellular weaponry. BioEssays. 17:1995;351-362
75. Thomas P., Beddington R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6:1996;1487-1496
76. Vacelet J., Boury-Esnault N. Carnivorous sponges. Nature. 373:1995;333-335
77. Westfall J.A. Ultrastructure of synapses in the first-evolved nervous systems. J. Neurocytol. 25:1996;735-746
78. Westfall J.A., Elliott C.F., Carlin R.W. Ultrastructural evidence for two-cell and three-cell neural pathways in the tentacle epidermis of the sea anemone Aiptasia pallida. J. Morphol. 251:2002;83-92
79. Yum S., Takahashi T., Hatta M., Fujisawa T. The structure and expression of a preprohormone of a neuropeptide, hym-176 in hydra magnipapillata. FEBS Lett. 439:1998;31-34