Distribution of GAD-immunoreactive neurons in the diencephalon of the African lungfish Protopterus annectens: Colocalization of GAD and NPY in the preoptic area

Journal of Comparative Neurology

Volumn 419, Issue 2, 2000, Pages 223-232

  Trabucchi, Michele ^a,b   Chartrel, Nicolas ^a   Pelletier, Georges ^c   Vallarino, Mauro ^b   Vaudry, Hubert ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b UNIVERSITY OF GENOA   (Italy)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

Comparative neuroanatomy; Dipnoans; Evolution; Glutamic acid decarboxylase; Neuropeptide tyrosine

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE DECARBOXYLASE; NEUROPEPTIDE Y;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; DIENCEPHALON; EVOLUTION; FISH; HYPOPHYSIS INTERMEDIATE LOBE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; NEUROANATOMY; NEWBORN; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; THALAMUS;

ANIMALS; DIENCEPHALON; FISHES; GLUTAMATE DECARBOXYLASE; IMMUNOHISTOCHEMISTRY; NEURONS; NEUROPEPTIDE Y; PREOPTIC AREA; TISSUE DISTRIBUTION;

EID: 0034106936     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000403)419:2<223::AID-CNE6>3.0.CO;2-1     Document Type: Article

References (83)

1. Adjeroud S, Tonon MC, Lamacz M, Leneveu E, Stoeckel ME, Tappaz ML, Cazin L, Danger JM, Bernard C, Vaudry H. 1986. GABA-ergic control of α-melanocyte-stimulating hormone (α-MSH) release by frog neurointermediate lobe in vitro. Brain Res Bull 17:717-724.
2. Anadón R, Adrio F, Rodríguez-Moldes I. 1998. Distribution of GABA immunoreactivity in the central and peripheral nervous system of amphioxus (Branchiostoma lanceolatum Pallas). J Comp Neurol 401: 293-307.
3. Aste N, Viglietti-Panzica C, Fasolo A, Andreone C, Vaudry H, Pelletier G, Panzica GC. 1991. Localization of neuropeptide Y-immunoreactive cells and fibers in the brain of the Japanese quail. Cell Tissue Res 265:219-230.
4. Barale E, Fasolo A, Girardi E, Artero C, Franzoni MF. 1996. Immunohistochemical investigation of γ-aminobutyric acid ontogeny and transient expression in the central nervous system of Xenopus laevis tadpoles. J Comp Neurol 368:285-294.
5. Bemis WE, Burggren WW, Kemp NE. 1986. The biology and evolution of lungfishes. New York: Alan R Liss.
6. Bennis M, Calas A, Geffard M, Gamrani H. 1991. Distribution of GABA immunoreactive systems in the forebrain and midbrain of the chameleon. Brain Res Bull 26:891-898.
7. Blanton MG, Shen JM, Kriegstein AR. 1987. Evidence for the inhibitory neurotransmitter γ-aminobutyric acid in aspiny and sparsely spiny nonpyramidal neurons of the turtle dorsal cortex. J Comp Neurol 259:277-297.
8. Bosma PT, Blasquez M, Collins MA, Bishop JD, Drouin G, Priede IG, Docherty K, Trudeau VL. 1999. Multiplicity of glutamic acid decarboxylases (GAD) in vertebrates: molecular phylogeny and evidence for a new GAD paralog. Mol Biol Evol 16:397-404.
9. Brüstle O, Pilgrim C, Gaymann W, Reisert I. 1988. Abundant GABAergic innervation of rat posterior pituitary revealed by inhibition of GABA-transaminase. Cell Tissue Res 251:59-64.
10. Chartrel N, Conlon JM, Danger JM, Fournier A, Tonon MC, Vaudry H. 1991. Characterization of melanotropin-release inhibiting factor (melanostatin) from frog brain: homology with human neuropeptide Y. Proc Natl Acad Sci USA 88:3862-3866.
11. Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue TL. 1985. The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159-1181.
12. Danger JM, Guy J, Benyamina M, Jégou S, Leboulenger F, Coté J, Tonon MC, Pelletier G, Vaudry H. 1985. Localization and identification of neuropeptide Y (NPY)-like immunoreactivity in the frog brain. Peptides 6:1225-1233.
13. Danger JM, Leboulenger F, Guy J, Tonon MC, Benyamina M, Martel, JC, Saint-Pierre S, Pelletier G, Vaudry H. 1986. Neuropeptide Y in the intermediate lobe of the frog pituitary acts as an α -MSH-release inhibiting factor. Life Sci 39:1183-1192.
14. Danger JM, Tonon MC, Lamacz M, Martel JC, Saint-Pierre S, Pelletier G, Vaudry H. 1987. Melanotropin-release inhibiting action of neuropeptide Y: structure activity relationships. Life Sci 40:1853-1858.
15. Danger JM, Tonon MC, Jenks BG, Saint-Pierre S, Martel JC, Fasolo A, Breton B, Quiron R, Pelletier G, Vaudry H. 1990. Neuropeptide Y: localization in the central nervous system and neuroendocrine functions. Fundam Clin Pharmacol 4:307-340.
16. Danger JM, Breton B, Vallarino M, Fournier A, Pelletier G, Vaudry H. 1991. Neuropeptide-Y in the trout brain and pituitary: localization, characterization, and action on gonadotropin release. Endocrinology 128:2360-2368.
17. Davila JC, de la Calle A, Gutierrez A, Megias M, Andreu MJ, Guirado S. 1991. Distribution of neuropeptide Y (NPY) in the cerebral cortex of the lizards Psammodromus algirus and Podarcis hispanica: co-localization of NPY, somatostatin, and GABA. J Comp Neurol 308:397-408.
18. De Quidt ME, Emson PC. 1986. Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system. II. Immunocytochemical analysis. Neuroscience 18:545-618.
19. Denizot JP, Clausse S, Elekes K, Geffard M, Grant K, Libouban S. 1987. Convergence of electrotonic club ending, GABA- and serotoninergic terminals on second order neurons of the electrosensory pathway in mormyrid fish, Gnathonemus petersii and Brienomyrus niger (Teleostei). Cell Tissue Res 249:301-309.
20. De Rijk EPCT, Jenks BG, Vaudry H, Roubos EW. 1990. GABA and neuropeptide Y co-exist in axons innervating the neurointermediate lobe of the pituitary ofXenopus laevis - an immunoelectron microscopic study. Neuroscience 38:495-502.
21. De Rijk EPCT, van Strien FJ, Roubos EW. 1992. Demonstration of coexisting catecholamine (dopamine), amino acid (GABA), and peptide (NPY) involved in inhibition of melanotrope cell activity in Xenopus laevis: a quantitative ultrastructural, freeze-substitution immunocytochemical study. J Neurosci 12:864-871.
22. Domenici L, Waldvogel HJ, Matute C, Streit P. 1988. Distribution of GABA-like immunoreactivity in the pigeon brain. Neuroscience 25: 931-950.
23. Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ. 1991. Two genes encode distinct glutamate decarboxylases. Neuron 7:91-100.
24. Esclapez M, Tillakaratne NJ, Kaufman DL, Tobin AJ, Houser CR. 1994. Comparative localization of two forms of glutamic acid decarboxylase and their mRNAs in rat brain supports the concept of functional differences between the forms. J Neurosci 14:1834-1855.
25. Fabri M, Manzoni T. 1996. Glutamate decarboxylase immunoreactivity in corticocortical projecting neurons of rat somatic sensory cortex. Neuroscience 72:435-448.
26. Feldberg W, Rocha E, Silva MJ. 1978. Vasopressin release produced in anaesthetized cats by antagonists of gamma-aminobutyric acid and glycine. Br J Pharmacol 62:99-106.
27. François-Bellan AM, Kachidian P, Dusticier G, Tonon MC, Vaudry H, Bosler O. 1990. GABA neurons in the rat suprachiasmatic nucleus: involvement in chemospecific synaptic circuitry and evidence for GAD-peptide colocalization. J Neurocytol 19:937-947.
28. Franzoni MF, Morino P. 1989. The distribution of GABA-like-immunoreactive neurons in the brain of the newt, Trituras cristatus carnifex, and the green frog, Rana esculenta. Cell Tissue Res 255: 155-166.
29. Granda RH, Grassland WJ. 1989. GABA-like immunoreactivity of neurons in the chicken diencephalon and mesencephalon. J Comp Neurol 287: 455-469.
30. 3H]GABA accumulation. Brain Res 370:241-249.
31. Hendry SHC, Jones EG, DeFelipe J, Schmechel D, Brandon C, Emson PC. 1984. Neuropeptide-containing neurons of the cerebral cortex are also GABAergic. Proc Natl Acad Sci USA 81:6526-6530.
32. Hökfelt T, Millhorn D, Seroogy K, Tsuruo Y, Ceccatelli S, Lindh B, Meister B, Melander T, Schalling M, Bartfai T, Terenius L. 1987. Coexistence of peptides with classical neurotransmitters. Experientia 43:768-780.
33. Horvath TL, Bechmann I, Naftolin F, Kalra SP, Leranth C. 1997. Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus: GABAergic and non-GABAergic subpopulations. Brain Res 756:283-286.
34. Jansen K, Fabro C, Artero C, Feuilloley M, Vaudry H, Fasolo A, Franzoni MF. 1997. Characterization of pars intermedia connections in amphibians by biocytin tract tracing and immunofluorescence aided by confocal microscopy. Cell Tissue Res 287:297-304.
35. Kah O, Dubourg P, Martinoli MG, Geffard M, Calas A. 1987a. Morphological evidence for a direct neuroendocrine GABAergic control of the anterior pituitary in teleosts. Experientia 43:300-302.
36. Kah O, Dubourg P, Martinoli MG, Rabbi M, Gonnet F, Geffard M, Calas A. 1987b. Central GABAergic innervation of the pituitary in goldfish: a radioautographic and immunocytochemical study at the electron microscope level. Gen Comp Endocrinol 67:324-332.
37. Kawaja MD, Flumerfelt BA, Hrycyshyn AW. 1989. Glutamate decarboxylase immunoreactivity in the rat interpeduncular nucleus: a light and electron microscope investigation. Neuroscience 30:741-753.
38. King JA, Millar RP, Vallarino M, Pierantoni R. 1995. Localization and characterization of gonadotropin-releasing hormones in the brain, gonads, and plasma of a dipnoi (lungfish, Protopterus annectens). Regul Pept 57:163-174.
39. Louiset E, van de Put FHMM, Tonon MC, Basille C, Jenks BG, Vaudry H, Cazin L. 1990. Electrophysiological evidence for the existence of GABAA receptors in cultured frog melanotrophs. Brain Res 517: 151-156.
40. Martin SC, Heinrich G, Sandell JH. 1998. Sequence and expression of glutamic acid decarboxylase isoforms in the developing zebrafish. J Comp Neurol 396:253-266.
41. Martinoli MG, Dubourg P, Geffard M, Calas A, Kah O. 1990. Distribution of GABA-immunoreactive neurons in the forebrain of the goldfish, Carassius auratus. Cell Tissue Res 260:77-84.
42. Médina M, Repérant J, Dufour S, Ward R, Le Belle N, Miceli D. 1994. The distribution of GABA-immunoreactive neurons in the brain of the silver eel (Anguilla anguilla L.). Anat Embryol 189:25-39.
43. Meister B, Ceccatelli T, Hökfelt T, Anden NE, Anden M, Theodorsson E. 1989. Neurotransmitters, neuropeptides and binding sites in the rat mediobasal hypothalamus: effects of monosodium glutamate (MSG) lesions. Exp Brain Res 76:343-368.
44. Miles RS. 1977. Dipnoan (lungfish) skull and the relationships of the group: a study based on new species from the Devonian of Australia. Zool J Linn Soc 61:1-328.
45. Mugnaini E, Oertel WH. 1985. An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunocytochemistry. In: Björklund A, Hökfelt T, editors. Handbook of chemical neuroanatomy, vol 4, part I. Amsterdam: Elsevier. p 436-608.
46. Naujoks-Manteuffel C, Himstedt W, Glasener-Cipollone G. 1994. Distribution of GABA-immunoreactive neurons in the brain of adult and developing salamanders (Pleurodeles waltli, Trituras alpestris). Cell Tissue Res 276:485-501.
47. Nicholson C. 1999. Signals that go with the flow. Trends Neurosci 22: 143-145.
48. Nicholson FB, Montgomery JC, Faull RL. 1994. GABA, muscarinic cholinergic, excitatory amino acid, neurotensin and opiate binding sites in the octavolateralis column and cerebellum of the skate Raja nasuta (Pisces: Rajidae). Brain Res 652:40-48.
49. Northcutt RG. 1977. Retinofugal projections in the lepidosirenid lung-fishes. J Comp Neurol 174:553-574.
50. Oertel WH, Schmechel DE, Tappaz ML, Kopin IJ. 1981. Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6:2689-2700.
51. Oertel WH, Mugnaini E, Tappaz ML, Weise VK, Dahl AL, Schmechel DE, Kopin IJ. 1982. Central GABAergic innervation of neurointermediate pituitary lobe: biochemical and immunocytochemical study in the rat. Proc Natl Acad Sci USA 79:675-679.
52. Parker D, Söderberg C, Zotova E, Shupliakov O, Langel Ü, Bartfai T, Larhammar D, Brodin L, Grillner S. 1998. Co-localized neuropeptide Y and GABA have complementary presynaptic effects on sensory synaptic transmission. Eur J Neurosci 10:2856-2870.
53. Pelletier G, Désy L, Kerkérian L, Côté J. 1984. Immunocytochemical localization of neuropeptide Y (NPY) in the human hypothalamus. Cell Tissue Res 238:203-205.
54. Perroteau I, Danger JM, Biffo S, Pelletier G, Vaudry H, Fasolo A. 1988. Distribution and characterization of neuropeptide Y-like immunoreactivity in the brain of the crested newt. J Comp Neurol 275:309-325.
55. Polgár E, Shehab SA, Watt C, Todd AJ. 1999. GABAergic neurons that contain neuropeptide Y selectively target cells with the neurokinin 1 receptor in laminae III and FV of the rat spinal cord. J Neurosci 19:2637-2646.
56. Pontet A, Danger JM, Dubourg P, Pelletier G, Vaudry H, Calas A, Kah O. 1989. Distribution and characterization of neuropeptide Y-like immunoreactivity in the brain and pituitary of the goldfish. Cell Tissue Res 255:529-538.
57. Rabhi M, Onteniente B, Kah O, Geffard M, Calas A. 1987. Immunocytochemical study of the GABAergic innervation of the mouse pituitary by use of antibodies against gamma-aminobutyric acid (GABA). Cell Tissue Res 247:33-40.
58. Reiner A, Northcutt RG. 1987. An immunohistochemical study of the telencephalon of the African lungfish, Protopterus annectens. J Comp Neurol 256:463-481.
59. Reiner A, Oliver JR. 1987. Somatostatin and neuropeptide Y are almost exclusively found in the same neurons in the telencephalon of the turtles. Brain Res 426:149-156.
60. Roberts A, Dale N, Ottersen OP, Storm-Mathisen J. 1987. The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J Comp Neurol 261:435-449.
61. Romer AS. 1966. Vetebrate paleontology, 3rd ed. Chicago: University of Chicago Press.
62. Rosen DE, Forey PL, Gardiner BG, Patterson C. 1981. Lungfishes, tetrapods, paleontology, and plesiomorphy. Bull Am Mus Natl Hist 167: 159-276.
63. Sakaue M, Saito N, Taniguchi H, Baba S, Tanaka C. 1988. Immunohistochemical localization of γ-aminobutyric acid in the rat pituitary gland and related hypothalamic regions. Brain Res 446:343-353.
64. Schotland JL, Shupliakov O, Grillner S, Brodin L. 1996. Synaptic and nonsynaptic monoaminergic neuron systems in the lamprey spinal cord. J Comp Neurol 372:229-244.
65. Sloley BD, Kah O, Trudeau VL, Dulka JG, Peter RE. 1992. Amino acid neurotransmitters and dopamine in brain and pituitary of the goldfish: involvement in the regulation of gonadotropin secretion. J Neurochem 58:2254-2262.
66. Tappaz ML, Oertel WH, Wassef M, Mugnaini E. 1982. Central GABAergic neuroendocrine regulations: pharmacological and morphological evidence. In: Buijs RM, Pévet P, Swaab DF, editors. Chemical transmission in the brain, progress in brain research, vol. 55. Amsterdam: Elsevier Biomedical Press. p 77-96.
67. Thind KK, Goldsmith PC. 1995. Glutamate and GABAergic neurointeractions in the monkey hypothalamus: a quantitative immunomorphological study. Neuroendocrinology 61:471-485.
68. Tonon MC, Bosler O, Stoeckel ME, Pelletier G, Tappaz M, Vaudry H. 1992. Co-localization of tyrosine hydroxylase, GABA and neuropeptide Y within axon terminals innervating the intermediate lobe of the frog Rana ridibunda. J Comp Neurol 319:599-605.
69. Tuinhof R, Artero C, Fasolo A, Franzoni MF, Donkelaar HJT, Wismans PGP, Roubos EW. 1994. Involvement of retinohypothalamic input, suprachiasmatic nucleus, magnocellular nucleus and locus coeruleus in control of melanotrope cells of Xenopus laevis: a retrograde and anterograde tracing study. Neuroscience 61:411-420.
70. Ubink R, Tuinhof R, Roubos EW. 1998. Identification of suprachiasmatic melanotrope-inhibiting neurons in Xenopus laevis: a confocal laser-scanning microscopy study. J Comp Neurol 397:60-68.
71. 2+ currents. J Physiol (Lond) 475:185-195.
72. Vallarino M, Danger JM, Fasolo A, Pelletier G, Saint-Pierre S, Vaudry H. 1988. Distribution and characterization of neuropeptide Y in the brain of an elasmobranch fish. Brain Res 448:67-76.
73. Vallarino M, Tranchand-Bunel D, Vaudry H. 1992. Alpha-melanocyte-stimulating hormone (α-MSH) in the brain of the African lungfish, Protopterus annectens: immunohistochemical localization and biochemical characterization. J Comp Neurol 322:266-274.
74. Vallarino M, Feuilloley M, Thoumas JL, Demorgny R, Masini MA, Vaudry H. 1995a. Distribution of FMRFamide-like immunoreactivity in the brain of the lungfish Protopterus annectens. Peptides 16:1187-1196.
75. Vallarino M, Tranchand-Bunel D, Thoumas JL, Masini MA, Conlon JM, Fournier A, Pelletier G, Vaudry H. 1995b. Neuropeptide tyrosine in the brain of the African lungfish, Protopterus annectens: immunohistochemical localization and biochemical characterization. J Comp Neurol 356:537-551.
76. Vallarino M, Goula D, Trabucchi M, Masini MA, Chartrel N, Vaudry H. 1996. Immunocytochemical localization of atrial natriuretic factor and autoradiographic distribution of atrial natriuretic factor binding sites in the brain of the African lungfish, Protopterus annectens. J Comp Neurol 375:345-362.
77. Vallarino M, Trabucchi M, Masini MA, Chartrel N, Vaudry H. 1997. Immunocytochemical localization of somatostatin and autoradiographic distribution of somatostatin binding sites in the brain of the African lungfish, Protopterus annectens. J Comp Neurol 388:337-353.
78. Vallarino M, Thoumas JL, Masini MA, Trabucchi M, Chartrel N, Vaudry H. 1998. Immunocytochemical localization of enkephalins in the brain of the African lungfish, Protopterus annectens, provides evidence for differential distribution of met-enkephalin and leu-enkephalin. J Comp Neurol 396:275-287.
79. Vallarino M, Masini MA, Trabucchi M, Mathieu M, Vaudry H. 1998. Autoradiographic distribution of neuropeptide tyrosine binding sites in the brain of the African lungfish, Protopterus annectens. Neurosci Lett 254:5-8.
80. Verburg van Kemenade BML, Jenks BG, Danger JM, Vaudry H, Pelletier G, Saint-Pierre S. 1987a. An NPY-like peptide may function as MSH-release inhibiting factor in Xenopus laevis. Peptides 8:61-67.
81. Verburg-van Kemenade BM, Jenks BG, Lenssen FJ, Vaudry H. 1987b. Characterization of gamma-aminobutyric acid receptors in the neurointermediate lobe of the amphibian Xenopus laevis. Endocrinology 120:622-628.
82. Yáñez J, Rodríguez M, Pérez S, Adrio F, Rodríguez-Moldes I, Manso MJ, Anadón R. 1997. The neuronal system of the saccus vasculosus of trout (Salmo trutta fario and Oncorhynchus mykiss): an immunocytochemical and nerve tracing study. Cell Tissue Res 288:497-507.
83. Zoli M, Torri C, Ferrari R, Jansson A, Zini I, Fuxe K, Agnati LF. 1998. The emergence of the volume transmission concept. Brain Res Rev 26:136-147.