The spatial relationship of γ-aminobutyric acid (GABA) neurons and gonadotropin-releasing hormone (GnRH) neurons in larval and adult sea lamprey, Petromyzon marinus

Brain, Behavior and Evolution

Volumn 60, Issue 1, 2002, Pages 1-12

  Reed, Karen L ^a   MacIntyre, Janet K ^a   Tobet, Stuart A ^b   Trudeau, Vance L ^c   MacEachern, Lisa ^c   Rubin, Beverly S ^d   Sower, Stacia A ^a  

^a UNIVERSITY OF NEW HAMPSHIRE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF OTTAWA   (Canada)

^d TUFTS MEDICAL CENTER   (United States)

Author keywords

Development; GABA; Glutamic acid decarboxylase; Gonadotropin releasing hormone; Lamprey

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMATE DECARBOXYLASE; GLUTAMIC ACID; GONADORELIN; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; BRAIN THIRD VENTRICLE; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; FERTILIZATION; HYPOTHALAMUS; IMMUNOCHEMISTRY; IN SITU HYBRIDIZATION; LAMPREY; LARVAL STAGE; MALE; NONHUMAN; OLFACTORY BULB; PETROMYZON MARINUS; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN SYNTHESIS; TELENCEPHALON;

ANIMALS; CULTURE TECHNIQUES; GAMMA-AMINOBUTYRIC ACID; GONADOTROPIN-RELEASING HORMONE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LAMPREYS; NEURONS;

PETROMYZON MARINUS; PETROMYZONTIDAE;

EID: 0036380315     PISSN: 00068977     EISSN: None     Source Type: Journal    
DOI: 10.1159/000064117     Document Type: Article

References (62)

1. Adler, B.A., and W.R. Crowley (1986) Evidence for gamma-aminobutyric acid modulation of ovarian hormonal effects on luteinizing hormone secretion and hypothalamic catecholamine activity in the female rat. Endocrinology, 118: 91-97.
2. Anadón, R., F. Adrio, and I. Rodriguez-Moldes (1998) Distribution of GABA immunoreactivity in the central and peripheral nervous system of amphioxus (Branchiostoma lanceolatum Pallas). J. Comp. Neurol., 401: 293-307.
3. Anadón, R., M. Meléndez-Ferro, E. Pérez-Costas, M. A. Pombal, and M. C. Rodicio (1998) Centrifugal fibers are the only GABAergic structures of the retina of the larval sea lamprey: An immunocytochemical study. Brain Res., 728: 297-302.
4. Barale, E., A. Fasolo, E. Girardi, C. Artero, and M.F. Franzoni (1996) Immunohistochemical investigation of gamma-aminobutyric acid ontogeny and transient expression in the central nervous system of Xenopus laevis tadpoles. J. Comp. Neurol., 368: 285-294.
5. Batueva, V., E.I. Suderevskya, N.P. Vesselkin, J. Pierre, and J. Repérant (1990) Localisation of GABA-immunopositive cells in the river lamprey spinal cord. J. Hirnforsch., 31: 739-745.
6. Bennis, M., A. Calas, M. Geffard, and H. Gamrani (1991) Distribution of GABA immunoreactive systems in the forebrain and midbrain of the chameleon. Brain Res. Bull., 26: 891-898.
7. Bergen, H.T., J.F. Hejtmancik, and D. W. Pfaff (1991) Effects of gamma-aminobutyric acid receptor agonists and antagonist on LHRH-synthesizing neurons as detected by immunocytochemistry and in situ hybridization. Exp. Brain Res., 87: 46-56.
8. Bless, E.P., W.A. Westaway, G.A. Schwarting, and S. A. Tobet (2000) Effects of gamma-aminobutyric acid(A) receptor manipulation on migrating gonadotropin-releasing hormone neurons through the entire migratory route in vivo and in vitro. Endocrinology, 141: 1254-1262.
9. Bosma, P.T., M. Blazquez, M.A. Collins, J. D. Bishop, G. Drouin, I. G. Priede, K. Docherty, and V.L. Trudeau (1999) Multiplicity of glutamic acid decarboxylases (GAD) in vertebrates: Molecular phylogeny and evidence for a new GAD paralog. Mol. Biol. Evol., 16: 397-404.
10. Braissant, O., and W. Wahli (1998) Differential expression of peroxisome proliferator-activated receptor-alpha, -beta, and -gamma during rat embryonic development. Endocrinology, 139: 2748-2754.
11. Brodin, L., N. Dale, J. Christenson, J. Storm-Mathisen, T. Hökfelt, and S. Grillner (1990) Three types of GABA-immunoreactive cells in the lamprey spinal cord. Brain Res., 508: 172-175.
12. Cherubini, E., and F. Conti (2001) Generating diversity at GABAergic synapses. Trends Neurosci., 24: 155-162.
13. Doldan, M.J., B. Prego, B.I. Holmqvist, and E. de Miguel (1999) Distribution of GABA-immunolabeling in the early zebrafish (Danio rerio) brain. Eur. J. Morphol., 37: 126-129.
14. Domenici, L., H.J. Waldvogel, C. Matute, and P. Streit (1988) Distribution of GABA-like immunoreactivity in the pigeon brain. Neuroscience, 25: 931-950.
15. Ekström, P., and L.M. Ohlin (1995) Ontogeny of GABA-immunoreactive neurons in the central nervous system in a teleost, Gasterosteus aculeatus L. J. Chem. Neuroanat., 9: 271-288.
16. Favit, A., W.C. Wetsel, and A. Negro-Vilar (1993) Differential expression of gamma-aminobutyric acid receptors in immortalized luteinizing hormone-releasing hormone neurons. Endocrinology, 133: 1983-1989.
17. Feleder, C., H. Jarry, S. Leonhardt, W. Wuttke, and J.A. Moguilevsky (1996) The GABAergic control of gonadotropin-releasing hormone secretion in male rats during sexual maturation involves effects on hypothalamic excitatory and inhibitory amino acid systems. Neuroendocrinology, 64: 305-312.
18. Flugge, G., W.H. Oertel, and W. Wuttke (1986) Evidence for estrogen-receptive GABAergic neurons in the preoptic/anterior hypothalamic area of the rat brain. Neuroendocrinology, 43: 1-5.
19. Franzoni, M.F., and P. Morino (1989) The distribution of GABA-like-immunoreactive neurons in the brain of the newt, Triturus cristatus carnifex, and the green frog, Rana esculenta. Cell Tissue Res., 255: 155-166.
20. Fueshko, S.M., S. Key, and S. Wray (1998) GABA inhibits migration of luteinizing hormone-releasing hormone neurons in embryonic olfactory explants. J. Neurosci., 18: 2560-2569.
21. Herbison, A.E. (1998) Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr. Rev., 19: 302-330.
22. Jarry, H., S. Leonhardt, and W. Wuttke (1991) Gamma-aminobutyric acid neurons in the preoptic/anterior hypothalamic area synchronize the phasic activity of the gonadotropin-releasing hormone pulse generator in ovariectomized rats. Neuroendocrinology, 53: 261-267.
23. Kah, O., P. Dubourg, M. G. Martinoli, M. Rabhi, F. Gonnet, M. Geffard, and A. Calas (1987) Central GABAergic innervation of the pituitary in goldfish: A radioautographic and immunocytochemical study at the electron microscope level. Gen. Comp. Endocrinol., 67: 324-332.
24. Kah, O., V.L. Trudeau, B.D. Sloley, J.P. Chang, P. Dubourg, K.L. Yu, and R.E. Peter (1992) Influence of GABA on gonadotrophin release in the goldfish. Neuroendocrinology, 55: 396-404.
25. Katarova, Z., G. Sekerkova, S. Prodan, E. Mugnaini, and G. Szabo (2000) Domain-restricted expression of two glutamic acid decarboxylase genes in midgestation mouse embryos. J. Comp. Neurol., 424: 607-627.
26. King, J.C., S.A. Sower, and E.L. Anthony (1988) Neuronal systems immunoreactive with antiserum to lamprey gonadotropin-releasing hormone in the brain of Petromyzon marinus. Cell Tissue Res., 253: 1-8.
27. Kusano, K., S. Fueshko, H. Gainer, and S. Wray (1995) Electrical and synaptic properties of embryonic luteinizing hormone-releasing hormone neurons in explant cultures. Proc. Natl. Acad. Sci. USA, 92: 3918-3922.
28. Lariviere, K., L. MacEachern, G. Majchrzak, V. Greco, S. Chiu, G. Drouin, and V. L. Trudeau (2002) Multiplicity of glutamic acid decarboxylase: Early gene duplication and the existence of novel vertebrate forms. Mol. Biol. Evol., submitted.
29. Lauder, J.M. (1993) Neurotransmitters as growth regulatory signals: Role of receptors and second messengers. Trends Neurosci., 16: 233-240.
30. Lauder, J.M., V.K. Han, P. Henderson, T. Verdoorn, and A. C. Towle (1986) Prenatal ontogeny of the GABAergic system in the rat brain: An immunocytochemical study. Neuroscience, 19: 465-493.
31. Leranth, C., N.J. MacLusky, H. Sakamoto, M. Shanabrough, and F. Naftolin (1985) Glutamic acid decarboxylase-containing axons synapse on LHRH neurons in the rat medial preoptic area. Neuroendocrinology, 40: 536-539.
32. Mananos, E.L., I. Anglade, J. Chyb, C. Saligaut, B. Breton, and O. Kah (1999) Involvement of gamma-aminobutyric acid in the control of GTH-1 and GTH-2 secretion in male and female rainbow trout. Neuroendocrinology, 69: 269-280.
33. Martinoli, M.G., P. Dubourg, M. Geffard, A. Calas, and O. Kah (1990) Distribution of GABA-immunoreactive neurons in the forebrain of the goldfish, Carassius auratus. Cell Tissue Res., 260: 77-84.
34. McCann, S.M., E. Vijayan, A. Negro-Vilar, H. Mizunuma, and H. Mangat (1984) Gamma aminobutyric acid (GABA), a modulator of anterior pituitary hormone secretion by hypothalamic and pituitary action. Psychoneuroendocrinology, 9: 97-106.
35. Medina, M., J. Repérant, S. Dufour, R. Ward, N. Le Belle, and D. Miceli (1994) The distribution of GABA-immunoreactive neurons in the brain of the silver eel (Anguilla anguilla L.). Anat. Embryol. (Berl.), 189: 25-39.
36. Meléndez-Ferro, M., E. Pérez-Costas, M.J. González, M.A. Pombal, R. Anadón, and M.C. Rodicio (2000) GABA-immunoreactive internuclear neurons in the oculomotor system of lampreys. Brain Res., 855: 150-157.
37. Meléndez-Ferro, M., E. Pérez-Costas, R. Rodríguez-Muñoz, M.P. Gómez-López, R. Anadón, and M.C. Rodicio (2001) GABA immunoreactivity in the olfactory bulbs of the adult sea lamprey. Brain Res., 893: 253-260.
38. Meléndez-Ferro, M., B. Villar-Cheda, X.M. Abalo, E. Pérez-Costas, R. Rodríguez-Muñoz, W.J. Degrip, J. Yáñez, M. C. Rodicio, and R. Anadón (2002) Early development of the retina and pineal complex in the sea lamprey: Comparative immunocytochemical study. J. Comp. Neurol., 442: 250-265.
39. Mitsushima, D., D.L. Hei, and E. Terasawa (1994) gamma-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc. Natl. Acad. Sci. USA, 91: 395-399.
40. Mitsushima, D., F. Marzban, L.L. Luchansky, A.J. Burich, K.L. Keen, M. Durning, T.G. Golos, and E. Terasawa (1996) Role of glutamic acid decarboxylase in the prepubertal inhibition of the luteinizing hormone releasing hormone release in female rhesus monkeys. J. Neurosci., 16: 2563-2573.
41. Muske, L.E. (1993) Evolution of gonadotropin-releasing hormone (GnRH) neuronal systems. Brain Behav. Evol., 42: 215-230.
42. Piavis, G.W. (1961) Embryological stages in the sea lamprey and effects of temperature on development. US Fish Wildlife Serv. Fish. Bull., 182: 111-143.
43. Rio, J.P., N.P. Vesselkin, E. Kirpitchnikova, N. B. Kenigfest, C. Versaux-Botteri, and J. Anadón Repérant (1993) Presumptive GABAergic centrifugal input to the lamprey retina: A double-labeling study with axonal tracing and GABA immunocytochemistry. Brain Res., 600: 9-19.
44. Rio, J.P., N.P. Vesselkin, J. Repérant, N.B. Kenigfest, D. Miceli, and V. Adanina (1996) Retinal and nonretinal inputs upon retinopedal RMN neurons in the lamprey: A light and electron microscopic study combining HRP axonal tracing and GABA immunocytochemistry. J. Chem. Anat., 12: 51-70.
45. Roberts, A., N. Dale, O.P. Ottersen, and J. Storm-Mathisen (1987) The early development of neurons with GABA immunoreactivity in the CNS of Xenopus laevis embryos. J. Comp. Neurol., 261: 435-449.
46. Schmitz, G.G., T. Walter, R. Seibl, and C. Kessler (1991) Nonradioactive labeling of oligonucleotides in vitro with the hapten digoxigenin by tailing with terminal transferase. Anal. Biochem., 192: 222-231.
47. Senthilkumaran, B., K. Okuzawa, K. Gen, and H. Kagawa (2001) Effects of serotonin, GABA and neuropeptide Y on seabream gonadotropin releasing hormone release in vitro from preoptic-anterior hypothalamus and pituitary of red sea-bream, Pagrus major. J. Neuroendocrinol., 13: 395-400.
48. Sloley, B.D., O. Kah, V.L. Trudeau, J.G. Dulka, and R.E. Peter (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.
49. Sower, S.A., Y.C. Chiang, S. Lovas, and J.M. Conlon (1993) Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain. Endocrinology, 132: 1125-1131.
50. Suzuki, K., R.L. Gamble, and S.A. Sower (2000) Multiple transcripts encoding lamprey gonadotropin-releasing hormone-I precursors. J. Mol. Endocrinol., 24: 365-376.
51. Tobet, S.A., T.W. Chickering, J.C. King, E.G. Stopa, K. Kim, V. Kuo-Leblank, and G.A. Schwarting (1996a) Expression of gamma-aminobutyric acid and gonadotropin-releasing hormone during neuronal migration through the olfactory system. Endocrinology, 137: 5415-5420.
52. Tobet, S.A., T.W. Chickering, and S.A. Sower (1996b) Relationship of gonadotropin-releasing hormone (GnRH) neurons to the olfactory system in developing lamprey (Petromyzon marinus). J. Comp. Neurol., 376: 97-111.
53. Tobet, S.A., M. Nozaki, J.H. Youson, and S.A. Sower (1995) Distribution of lamprey gonadotropin-releasing hormone-III (GnRH-III) in brains of larval lamprey (Petromyzon marinus). Cell Tissue Res., 279: 261-270.
54. Tobet, S.A., S.A. Sower, and G.A. Schwarting (1997) Gonadotropin-releasing hormone containing neurons and olfactory fibers during development: From lamprey to mammals. Brain Res. Bull., 44: 479-486.
55. Trabucchi, M., N. Chartrel, G. Pelletier, M. Vallarino, and H. Vaudry (2000) Distribution of GAD-immunoreactive neurons in the diencephalon of the african lungfish, Protopterus annectens: Colocalization of GAD and NPY in the preoptic area. J. Comp. Neurol., 419: 223-232.
56. A receptors, dopamine, and sex steroids. Am. J. Physiol., 265: R348-355.
57. Trudeau, V.L., B.D. Sloley, and R.E. Peter (1993b) Norepinephrine turnover in the goldfish brain is modulated by sex steroids and GABA. Brain Res., 624: 29-34.
58. Trudeau, V.L., B.D. Sloley, and R.E. Peter (1993c) Testosterone enhances GABA and taurine but not N-methyl-D,L-aspartate stimulation of gonadotropin secretion in the goldfish: Possible sex steroid feedback mechanisms. J. Neuroendocrinol., 5: 129-136.
59. Trudeau, V.L., D. Spanswick, E.J. Fraser, K. Lariviere, D. Crump, S. Chiu, M. MacMillan, and R.W. Schulz (2000a) The role of amino acid neurotransmitters in the regulation of pituitary gonadotropin release in fish. Biochem. Cell. Biol., 78: 241-259.
60. Trudeau, V.L., P.T. Bosma, M. Collins, I.G. Priede, and K. Docherty (2000b) Sexually dimorphic expression of glutamate decarboxylase mRNA in the hypothalamus of the deep sea armed grenadier, Coryphaenoides (Nematonurus) armatus. Brain Behav. Evol., 56: 269-275.
61. Von Bartheld, C.S., and E.W. Rubel (1989) Transient GABA immunoreactivity in cranial nerves of the chick embryo. J. Comp. Neurol., 286: 456-471.
62. Wray, S., S.M. Fueshko, K. Kusano, and H. Gainer (1996) GABAergic neurons in the embryonic olfactory pit/vomeronasal organ: Maintenance of functional GABAergic synapses in olfactory explants. Dev. Biol., 180: 631-645.