Histochemistry

, Volume 98, Issue 1, pp 51–66 | Cite as

Immunocytochemical localization of a galanin-like peptidergic system in the brain of two urodele and two anuran species (Amphibia)

  • M. Olivereau
  • J. M. Olivereau
Article

Summary

Galanin-like immunoreactivity was localized in the brain of Urodela (Ambystoma, Pleurodeles) and Anura (Bufo, Xenopus) by immunocytochemistry with anti-porcine galanin antiserum. In the four species, immunoreactive perikarya were observed in the telencephalon (striatum, amygdala), diencephalon preoptic area mainly along the anterodorsal wall of the preoptic recessus, suprachiasmatic nucleus, lateral hypothalamus, ventral and dorsal infundibular nuclei, paraventricular organ, and rhombencephalon (nucleus of the solitary tract). Galaninergic fibres extended in similar regions and in the medial septum, ventral telencephalon, ventral hypothalamus, median eminence, and various mesencephalic and rhombencephalic regions. Contacts with the cerebrospinal fluid cavity occurred along the preoptic recessus (Ambystoma) and the ventral infundibular wall (all species). Fibres were scarce in the neurohypophysis. The distal and intermediate lobes of the pituitary were virtually devoid of immunoreactivity. The galaninergic system appeared more developed in adult amphibia than in young animals, suggesting the stimulating influence of sex steroids on the expression of galanin as previously described inAnguilla. The extensive distribution of the galanin-like immunoreactive neurons in amphibian brains suggests that this peptide may act as a neuromodulatur and/or neurotransmitter.

Keywords

Lateral Hypothalamus Median Eminence Suprachiasmatic Nucleus Medial Septum Anuran Species 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andersen AC, Pelletier G, Eberlé AN, Leroux P, Jégou S, Vaudry H (1986) Localization of melanin-concentrating hormone-like immunoreactivity in the brain and pituitary of the frogRana ridibunda. Peptides 7:941–952Google Scholar
  2. Andersen AC, Danger JM, Fasolo A, Kah O, Tonon MC, Vaudry H (1988) Immunohistochemical localization of gonadotropin-releasing hormone-associated peptide in the brain of the frog. J Comp Neurol 273:241–251Google Scholar
  3. Arai R, Onteniente B, Trembleau A, Landry M, Calas A (1990) Hypothalamic galanin-immunoreactive neurons projecting to the posterior lobe of the rat pituitary: a combined retrograde tracing and immunohistochemical study. J Comp Neurol 299:405–420Google Scholar
  4. Batten TFC, Moons L, Cambre M, Vandesande F (1990) Anatomical distribution of galanin-like immunoreactivity in the brain and pituitary of teleost fishes. Neurosci Lett 111:12–17Google Scholar
  5. Benyamina M, Delbende C, Jégou S, Leroux P, Leboulenger F, Tonon MC, Guy J, Pelletier G, Vaudry H (1986) Localization and identification of α-melanocyte-stimulating hormone (α-MSH) in the frog brain. Brain Res 366:230–237Google Scholar
  6. Berrettini WH, Kaye WH, Sunderland T, May C, Gwirtsman HE, Mellow A, Albright A (1988) Galanin immunoreactivity in human CSF; studies in eating disorders and Alzheimer's disease. Neuropsychobiology 19:64–68Google Scholar
  7. Bersani M, Johnsen AH, Hojrup P, Dunning BE, Andreasen JJ, Holst JJ (1991) Human galanin. Primary structure and identification of two molecular forms. FEBS Lett 283:189–194Google Scholar
  8. Blähser S, Vigh-Teichmann I, Ueck M (1982) Cerebrospinal fluid-contacting neurons and other somatostatin-immunoreactive perikarya in brains of tadpoles ofXenopus leavis. Cell Tissue Res 224:693–697Google Scholar
  9. Chieffi G, Pierantoni R, Fasano S (1991) Immunoreactive GnRH in hypothalamic and extrahypothalamic areas. Int Rev Cytol 127:1–56Google Scholar
  10. Courtice GP (1991) Effect of neuropeptide Y and galanin on autonomic control of heart rate in the toad,Bufo marinus. J Autonom Nerv Syst 33:231–238Google Scholar
  11. 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 6:1225–1236Google Scholar
  12. Di Meglio M, Morrell JI, Pfaff DW (1987) Localization of steroid-concentrating cells in the central nervous system of the frogRana esculenta. Gen Comp Endocrinol 67:149–154Google Scholar
  13. Doerr-Schott J, Garaud JC, Clauss RO (1979) Immunohistochemical localization of a gastrin-like peptide in the brain of an amphibian,Xenopus laevis Daud. Cell Tissue Res 203:65–78Google Scholar
  14. Doerr-Schott J, Dubois MP, Lichte C (1981) Immunohistochemical localization of substances reactive to antisera against α- and β-endorphin and met-enkephalin in the brain ofRana temporaria L. Cell Tissue Res 217:79–92Google Scholar
  15. Evans HF, Shine J (1991) Human galanin. Molecular cloning reveals a unique structure. Endocrinology 129:1682–1684Google Scholar
  16. Fasolo A, Andreone C, Vandesande F (1984) Immunohistochemical localization of corticotropin-releasing factor (CRF)-like immunoreactivity in the hypothalamus of the newt,Triturus cristatus. Neurosci Lett 49:135–142Google Scholar
  17. Franzoni MF, Thibault J, Fasolo A, Martinoli MG, Scaranari F, Calas A (1986) Organization of tyrosine-hydroxylase immunopositive neurons in the brain of the crested newt,Triturus cristatus carnifex. J Comp Neurol 251:121–134Google Scholar
  18. Gaudino G, Fasolo A (1980) Substance P-related peptides in the hypothalamus of amphibia. Cell Tissue Res 211:241–250Google Scholar
  19. Gonzalez A, Smeets WJAJ (1991) Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuranRana ridibunda and the urodelePleurodeles waltlii. J Comp Neurol 303:457–478Google Scholar
  20. Holmqvist BI, Ekström P (1991) Galanin-like immunoreactivity in the brain of teleosts. Distribution and relation to substance P, vasotocin, and isotocin in the Atlantic salmon (Salmo salar). J Comp Neurol 306:361–381Google Scholar
  21. Horsten G, Vandesande F (1991) Localization of galanin in the brain of the frog (Rana temporaria): an immunocytochemical study. Gen Comp Endocrinol 82:266Google Scholar
  22. Kaplan LM, Spindel ER, Isselbacher KJ, Chin WW (1988) Tissue-specific expression of the rat galanin gene. Proc Natl Acad Sci USA 85:1065–1069Google Scholar
  23. Kelley DB, Morrell JI, Pfaff DW (1975) Autoradiographic localization of hormone-concentrating cells in the brain of an amphibian,Xenopus laevis. I. Testosterone. J Comp Neurol 164:47–62Google Scholar
  24. Kelley DB, Lieberburg I, McEwen BS, Pfaff DW (1978) Autoradiographic and biochemical studies of steroid hormone concentrating cells in the brain ofRana pipiens. Brain Res 140:287–305Google Scholar
  25. Konopka LM, Parsons RL (1989) Characteristics of the galanin-induced depolarization of mudpuppy parasympathetic post-ganglionic neurons. Neurosci Lett 99:142–146Google Scholar
  26. Konopka LM, McKeon TW, Parsons RL (1989) Galanin-induced hyperpolarization and decreased membrane excitability of neurones in mudpuppy cardiac ganglia. J Physiol 410:107–122Google Scholar
  27. Lamacz M, Hindelang C, Tonon MC, Vaudry H, Stoeckel ME (1989) Three distinct thyrotropin-releasing hormone-immunoreactive axonal systems project in the median eminence-pituitary complex of the frogRana ridibunda. Immunocytochemical evidence for a co-localization of thyrotropin-releasing hormone and mesotocin in fibers innervating pars intermedia cells. Neuroscience 32:451–462Google Scholar
  28. Lázár GY, Liposits ZS, Tóth P, Trasti SC, Maderdrut JL, Merchenthaler I (1991) Distribution of galanin-like immunoreactivity in the brain ofRana esculenta andXenopus laevis. J Comp Neurol 310:45–67Google Scholar
  29. Lundquist CT, Rökaeus 0A, Nassel DR (1991) Galanin immunoreactivity in the blowfly nervous system. Localization and chromatographic analysis. J Comp Neurol 312:77–96Google Scholar
  30. McKeon TW, Parsons RL (1990) Galanin immunoreactivity in the mudpuppy cardiac ganglion. J Autonom Nerv Syst 31:135–140Google Scholar
  31. McKeon TW, Carraway RE, Konopka LM, Parsons RL (1990) Distribution of galanin-like peptides in various tissues ofNecturus maculosus. A biochemical and immunohistochemical analysis. Cell Tissue Res 262:461–466Google Scholar
  32. McKeon TW, Konopka LM, Parsons RL (1991) Galanin as an inhibitory transmitter in the mudpuppy cardiac ganglion. J Autonom Nerv Syst 33:119–120Google Scholar
  33. Merchenthaler I (1991) The hypophysiotropic galanin system of the rat brain. Neuroscience 44:643–654Google Scholar
  34. Merchenthaler I, Lázár G, Maderdrut JL (1989) Distribution of proenkephalin-derived peptides in the brain ofRana esculenta. J Comp Neurol 281:23–39Google Scholar
  35. Mimnagh KM, Bolaffi JL, Montgomery NM, Kaltenbach JC (1987) Thyrotropin-releasing hormone (TRH): immunohistochemical distribution in tadpole and frog brain. Gen Comp Endocrinol 66:394–404Google Scholar
  36. Morrell JI, Pfaff DW (1978) A neuroendocrine approach to brain function: localization of sex steroid concentrating cells in vertebrate brains. Am Zool 18:447–460Google Scholar
  37. Morrell JI, Kelley DB, Pfaff DW (1975) Autoradiographic localization of hormone-concentrating cells in the brain of an amphibian,Xenopus laevis. II. Estradiol. J Comp Neurol 164:63–78Google Scholar
  38. Morris JL, Gibbins IL, Osborne PB (1989) Galanin-like immunoreactivity in sympathetic and parasympathetic neurons of the toadBufo marinus. Neurosci Lett 102:142–148Google Scholar
  39. Mulatero B, Fasolo A (1991) Calcitonin gene-related peptide immunoreactivity in the hypothalamo-hypophysial system of the green frog,Rana esculenta. Gen Comp Endocrinol 81:349–356Google Scholar
  40. Mulatero B, Boulay D, Panzanelli P, Andreone C, Vandesande F, Vaudry H, Fasolo A (1991) Galanin-like positive neuronal systems in the newt brain. Gen Comp Endocrinol 82:264Google Scholar
  41. Neary TJ, Northcutt RG (1983) Nuclear organization of the bullfrog diencephalon. J Comp Neurol 213:262–278Google Scholar
  42. Netchitailo P, Feuilloley M, Pelletier G, Leboulenger F, Cantin M, Gutkowska J, Vaudry H (1987) Atrial natriuretic factor-like immunoreactivity in the central nervous system of the frog. Neuroscience 22:341–360Google Scholar
  43. Norberg A, Sillard R, Carlquist M, Jörnvall H, Mutt V (1991) Chemical detection of natural peptides by specific structure. Isolation of chicken galanin by monitoring for its N-terminal dipeptide, and determination of the amino acid sequence. FEBS Lett 288:151–153Google Scholar
  44. O'Halloran DJ, Jones PM, Steel JH, Gon G, Giaid A, Ghatei MA, Polak JM, Bloom SR (1990) Effect of endocrine manipulation on anterior pituitary galanin in the rat. Endocrinology 127:467–475Google Scholar
  45. Olivereau M, Olivereau JM (1991a) Immunocytochemical localization of a galanin-like peptidergic system in the brain and pituitary of some teleost fish. Histochemistry 96:343–354Google Scholar
  46. Olivereau M, Olivereau J (1991b) Galanin-like immunoreactivity is increased in the brain of estradiol- and methyltestosterone-treated eels. Histochemistry 96:487–498Google Scholar
  47. Olivereau M, Vandesande F, Boucique E, Ollevier F, Olivereau JM (1987) Immunocytochemical localization and spatial relation to the adenohypophysis of a somatostatin-like and a corticotropin-releasing factor-like peptide in the brain of four amphibian species. Cell Tissue Res 247:317–324Google Scholar
  48. Parsons RL, Konopka LM (1990) Galanin-induced hyperpolarization of mudpuppy neurons is calcium dependent. Neurosci Lett 115:207–212Google Scholar
  49. Parsons RL, Konopka LM (1991) Analysis of the galanin-induced decrease in membrane excitability in mudpuppy parasympathetic neurons. Neuroscience 43:647–660Google Scholar
  50. Parsons RL, Neel DS, Konopka LM, McKeon TW (1989) The presence and possible role of a galanin-like peptide in the mudpuppy heart. Neuroscience 29:749–760Google Scholar
  51. 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 275:309–325Google Scholar
  52. Prasada Rao PD, Hartwig HG (1974) Monoaminergic tracts of the diencephalon and innervation of the pars intermedia inRana temporaria. A fluorescence and microspectrofluorimetric study. Cell Tissue Res 151:1–26Google Scholar
  53. Rökaeus Å, Brownstein MJ (1986) Construction of a porcine adrenal medullary cDNA library and nucleotide sequence analysis of two clones encoding a galanin precursor. Proc Natl Acad Sci USA 83:6287–6291Google Scholar
  54. Rökaeus Å, Calquist M (1988) Nucleotide sequence analysis of cDNA encoding a bovine galanin precursor protein in the adrenal medulla and chemical isolation of bovine gut galanin. FEBS Lett 234:400–406Google Scholar
  55. Schmidt WE, Kratzin H, Eckart K, Drevs D, Mundkowski G, Clemens A, Katsoulis S, Schäfer H, Gallwitz B, Creutzfeldt W (1991) Isolation and primary structure of pituitary human galanin, a 30-residue nonamidated neuropeptide. Proc Natl Acad Sci USA 88:11435–11439Google Scholar
  56. Seki T, Nakai Y, Shioda S, Mitsuura T, Kikuyama S (1983) Distribution of immunoreactive thyrotropin-releasing hormone in the forebrain and hypophysis of the bullfrog,Rana catesbeiana. Cell Tissue Res 233:507–516Google Scholar
  57. Shioda S, Nakai Y, Iwai C, Sunayama H (1989) Co-existence of THR with mesotocin in the same axon terminals of the bullfrog pars nervosa as revealed by double immunocytochemistry. Neurosci Lett 98:25–28Google Scholar
  58. Terlou M, Ploemacher RE (1973) The distribution of monoamines in the tel-, di- and mesencephalon ofXenopus laevis tadpoles, with special reference to the hypothalamo-hypophysial system. Z Zellforsch 137:521–540Google Scholar
  59. Tonon MC, Burlet A, Lauber M, Cuet P, Jégou S, Gouteux L, Ling N, Vaudry H (1985) Immunohistochemical localization and radioimmunoassay of corticotropin-releasing factor in the forebrain and hypophysis of the frogRana ridibunda. Neuroen-docrinology 40:109–119Google Scholar
  60. Vallarino M, Feuilloley M, Vandesande F, Vaudry H (1991) Immunohistochemical mapping of galanin-like immunoreactivity in the brain of the dogfishScyliorhinus canicula. Peptides 12:351–357Google Scholar
  61. Vandesande F, Dierickx K (1980) Immunocytochemical localization of somatostatin-containing neurons in the brain ofRana temporaria. Cell Tissue Res 205:43–53Google Scholar
  62. Vrontakis ME, Torsello A, Friesen HG (1991) Galanin. J Endocrinol Invest 14:785–794Google Scholar
  63. Wolfbauer C, Skofitsch G (1989) Immunohistochemical localization of galanin and calcitonin-gene related peptide in the brain of the frog,Rana temporaria. Gen Comp Endocrinol 74:295Google Scholar
  64. Yui R (1983) Immunohistochemical studies on peptide neurons in the hypothalamus of the bullfrogRana catesbeiana. Gen Comp Endocrinol 49:195–209Google Scholar
  65. Zoeller RT, Conway KM (1989) Neurons expressing thyrotropin-releasing hormone-like messenger ribonucleic acid are widely distributed inXenopus laevis brain. Gen Comp Endocrinol 76:139–146Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • M. Olivereau
    • 1
  • J. M. Olivereau
    • 2
  1. 1.Laboratoire de PhysiologieInstitut OcéanographiqueParisFrance
  2. 2.Université René DescartesClichyFrance

Personalised recommendations