Cell and Tissue Research

, Volume 255, Issue 3, pp 495–504 | Cite as

Galanin-, neuropeptide Y- and enkephalin-like immunoreactivities in catecholamine-storing paraganglia of the fetal guinea pig and newborn pig

  • G. Fried
  • B. Meister
  • M. Wikström
  • L. Terenius
  • M. Goldstein
Article
Accepted:

Summary

The occurrence and distribution of several neuropeptides and transmitter enzymes have been investigated by means of indirect immunofluorescence histochemistry in preaortal and carotid body-like paraganglia of the fetal guinea pig and the newborn pig. Preaortal paraganglia from the celiac and inferior mesenteric ganglion regions in fetal guinea pigs showed cell bodies immunoreactive (IR) for tyrosine hydroxylase (TH), dopamine β-hydroxylase (DBH), neuropeptide Y (NPY), galanin (GAL) and metenkephalin (ENK). Almost all cells were IR for TH and DBH, whereas NPY-like immunoreactivity (-LI), GAL-LI and ENK-LI occurred less frequently. Direct double-labeling revealed the coexistence of NPY/GAL, NPY/ENK and GAL/ENK in paraganglion cells from the celiac and inferior mesenteric region. Nerve fibers and terminals were IR for ENK; fibers IR for calcitonin-gene-related peptide (CGRP) were present in the inferior mesenteric ganglion region. Preaortal paraganglia cells from the newborn pig showed TH-LI, DBH-LI, GAL-LI and ENK-LI, the distribution pattern being similar to that seen in the guinea pig; however, NPY-LI was absent. Carotid-body-like paraganglia from the newborn pig showed cell bodies IR to TH, GAL and ENK. Few cells were seen with DBH-LI. A rich supply of nerve fibers with CGRP-LI was present; some fibers exhibited ENK-LI and CCK-LI. In the adjacent superior cervical ganglion, ganglion cell bodies showed immunoreactivity to TH, DBH and NPY. A small number of cells were positive for GAL, CGRP and vasoactive intestinal polypeptide (VIP). Physiological activation of the paraganglia, leading to release or increase in catecholamines, may also change the content of the neuropeptides present in the paraganglia.

Key words

Paraganglia Neuropeptide Immunocyto chemistry Noradrenaline Dopamine Cholecystokinin Calcitonin gene-related peptide Vasoactive intestinal polypeptide Guinea pig Pig 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen JM, Adrian TE, Polak JM, Bloom SR (1983) Neuropeptide Y (NPY) in the adrenal gland. J Autonom Nerv Syst 9:559–564Google Scholar
  2. Bauer FE, Adrian TE, Yanaihara N, Polak JM, Bloom SR (1986a) Chromatographic evidence for high-molecular-mass galanin immunoreactivity in pig and cat adrenal glands. FEBS Lett 201:327–331Google Scholar
  3. Bauer FE, Hacker GW, Terenghi G, Adrian TE, Polak JM, Bloom SR (1986b) Localization and molecular forms of galanin in human adrenals: elevated levels in pheochromocytomas. J Clin Endocrinol Metab 63:1372–1378Google Scholar
  4. Blessing WW, Howe PRC, Joh TH, Oliver JR, Willoughby JO (1986) Distribution of tyrosine hydroxylase and neuropeptide Y-like immunoreactive neurons in rabbit medulla oblongata, with attention to colocalization studies, presumptive adrenaline-synthesizing perikarya, and vagal preganglionic cells. J Comp Neurol 248:283–300Google Scholar
  5. Brain SD, Williams TJ, Tippins JR, Morris HR, MacIntyre I (1985) Calcitonin gene-related peptide is a potent vasodilator. Nature 313:54–56Google Scholar
  6. Brundin T (1966) Studies on the preaortal paraganglia of newborn rabbits. Acta Physiol Scand 70: Suppl 290, 1–54Google Scholar
  7. Böck P (1982) The paraganglia. In: Oksche A, Vollrath L (eds) Handbuch der Mikroskopischen Anatomie, Vol VI/8. Springer, Berlin Heidelberg New YorkGoogle Scholar
  8. Carlsöö B, Dahlquist Å, Domeij S, Hellström S, Dedo HH, Izdebski K (1983) Carotid-body-like tissue within the recurrent laryngeal nerve: An endoneural chemosensitive micro-organ? Am J Otolaryngol 4:334–343Google Scholar
  9. Coons AH (1958) Fluorescent antibody methods. In: Danielli JF (ed) General Cytochemical Methods Academic Press, New York, pp 399–422Google Scholar
  10. Colombo M, Kummer W, Heym C (1987) Immunohistochemistry of opioid peptides in guinea-pig paraganglia. Exp Brain Res 16:67–72Google Scholar
  11. Coupland RE (1953) On the morphology and adrenaline-noradrenaline content of chromaffin tissue. J Endocrinol 9:194–203Google Scholar
  12. Coupland RE (1965) The natural history of the chromaffin cell. Longmans, LondonGoogle Scholar
  13. Coupland RE, Kent C, Kent SE (1982) Normal function of extraadrenal chromaffin tissues in the young rabbit and guinea-pig. J Endocrinol 92:433–442Google Scholar
  14. Dahlqvist Å, Hellström S, Carlsöö B, Pequignot JM (1987) Paraganglia of the rat recurrent laryngeal nerve after long-term hypoxia: a morphometric and biochemical study. J Neurocytol 16:289–297Google Scholar
  15. Dahlqvist Å, Pequignot J-M, Hellström S, Carlsöö B, Peyrin L (1986) Catecholamines of endoneurial laryngeal paraganglia in the rat. Acta Physiol Scand 127:257–261Google Scholar
  16. Dalsgaard C-J, Hökfelt T, Elfvin L-G, Terenius L (1982) Enkephalin-containing sympathetic preganglionic neurons projecting to the inferior mesenteric ganglion: evidence from combined retrograde tracing and immunohistochemistry. Neuroscience 7:2039–2050Google Scholar
  17. Daalsgard C-J, Vincent SR, Hökfelt T, Christensson I, Terenius L (1983) Separate origins for the dynorphin and enkephalin immunoreactive fibers in the inferior mesenteric ganglion of the guinea-pig. J Comp Neurol 221:482–489Google Scholar
  18. Evans CJ, Erdelyi E, Hunter J, Barchas JD (1985) Co-localization and characterization of immunoreactive peptides derived from two opioid precursors in guinea-pig adrenal glands. J Neurosci 5:3423–3427Google Scholar
  19. Fahrenkrug J, Pedersen JH (1984) Development and validation of a specific radioimmunoassay for PHI in plasma. Clin Chim Acta 143:183–192Google Scholar
  20. Frey P (1985) Cholecystokinin octapeptide (CCK 26–33), nonsulfated octapeptide ad tetrapeptide (CCK 30–33) in rat brain: Analysis by high pressure liquid chromatography (HPLC) and radioimmunoassay (RIA). Neurochem Int 5:811–815Google Scholar
  21. Fried G, Terenius L, Hökfelt T, Goldstein M (1985) Evidence for the differential localization of noradrenaline and neuropeptide Y (NPY) in neuronal storage vesicles isolated from rat vas deferens. J Neurosci 5:450–458Google Scholar
  22. Fried G, Terenius L, Brodin E, Efendic S, Dockray G, Fahrenkrug J, Goldstein M, Hökfelt T (1986) Neuropeptide Y, enkephalin and noradrenaline coexist in sympathetic neurons innervating the bovine spleen. Cell Tissue Res 243:495–508Google Scholar
  23. Fried G, Wikström M, Lagercrantz H (1988) Postnatal development of catecholamines and response to hypoxia in adrenals and paraganglia from newborn rabbits. J Autonom Nerv Syst 24:65–70Google Scholar
  24. Goldstein M, Anagnoste B, Freedman LS, Roffman M, Ebstein RP, Park DH, Fuxe K, Hökfelt T (1973) Characterization, localization and regulation of catecholamine synthesizing enzymes. In: Usdin E, Snyder S (eds) Frontiers in Catecholamine Research. Pergamon, New York, pp 69–78Google Scholar
  25. Hanson G, Jones L, Fidone S (1986) Physiological chemoreceptor stimulation decreases enkephalin and substance P in the carotid body. Peptides 7:767–769Google Scholar
  26. Helen P, Panula P, Yang H-Y, Hervonen A, Rapoport SI (1984) Location of substance P-, bombesin-gastrin-releasing peptide, (Met)enkephalin and (Met)-enkephalin-arg-phe-like immunoreactivities in adult human sympathetic ganglia. Neuroscience 12:907–916Google Scholar
  27. Hervonen A, Korkala O (1972) The effect of hypoxia on the catecholamine content of human fetal abdominal paraganglia and adrenal medulla. Acta Obstet Gynecol Scand 51:17–24Google Scholar
  28. Hervonen A, Pickel VM, Joh TH, Reis DJ, Linnoila I, Kanerva L, Miller RJ (1980) Immunocytochemical demonstration of the catecholamine-synthesizing enzymes and neuropeptides in the catecholamine-storing cells of human fetal sympathetic nervous system. In: Eränkö O (ed) Histochemistry and cell biology of autonomic neurons, SIF cells and paraneurons. Raven Press, New York, pp 373–378Google Scholar
  29. Järvi R, Helen P, Pelto-Huikko M, Hervonen A (1986) Neuropeptide Y (NPY)-like immunoreactivity in rat sympathetic neurons and small granule-containing cells. Neurosci Lett 67:223–227Google Scholar
  30. Johnson DG, de C Nogueira-Araujo GM (1981) A simple method of reducing fading of immunofluorescence during microscopy. J Immunol Methods 43:349–350CrossRefPubMedGoogle Scholar
  31. Jones CT, Roebuck MM, Walker DW, Lagercrantz H, Johnston BM (1987) Cardiovascular, metabolic and endocrine effects of chemical sympathectomy and of adrenal demedullation in fetal sheep. J Dev Physiol 9:347–367Google Scholar
  32. Ju G, Hökfelt T, Fischer JA, Frey P, Rehfeld JF, Dockray GJ (1986) Does cholecystokinin-like immunoreactivity in rat primary sensory neurons represent calcitonin gene-related peptide? Neurosci Lett 68:305–310Google Scholar
  33. Kohn A (1903) Die Paraganglien. Arch Mikrosk Anat 62:263–365Google Scholar
  34. Kondo H, Kuramoto H, Fujita T (1986) Neuropeptide tyrosinelike immunoreactive nerve fibers in the carotid body chemoreceptor of rats. Brain Res 372:353–356Google Scholar
  35. Kummer W (1987a) Calcitonin gene-related peptide-immunoreactive nerve fibres in carotid body and carotid sinus. Exp Brain Res 16:84–88Google Scholar
  36. Kummer W (1987b) Galanin- and neuropeptide Y-like immunoreactivities coexist in paravertebral sympathetic neurones of the cat. Neurosci Lett 78:127–131Google Scholar
  37. Kummer W, Addicks K, Henkel H, Heym C (1985) Cholecystokinin-like immunoreactivity in cat extra-adrenal paraganglia. Neurosci Lett 55:207–210Google Scholar
  38. Kummer W, Heym C, Colombo M, Lang R (1986) Immunohistochemical evidence for extrinsic and intrinsic opioid systems in the guinea-pig superior cervical ganglion. Anat Embryol (Berl) 174:401–405Google Scholar
  39. Kuramoto H, Kondo H, Fujita T (1986) Neuropeptide tyrosine (NPY)-like immunoreactivity in adrenal chromaffin cells. Anat Rec 214:321–328Google Scholar
  40. Kuramoto H, Kondo H, Fujita T (1987) Calcitonin gene-related peptide (CGRP)-like immunoreactivity in scattered chromaffin cells and nerve fibres in the adrenal gland of rats. Cell Tissue Res 247:309–315Google Scholar
  41. Landis SC, Fredieu JR (1986) Coexistence of calcitonin gene-related peptide and vasoactive intestinal peptide in cholinergic sympathetic innervation of rat sweat glands. Brain Res 377:177–181CrossRefPubMedGoogle Scholar
  42. Lindh B, Hökfelt T, Elfvin LG, Terenius L, Fahrenkrug J, Elde R, Goldstein M (1986) Topography of NPY-, somatostatin-, and VIP-immunoreactive, neuronal subpopulations in the guinea-pig celiac-superior mesenteric ganglion and their projection to the pylorus. J Neurosci 6:2371–2383Google Scholar
  43. Lindh B, Hökfelt T, Elfvin L-G (1987a) Peptides and transmitters in para- and prevertebral ganglia and their projections. Exp Brain Res 16:28–33Google Scholar
  44. Lindh B, Lundberg JM, Hökfelt T, Elfvin LG, Fahrenkrug J, Fischer J (1987b) Coexistence of CGRP- and VIP-like immunoreactivities in a population of neurons in the cat stellate ganglia. Acta Physiol Scand 131:475–476Google Scholar
  45. Lindh B, Hökfelt T, Elfvin L-G (1988) Distribution and origin of peptide-containing nerve fibers in the celiac superior mesenteric ganglion of the guinea-pig. Neuroscience 26:1037–1071Google Scholar
  46. Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effect of NPY on sympathetic function. Acta Physiol Scand 116:477–480Google Scholar
  47. Lundberg JM, Terenius L, Hökfelt T, Goldstein M (1983) High levels of neuropeptide Y (NPY) in peripheral noradrenergic neurons in various mammals including man. Neurosci Lett 42:167–172Google Scholar
  48. Lundberg JM, Terenius L, Hökfelt T, Tatemoto K (1984) Comparative immunohistochemical and biochemical analysis of pancreatic polypeptide-like peptides with special reference to presence of neuropeptide Y in central and peripheral neurons. J Neurosci 4:2376–2386Google Scholar
  49. Lundberg JM, Hökfelt T, Hemsen A, Theodorsson-Norheim E, Pernow J, Hamberger B, Goldstein M (1986) Neuropeptide Y-like immunoreactivity in adrenaline cells of adrenal medulla. Regul Pept 13:169–182Google Scholar
  50. Macrae IM, Furness JB, Costa M (1986) Distribution of subgroups of noradrenaline neurons in the coeliac ganglion. Cell Tissue Res 244:173–180Google Scholar
  51. Markey KA, Kondo S, Shenkman L, Goldstein M (1980) Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol Pharmacol 17:79–85Google Scholar
  52. McDonald DM, Blewett RW (1981) Location and size of carotidbody-like organs (paraganglia) revealed in rats by the permeability of blood vessels to Evans blue dye. J Neurocytol 10:607–643PubMedGoogle Scholar
  53. Pelto-Huikko M, Salminen T (1987) Localization of calcitonin gene-related peptide (CGRP) in chromaffin cells and nerve terminals in the adrenal medulla. Exp Brain Res 16:73–77Google Scholar
  54. Rosenfeld MG, Mermod JJ, Amara SG, Swanson LW, Sawchenko PE, Rivier J, Vale WW, Evans RM (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissuespecific RNA processing. Nature 304:129–135Google Scholar
  55. 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
  56. Schultzberg M, Lundberg JM, Hökfelt T, Terenius L, Brandt J, Elde RP, Goldstein M (1978) Enkephalin-like immunoreactivity in gland cells and nerve terminals of the adrenal medulla. Neuroscience 3:1169–1186Google Scholar
  57. Schultzberg M, Hökfelt T, Terenius L, Elfvin L-G, Lundberg JM, Brandt J, Elde RP, Goldstein M (1979) Enkephalin immunoreactive nerve fibers and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience 4:249–270Google Scholar
  58. Skofitsch G, Jacobowitz DM (1985a) Immunohistochemical mapping of galanin-like neurons in the rat central nervous system. Peptides 6:509–546Google Scholar
  59. Skofitsch G, Jacobowitz DM (1985b) Calcitonin gene-related peptide: Detailed immunohistochemical distribution in the central nervous system. Peptides 6:721–745Google Scholar
  60. Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y — a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660Google Scholar
  61. Tatemoto K, Rökaeus A, Jörnvall H, McDonald TJ, Mutt V (1983) Galanin — a novel biologically active peptide from porcine intestine. FEBS Lett 164:124–128Google Scholar
  62. Vaalasti A, Pelto-Huikko M, Tainio H, Hervonen A (1985) Lightand electron-microscopic demonstration of enkephalin-like immunoreactivity in paraganglia of the human urinary bladder. Cell Tissue Res 239:683–687Google Scholar
  63. Varndell IM, Tapia FJ, de Mey J, Rush RA, Bloom SR, Polak JM (1982) Electron immunocytochemical localization of enkephalin-like material in catecholamine-containing cells of thecarotid body, the adrenal medulla, and pheochromocytoma of man and other mammals. J Histochem Cytochem 30:682–690Google Scholar
  64. Vincent SR, Dalsgaard C-J, Schultzberg M, Hökfelt T, Christensson I, Terenius L (1984) Dynorphin-immunoreactive neurons in the autonomic nervous system. Neuroscience 11:973–987Google Scholar
  65. Wessendorf MW, Elde RP (1985) Characterization of immunofluorescence technique for the demonstration of coexisting transmitters within nerve fibers and terminals. J Histochem Cytochem 33:984–994Google Scholar
  66. Zamboni L, de Martino C (1967) Buffered picric acid formaldehyde: A new rapid fixative for electron microscopy. J Cell Biol 148a:35Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • G. Fried
    • 1
    • 3
  • B. Meister
    • 2
  • M. Wikström
    • 1
  • L. Terenius
    • 4
  • M. Goldstein
    • 5
  1. 1.Department of PhysiologyKarolinska InstitutetStockholmSweden
  2. 2.Department of Histology and NeurobiologyKarolinska InstitutetStockholmSweden
  3. 3.Department of Obstetrics and GynecologyKarolinska InstitutetStockholmSweden
  4. 4.Department of PharmacologyUppsala UniversityUppsalaSweden
  5. 5.Neurochemistry Research Unit, New York University Medical CenterNew YorkUSA

Personalised recommendations