Experimental Brain Research

, Volume 67, Issue 2, pp 420–428 | Cite as

Somatostatin- and enkephalin-like immunoreactivities are frequently colocalized in neurons in the caudal brain stem of rat

  • D. E. Millhorn
  • T. Hökfelt
  • L. Terenius
  • A. Buchan
  • J. C. Brown
Article
Received:
Accepted:

Summary

The medulla oblongata and pons of colchicine treated rats were analyzed with a doublestaining technique using mouse monoclonal antibodies to somatostatin and rabbit polyclonal antibodies raised against methionine-enkephalin. Numerous cells reacted with both antisera but cells reacting with only one antiserum were also observed. Double-stained cells were most frequently encountered at all levels of the nucleus tractus solitarii, in a well defined group in the caudal medullary reticular formation, along the lateral ventral surface of the medulla oblongata, dorsolateral to the inferior olive and in the nucleus raphe magnus. These findings provide further examples of coexistence of two peptides and indicate the possibility that somatostatin-and enkephalin-like peptides are co-released.

Key words

Peptides Coexistence Nucleus tractussolitarii Ventral medulla Immunohistochemistry Rat 
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. Armstrong DM, Miller RJ, Beaudet A, Pickel VM (1984) Enkephalin-like immunoreactivity in rat area postrema: ultrastructural localization and coexistence with serotonin. Brain Res 310: 269–278Google Scholar
  2. Aronin N, DiFiglia M, Graveland GA, Schwartz WJ, WU JY (1984) Localization of immunoreactive enkephalins in GABA synthesizing neurons of the rat neostriatum. Brain Res 300: 376–380Google Scholar
  3. Bolme P, Fuxe K, Agnati LF, Bradley R, Smythies J (1978) Cardiovascular effects of morphine and opioid peptides following intracisternal administration in chloralose-anaesthetized rats. Eur J Pharmacol 48: 319–324Google Scholar
  4. Brazeau P, Vale W, Burgus R, Ling N, Butcher M, Rivier J, Guillemin R (1973) Hypothalamic polypeptide that inhibits the secretion of immunoreactive pituitary growth hormone. Science 179: 77–79Google Scholar
  5. Buchan AMJ, Sikora LKJ, Levy JG, McIntosh CHS, Dyck I, Brown JC (1985) An immunocytochemical investigation with monoclonal antibodies to somatostatin. Histochemistry 83: 175–180Google Scholar
  6. Chan-Palay V, Palay SL (eds) (1984) Coexistence of neuroactive substances in neurons. John Wiley and Sons, New YorkGoogle Scholar
  7. Charnay Y, Léger L, Dray F, Bérod A, Jouvet M, Pujol JF, Dubois PM (1982) Evidence for the presence of enkephalin in catecholaminergic neurons of cat locus coeruleus. Neurosci Lett 30: 147–151Google Scholar
  8. Chronwall BM, Chase TN, O'Donohue TL (1984) Coexistence of neuropeptide Y and somatostatin in rat and human cortical and rat hypothalamic neurons. Neurosci Lett 52: 213–217Google Scholar
  9. Coons AH (1958) Fluorescent antibody methods. In: Danielli JF (ed) General cytochemical methods. Academic Press, New York, pp 399–422Google Scholar
  10. Cuello AC (ed) (1982) Co-transmission. MacMillan, London and BasingtokeGoogle Scholar
  11. Finley JCW, Maderdrut JL, Petrusz P (1981a) The immunohistochemical localization of enkephalin in the central nervous system of the rat. J Comp Neurol 198: 541–565Google Scholar
  12. Finley JCW, Maderdrut JL, Roger LJ, Petrusz (1981b) The immunocytochemical localization of somatostatin-containing neurons in the rat central nervous system. Neuroscience 6: 2173–2192Google Scholar
  13. Glazer EJ, Steinbusch H, Verhofstad A, Basbaum AI (1981) Serotonin neurons in nucleus raphe dorsalis and paragigantocellularis of the cat contain enkephalin. J Physiol (Paris) 77: 241–245Google Scholar
  14. Härfstrand A, Kalia M, Fuxe K, Kaijser L, Agnati L (1984) Somatostatin-induced apnea: interaction with hypoxia and hypercapnea in the rat. Neurosci Lett 50: 37–42Google Scholar
  15. Härfstrand A, Fuxe K, Kalia M, Agnati L (1985) Somatostatin induced apnoea: prevention by central and peripheral administration of the opiate receptor blocking agent naloxone. Acta Physiol Scand 125: 91–95Google Scholar
  16. Hassen AH, Feurstein G, Pfeiffer A, Faden AI (1982) s versus μ receptors: cardiovascular and respiratory effects of opiate agonists microinjected into nucleus tractur solitarius of cats. Regul Pept 4: 299–309Google Scholar
  17. 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: 6526–6530Google Scholar
  18. Hökfelt T, Elde R, Johansson O, Terenius L, Stein L (1977) The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system. Neurosci Lett 5: 25–31Google Scholar
  19. Hökfelt T, Terenius L, Kuypers HGJM, Dann O (1979) Evidence for enkephalin immunoreactive neurons in the medulla oblongata projecting to the spinal cord. Neurosci Lett 14: 55–60Google Scholar
  20. Hökfelt T, Johansson O, Ljungdahl Å, Lundberg JM, Schultzberg M (1980) Peptidergic neurons. Nature (London) 284: 515–521Google Scholar
  21. Hökfelt T, Holets VR, Staines W, Meister B, Melander T, Schalling M, Schultzberg M, Freedman J, Björklund H, Olson L, Lindh B, Elfvin L-G, Lundberg JM, Lindgren JÅ, Samuelsson B, Pernow B, Terenius L, Post C, Everitt B, Goldstein M (1986) Coexistence of neuronal messengers —an overview. In: Hökfelt T, Fuxe K, Pernow B (eds) Progress in brain research, Vol 68. Elsevier, Amsterdam, pp 33–70Google Scholar
  22. Holets V, Elde R (1982) The differential distribution and relationship of serotoninergic and peptidergic fibers to sympathoadrenal neurons in the intermediolateral cell column of the rat: a combined retrograde axonal transport and immunofluorescence study. Neuroscience 7: 1155–1174Google Scholar
  23. Hughes J, Smith TW, Kosterlitz HW, Fothergill LH, Morgan BA, Morris HR (1975) Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature (Lond) 258: 577–579Google Scholar
  24. Hunt SP, Lovick TA (1982) The distribution of serotonin, metenkephalin and β-lipotropin-like immunoreactivity in neuronal perikarya of the cat brain stem. Neurosci Lett 30: 139–145Google Scholar
  25. Jirikovski G, Reisert I, Pilgrim Ch, Oertel WH (1984) Coexistence of glutamate decarboxylase and somatostatin immunoreactivity in cultured hippocampal neurons of the rat. Neurosci Lett 46: 35–39Google Scholar
  26. Johansson O, Hökfelt T, Pernow B, Jeffcoate SL, White N, Steinbusch HWM, Verhofstad AAJ, Emson PC, Spindel E (1981) Immunohistochemical support for three putative transmitters in one neuron: coexistence of 5-hydroxytryptamine, substance P and thyrotropin releasing hormone-like immunoreactivity in medullary neurons projecting to the spinal cord. Neuroscience 6: 1857–1881Google Scholar
  27. Johansson O, Hökfelt T, Elde R (1984) Immunohistochemical distribution of somatostatin-like immunoreactivity in the central nervous system of the adult rat. Neuroscience 13: 265–339Google Scholar
  28. Johnson DG, De C Nogueira Araujo GM (1981) A simple method of reducing the facing of immunofluorescence during microscopy. J Immunol Meth 43: 349–350Google Scholar
  29. Kalia M, Fuxe K, Agnati LF, Hökfelt T, Härfstrand A (1984a) Somatostatin produces apnea and is localized in medullary respiratory nuclei: a possible role in apneic syndromes. Brain Res 296: 339–344Google Scholar
  30. Kalia M, Fuxe K, Hökfelt T, Johansson O, Lang R, Ganten D, Cuello C, Terenius L (1984b) Distribution of neuropeptide immunoreactive nerve terminals within the subnuclei of the nucleus of the tractus solitarius of the rat. J Comp Neurol 222: 409–444Google Scholar
  31. Laubie M, Schmitt H, Vincent M, Remond G (1977) Central cardiovascular effects of morphinomimetic peptides in dogs. Eur J Pharmacol 46: 67–71Google Scholar
  32. Maley B, Elde R (1982) Immunohistochemical localization of putative neurotransmitters within the feline nucleus tractus solitarii. Neuroscience 7: 2469–2490Google Scholar
  33. Martin R, Voigt KH (1981) Enkephalins co-exist with oxytocin and vasopressin in nerve terminals of rat neurohypophysis. Nature (London) 289: 502–504Google Scholar
  34. Maurer R, Gaehwiler BH, Buescher HH, Hill RC, Roemer D (1982) Opiate antagonistic properties of an octa-peptide somatostatin analog. Proc Natl Acad Sci USA 79: 4815–4817Google Scholar
  35. Merchenthaler I, Maderdrut JL, Dockray GJ (1986) Immunocytochemical localization of proenkephalin-derived peptides in the central nervous system of the rat. Neuroscience 17: 325–348Google Scholar
  36. Oertel WH, Graybiel AM, Mugnaini E, Elde RP, Schmechel DE, Kopin IJ (1983) Coexistence of glutamic acid decarboxylaselike immunoreactivity and somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami. J Neurosci 3: 1322–1332Google Scholar
  37. Osborne NN (ed) (1983) Dale's principle and communication between neurones. Pergamon Press, Oxford and New YorkGoogle Scholar
  38. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New YorkGoogle Scholar
  39. Petrusz P, Merchenthaler I, Maderdrut JL (1985) Distribution of enkephalin-containing neurons in the central nervous system. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, Vol 4. GABA and neuropeptides in the CNS, Part 1. Elsevier, Amsterdam, pp 273–334Google Scholar
  40. Platt JL, Michael AF (1983) Retardation of fading and enhancement of intensity of immunofluorescence by p-pheny-lenediamine. J Histochem Cytochem 31: 840–842Google Scholar
  41. Rezek M, Havlicek V, Leybin L, La Bella FS, Friesen H (1978) Opiate-like naloxone-reversible actions of somatostatin given intracerebrally. Can J Physiol Pharmacol 56: 227–231Google Scholar
  42. Sar M, Stumpf WE, Miller RJ, Chang K-J, Cuatrecasas P (1978) Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol 182: 17–38Google Scholar
  43. Schaz K, Stock G, Simon W, Schlor K-H, Unger T, Rockhold R, Ganten D (1980) Enkephalin effects on blood pressure, heart rate, and baroreceptor reflex. Hypertension 2: 395–407Google Scholar
  44. Schmechel DE, Vickrey BG, Fitzpatrick D, Elde RP (1984) GABAergic neurons of mammalian cerebral cortex: widespread subclass defined by somatostatin content. Neurosci Lett 47: 227–232Google Scholar
  45. 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
  46. Shiosaka S, Takatsuki K, Sakanaka M, Inagaki S, Takagi H, Senba Y, Kawai Y, Tohyama M (1981) Ontogeny of somatostatin-containing neurons system of the rat: immunohistochemical observations. I. Lower brain stem. J Comp Neurol 203: 173–188Google Scholar
  47. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu J-Y (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatinor cholecystokinin-immunoreactive material. Neuroscience 14: 2590–2603Google Scholar
  48. Sitsen JMA, Van Ree JM, De Jong W (1982) Cardiovascular and respiratory effects of β-endorphin in anesthetized and conscious rats. J Cardiovasc Pharmacol 4: 883–888Google Scholar
  49. Terenius L (1976) Somatostatin and ACTH are peptides with partial antagonist-like selectivity for opiate receptors. Eur J Pharmacol 38: 211–213Google Scholar
  50. Tramu G, Beauvillain JC, Croix Leonardelli J (1981) Comparative immunocytochemical localization of enkephalin and somatostatin in the median eminence, hypothalamus and adjacent areas of the guinea-pig brain. Brain Res 215: 235–255Google Scholar
  51. Uhl GR, Goodman RR, Kuhar MJ, Childers SR, Snyder SH (1979) Immunohistochemical mapping of enkephalin containing cell bodies, fibers and nerve terminals in the brain stem of the rat. Brain Res 166: 75–94Google Scholar
  52. Vincent SR, Johansson O, Hökfelt T, Meyerson B, Sachs C, Elde RP, Terenius L, Kimmel J (1982) Neuropeptide coexistence in human cortical neurones. Nature 298: 65–67Google Scholar
  53. Vincent SR, Johansson O, Hökfelt T, Skirboll L, Elde RP, Terenius L, Kimmel J, Goldstein M (1983) NADPH-diaphorase: a selective histochemical marker for striatal neurons containing both somatostatin- and avian pancreatic polypeptide (APP)-like immunoreactivities. J Comp Neurol 217: 252–263Google Scholar
  54. Vincent SR, McIntosh CHS, Buchanan AMJ, Brown JC (1985) Central somatostatin systems revealed with monoclonal antibodies. J Comp Neurol 238: 169–187Google Scholar
  55. Wamsley JK, III, Young WS, Kuhar MJ (1980) Immunohistochemical localization of enkephalin in rat forebrain. Brain Res 190: 153–174Google Scholar
  56. Yamazoe M, Shiosaka S, Shibasaki T, Ling N, Tateishi K, Hashimura E, Hamaoka T, Kimmel JR, Matsuo H, Tohyama M (1984) Distribution of six neuropeptides in the nucleus tractus solitarii of the rat: an immunohistochemical analysis. Neuroscience 13: 1243–1266Google Scholar
  57. Yukimura T, Stock G, Stumpf H, Unger T, Ganten D (1981) Effects of (D-Ala2)-methionine enkephalin on blood pressure, heart rate and baroreceptor sensitivity in conscious cats. Hypertension 3: 528–533Google Scholar
  58. Zamboni L, De Martino S (1967) Buffered acid formaldehyde: a new rapid fixative for electron microscopy. J Cell Biol 148A: 35Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • D. E. Millhorn
    • 1
  • T. Hökfelt
    • 1
  • L. Terenius
    • 2
  • A. Buchan
    • 3
  • J. C. Brown
    • 3
  1. 1.Department of HistologyKarolinska InstituteStockholmSweden
  2. 2.Department of PharmacologyUppsala UniversityUppsalaSweden
  3. 3.Medical Research Council of Canada, Regulatory Peptide GroupUniversity of British ColumbiaVancouverCanada

Personalised recommendations