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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1977 Jul;74(7):3086–3089. doi: 10.1073/pnas.74.7.3086

Serotonergic neurons in the peripheral nervous system: identification in gut by immunohistochemical localization of tryptophan hydroxylase.

M D Gershon, C F Dreyfus, V M Pickel, T H Joh, D J Reis
PMCID: PMC431418  PMID: 331327

Abstract

A specific antibody to tryptophan hydroxylase [L-tryptophan, tetrahydropteridine:oxygen oxidoreductase (5-hydroxylating), EC 1.14.16.4] has been used to localize the enzyme immunohistochemically in neurons of the mammalian gut. The enzyme was found in perikarya of intestinal neurons of mice, rats, and guinea pigs. Neurons containing the enzyme survived for up to 3 weeks in organotypic tissue culture and were intrinsic to the gut. These neurons are probably serotonergic and are the first such neurons to be found in the peripheral nervous system.

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Selected References

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  1. Ahlman H., Enerbäck L. A cytofluorometric study of the myenteric plexus in the guinea pig. Cell Tissue Res. 1974;153(4):419–434. doi: 10.1007/BF00231538. [DOI] [PubMed] [Google Scholar]
  2. BENSLEY S. H. Pinacyanol erthrosinate as a stain for mast cells. Stain Technol. 1952 Sep;27(5):269–273. doi: 10.3109/10520295209105090. [DOI] [PubMed] [Google Scholar]
  3. Baumgarten H. G., Björklund A., Lachenmayer L., Nobin A., Rosengren E. Evidence for the existence of serotonin-, dopamine-, and noradrenaline-containing neurons in the gut of Lampetra fluviatilis. Z Zellforsch Mikrosk Anat. 1973 Jul 26;141(1):33–54. doi: 10.1007/BF00307395. [DOI] [PubMed] [Google Scholar]
  4. Bianchi C., Beani L., Crema C. Effects of metoclopramide on isolated guinea-pig colon. 2. Interference with ganglionic stimulant drugs. Eur J Pharmacol. 1970;12(3):332–341. doi: 10.1016/0014-2999(70)90085-3. [DOI] [PubMed] [Google Scholar]
  5. Bülbring E., Gershon M. D. 5-hydroxytryptamine participation in the vagal inhibitory innervation of the stomach. J Physiol. 1967 Oct;192(3):823–846. doi: 10.1113/jphysiol.1967.sp008334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cook R. D., Peterson E. R. The growth of smooth muscle and sympathetic ganglia in organotypic tissue cultures. Light and electron microscopy. J Neurol Sci. 1974 May;22(1):25–38. doi: 10.1016/0022-510x(74)90051-3. [DOI] [PubMed] [Google Scholar]
  7. Dreyfus C. F., Bornstein M. B. Synthesis of serotonin by neurons of the myenteric plexus in situ and in organotypic tissue culture. Brain Res. 1977 Jun 3;128(1):125–139. doi: 10.1016/0006-8993(77)90240-2. [DOI] [PubMed] [Google Scholar]
  8. Dreyfus C. F., Sherman D. L., Gershon M. D. Uptake of serotonin by intrinsic neurons of the myenteric plexus grown in organotypic tissue culture. Brain Res. 1977 Jun 3;128(1):109–123. doi: 10.1016/0006-8993(77)90239-6. [DOI] [PubMed] [Google Scholar]
  9. Dubois A., Jacobowitz D. M. Failure to demonstrate serotonergic neurons in the myenteric plexus of the rat. Cell Tissue Res. 1974;150(4):493–496. doi: 10.1007/BF00225972. [DOI] [PubMed] [Google Scholar]
  10. Furness J. B., Costa M. The nervous release and the action of substances which affect intestinal muscle through neither adrenoreceptors nor cholinoreceptors. Philos Trans R Soc Lond B Biol Sci. 1973 Mar 15;265(867):123–133. doi: 10.1098/rstb.1973.0015. [DOI] [PubMed] [Google Scholar]
  11. Fuxe K., Jonsson G. A modification of the histochemical fluorescence method for the improved localization of 5-hydroxytryptamine. Histochemie. 1967;11(2):161–166. doi: 10.1007/BF00571721. [DOI] [PubMed] [Google Scholar]
  12. Gershon M. D., Altman R. F. An analysis of the uptake of 5-hydroxytryptamine by the myenteric plexus of the small intestine of the guinea pig. J Pharmacol Exp Ther. 1971 Oct;179(1):29–41. [PubMed] [Google Scholar]
  13. Gershon M. D., Robinson R. G., Ross L. L. Serotonin accumulation in the guinea-pig myenteric plexus: ion dependence, structure-activity relationship and the effect of drugs. J Pharmacol Exp Ther. 1976 Sep;198(3):548–561. [PubMed] [Google Scholar]
  14. Joh T. H., Shikimi T., Pickel V. M., Reis D. J. Brain tryptophan hydroxylase: purification of, production of antibodies to, and cellular and ultrastructural localization in serotonergic neurons of rat midbrain. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3575–3579. doi: 10.1073/pnas.72.9.3575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jonakait G. M., Tamir H., Rapport M. M., Gershon M. D. Detection of a soluble serotonin-binding protein in the mammalian myenteric plexus and other peripheral sites of serotonin storage. J Neurochem. 1977 Feb;28(2):277–284. doi: 10.1111/j.1471-4159.1977.tb07745.x. [DOI] [PubMed] [Google Scholar]
  16. Kottegoda S. R. An analysis of possible nervous mechanisms involved in the peristaltic reflex. J Physiol. 1969 Feb;200(3):687–712. doi: 10.1113/jphysiol.1969.sp008717. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuhar M. J., Aghajanian G. K., Roth R. H. Tryptophan hydroxylase activity and synaptosomal uptake of serotonin in discrete brain regions after midbrain raphe lesions: correlations with serotonin levels and histochemical fluorescence. Brain Res. 1972 Sep 15;44(1):165–176. doi: 10.1016/0006-8993(72)90372-1. [DOI] [PubMed] [Google Scholar]
  18. Kuhar M. J., Roth R. H., Aghajanian G. K. Selective reduction of tryptophan hydroxylase activity in rat forebrain after midbrain raphe lesions. Brain Res. 1971 Dec 10;35(1):167–176. doi: 10.1016/0006-8993(71)90602-0. [DOI] [PubMed] [Google Scholar]
  19. Kuhar M. J., Roth R. H., Aghajanian G. K. Synaptosomes from forebrains of rats with midbrain raphe lesions: selective reduction of serotonin uptake. J Pharmacol Exp Ther. 1972 Apr;181(1):36–45. [PubMed] [Google Scholar]
  20. Pickel V. M., Joh T. H., Reis D. J. Immunohistochemical localization of tyrosine hydroxylase in brain by light and electron microscopy. Brain Res. 1975 Feb 28;85(2):295–300. doi: 10.1016/0006-8993(75)90084-0. [DOI] [PubMed] [Google Scholar]
  21. Robinson R. G., Gershon M. D. Synthesis and uptake of 5-hydroxytryptamine by the myenteric plexus of the guinea-pig ileum. A histochemical study. J Pharmacol Exp Ther. 1971 Aug;178(2):311–324. [PubMed] [Google Scholar]
  22. Rothman T. P., Ross L. L., Gershon M. D. Separately developing axonal uptake of 5-hydroxytryptamine and norepinephrine in the fetal ileum of the rabbit. Brain Res. 1976 Oct 22;115(3):437–456. doi: 10.1016/0006-8993(76)90360-7. [DOI] [PubMed] [Google Scholar]
  23. Sternberger L. A., Hardy P. H., Jr, Cuculis J. J., Meyer H. G. The unlabeled antibody enzyme method of immunohistochemistry: preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem. 1970 May;18(5):315–333. doi: 10.1177/18.5.315. [DOI] [PubMed] [Google Scholar]
  24. Tamir H., Huang Y. L. Binding of serotonin to soluble protein from synaptosomes. Life Sci. 1974 Jan 1;14(1):83–93. doi: 10.1016/0024-3205(74)90248-3. [DOI] [PubMed] [Google Scholar]

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