Skip to main content
Log in

Distribution of neuropeptide Y-like immunoreactivity in the normoganglionic and aganglionic segments of human colon

  • Regular Papers
  • Published:
Acta Neuropathologica Aims and scope Submit manuscript

Summary

The localisation and distribution of neuropeptide Y (NPY)-like immunoreactivity were studied by use of immunohistochemical methods in gut tissues from 19 patients with Hirschsprung's disease, including 4 cases of long segment aganglionosis. In the normoganglionic segment, immunoreactive cell bodies and nonvaricose processes were seen within both myenteric and submucous plexuses. A scarce supply of varicose fibres was found in the lamina propria mucosae, muscularis mucosae and longitudinal muscle layer. NPY fibres were more frequently encountered in the circular muscle layer, although with a weakly immunostaining intensity. In addition, blood vessels in the submucosal connective tissue were surrounded by a typical plexus of varicose, NPY-positive fibres. Immunoreactive endocrine cells could be detected in the colonic epithelium. In the aganglionic segment, numerous nerve fasciculi comprising a small to moderate number of NPY fibres with varicosities were observed throughout the entire layer of the colonic wall. A few varicose, NPY-positive fibres were also contained in the relatively large, hypertrophic nerve fasciculi located in the intermuscular zone and submucosal connective tissue. NPY-immunoreactive fasciculi were more densely distributed in the distal aganglionic segment than in the proximal aganglionic one. On the other hand, the distribution of NPY-positive fibres in long segment aganglionosis was quite different from that in short segment type; in cases of long segment type, no immunoreactive nerve fibres were detected within the circular muscle layer of the proximal aganglionic segment near the oligoganglionic segment and only a few fibres were observed within the hypertrophic nerve bundle of the intermuscular zone. The present results suggest that NPY-like immunoreactive nerves in the human colon have a dual origin of intrinsic and extrinsic elements. The origin and nature of extrinsic NPY nerve fibres in the human colon are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bennet A, Garrett JR, Howard ER (1968) Adrenergic myenteric nerves in Hirschsprung's disease. Br Med J 1:487–489

    Google Scholar 

  2. Bishop AE, Polak JM, Lake BD, Bryant MG, Bloom SR (1981) Abnormalities of the colonic regulatory peptides in Hirschsprung's disease. Histopathology 5:679–688

    Google Scholar 

  3. Burkhardt-Holm P, Holmgren S (1989) A comparative study of neuropeptides in the intestine of two stomachless teleosts (Poecilia reticulata, Leuciscus idus melanotus) under conditions of feeding and starvation. Cell Tissue Res 255:245–254

    Google Scholar 

  4. Clarke JG, Davies GJ, Kerwin R, Hackett D, Larkin S, Dawbarn D, Lee Y, Bloom SR, Yacoub M, Maseri A (1987) Coronary artery infusion of neuropeptide Y in patients with angina pectoris. Lancet 1:1057–1059

    Google Scholar 

  5. Ehrenpreis TH, Norberg KA, Wirsén C (1968) Sympathetic innervation of the colon in Hirschsprung;s disease: a histochemical study. J Pediat Surg 3:43–49

    Google Scholar 

  6. Ekblad E, Edvinsson L, Wahlestedt C, Uddman R, Håkanson R, Sundler F (1984) Neuropeptide Y co-exists and co-operates with noradrenaline in perivascular nerve fibres. Regul Pept 8:225–235

    Google Scholar 

  7. Ekblad E, Wahlestedt C, Ekelund M, Håkanson R, Sundler F (1984) Neuropeptide Y in the gut and pancreas: distribution and possible vasomotor function. Front Horm Res 12:85–90

    Google Scholar 

  8. El-Salhy M, Grimelius L, Wilander E, Ryberg B, Terenius L, Lundberg JM, Tatemoto K (1983) Immunocytochemical identification of polypeptide YY (PYY) cells in the human gastrointestinal tract. Histochemistry 77:15–23

    Google Scholar 

  9. Furness JB, Costa M, Emcon PC, Håkanson R, Moghimzadeh E, Sundler F, Taylor IL, Chance RE (1983) Distribution, pathways and reactions to drug treatment of nerves with neuropeptide Y- and pancreatic polypeptide-like immunoreactivity in the guinea-pig digestive tract. Cell Tissue Res 234:71–92

    Google Scholar 

  10. Gabella G (1979) Innervation of the gastrointestinal tract. Int Rev Cytol 59:129–193

    Google Scholar 

  11. Gannon BT, Noblet HR, Burnstock G (1969) Adrenergic innervation of bowel in Hirschsprung's disease. Br Med J 3:338–340

    Google Scholar 

  12. Garrett JR, Howard ER, Nixon HH (1969) Autonomic nerves in rectum and colon in Hirschsprung's disease. Arch Dis Child 44:406–417

    Google Scholar 

  13. Hamada Y, Bishop AE, Federici G, Rivosecchi M, Talbot IC, Polak JM (1987) Increased neuropeptide Y-immunoreactive innervation of aganglionic bowel in Hirschsprung's disease. Virchows Arch [A] 411:369–377

    Google Scholar 

  14. Hirose R, Nada O, Kawana T, Ikeda K, Goto S, Taguchi T, Toyohara T (1989) An immunohistochemical study of somatostatin-containing nerves in the aganglionic colon of human and rat. Acta Neuropathol 78:372–379

    Google Scholar 

  15. Howard ER (1973) Histochemistry in the diagnosis and investigation of congenital aganglionosis (Hirschsprung's disease). Am Surg 39:602–607

    Google Scholar 

  16. Ikeda K (1967) New techniques in the surgical treatment of Hirschsprung's disease. Surgery 61:503–508

    Google Scholar 

  17. Kawana T, Nada O, Ikeda K (1988) An immunohistochemical study of glial fibrillary acidic (GFA) protein and S-100 protein in the colon affected by Hirschsprung's disease. Acta Neuropathol 76:159–165

    Google Scholar 

  18. Kawana T, Nada O, Ikeda K, Goto S, Hirose R, Taguchi T, Kubota M, Toyahara T, Shono T (1989) Distribution and localization of glial fibrillary acidic (GFA) protein in colons affected by Hirschsprung's disease. J Pediatr Surg 24:448–452

    Google Scholar 

  19. Larsson LT, Malmfors G, Sundler F (1988) Neuropeptide Y, calcitonin gene-related peptide, and galanin in Hirschsprung's disease: an immunohistochemical study. J Pediatr Surg 23:342–345

    Google Scholar 

  20. Lolova I, Davidoff M, Itzev D, Apostolov A, Ivanchev Iv (1986) Distribution of substance P-, methionine-enkephalin-, somatostatin- and serotonin-immunoreactive nerve elements of the large bowel in Hirschsprung's disease. Zentralbl Allg Pathol Anat 131:25–32

    Google Scholar 

  21. Lundberg JM, Terenius L, Hökfelt T, Goldstein M (1983) High levels of neuropeptide Y in peripheral noradrenergic neurons in various mammals including man. Neurosci Lett 42:167–172

    Google Scholar 

  22. Meier-Ruge W (1974) Hirschsprung's disease: its aetiology, pathogenesis and differential diagnosis. Curr Top Pathol 59:131–179

    Google Scholar 

  23. Nakagawa Y, Perentes E (1988) Are intestinal endocrine cells affected in Hirschsprung's disease? An immunohistochemical study with anti-Leu-7 monoclonal antibody. J Pediatr Surg 23:957–961

    Google Scholar 

  24. Pernow J, Svenberg T, Lundberg JM (1987) Actions of calcium antagonists on pre- and postjunctional effects of neuropeptide Y on human peripheral blood vessles in vitro. Eur J Pharmacol 136:207–218

    Google Scholar 

  25. Sundler F, Moghimzadeh E, Håkanson R, Ekelund M, Emson P (1983) Nerve fibers in the gut and pancreas of the rat displaying neuropeptide-Y immunoreactivity. Cell Tissue Res 230:487–493

    Google Scholar 

  26. Sundler F, Håkanson R, Ekblad E, Uddman R, Wahlestedt C (1986) Neuropeptide Y in the peripheral adrenergic and enteric nervous systems. Int Rev Cytol 102:243–269

    Google Scholar 

  27. Taguchi T, Tanaka K, Ikeda K, Matsubayashi S, Yanaihara N (1983) Peptidergic innervation irreglarities in Hirschsprung's disease. Virchows Arch [A] 401:223–235

    Google Scholar 

  28. Tatemoto K (1982) Neuropeptide Y: complete amino acid sequence of the brain peptide. Proc Natl Acad Sci USA 79:5485–5489

    Google Scholar 

  29. Tatemoto K, Carlquist M, Mutt V (1982) Neuropeptide Y: a novel brain peptide with structural similarities to peptide YY and pancreatic polypeptide. Nature 296:659–660

    Google Scholar 

  30. Toyohara T, Nada O, Nagasaki A, Goto S, Ikeda K (1985) An immunohistochemical study of serotoninergic nerves in the colon and rectum of children with Hirschsprung's disease. Acta Neuropathol (Berl) 68:306–310

    Google Scholar 

  31. Toyohara T, Nada O, Ikeda K (1986) Influence of ischemia on noradrenergic nerves in the terminal colon of humans and rats. Fur Surg Res 18:349–355

    Google Scholar 

  32. Uddman R, Ekblad E, Edvinsson L, Håkanson R, Sundler F (1985) Neuropeptide Y-like immunoreactivity in perivascular nerve fibres of the guinea-pig. Regul Pept 10:243–257

    Google Scholar 

  33. Vaillant C, Bu'Lock A, Dimaline R, Dockray GJ (1982) Distribution and development of peptidergic nerves and gut endocrine cells in mice with congenital aganglionic colon, and their normal littermates. Gastroenterology 82:291–300

    Google Scholar 

  34. Wang YN, McDonald JK, Wyatt RJ (1987) Immunocytochemical localization of neuropeptide Y-like immunoreactivity in adrenergic and non-adrenergic neurons of the rat gastrointestinal tract. Peptides 8:145–151

    Google Scholar 

  35. Wiley J, Owyang C (1987) Neuropeptide Y inhibits cholinergic transmission in the isolated guinea pig colon: mediation through α-adrenergic receptors. Proc Natl Acad Sci USA 84:2047–2051

    Google Scholar 

  36. Woźniak W, Skowrońska U (1967) Comparative anatomy of the pelvic plexus in cat, dog, rabbit, macaque and man. Anat Anz 120:457–473

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kawana, T., Nada, O., Hirose, R. et al. Distribution of neuropeptide Y-like immunoreactivity in the normoganglionic and aganglionic segments of human colon. Acta Neuropathol 80, 469–474 (1990). https://doi.org/10.1007/BF00294605

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00294605

Key words

Navigation