Skip to main content
PMC home page
Journal of Anatomy logoLink to Journal of Anatomy
. 2000 Feb;196(Pt 2):233–241. doi: 10.1046/j.1469-7580.2000.19620233.x

Peptidergic hormones and neuropeptides, and aminergic neurotransmitters of the pancreatic islets of the Houbara bustard (Chlamydotis undulata)

E P K MENSAH-BROWN 1 ,✉, T A BAILEY 2 , D J PALLOT 1 , A GARNER 3
PMCID: PMC1468056  PMID: 10739019

Abstract

Immunoreactivity to insulin (Ins), somatostatin (Som), glucagon (Glu) and pancreatic polypeptide (PP) was found in 70%, 22%, 15% and 11% respectively of Houbara pancreatic endocrine islet cells. Whilst Ins occurred centrally and SOM was observed both in peripherally and centrally located islets, the other hormones were localised in peripheral islet cells; Som was also observed in neuronal cell bodies and nerve fibres. In addition, the islet cells contained substance P (SP) (65%) in the centre and vasoactive intestinal polypeptide (VIP) (2%) at the periphery. Immunoreactivity to choline acetyltransferase (ChAT), VIP and galanin (Gal) occurred in the walls of blood vessels located mainly at the periphery of islets. Occasionally, VIP and Gal immunoreactive varicose nerve terminals and ChAT immunoreactive cell bodies were also observed in the centre of islets. SP neuronal cell bodies were not observed but prominent SP immunoreactive varicose terminals were discernible in capillary walls within the islets. Neuropeptide Y (NPY) immunoreactive neurons were detected in neuronal cell bodies located mainly peripherally. Neuronal nitric oxide synthase (nNOS) immunoreactivity occurred in neuronal cell bodies and nerve fibres mainly at the periphery and also in centrally located islet endocrine cells. Immunoreactivity to tyrosine hydroxylase (TH) was similar in distribution to that of ChAT. In comparison with other avian species, the islets of the dorsal pancreatic lobe of the bustard contain all the peptidergic hormones normally present in the islets of other avian species, but are not segregated into dark A and light B cells. Many of the insulin containing cells also contained SP. The islets also contained several neuropeptides which are probably involved in their regulation.

Keywords: Innervation, varicosities, pancreatic islets, endocrine cells

Full Text

The Full Text of this article is available as a PDF (777.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alumets J., Håkanson R., Sundler F. Distribution, ontogeny and ultrastructure of pancreatic polypeptide (PP) cells in the pancreas and gut of the chicken. Cell Tissue Res. 1978 Dec 12;194(3):377–386. doi: 10.1007/BF00236159. [DOI] [PubMed] [Google Scholar]
  2. Bailey T. A., Mensah-Brown E. P., Samour J. H., Naldo J., Lawrence P., Garner A. Comparative morphology of the alimentary tract and its glandular derivatives of captive bustards. J Anat. 1997 Oct;191(Pt 3):387–398. doi: 10.1046/j.1469-7580.1997.19130387.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bishop A. E., Polak J. M., Green I. C., Bryant M. G., Bloom S. R. The location of VIP in the pancreas of man and rat. Diabetologia. 1980 Jan;18(1):73–78. doi: 10.1007/BF01228307. [DOI] [PubMed] [Google Scholar]
  4. Brunicardi F. C., Shavelle D. M., Andersen D. K. Neural regulation of the endocrine pancreas. Int J Pancreatol. 1995 Dec;18(3):177–195. doi: 10.1007/BF02784941. [DOI] [PubMed] [Google Scholar]
  5. De Giorgio R., Parodi J. E., Brecha N. C., Brunicardi F. C., Becker J. M., Go V. L., Sternini C. Nitric oxide producing neurons in the monkey and human digestive system. J Comp Neurol. 1994 Apr 22;342(4):619–627. doi: 10.1002/cne.903420409. [DOI] [PubMed] [Google Scholar]
  6. De Giorgio R., Sternini C., Brecha N. C., Widdison A. L., Karanjia N. D., Reber H. A., Go V. L. Patterns of innervation of vasoactive intestinal polypeptide, neuropeptide Y, and gastrin-releasing peptide immunoreactive nerves in the feline pancreas. Pancreas. 1992;7(3):376–384. doi: 10.1097/00006676-199205000-00016. [DOI] [PubMed] [Google Scholar]
  7. Dunning B. E., Taborsky G. J., Jr Galanin--sympathetic neurotransmitter in endocrine pancreas? Diabetes. 1988 Sep;37(9):1157–1162. doi: 10.2337/diab.37.9.1157. [DOI] [PubMed] [Google Scholar]
  8. Dunning B. E., Taborsky G. J., Jr Neural control of islet function by norepinephrine and sympathetic neuropeptides. Adv Exp Med Biol. 1991;291:107–127. doi: 10.1007/978-1-4684-5931-9_10. [DOI] [PubMed] [Google Scholar]
  9. Edwin N., Leigh C. M. The endocrine pancreas in the Australian wedge-tailed eagle (Aquila audax)--an immunocytochemical study. Eur J Histochem. 1993;37(3):219–224. [PubMed] [Google Scholar]
  10. Ekblad E., Alm P., Sundler F. Distribution, origin and projections of nitric oxide synthase-containing neurons in gut and pancreas. Neuroscience. 1994 Nov;63(1):233–248. doi: 10.1016/0306-4522(94)90019-1. [DOI] [PubMed] [Google Scholar]
  11. Hazelwood R. L. Pancreatic hormones, insulin/glucagon molar ratios, and somatostatin as determinants of avian carbohydrate metabolism. J Exp Zool. 1984 Dec;232(3):647–652. doi: 10.1002/jez.1402320333. [DOI] [PubMed] [Google Scholar]
  12. Hiramatsu K., Ohshima K. Immunohistochemical study on the distribution of galanin-containing nerves in the chicken pancreas. Histol Histopathol. 1995 Apr;10(2):283–288. [PubMed] [Google Scholar]
  13. Hiramatsu K., Oshima K. Immunocytochemical study on the innervation of the chicken pancreas by vasoactive intestinal polypeptide (VIP)-containing nerves. Histol Histopathol. 1997 Oct;12(4):961–965. [PubMed] [Google Scholar]
  14. Holst J. J., Fahrenkrug J., Knuhtsen S., Jensen S. L., Poulsen S. S., Nielsen O. V. Vasoactive intestinal polypeptide (VIP) in the pig pancreas: role of VIPergic nerves in control of fluid and bicarbonate secretion. Regul Pept. 1984 Apr;8(3):245–259. doi: 10.1016/0167-0115(84)90066-1. [DOI] [PubMed] [Google Scholar]
  15. Jansson L., Sandler S. The nitric oxide synthase II inhibitor NG-nitro-L-arginine stimulates pancreatic islet insulin release in vitro, but not in the perfused pancreas. Endocrinology. 1991 Jun;128(6):3081–3085. doi: 10.1210/endo-128-6-3081. [DOI] [PubMed] [Google Scholar]
  16. Jensen S. L., Fahrenkrug J., Holst J. J., Nielsen O. V., Schaffalitzky de Muckadell O. B. Secretory effects of VIP on isolated perfused porcine pancreas. Am J Physiol. 1978 Oct;235(4):E387–E391. doi: 10.1152/ajpendo.1978.235.4.E387. [DOI] [PubMed] [Google Scholar]
  17. Larsson L. I., Fahrenkrug J., Holst J. J., Schaffalitzky de Muckadell O. B. Innervation of the pancreas by vasoactive intestinal polypeptide (VIP) immunoreactive nerves. Life Sci. 1978 Mar;22(9):773–780. doi: 10.1016/0024-3205(78)90246-1. [DOI] [PubMed] [Google Scholar]
  18. Lindskog S., Ahrén B., Dunning B. E., Sundler F. Galanin-immunoreactive nerves in the mouse and rat pancreas. Cell Tissue Res. 1991 May;264(2):363–368. doi: 10.1007/BF00313975. [DOI] [PubMed] [Google Scholar]
  19. Liu H. P., Leong S. K., Tay S. S. Localization of NADPH-diaphorase positive neurons in the pancreas of the mouse, rat, chick, kitten and monkey. J Hirnforsch. 1994;35(4):501–510. [PubMed] [Google Scholar]
  20. Lucini C., Castaldo L., Lai O. An immunohistochemical study of the endocrine pancreas of ducks. Eur J Histochem. 1996;40(1):45–52. [PubMed] [Google Scholar]
  21. McDonald T. J., Brooks B. D., Rokaeus A., Tinner B., Staines W. A. Pancreatic galanin: molecular forms and anatomical locations. Pancreas. 1992;7(6):624–635. [PubMed] [Google Scholar]
  22. Messell T., Harling H., Böttcher G., Johnsen A. H., Holst J. J. Galanin in the porcine pancreas. Regul Pept. 1990 Apr 24;28(2):161–176. doi: 10.1016/0167-0115(90)90015-o. [DOI] [PubMed] [Google Scholar]
  23. Oomori Y., Iuchi H., Ishikawa K., Satoh Y., Ono K. Immunocytochemical study of tyrosine hydroxylase and dopamine beta-hydroxylase immunoreactivities in the rat pancreas. Histochemistry. 1994 Jun;101(5):313–323. doi: 10.1007/BF00268992. [DOI] [PubMed] [Google Scholar]
  24. Satoh S., Furuse M., Choi Y. H., Okumura J. Cholecystokinin is not a major regulator in the digestive system in the chicken. Experientia. 1994 Sep 15;50(9):812–814. doi: 10.1007/BF01956461. [DOI] [PubMed] [Google Scholar]
  25. Schmidt H. H., Warner T. D., Ishii K., Sheng H., Murad F. Insulin secretion from pancreatic B cells caused by L-arginine-derived nitrogen oxides. Science. 1992 Feb 7;255(5045):721–723. doi: 10.1126/science.1371193. [DOI] [PubMed] [Google Scholar]
  26. Stagner J. I., Samols E. Modulation of insulin secretion by pancreatic ganglionic nicotinic receptors. Diabetes. 1986 Aug;35(8):849–854. doi: 10.2337/diab.35.8.849. [DOI] [PubMed] [Google Scholar]
  27. Su H. C., Bishop A. E., Power R. F., Hamada Y., Polak J. M. Dual intrinsic and extrinsic origins of CGRP- and NPY-immunoreactive nerves of rat gut and pancreas. J Neurosci. 1987 Sep;7(9):2674–2687. doi: 10.1523/JNEUROSCI.07-09-02674.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sundler F., Alumets J., Håkanson R., Fahrenkrug J., Schaffalitzky de Muckadell O. Peptidergic (VIP) nerves in the pancreas. Histochemistry. 1978 Mar 2;55(2):173–176. doi: 10.1007/BF00493519. [DOI] [PubMed] [Google Scholar]
  29. Tomita T., Doull V., Pollock H. G., Kimmell J. R. Regional distribution of pancreatic polypeptide and other hormones in chicken pancreas: reciprocal relationship between pancreatic polypeptide and glucagon. Gen Comp Endocrinol. 1985 May;58(2):303–310. doi: 10.1016/0016-6480(85)90346-6. [DOI] [PubMed] [Google Scholar]
  30. Vaillant C., Dimaline R., Dockray G. J. The distribution and cellular origin of vasoactive intestinal polypeptide in the avian gastrointestinal tract and pancreas. Cell Tissue Res. 1980;211(3):511–523. doi: 10.1007/BF00234405. [DOI] [PubMed] [Google Scholar]
  31. Van der Zee E. A., Buwalda B., Strubbe J. H., Strosberg A. D., Luiten P. G. Immunocytochemical localization of muscarinic acetylcholine receptors in the rat endocrine pancreas. Cell Tissue Res. 1992 Jul;269(1):99–106. doi: 10.1007/BF00384730. [DOI] [PubMed] [Google Scholar]
  32. Verchere C. B., Kowalyk S., Koerker D. J., Baskin D. G., Taborsky G. J., Jr Evidence that galanin is a parasympathetic, rather than a sympathetic, neurotransmitter in the baboon pancreas. Regul Pept. 1996 Dec 3;67(2):93–101. doi: 10.1016/s0167-0115(96)00120-6. [DOI] [PubMed] [Google Scholar]
  33. Weir G. C., Goltsos P. C., Steinberg E. P., Patel Y. C. High concentration of somatostatin immunoreactivity in chicken pancreas. Diabetologia. 1976 May;12(2):129–132. doi: 10.1007/BF00428977. [DOI] [PubMed] [Google Scholar]
  34. el-Salhy M., Grimelius L., Emson P. C., Falkmer S. Polypeptide YY- and neuropeptide Y-immunoreactive cells and nerves in the endocrine and exocrine pancreas of some vertebrates: an onto- and phylogenetic study. Histochem J. 1987 Feb;19(2):111–117. doi: 10.1007/BF01682755. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES