Skip to main content
NCBI home page
Thorax logoLink to Thorax
. 1987 Jun;42(6):431–439. doi: 10.1136/thx.42.6.431

Regulatory peptides in the respiratory tract of Macaca fascicularis.

M A Ghatei 1, D R Springall 1, I M Richards 1, J A Oostveen 1, R L Griffin 1, A Cadieux 1, J M Polak 1, S R Bloom 1
PMCID: PMC460775  PMID: 2443994

Abstract

The quantitative distribution and localisation of seven regulatory peptides (vasoactive intestinal peptide (VIP), peptide histidine methionine (PHM), calcitonin gene related peptide (CGRP), galanin, substance P, neuropeptide tyrosine (Y), and bombesin like peptides) were determined by radioimmunoassay and immunocytochemistry in six different regions of the respiratory tract of the cynomolgus monkey, Macaca fascicularis. In general, peptide concentrations were higher in the airways than in lung tissue itself. VIP and PHM were found in greatest abundance and in equimolar concentrations. Concentrations of substance P, neuropeptide Y, and bombesin were substantially lower. Immunocytochemistry localised all the peptides to nerve fibres, whose density generally paralleled the tissue concentrations by radioimmunoassay except in the case of bombesin, which was not detected. VIP, PHM, and galanin were mostly associated with glands of trachea and bronchus and with blood vessels and smooth muscle; CGRP and substance P were found principally beneath airway epithelium and around smooth muscle fibres and blood vessels; neuropeptide Y was found around blood vessels and seromucous glands only. The pattern of peptide distribution in the Macaca fascicularis respiratory tract is similar to that previously reported in human postmortem material, suggesting that the cynomolgus monkey may be a useful model for examining the pathophysiological role of peptides in human respiratory disease.

Full text

PDF
431

Images in this article

435Image
on p.435
435Image
on p.435
436Image
on p.436
436Image
on p.436
437Image
on p.437
437Image
on p.437

Selected References

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

  1. Allen J. M., Yeats J. C., Adrian T. E., Bloom S. R. Radioimmunoassay of neuropeptide Y. Regul Pept. 1984 Jan;8(1):61–70. doi: 10.1016/0167-0115(84)90029-6. [DOI] [PubMed] [Google Scholar]
  2. Barnes P. J., Dixon C. M. The effect of inhaled vasoactive intestinal peptide on bronchial reactivity to histamine in humans. Am Rev Respir Dis. 1984 Aug;130(2):162–166. doi: 10.1164/arrd.1984.130.2.162. [DOI] [PubMed] [Google Scholar]
  3. Bauer F. E., Christofides N. D., Hacker G. W., Blank M. A., Polak J. M., Bloom S. R. Distribution of galanin immunoreactivity in the genitourinary tract of man and rat. Peptides. 1986 Jan-Feb;7(1):5–10. doi: 10.1016/0196-9781(86)90052-5. [DOI] [PubMed] [Google Scholar]
  4. Bell J. B., Gould R. P., Hyatt P. J., Tait J. F., Tait S. A. Properties of rat adrenal zona reticularis cells: preparation by gravitational sedimentation. J Endocrinol. 1978 Apr;77(1):25–41. doi: 10.1677/joe.0.0770025. [DOI] [PubMed] [Google Scholar]
  5. Cadieux A., Springall D. R., Mulderry P. K., Rodrigo J., Ghatei M. A., Terenghi G., Bloom S. R., Polak J. M. Occurrence, distribution and ontogeny of CGRP immunoreactivity in the rat lower respiratory tract: effect of capsaicin treatment and surgical denervations. Neuroscience. 1986 Oct;19(2):605–627. doi: 10.1016/0306-4522(86)90285-x. [DOI] [PubMed] [Google Scholar]
  6. Cheung A., Polak J. M., Bauer F. E., Cadieux A., Christofides N. D., Springall D. R., Bloom S. R. Distribution of galanin immunoreactivity in the respiratory tract of pig, guinea pig, rat, and dog. Thorax. 1985 Dec;40(12):889–896. doi: 10.1136/thx.40.12.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Christofides N. D., Polak J. M., Bloom S. R. Studies on the distribution of PHI in mammals. Peptides. 1984 Mar-Apr;5(2):261–266. doi: 10.1016/0196-9781(84)90216-x. [DOI] [PubMed] [Google Scholar]
  8. Christofides N. D., Yiangou Y., Piper P. J., Ghatei M. A., Sheppard M. N., Tatemoto K., Polak J. M., Bloom S. R. Distribution of peptide histidine isoleucine in the mammalian respiratory tract and some aspects of its pharmacology. Endocrinology. 1984 Nov;115(5):1958–1963. doi: 10.1210/endo-115-5-1958. [DOI] [PubMed] [Google Scholar]
  9. Church M. K., Warner J. O. Sodium cromoglycate and related drugs. Clin Allergy. 1985 Jul;15(4):311–320. doi: 10.1111/j.1365-2222.1985.tb02998.x. [DOI] [PubMed] [Google Scholar]
  10. Cuttitta F., Carney D. N., Mulshine J., Moody T. W., Fedorko J., Fischler A., Minna J. D. Bombesin-like peptides can function as autocrine growth factors in human small-cell lung cancer. 1985 Aug 29-Sep 4Nature. 316(6031):823–826. doi: 10.1038/316823a0. [DOI] [PubMed] [Google Scholar]
  11. Cutz E., Chan W., Track N. S. Bombesin, calcitonin and leu-enkephalin immunoreactivity in endocrine cells of human lung. Experientia. 1981 Jul 15;37(7):765–767. doi: 10.1007/BF01967969. [DOI] [PubMed] [Google Scholar]
  12. Ghatei M. A., Gu J., Mulderry P. K., Blank M. A., Allen J. M., Morrison J. F., Polak J. M., Bloom S. R. Calcitonin gene-related peptide (CGRP) in the female rat urogenital tract. Peptides. 1985 Sep-Oct;6(5):809–815. doi: 10.1016/0196-9781(85)90306-7. [DOI] [PubMed] [Google Scholar]
  13. Ghatei M. A., Sheppard M. N., Henzen-Logman S., Blank M. A., Polak J. M., Bloom S. R. Bombesin and vasoactive intestinal polypeptide in the developing lung: marked changes in acute respiratory distress syndrome. J Clin Endocrinol Metab. 1983 Dec;57(6):1226–1232. doi: 10.1210/jcem-57-6-1226. [DOI] [PubMed] [Google Scholar]
  14. Ghatei M. A., Sheppard M. N., O'Shaughnessy D. J., Adrian T. E., McGregor G. P., Polak J. M., Bloom S. R. Regulatory peptides in the mammalian respiratory tract. Endocrinology. 1982 Oct;111(4):1248–1254. doi: 10.1210/endo-111-4-1248. [DOI] [PubMed] [Google Scholar]
  15. Ghatei M. A., Stratton M. R., Allen J. M., Joplin G. F., Polak J. M., Bloom S. R. Co-secretion of calcitonin gene-related peptide, gastrin-releasing peptide and ACTH by a carcinoid tumour metastasizing to the cerebellum. Postgrad Med J. 1987 Feb;63(736):123–130. doi: 10.1136/pgmj.63.736.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gu J., Islam K. N., Polak J. M. Repeated application of first-layer antiserum improves immunofluorescence staining: a modification of the indirect immunofluorescence staining procedure. Histochem J. 1983 May;15(5):475–482. doi: 10.1007/BF01002701. [DOI] [PubMed] [Google Scholar]
  17. Itoh N., Obata K., Yanaihara N., Okamoto H. Human preprovasoactive intestinal polypeptide contains a novel PHI-27-like peptide, PHM-27. Nature. 1983 Aug 11;304(5926):547–549. doi: 10.1038/304547a0. [DOI] [PubMed] [Google Scholar]
  18. Johnson D. E., Lock J. E., Elde R. P., Thompson T. R. Pulmonary neuroendocrine cells in hyaline membrane disease and bronchopulmonary dysplasia. Pediatr Res. 1982 Jun;16(6):446–454. doi: 10.1203/00006450-198206000-00009. [DOI] [PubMed] [Google Scholar]
  19. Linnoila R. I., Nettesheim P., DiAugustine R. P. Lung endocrine-like cells in hamsters treated with diethylnitrosamine: alterations in vivo and in cell culture. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5170–5174. doi: 10.1073/pnas.78.8.5170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lundberg J. M., Hökfelt T., Martling C. R., Saria A., Cuello C. Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tissue Res. 1984;235(2):251–261. doi: 10.1007/BF00217848. [DOI] [PubMed] [Google Scholar]
  21. Lundberg J. M., Terenius L., Hökfelt T., Goldstein M. High levels of neuropeptide Y in peripheral noradrenergic neurons in various mammals including man. Neurosci Lett. 1983 Dec 2;42(2):167–172. doi: 10.1016/0304-3940(83)90401-9. [DOI] [PubMed] [Google Scholar]
  22. McGregor G. P., Bloom S. R. Radioimmunoassay of substance P and its stability in tissue. Life Sci. 1983 Feb 7;32(6):655–662. doi: 10.1016/0024-3205(83)90211-4. [DOI] [PubMed] [Google Scholar]
  23. Melander T., Hökfelt T., Rökaeus A., Fahrenkrug J., Tatemoto K., Mutt V. Distribution of galanin-like immunoreactivity in the gastro-intestinal tract of several mammalian species. Cell Tissue Res. 1985;239(2):253–270. doi: 10.1007/BF00218003. [DOI] [PubMed] [Google Scholar]
  24. Middendorf W. F., Russell J. A. Innervation of airway smooth muscle in the baboon: evidence for a nonadrenergic inhibitory system. J Appl Physiol Respir Environ Exerc Physiol. 1980 Jun;48(6):947–956. doi: 10.1152/jappl.1980.48.6.947. [DOI] [PubMed] [Google Scholar]
  25. Mitchell S. J., Bloom S. R. Measurement of fasting and postprandial plasma VIP in man. Gut. 1978 Nov;19(11):1043–1048. doi: 10.1136/gut.19.11.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mulderry P. K., Ghatei M. A., Rodrigo J., Allen J. M., Rosenfeld M. G., Polak J. M., Bloom S. R. Calcitonin gene-related peptide in cardiovascular tissues of the rat. Neuroscience. 1985 Mar;14(3):947–954. doi: 10.1016/0306-4522(85)90156-3. [DOI] [PubMed] [Google Scholar]
  27. Patterson R., Talbot C. H., Booth B. H. Immunoglobulin E-mediated respiratory responses of subhuman primates. Reproducibility and effect of certain pharmacologic agents. Am Rev Respir Dis. 1970 Sep;102(3):412–421. doi: 10.1164/arrd.1970.102.3.412. [DOI] [PubMed] [Google Scholar]
  28. Richardson J. B. Noradrenergic inhibitory innervation of the lung. Lung. 1981;159(6):315–322. doi: 10.1007/BF02713931. [DOI] [PubMed] [Google Scholar]
  29. Richardson J., Béland J. Nonadrenergic inhibitory nervous system in human airways. J Appl Physiol. 1976 Nov;41(5 Pt 1):764–771. doi: 10.1152/jappl.1976.41.5.764. [DOI] [PubMed] [Google Scholar]
  30. Rosenfeld M. G., Mermod J. J., Amara S. G., Swanson L. W., Sawchenko P. E., Rivier J., Vale W. W., Evans R. M. Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing. Nature. 1983 Jul 14;304(5922):129–135. doi: 10.1038/304129a0. [DOI] [PubMed] [Google Scholar]
  31. Rökaeus A., Melander T., Hökfelt T., Lundberg J. M., Tatemoto K., Carlquist M., Mutt V. A galanin-like peptide in the central nervous system and intestine of the rat. Neurosci Lett. 1984 Jun 15;47(2):161–166. doi: 10.1016/0304-3940(84)90423-3. [DOI] [PubMed] [Google Scholar]
  32. Sabate M. I., Stolarsky L. S., Polak J. M., Bloom S. R., Varndell I. M., Ghatei M. A., Evans R. M., Rosenfeld M. G. Regulation of neuroendocrine gene expression by alternative RNA processing. Colocalization of calcitonin and calcitonin gene-related peptide in thyroid C-cells. J Biol Chem. 1985 Mar 10;260(5):2589–2592. [PubMed] [Google Scholar]
  33. Sheppard M. N., Polak J. M., Allen J. M., Bloom S. R. Neuropeptide tyrosine (NPY): a newly discovered peptide is present in the mammalian respiratory tract. Thorax. 1984 May;39(5):326–330. doi: 10.1136/thx.39.5.326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Stahlman M. T., Kasselberg A. G., Orth D. N., Gray M. E. Ontogeny of neuroendocrine cells in human fetal lung. II. An immunohistochemical study. Lab Invest. 1985 Jan;52(1):52–60. [PubMed] [Google Scholar]
  35. Tatemoto K., Rökaeus A., Jörnvall H., McDonald T. J., Mutt V. Galanin - a novel biologically active peptide from porcine intestine. FEBS Lett. 1983 Nov 28;164(1):124–128. doi: 10.1016/0014-5793(83)80033-7. [DOI] [PubMed] [Google Scholar]
  36. Terenghi G., McGregor G. P., Bhuttacharji S., Wharton J., Bloom S. R., Polak J. M. Vagal origin of substance P-containing nerves in the guinea pig lung. Neurosci Lett. 1983 Apr 29;36(3):229–235. doi: 10.1016/0304-3940(83)90005-8. [DOI] [PubMed] [Google Scholar]
  37. Uddman R., Sundler F. Vasoactive intestinal polypeptide nerves in human upper respiratory tract. ORL J Otorhinolaryngol Relat Spec. 1979;41(4):221–226. doi: 10.1159/000275461. [DOI] [PubMed] [Google Scholar]
  38. Wharton J., Polak J. M., Bloom S. R., Ghatei M. A., Solcia E., Brown M. R., Pearse A. G. Bombesin-like immunoreactivity in the lung. Nature. 1978 Jun 29;273(5665):769–770. doi: 10.1038/273769a0. [DOI] [PubMed] [Google Scholar]
  39. Wharton J., Polak J. M., Bloom S. R., Will J. A., Brown M. R., Pearse A. G. Substance P-like immunoreactive nerves in mammalian lung. Invest Cell Pathol. 1979 Jan-Mar;2(1):3–10. [PubMed] [Google Scholar]

Articles from Thorax are provided here courtesy of BMJ Publishing Group

RESOURCES