Skip to main content

Neurogenic Inflammation

  • Chapter
Inflammatory Mediators

Abstract

Sensory C-fibres are assumed to have a dual function in response to injury. Besides their central activity, they appear to contribute to inflammatory reactions in the periphery (1–3). Antidromic electrical stimulation as well as stimulation by chemical irritants or noxious heat lead to vasodilatation and plasma protein extravasation (4–6). These responses, which are also called “neurogenic inflammation” (see 7,8) are assumed to be caused by a mediator released from peripheral endings of C-fibres. Many of the criteria for being the mediator of these effects are fulfilled by substance P (SP) (9). However, two SP-related peptides have recently been isolated from mammalian spinal cord, i.e. neurokinin A (NKA) (10–12) and neurokinin B (NKB) (10,13). A common precursor gene for SP and NKA has been identified in the CNS (11), the mRNA of which is also present in sensory neurones (14). Thus, it can be assumed that SP coexists with NKA. Additionally, SP seems to coexist with calcitonin gene-related peptide (CGRP) in cells of spinal ganglia (15) and a release of CGRP from sensory neurones in culture has been demonstrated (16).

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 69.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Dale, D.M. (1935). Pharmacology and nerve endings. Proc. R. Soc. Med., 28, 319–332.

    Google Scholar 

  2. Chapman, L.F. and Goodell, H. (1964). The participation of the nervous system in the inflammatory reaction. Ann. N.Y. Acad. Sci., 116, 990–1017.

    Google Scholar 

  3. Jancso, N., Jancso-Gabor, A. and Szolcsanyi, J. (1968). The role of sensory nerve endings in neurogenic inflammation induced in human skin and in the eye and paw of the rat. Br. J. Pharmacol., 32, 32–41.

    Google Scholar 

  4. Bayliss, W.M. (1901). On the origin from the spinal cord of the vasodilator fibres of the hind limb, and on the nature of these fibres. J. Physiol., 26, 173–209.

    Article  Google Scholar 

  5. Jancso, N., Jancso-Gabor, A. and Szolcsanyi, J. (1967). Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol., 31, 138–151.

    Google Scholar 

  6. Lembeck, F. and Holzer, P. (1979). Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn-Schmiedeberg’s Arch. Pharmacol., 310, 175–183.

    Google Scholar 

  7. Lembeck, F. (1983). Mediators of vasodilatation in the skin. Br. J. Dermatol., 109, Suppl. 25, 1–9.

    Google Scholar 

  8. Foreman, J.C. and Jordan, C.C. (1984). Neurogenic inflammation. Trends Pharmacol. Sci., 5, 116–119.

    Google Scholar 

  9. Pernow, B. (1983). Substance P. Pharmacol. Rev., 35, 85–141.

    Google Scholar 

  10. Kimura, S., Okada, M., Sugita, Y., Kanzawa, I. and Munekata, E. (1983). Novel neuropeptides, neurokinin a and 3, isolated from porcine spinal cord. Proc. Jap. Acad. Ser B. 59, 101–104.

    Google Scholar 

  11. Nawa, H., Hirose, T., Takashima, H., Inayama, S. and Nakanishi, S. (1983). Nucleotide sequence of cloned cDNAs for two types of bovine brain substance P precursor. Nature, 306, 32–36.

    Article  Google Scholar 

  12. Minamino, N., Kangawa, K., Fukuda, A. and Matsuo, H. (1984). Neuromedin L: a novel mammalian tachykinin identified in porcine spinal cord. Neuropeptides, 4, 157–166.

    Article  Google Scholar 

  13. Kangawa, K., Minamino, N., Fukuda, A. and Matsuo, H. (1983). Neuromedin K: a novel mammalian tachykinin identified in porcine spinal cord. Biochem. Biophys. Res. Commun., 114, 533–540.

    Google Scholar 

  14. Nawa, H., Kotani, H. and Nakanishi, S. (1984). Tissue-specific generation of two preprotachykinin mRNAs from one gene by alternative RNA splicing. Nature, 312, 729–734.

    Article  Google Scholar 

  15. Wiesenfeld-Hallin, Z., Hokfelt, T., Lundberg, J., Forssman, W.G., Reinecke, M., Tschopp, F.A. and Fischer, J.A. (1984). Immunoreactive calcitonin gene-related peptide and substance P co-exist in sensory neurones to the spinal cord and interact in spinal behavioural responses of the rat. Neurosci. Letters, 52, 199–204.

    Google Scholar 

  16. Mason, R.T., Peterfreund, R.A., Sawchenko, P.E., Carrigan, A.Z., Rivier, J.E. and Vale, W.W. (1984). Release of the predicted caicitonin gene-related peptide from cultured rat trigeminal ganglion cells. Nature, 308, 653–655.

    Article  Google Scholar 

  17. Theodorsson-Norheim, E., Brodin, E., Norheim, I. and Rosell, S. (1984). Antisera raised against eledoisin and kassinen detect immunoreactive material in rat tissue extracts: tissue distribution and Chromatographic characterization. Regulatory Peptides, 9, 229–244.

    Article  Google Scholar 

  18. Gamse, R., Molnar, A. and Lembeck, F. (1979). Substance P release from spinal cord slices by capsaicin. Life Sci., 25, 629–636.

    Article  Google Scholar 

  19. Brain, S.D., Williams, T.J., Tippins, J.R., Morris, H.R. and McIntyre, I. (1985). Calcitonin gene-related peptide is a potent vasodilator. Nature, 313, 54–56.

    Article  Google Scholar 

  20. Gibbins, I.L., Furness, J.B., Costa, M., Mclntyre, I., Hillyard, C. and Girgis, S. (1985). Co-existence of calcitonin gene-related peptide, dynorphin and cholecystokinin in substance P-containing dorsal root ganglion neurones of the guinea-pig. Neurosci., Letters Suppl. 19, 65.

    Google Scholar 

  21. Gamse, R., Holzer, P. and Lembeck, F. (1980). Decrease of substance P in primary afferent neurones and impairment of neurogenic plasma extravasation by capsaicin. Br. J. Pharmac, 68, 207–213.

    Article  Google Scholar 

  22. Maggio, J.E. and Hunter, J.C. (1984). Regional distribution of kassinin-like immunoreactivity in rat central and peripheral tissues and the effect of capsaicin. Brain Res., 307, 370–373.

    Article  Google Scholar 

  23. Holmdahl, G., Hakanson, R., Leander, S., Roseel, S., Folkers, F. and Sundler, F. (1981). A substance P antagonist, [D-Pro 2, D-Trp 7,9]SP, inhibits inflammatory responses in the rabbit eye. Science, 214, 1029–1031.

    Article  Google Scholar 

  24. Lembeck, F., Donnerer, J. and Bartho, L. (1982). Inhibition of neurogenic vasodilation and plasma extravasation by substance P antagonists, somatostatin and [D-met 2, pro5] enkephalinamide. Eur. J.Pharmacol., 85, 171–176.

    Google Scholar 

  25. Lundberg, J.M., Saria, A., Brodin, E., Rosell, S. and Folkers, K. (1983). A substance P antagonist inhibits vagally induced increase in vascular permeability and bronchial smooth muscle contraction in the guinea-pig. Proc. Natl. Acad. Sci. USA 80, 1120–1124.

    Article  Google Scholar 

  26. Hunter, J.C. and Maggio, J.E. (1984). A pharmacological study with substance K: evidence for multiple types of tachykinin receptors. Eur. J. Pharmacol., 105, 149–153.

    Google Scholar 

  27. Williams, T.J. and Peck, M.J. (1977). Role of prostaglandin-mediated vasodilatation in inflammation. Nature, 270, 530–532.

    Article  Google Scholar 

  28. Svensjo, E. (1978). Bradykinin and prostaglandin E1, E2 and F2α -induced macromolecular leakage in the hamster cheek poucn. Prostaglandins and Medicine, 1, 397–410.

    Article  Google Scholar 

  29. Grega, G.J., Svensjo, E. and Haddy, F.J. (1981). Macromolecular permeability of the microvascular membranes. Physiological and pharmacological regulation. Microcirculation, 1., 325–341.

    Google Scholar 

  30. Chahl, L.A. (1977). Interactions of substance P with putative mediators of inflammation and ATP. Eur. J. Pharmacol., 44, 45–49.

    Google Scholar 

  31. Jancso, G., Kiraly, E. and Jancso-Gabor, A. (1980). Chemosensitive pain fibres and inflammation. Int. J. Tiss. Reac. 11, 57–66.

    Google Scholar 

  32. Saria, A., Lundberg, J.M. Skofitsch, G. and Lembeck, F. (1983). Vascular protein leakage in various tissue induced by substance P, capsaicin, bradykinin, serotonin, histamine and by antigen challenge. Naunyn-Schmiedeberg’s Arch. Pharmacol., 324, 212–218.

    Google Scholar 

  33. Szolcsanyi, J., Aranko-Gabor, J. and Salamon, J. (1976). Vascular permeability increasing effect of electric stimulation of peripheral nerves, sensory ganglia and spinal roots. Acta Physiol. Acad. Sci. Hung., 47, 255.

    Google Scholar 

  34. Lundberg, J.M. and Saria, A. (1982). Capsaicin-sensitive vagal neurons involved in control of vascular permeability in rat trachea. Acta Physiol. Scand., 115, 521–524.

    Google Scholar 

  35. Saria, A. and Lundberg, J.M. (1983). Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues. J. Neurosci. Methods, 8, 41–49.

    Google Scholar 

  36. Lundberg, J.M. and Saria, A. (1983). Capsaicin-induced desensitization of airway mucosa to cigarette smoke, mechanical and chemical irritants. Nature, 302, 251–253.

    Article  Google Scholar 

  37. Lundblad, L., Saria, A., Lundberg, J.M. and Anggard, A. (1983). Increased vascular permeability in rat nasal mucosa induced by substance P and stimulation of capsaicin-sensitive trigeminal neurones. Acta Otolaryngol., 96, 479–484.

    Article  Google Scholar 

  38. Lundberg, J.M., Brodin, E. and Saria, A. (1983). Effects and distribution of vagal capsaicin-sensitive substance P neurones with special reference to the trachea and lungs. Acta Physiol. Scand., 119, 243–252.

    Google Scholar 

  39. Lundberg, J.M., Saria, A. and Martling, C.R. (1983). Capsaicin pretreatment abolishes cigarette smoke-induced oedema in rat tracheo-bronchial mucosa. Eur. J. Pharmacol., 86, 317–318.

    Google Scholar 

  40. Lundberg, J.M., Martling, C.R. and Saria, A. (1983). Substance P and capsaicin-induced contraction of human bronchi. Acta Physiol. Scand. 119, 49–53.

    Google Scholar 

  41. Lundberg, J.M., Martling, C.R., Saria, A., Folkers, K. and Rosell, S. (1983). Cigarette smoke-induced airway oedema due to activation of capsaicin-sensitive vagal afferents and substance P release. Neuroscience 10, 1361–1368.

    Article  Google Scholar 

  42. Saria, A. and Lundberg, J.M. (1984). Activation of sensory substance P neurones in the respiratory tract by cigarette smoke, mechanical and chemical irritants. In Frontiers in Hormone Research, Vol. 12, (eds. M. Ratzenhofer, H. Hofler, G.F. Walter), Karger, Basel, pp. 123–126.

    Google Scholar 

  43. Lundberg, J.M., Brodin, E., Hua, X. and Saria, A. (1984). Vascular permeability changes and smooth muscle contraction in relation to capsaicin-sensitive substance P afferents in the guinea-pig. Acta Physiol. Scand., 120, 217–227.

    Google Scholar 

  44. Lundberg, J.M., Hokfelt, T., Martling, C.R., Saria, A. and Cuello, A.C. (1984). Substance P-immunoreactive sensory nerves in the lower respiratory tract of various animals including man. Cell Tissue Research, 235, 251–261.

    Article  Google Scholar 

  45. Saria, A., Theodorsson-Norheim, E., Gamse, R. and Lundberg, J.M. (1985). Release of substance P- and substance K-like immunoreactivities from the isolated perfused guinea-pig lung. Eur. J. Pharmacol., 106, 207–208.

    Google Scholar 

  46. Saria, A. (1984). Substance P in sensory nerve fibres contributes to the development of oedema in the rat hind paw after thermal injury. Br. J.Pharmacol., 82, 217–222.

    Google Scholar 

  47. Widdicombe, J.G. (1981). Nervous receptors in the respiratory tract and lungs. In Lung Histology in Health and Disease, Vol. 17, pt. 1 (ed. T. Hornbein), pp. 429–472).

    Google Scholar 

  48. Saria, A., Lundberg, J.M., Hua, X.and Lembeck, F. (1983). Capsaicin-induced substance P release and sensory control of vascular permeability in the guinea-pig ureter. Neurosci. Letters, 41, 167–172.

    Google Scholar 

  49. Bill, A., Stjernschantz, J., Mandahl, A., Brodin, E. and Nilsson, G. (1979). Substance P: release on trigeminal nerve stimulation, effects in the eye. Acta Physiol. Scand., 106, 371–373.

    Google Scholar 

  50. Stjernschantz, J., Geijer, C. and Bill, A. (1979). Electrical stimulation of the fifth cranial nerve in rabbits: effects on ocular blood flow, extravascular albumin content and intraocular pressure. Exp. Eye Res., 28, 229–238.

    Article  Google Scholar 

  51. Bjorkroth, U. (1983). Inhibition of smooth muscle contractions induced by capsaicin and electrical transmural stimulation by a substance P antagonist. Acta Physiol. Scand. Suppl. 515, 11–16.

    Google Scholar 

  52. Leander, S., Hakanson, R., Rosell, S., Folkers, K., Sundler, F. and Tornquist, K. (1981). A specific substance P antagonist blocks smooth muscle contractions induced by non-cholinergic, non-adrenergic nerve stimulation. Nature, 294, 467–470.

    Article  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Copyright information

© 1985 The Contributors

About this chapter

Cite this chapter

Saria, A., Lundberg, J.M. (1985). Neurogenic Inflammation. In: Higgs, G.A., Williams, T.J. (eds) Inflammatory Mediators. Satellite Symposia of the IUPHAR 9th International Congress of Pharmacology. Palgrave Macmillan, London. https://doi.org/10.1007/978-1-349-07834-9_8

Download citation

Publish with us

Policies and ethics