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Neurogenic Inflammation

A Model for Studying Efferent Actions of Sensory Nerves

  • Chapter
Frontiers in Arterial Chemoreception

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 410))

Abstract

Cytoplasmic vesicles, resembling synaptic vesicles of efferent nerve fibers,* are a distinctive feature of sensory nerve fibers that innervate glomus cells of the carotid body (Biscoe et al, 1970; Kobayashi & Uehara, 1970; McDonald & Mitchell, 1975). Ultrastructural studies have shown that some vesicles cluster at synaptic junctions where sensory nerves are presynaptic to glomus cells (McDonald & Mitchell, 1975; Verna, 1979; Pallot, 1987). This finding has led to speculation that substances from sensory nerves influence glomus cells (McDonald & Mitchell, 1975). Indeed, the phenomenon of “efferent inhibition” (Neil & O’Regan, 1969, 1971), in which electrical stimulation of the carotid sinus nerve inhibits chemoreceptor firing, has been interpreted as an efferent action of sensory nerves on glomus cells (McDonald & Mitchell, 1981). Although there are other interpretations of the mechanism underlying efferent inhibition (Biscoe, 1971; Sampson et al, 1976; O’Regan, 1977, 1981; Acker & O’Regan, 1981), the morphological evidence that sensory nerves are presynaptic to glomus cells is compelling.

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References

  • Abelli L, Maggi CA, Rovero P, Del Bianco E, Regoli D, Drapeau G & Giachetti A (1991) Effect of synthetic tachykinin analogues on airway microvascular leakage in rats and guinea-pigs: evidence for the involvement of NK-1 receptors. J Auton Pharmacol 11: 267–275

    Article  PubMed  CAS  Google Scholar 

  • Acker H & O’Regan RG (1981) The effects of stimulation of autonomic nerves on carotid body blood flow in the cat. J Physiol, London 315: 99–110

    CAS  Google Scholar 

  • Baluk P, Nadel JA & McDonald DM (1992) Substance P-immunoreactive sensory axons in the rat respiratory tract: a quantitative study of their distribution and role in neurogenic inflammation. J Comp Neurol 319: 586–598

    Article  PubMed  CAS  Google Scholar 

  • Baluk P, Bowden JJ, Lefevre PL & McDonald DM (1995) Increased expression of substance P (NK1) receptors on airway blood vessels of rats with Mycoplasma pulmonis infection. Am J Respir Crit Care Med 151: A719

    Google Scholar 

  • Baluk P, Hirata A, Fujiwara T, Neal CR, Michel CC & McDonald DM (1996) Endothelial gaps in inflamed venules of rat airways: Time course of changes in permeability and morphology. Submitted for publication

    Google Scholar 

  • Barnes PJ (1991a) Neurogenic inflammation in airways. Intl Arch Allergy Appl Immunol 94: 303–309

    Article  CAS  Google Scholar 

  • Barnes PJ (1991b) Sensory nerves, neuropeptides, and asthma. Ann NY Acad Sci 629: 359–370

    Article  PubMed  CAS  Google Scholar 

  • Barnes PJ (1992) Neural mechanisms in asthma. Br Med Bull 48: 149–168

    PubMed  CAS  Google Scholar 

  • Biscoe TJ (1971) Carotid body: structure and function. Physiol Rev 51: 427–495

    Google Scholar 

  • Biscoe TJ, Lall A & Sampson SR (1970) Electron microscopic and electrophysiological studies on the carotid body following intracranial section of the glossopharyngeal nerve. J Physiol, London 208: 133–152

    CAS  Google Scholar 

  • Bowden JJ, Garland A, Baluk P, Lefevre P, Grady E, Vigna SR, Bunnett NW & McDonald DM (1994a) Direct observation of substance P-induced internalization of neurokinin 1 (NK1) receptors at sites of inflammation. Proc Natl Acad Sci USA 91: 8964–8968

    Article  PubMed  CAS  Google Scholar 

  • Bowden JJ, Schoeb TR, Lindsey JR & McDonald DM (1994b) Dexamethasone and Oxytetracycline reverse the potentiation of neurogenic inflammation in airways of rats with Mycoplasma pulmonis infection. Am J Respir Crit Care Med 150: 1391–1401

    PubMed  CAS  Google Scholar 

  • Bowden JJ, Baluk P, Lefevre PM, Vigna SR & McDonald DM (1996) Substance P (NK1) receptor immunoreactiv-ity on endothelial cells of the rat tracheal mucosa. Am J Physiol 270: L404–L414

    PubMed  CAS  Google Scholar 

  • Carstairs J & Barnes P (1986) Autoradiographic mapping of substance P receptors in lung. Eur J Pharmacol 127: 295–296

    Article  Google Scholar 

  • Dalsgaard CJ & Lundberg JM (1984) Evidence for a spinal afferent innervation of the guinea pig lower respiratory tract as studied by the horseradish peroxidase technique. Neurosci Lett 23: 117–122

    Article  Google Scholar 

  • Delay-Goyet P & Lundberg JM (1991) Cigarette smoke-induced airway oedema is blocked by the NK1 antagonist, CP-96,345. Eur J Pharmacol 2: 157–158

    Article  Google Scholar 

  • Garland A, Ray DW, Doerschuk CM, Alger L, Eappon S, Hernandez C, Jackson M & Solway J (1991) Role of tachykinins in hyperpnea-induced bronchovascular hyperpermeability in guinea pigs. J Appl Physiol 70: 27–35

    PubMed  CAS  Google Scholar 

  • Hirata A, Baluk P, Fujiwara T & McDonald DM (1995) Location of focal silver staining at endothelial gaps in inflamed venules examined by scanning electron microscopy. Am J Physiol (Lung Cell Mol Physiol 13) 269: L403–L418

    CAS  Google Scholar 

  • Hoover D & Hancock J (1987) Autoradiographic localization of substance P binding sites in guinea-pig airways. J Auton Nerv Syst 19: 171–174

    Article  PubMed  CAS  Google Scholar 

  • Jancsó N (1960) Role of the nerve terminals in the mechanism of inflammatory reactions. Bull Millard Fillmore Hosp, Buffalo, NY 7: 53–77

    Google Scholar 

  • Jancsó N (1961) Inflammation and the inflammatory mechanisms. J Pharm Pharmacol 13: 577–594

    Article  PubMed  Google Scholar 

  • Jancsó N, Jancsó-Gábor A & Szolcsányi J (1967) Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br J Pharmacol Chemother 31: 138–151

    PubMed  Google Scholar 

  • Jancsó N, Jancsó-Gábor A & Szolcsányi 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 Chemother 33: 32–41

    PubMed  Google Scholar 

  • Joris I, DeGirolami U, Wortham K & Majno G (1982) Vascular labelling with Monastral blue B. Stain Technol 57: 177–183

    PubMed  CAS  Google Scholar 

  • Kobayashi S & Uehara M (1970) Occurrence of afferent synaptic complexes in the carotid body of the mouse. Arch Histol Jap 32: 193–201

    Article  PubMed  CAS  Google Scholar 

  • Krootila K, Oksala O, Zschauer A, Palkama A & Uusitalo H (1992) Inhibitory effect of methysergide on calcitonin gene-related peptide-induced vasodilatation and ocular irritative changes in the rabbit. Br J Pharmacol 106: 404–408

    Article  PubMed  CAS  Google Scholar 

  • Kummer W, Fischer A, Preissler U, Couraud J-Y & Heym C (1990) Immunohistochemistry of the guinea-pig trachea using an anti-idiotypic antibody recognizing substance P receptors. Histochemistry 93: 541–546

    Article  PubMed  CAS  Google Scholar 

  • Kummer W, Fischer A, Couraud J-Y & Heym C (1991) Immunohistochemistry of peptides (substance P and VIP) and peptide receptors in the trachea. J Auton Nerv Syst 33: 121–123

    Article  Google Scholar 

  • Kummer W, Fischer A, Kurkowski R & Heym C (1992) The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry. Neuroscience 49: 715–737

    Article  PubMed  CAS  Google Scholar 

  • Lei YH, Barnes PJ & Rogers DF (1992) Inhibition of neurogenic plasma exudation in guinea-pig airways by CP-96,345, a new non-peptide NK1 receptor antagonist. Br J Pharmacol 105: 261–262

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lundberg JM & Saria A (1983) Capsaicin-induced desensitization of airway mucosa to cigarette smoke, mechanical and chemical irritants. Nature 302: 251–253

    Article  PubMed  CAS  Google Scholar 

  • Lundberg JM, Saria A, Theodorsson-Norheim E, Brodin E, Hua X-Y, Martling C-R, Gamse R & Hökfelt TG (1985) Multiple tachykinins in capsaicin-sensitive afferents: occurrence, release and biological effects with special reference to irritation of the airways. In: Håkanson R & Sundler F (eds) Tachykinin Antagonists. New York: Elsevier North-Holland. pp 159–169

    Google Scholar 

  • Lundberg JM, Hökfelt T, Martling CR, Saria A & Cuello C (1984) Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tiss Res 235: 251–261

    CAS  Google Scholar 

  • Majno G & Palade GE (1961) Studies on inflammation. I. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Biophys Biochem Cytol 11: 571–604

    Article  PubMed  CAS  Google Scholar 

  • Majno G, Palade GE & Schoefl GI (1961) Studies on inflammation. II. The site of action of histamine and serotonin along the vascular tree: a topographic study. J Biophys Biochem Cytol 11: 607–625

    Article  PubMed  CAS  Google Scholar 

  • McDonald DM (1988a) Neurogenic inflammation in the rat trachea. I. Changes in venules, leucocytes and epithelial cells. J Neurocytol 17: 583–603

    Article  PubMed  CAS  Google Scholar 

  • McDonald DM (1988b) Respiratory tract infections increase susceptibility to neurogenic inflammation in the rat trachea. Am Rev Respir Dis 137: 1432–1440

    PubMed  CAS  Google Scholar 

  • McDonald DM (1994a) The concept of neurogenic inflammation in the respiratory tract. In: Kaliner MA, Barnes PJ, Kunkel GHH & Baraniuk JN (eds) Neuropeptides in Respiratory Medicine. New York: Marcel Dekker. pp 321–349

    Google Scholar 

  • McDonald DM (1994b) Endothelial gaps and permeability of venules in rat tracheas exposed to inflammatory stimuli. Am J Physiol 266: L61–L83

    PubMed  CAS  Google Scholar 

  • McDonald DM (1996) Neurogenic inflammation in the airways. In: Barnes P (ed) Autonomic Control of the Respiratory System. London: Harwood Academic Publishers. In press

    Google Scholar 

  • McDonald DM & Mitchell RA (1975) The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body. A quantitative ultrastructural analysis. J Neurocytol 4: 177–230

    Article  Google Scholar 

  • McDonald DM & Mitchell RA (1981) The neural pathway involved in “efferent inhibition” of chemoreceptors in the cat carotid body. J Comp Neurol 201: 457–476

    Article  PubMed  CAS  Google Scholar 

  • McDonald DM, Mitchell RA, Gabella G & Haskell A (1988) Neurogenic inflammation in the rat trachea. II. Identity and distribution of nerves mediating the increase in vascular permeability. J Neurocytol 17: 605–628

    Article  PubMed  CAS  Google Scholar 

  • McDonald DM, Schoeb TR & Lindsey JR (1991) Mycoplasma pulmonis infections cause long-lasting potentiation of neurogenic inflammation in the respiratory tract of the rat. J Clin Invest 87: 787–799

    Article  PubMed  CAS  Google Scholar 

  • Nadel JA (1992) Regulation of neurogenic inflammation by neutral endopeptidase. Am Rev Respir Dis 145: S48–S52

    Article  PubMed  CAS  Google Scholar 

  • Neil E & O’Regan RG (1969) Effects of sinus and aortic nerve efferents on arterial chemoreceptor function. J Physiol, London 200: 69P–71P

    CAS  Google Scholar 

  • Neil E & O’Regan RG (1971) The effects of electrical stimulation of the distal end of the cut sinus and aortic nerves on peripheral arterial chemoreceptor activity in the cat. J Physiol, London 215: 15–32

    CAS  Google Scholar 

  • O’Regan RG (1977) Control of carotid body chemoreceptors by autonomic nerves. Irish J Med Sci 146: 199–205

    Article  PubMed  Google Scholar 

  • O’Regan RG (1981) Responses of carotid body chemosensory activity and blood flow to stimulation of sympathetic nerves in the cat. J Physiol, London 315: 81–98

    Google Scholar 

  • Pallot DJ (1987) The mammalian carotid body. Adv Anat Embryol Cell Biol 102: 1–91

    Article  PubMed  CAS  Google Scholar 

  • Persson CGA (1991) Plasma exudation in the airways: mechanisms and function. Eur Respir J 4: 1268–1274

    PubMed  CAS  Google Scholar 

  • Petersson G, Bacci E, McDonald DM & Nadel JA (1993) Neurogenic plasma extravasation in the rat nasal mucosa is potentiated by peptidase inhibitors. J Pharmacol Exp Ther 264: 509–514

    PubMed  CAS  Google Scholar 

  • Sakamoto T, Elwood W, Barnes PJ & Chung KF (1992) Pharmacological modulation of inhaled sodium metabisul-phite-induced airway microvascular leakage and bronchoconstriction in the guinea-pig. Br J Pharmacol 107:481–487

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto T, Barnes PJ & Chung KF (1993) Effect of CP-96,345, a non-peptide NK1 receptor antagonist, against substance P-induced, bradykinin-induced and allergen-induced airway microvascular leakage and bronchoconstriction in the guinea pig. Eur J Pharmacol 231: 31–38

    Article  PubMed  CAS  Google Scholar 

  • Sampson SR, Aminoff M J, Jaffe RA & Vidruk EH (1976) A pharmacological analysis of neurally induced inhibition of carotid body chemoreceptor activity in cats. J Pharmacol Exp Ther 197: 119–125

    PubMed  CAS  Google Scholar 

  • Schoeb TR & Lindsey JR (1987) Exacerbation of murine respiratory mycoplasmosis by sialodacryoadenitis virus infection in gnotobiotic F344 rats. Vet Pathol 24: 392–399

    PubMed  CAS  Google Scholar 

  • Schoeb TR, Davidson MK & Lindsey JR (1982) Intracage ammonia promotes growth of Mycoplasma pulmonis in the respiratory tract of rats. Infect Immun 38: 212–217

    PubMed  CAS  Google Scholar 

  • Serti K, Wiedermann CJ, Kowalski ML, Hurtado S, Plutchok J, Linnoila I, Pert CB & Kaliner MA (1988) Substance P: the relationship between receptor distribution in rat lung and the capacity of substance P to stimulate vascular permeability. Am Rev Respir Dis 138: 151–159

    Article  Google Scholar 

  • Solway J & Leff AR (1991) Sensory neuropeptides and airway function. J Appl Physiol 71: 2077–2087

    PubMed  CAS  Google Scholar 

  • Springall DR, Cadieux A, Oliveira H, Su H, Royston D & Polak JM (1987) Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia. J Auton Nerv Syst 20: 155–166

    Article  PubMed  CAS  Google Scholar 

  • Stjernschantz J, Sears M & Mishima H (1982) Role of substance P in the antidromic vasodilation, neurogenic plasma extravasation and disruption of the blood-aqueous barrier in the rabbit eye. Naunyn-Schmiedeberg’s Arch Pharmacol 321: 329–335

    Article  CAS  Google Scholar 

  • Terenghi G, McGregor GP, Bhuttacharji S, Wharton J, Bloom SR & Polak JM (1983) Vagal origin of substance P-containing nerves in the guinea pig lung. Neurosci Lett 36: 229–239

    Article  PubMed  CAS  Google Scholar 

  • Tousignant C, Chan C-C, Guevremont D, Brideau C, Hale JJ, MacCoss M & Rodger IW (1993) NK2 receptors mediate plasma extravasation in guinea-pig lower airways. Br J Pharmacol 108: 383–386

    Article  PubMed  CAS  Google Scholar 

  • Umeno E, McDonald DM & Nadel JA (1990) Hypertonic saline increases vascular permeability in the rat trachea by producing neurogenic inflammation. J Clin Invest 85: 1905–1908

    Article  PubMed  CAS  Google Scholar 

  • Verna A (1979) Ultrastructure of the carotid body in the mammals. Intl Rev Cytol 60: 271–330

    Article  CAS  Google Scholar 

  • Vigna SR, Bowden JJ, McDonald DM, Fisher J, Okamoto A, McVey DC, Payan DG & Bunnett NW (1994) Characterization of antibodies to the rat substance P (NK-1) receptor and to a chimeric substance P receptor expressed in mammalian cells. J Neurosci 14: 834–845

    PubMed  CAS  Google Scholar 

  • Yager D, Shore S & Drazen JM (1991) Airway luminal liquid. Sources and role as an amplifier of bronchocon-striction. Am Rev Respir Dis 143: S52–S54

    PubMed  CAS  Google Scholar 

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McDonald, D.M., Bowden, J.J., Baluk, P., Bunnett, N.W. (1996). Neurogenic Inflammation. In: Zapata, P., Eyzaguirre, C., Torrance, R.W. (eds) Frontiers in Arterial Chemoreception. Advances in Experimental Medicine and Biology, vol 410. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5891-0_70

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  • DOI: https://doi.org/10.1007/978-1-4615-5891-0_70

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