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PMID: 14978204 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Subtypes of vagal afferent C-fibres in guinea-pig lungs.

The Journal of physiology ·Vol. 556 ·No. Pt 3 ·2004-05-01 ·Pages 905-17

Undem BJ, Chuaychoo B, Lee MG, Weinreich D, Myers AC, Kollarik M

Abstract

An ex vivo, vagally innervated, lung preparation was used to address the hypothesis that vagal C-fibres comprise at least two distinct phenotypes. Histological and extracellular electrophysiological experiments revealed that vagal C-fibres innervating the pulmonary system are derived from cell bodies situated in two distinct vagal sensory ganglia. The jugular (superior) ganglion neurones project C-fibres to both the extrapulmonary airways (larynx, trachea and bronchus) and the lung parenchymal tissue. By contrast, C-fibres from nodose (inferior) neurones innervate primarily structures within the lungs. Histologically, nodose neurones projecting lung C-fibres were different from the jugular neurones in that they were significantly less likely to express neurokinins. The nerve terminals within the lungs of both nodose and jugular C-fibres responded with action potential discharge to capsaicin and bradykinin application, but only the nodose C-fibre population responded with action potential discharge to the P2X selective receptor agonist alpha,beta-methylene-ATP. Whole cell patch clamp recording of capsaicin-sensitive nodose and jugular ganglion neurones retrogradely labelled from the lung tissue revealed that, like the nerve terminals, lung specific nodose C-fibre neurones express functional P2X receptors, whereas lung specific jugular C-fibres do not. The data support the hypothesis that both neural crest-derived neurones (jugular ganglia) and placode-derived neurones (nodose ganglia) project C-fibres in the vagus, and that these two C-fibre populations represent distinct phenotypes.

MeSH Terms
Action Potentials/drug effects,physiology Adenosine Triphosphate/analogs & derivatives,pharmacology Afferent Pathways/physiology Animals Bradykinin/pharmacology Bronchi/innervation Calcitonin Gene-Related Peptide/analysis Capsaicin/pharmacology Electrophysiology Ganglia/chemistry,physiology Guinea Pigs Immunohistochemistry In Vitro Techniques Laryngeal Nerves/physiology Lung/drug effects,innervation,physiology Male Nerve Fibers, Unmyelinated/classification,drug effects,physiology Neurofilament Proteins/analysis Nodose Ganglion/chemistry,physiology Patch-Clamp Techniques Physical Stimulation Substance P/analysis Trachea/innervation Vagus Nerve/physiology
Chemicals
Neurofilament Proteins Substance P Adenosine Triphosphate Calcitonin Gene-Related Peptide alpha,beta-methyleneadenosine 5'-triphosphate Capsaicin Bradykinin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Undem B J
Johns Hopkins School of Medicine, and University, Baltimore, MD, USA. [email protected]
Chuaychoo B
Lee M-G
Weinreich D
Myers A C
Kollarik M
References (35)
35 references, click to expand
  1. Identification and substance P content of vagal afferent neurons innervating the epithelium of the guinea pig trachea.
    Am J Respir Crit Care Med. 1999 Jun;159(6):1943-8 PMID: 10351943
  2. Nerve growth factor levels and localisation in human asthmatic bronchi.
    Eur Respir J. 2002 Nov;20(5):1110-6 PMID: 12449162
  3. Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation.
    J Clin Invest. 1996 Nov 15;98(10):2284-91 PMID: 8941645
  4. Afferent properties and reflex functions of bronchopulmonary C-fibers.
    Respir Physiol. 2001 Mar;125(1-2):47-65 PMID: 11240152
  5. Soma neurofilament immunoreactivity is related to cell size and fibre conduction velocity in rat primary sensory neurons.
    J Physiol. 1991 Apr;435:41-63 PMID: 1770443
  6. Adaptation of guinea-pig vagal airway afferent neurones to mechanical stimulation.
    J Physiol. 1999 Nov 15;521 Pt 1:239-47 PMID: 10562348
  7. The sensory and sympathetic innervation of guinea-pig lung and trachea as studied by retrograde neuronal tracing and double-labelling immunohistochemistry.
    Neuroscience. 1992 Aug;49(3):715-37 PMID: 1380140
  8. Airway receptors.
    Respir Physiol. 2001 Mar;125(1-2):3-15 PMID: 11240149
  9. Activation of pulmonary C fibres by adenosine in anaesthetized rats: role of adenosine A1 receptors.
    J Physiol. 1998 Apr 1;508 ( Pt 1):109-18 PMID: 9490825
  10. Expression of tachykinins in nonnociceptive vagal afferent neurons during respiratory viral infection in guinea pigs.
    Am J Respir Crit Care Med. 2002 Apr 15;165(8):1071-5 PMID: 11956047
  11. Mechanism of action of ATP on canine pulmonary vagal C fibre nerve terminals.
    J Physiol. 1996 Jan 1;490 ( Pt 1):265-75 PMID: 8745294
  12. Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers.
    J Neurocytol. 1990 Oct;19(5):789-801 PMID: 2077115
  13. Cells Expressing mRNA for Neurotrophins and their Receptors During Embryonic Rat Development.
    Eur J Neurosci. 1992 Oct;4(11):1140-1158 PMID: 12106420
  14. Interganglionic segregation of distinct vagal afferent fibre phenotypes in guinea-pig airways.
    J Physiol. 1996 Oct 15;496 ( Pt 2):521-30 PMID: 8910234
  15. Immunomodulation of afferent neurons in guinea-pig isolated airway.
    J Physiol. 1996 Mar 1;491 ( Pt 2):499-509 PMID: 8866873
  16. Early steps in the production of sensory neurons by the neurogenic placodes.
    Mol Cell Neurosci. 2002 Nov;21(3):502-11 PMID: 12498790
  17. Pharmacology of airway afferent nerve activity.
    Respir Res. 2001;2(4):234-44 PMID: 11686889
  18. Nerve growth factor-induced phenotypic switch in guinea pig airway sensory neurons.
    Am J Respir Crit Care Med. 2000 Jun;161(6):1985-90 PMID: 10852778
  19. Neurotrophins in bronchial asthma.
    Respir Res. 2001;2(5):265-8 PMID: 11686893
  20. Capsaicin-sensitive and -insensitive vagal bronchopulmonary C-fibres in the mouse.
    J Physiol. 2003 Sep 15;551(Pt 3):869-79 PMID: 12909686
  21. The plant lectin Bandeiraea simplicifolia I-B4 identifies a subpopulation of small diameter primary sensory neurones which innervate the skin in the rat.
    Neurosci Lett. 1993 Sep 3;159(1-2):17-20 PMID: 8264961
  22. Stimulation of 'irritant' receptors and afferent C-fibres in the lungs by prostaglandins.
    Nature. 1976 Dec 2;264(5585):451-3 PMID: 1004577
  23. Vertebrate cranial placodes I. Embryonic induction.
    Dev Biol. 2001 Apr 1;232(1):1-61 PMID: 11254347
  24. Changes in P2X receptor responses of sensory neurons from P2X3-deficient mice.
    Eur J Neurosci. 2001 Dec;14(11):1784-92 PMID: 11860473
  25. Bradykinin stimulates afferent vagal C-fibers in intrapulmonary airways of dogs.
    J Appl Physiol Respir Environ Exerc Physiol. 1980 Mar;48(3):511-7 PMID: 7372522
  26. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits.
    Pharmacol Rev. 2001 Mar;53(1):107-18 PMID: 11171941
  27. Allergic inflammation-induced neuropeptide production in rapidly adapting afferent nerves in guinea pig airways.
    Am J Physiol Lung Cell Mol Physiol. 2002 Apr;282(4):L775-81 PMID: 11880304
  28. Establishing neuronal identity in vertebrate neurogenic placodes.
    Development. 2000 Jul;127(14):3045-56 PMID: 10862742
  29. Characterization of vagal afferent subtypes stimulated by bradykinin in guinea pig trachea.
    J Pharmacol Exp Ther. 1999 May;289(2):682-7 PMID: 10215640
  30. Afferent vagal C fibre innervation of the lungs and airways and its functional significance.
    Rev Physiol Biochem Pharmacol. 1984;99:1-110 PMID: 6695127
  31. Evidence that distinct neural pathways mediate parasympathetic contractions and relaxations of guinea-pig trachealis.
    J Physiol. 1993 Nov;471:25-40 PMID: 7907144
  32. Vagal sensory receptors and their reflex effects.
    Physiol Rev. 1973 Jan;53(1):159-227 PMID: 4568412
  33. Retrograde tracing shows that CGRP-immunoreactive nerves of rat trachea and lung originate from vagal and dorsal root ganglia.
    J Auton Nerv Syst. 1987 Aug;20(2):155-66 PMID: 3312381
  34. Neurochemistry of the nodose ganglion.
    Prog Neurobiol. 1997 Jun;52(2):79-107 PMID: 9185234
  35. Impulse activity in afferent vagal C-fibres with endings in the intrapulmonary airways of dogs.
    Respir Physiol. 1977 Apr;29(2):125-42 PMID: 866808
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2004-05-01
Epub
2004-00-20
Pages
905-17
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1665007
Subset
IM
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