Home LiteratureArticle Details
PMID: 15802291 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Sensory transduction of pulmonary reactive oxygen species by capsaicin-sensitive vagal lung afferent fibres in rats.

The Journal of physiology ·Vol. 565 ·No. Pt 2 ·2005-06-01 ·Pages 563-78

Ruan T, Lin YS, Lin KS, Kou YR

Abstract

The mechanisms of sensory transduction of pulmonary reactive oxygen species (ROS) by capsaicin-sensitive vagal lung afferent fibres are unclear. To investigate the role of transient receptor potential vanilloid 1 (TRPV1) receptors and P2X purinoceptors in this sensory transduction, we recorded fibre activity (FA) from 132 fibres of this type in 132 anaesthetized and ventilated rats. Airway challenge of aerosolized H2O2 (0, 0.2 and 0.4%) produced a concentration-dependant fibre stimulation. The fibre responses to 0.4% H2O2 were attenuated by dimethylthiourea (a hydroxyl radical (.OH) scavenger; change in fibre activity (DeltaFA), -55+/-9%) or deferoxamine (an iron-chelator that prevents formation of .OH; DeltaFA, -59+/-9%), were prevented by catalase (an enzyme catalysing H2O2; DeltaFA, -96+/-3%) and were unaffected by the vehicle for dimethylthiourea, iron-saturated deferoxamine or heat-inactivated catalase. The fibre responses to 0.4% H2O2 were attenuated by capsazepine (a TRPV1 receptor antagonist; DeltaFA, -39+/-9%) or iso-pyridoxalphosphate-6-azophenyl-2',5'-disulphonate (iso-PPADS, a P2X receptor antagonist; DeltaFA, -51+/-9%), were further reduced by capsazepine and iso-PPADS in combination (DeltaFA, -70+/-13%), and were unaltered by their vehicles. The fibre responses to cigarette smoke (20 ml), an irritant that generates ROS, were attenuated by dimethylthiourea (DeltaFA, -61+/-9%) or capsazepine and iso-PPADS in combination (DeltaFA, -67+/-9%). These results suggest that both the TRPV1 and P2X receptors mediate the sensory transduction of ROS, especially H2O2 and .OH, by capsaicin-sensitive vagal lung afferent fibres.

MeSH Terms
Action Potentials/drug effects,physiology Animals Blood Pressure/drug effects Capsaicin/pharmacology Hydrogen Peroxide/pharmacology Ion Channels/physiology Lung/innervation,metabolism Lung Compliance/drug effects Male Neurons, Afferent/drug effects,physiology Oxidants/pharmacology Rats Rats, Sprague-Dawley Reactive Oxygen Species/metabolism Receptors, Purinergic P2/physiology Smoking Stimulation, Chemical TRPV Cation Channels Vagus Nerve/cytology,drug effects,physiology
Chemicals
Ion Channels Oxidants Reactive Oxygen Species Receptors, Purinergic P2 TRPV Cation Channels Trpv1 protein, rat Hydrogen Peroxide Capsaicin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ruan Ting
Institute of Physiology, School of Medicine, National Yang-Ming University, Taipei 112, Taiwan.
Lin You Shuei
Lin Kae-Shin
Kou Yu Ru
References (64)
64 references, click to expand
  1. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules.
    Mol Pharmacol. 2003 Oct;64(4):785-95 PMID: 14500734
  2. The involvement of hydroxyl radical and cyclooxygenase metabolites in the activation of lung vagal sensory receptors by circulatory endotoxin in rats.
    J Appl Physiol (1985). 2005 Feb;98(2):620-8 PMID: 15465891
  3. Hydrogen peroxide increases the activity of rat sympathetic preganglionic neurons in vivo and in vitro.
    Neuroscience. 2003;121(3):641-7 PMID: 14568024
  4. Subtypes of vagal afferent C-fibres in guinea-pig lungs.
    J Physiol. 2004 May 1;556(Pt 3):905-17 PMID: 14978204
  5. Prevention of granulocyte-mediated oxidant lung injury in rats by a hydroxyl radical scavenger, dimethylthiourea.
    J Clin Invest. 1984 Oct;74(4):1456-64 PMID: 6090504
  6. Stimulation of vagal pulmonary C-fibers by a single breath of cigarette smoke in dogs.
    J Appl Physiol (1985). 1989 May;66(5):2032-8 PMID: 2568354
  7. Hydrogen peroxide in the lung parenchyma stimulates vagally mediated phrenic activity.
    Chest. 1999 Nov;116(5):1365-8 PMID: 10559101
  8. Protective and defensive airway reflexes evoked by nasal exposure to wood smoke in anesthetized rats.
    J Appl Physiol (1985). 2000 Mar;88(3):863-70 PMID: 10710380
  9. Vagal and mediator mechanisms underlying the tachypnea caused by pulmonary air embolism in dogs.
    J Appl Physiol (1985). 2000 Apr;88(4):1247-53 PMID: 10749814
  10. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):6155-60 PMID: 10823958
  11. Chemotransduction properties of nodose ganglion cardiac afferent neurons in guinea pigs.
    Am J Physiol Regul Integr Comp Physiol. 2000 Aug;279(2):R433-9 PMID: 10938229
  12. Evidence for P(2)-purinoceptors contribution in H(2)O(2)-induced contraction of rat aorta in the absence of endothelium.
    Cardiovasc Res. 2000 Aug 18;47(3):574-85 PMID: 10963730
  13. Actions of reactive oxygen species on AH/type 2 myenteric neurons in guinea pig distal colon.
    Am J Physiol Gastrointest Liver Physiol. 2000 Nov;279(5):G893-902 PMID: 11052985
  14. Afferent properties and reflex functions of bronchopulmonary C-fibers.
    Respir Physiol. 2001 Mar;125(1-2):47-65 PMID: 11240152
  15. ATP affects both axons and Schwann cells of unmyelinated C fibres.
    Pain. 2001 Jun;92(3):343-50 PMID: 11376907
  16. Potentiation of capsaicin receptor activity by metabotropic ATP receptors as a possible mechanism for ATP-evoked pain and hyperalgesia.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6951-6 PMID: 11371611
  17. P2X receptors in peripheral neurons.
    Prog Neurobiol. 2001 Oct;65(2):107-34 PMID: 11403876
  18. Sensitivity of vagal afferent endings to chemical irritants in the rat lung.
    Respir Physiol. 2001 Sep;127(2-3):113-24 PMID: 11504584
  19. Exhaled nitric oxide and hydrogen peroxide in patients with chronic obstructive pulmonary disease: effects of inhaled beclomethasone.
    Am J Respir Crit Care Med. 2001 Sep 15;164(6):1012-5 PMID: 11587988
  20. Elevated concentrations of exhaled hydrogen peroxide in asthmatic patients.
    Chest. 2001 Oct;120(4):1136-9 PMID: 11591550
  21. Pharmacology of airway afferent nerve activity.
    Respir Res. 2001;2(4):234-44 PMID: 11686889
  22. Cell damage excites nociceptors through release of cytosolic ATP.
    Pain. 2002 Jan;95(1-2):41-7 PMID: 11790466
  23. Stimulation of pulmonary vagal C-fibres by anandamide in anaesthetized rats: role of vanilloid type 1 receptors.
    J Physiol. 2002 Mar 15;539(Pt 3):947-55 PMID: 11897863
  24. Protection against tissue damage in vivo by desferrioxamine: what is its mechanism of action?
    Free Radic Biol Med. 1989;7(6):645-51 PMID: 2695408
  25. Inhibitory effect of gas phase cigarette smoke on breathing: role of hydroxyl radical.
    Respir Physiol. 1990 Nov;82(2):227-38 PMID: 1963698
  26. Air embolism-induced lung injury in isolated rat lungs.
    J Appl Physiol (1985). 1992 Apr;72(4):1235-42 PMID: 1592709
  27. Biological effects of cigarette smoke, wood smoke, and the smoke from plastics: the use of electron spin resonance.
    Free Radic Biol Med. 1992 Dec;13(6):659-76 PMID: 1334034
  28. Activation of ischemia- and reperfusion-sensitive abdominal visceral C fiber afferents. Role of hydrogen peroxide and hydroxyl radicals.
    Circ Res. 1993 Jun;72(6):1266-75 PMID: 8388323
  29. Activation of cardiac vagal afferents by oxygen-derived free radicals in rats.
    Circ Res. 1994 May;74(5):895-903 PMID: 8156636
  30. Activation of cardiac vagal afferents in ischemia and reperfusion. Prostaglandins versus oxygen-derived free radicals.
    Circ Res. 1994 May;74(5):904-11 PMID: 8156637
  31. Capsazepine abolishes pulmonary chemoreflexes induced by capsaicin in anesthetized rats.
    J Appl Physiol (1985). 1994 May;76(5):1848-55 PMID: 8063640
  32. A new class of ligand-gated ion channel defined by P2x receptor for extracellular ATP.
    Nature. 1994 Oct 6;371(6497):516-9 PMID: 7523951
  33. Endotoxin-induced hydrogen peroxide production in intact pulmonary circulation of rat.
    Am J Respir Crit Care Med. 1995 Jul;152(1):348-54 PMID: 7599844
  34. Electrophysiological properties of P2X-purinoceptors in rat superior cervical, nodose and guinea-pig coeliac neurones.
    J Physiol. 1995 Apr 15;484 ( Pt 2):385-95 PMID: 7602533
  35. Effects of capsazepine against capsaicin- and proton-evoked excitation of single airway C-fibres and vagus nerve from the guinea-pig.
    Neuroscience. 1995 Aug;67(3):741-52 PMID: 7675200
  36. Ischemia- and reperfusion-sensitive cardiac sympathetic afferents: influence of H2O2 and hydroxyl radicals.
    Am J Physiol. 1995 Sep;269(3 Pt 2):H888-901 PMID: 7573532
  37. 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
  38. Early events in free radical-mediated damage of isolated nerve terminals: effects of peroxides on membrane potential and intracellular Na+ and Ca2+ concentrations.
    J Neurochem. 1996 May;66(5):2057-66 PMID: 8780036
  39. H2O2 sensitivity of afferent splanchnic C fiber units in vitro.
    J Neurophysiol. 1996 Jul;76(1):371-80 PMID: 8836231
  40. Cardiac vagal afferent stimulation by free radicals during ischaemia and reperfusion.
    Clin Exp Pharmacol Physiol. 1996 Aug;23(8):700-8 PMID: 8886494
  41. Alteration in cardiac sarcolemmal ATP receptors by oxyradicals.
    Ann N Y Acad Sci. 1996 Sep 30;793:1-12 PMID: 8906151
  42. Mechanisms of stimulation of vagal pulmonary C fibers by pulmonary air embolism in dogs.
    J Appl Physiol (1985). 1997 Mar;82(3):765-71 PMID: 9074961
  43. Involvement of hydroxyl radical in the immediate ventilatory responses to inhaled wood smoke in rats.
    Respir Physiol. 1997 Jan;107(1):1-13 PMID: 9089889
  44. Reflex apneic response evoked by laryngeal exposure to wood smoke in rats: neural and chemical mechanisms.
    J Appl Physiol (1985). 1997 Sep;83(3):723-30 PMID: 9292456
  45. Immunohistochemical study of the P2X2 and P2X3 receptor subunits in rat and monkey sensory neurons and their central terminals.
    Neuropharmacology. 1997 Sep;36(9):1229-42 PMID: 9364478
  46. Stimulation of vagal pulmonary C fibers by inhaled wood smoke in rats.
    J Appl Physiol (1985). 1998 Jan;84(1):30-6 PMID: 9451614
  47. Stimulation of pulmonary rapidly adapting receptors by inhaled wood smoke in rats.
    J Physiol. 1998 Apr 15;508 ( Pt 2):597-607 PMID: 9508820
  48. Capsaicin receptors mediate free radical-induced activation of cardiac afferent endings.
    Cardiovasc Res. 1998 May;38(2):348-55 PMID: 9709395
  49. Attenuation of ischemia-induced activation of cardiac sympathetic afferents following brief myocardial ischemia in cats.
    J Auton Nerv Syst. 1998 Jun 30;71(1):28-36 PMID: 9722192
  50. Receptors for purines and pyrimidines.
    Pharmacol Rev. 1998 Sep;50(3):413-92 PMID: 9755289
  51. Ion channels of nociception.
    Annu Rev Physiol. 1999;61:835-56 PMID: 10099712
  52. Effects of various reactive oxygen species on the guinea pig trachea and its epithelium.
    Jpn J Pharmacol. 2002 Mar;88(3):270-8 PMID: 11949881
  53. Antioxidant responses to oxidant-mediated lung diseases.
    Am J Physiol Lung Cell Mol Physiol. 2002 Aug;283(2):L246-55 PMID: 12114185
  54. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1.
    Nat Neurosci. 2002 Sep;5(9):856-60 PMID: 12161756
  55. Mechanisms of acid-induced activation of airway afferent nerve fibres in guinea-pig.
    J Physiol. 2002 Sep 1;543(Pt 2):591-600 PMID: 12205192
  56. A role for TRPV1 in bradykinin-induced excitation of vagal airway afferent nerve terminals.
    J Pharmacol Exp Ther. 2003 Mar;304(3):1275-9 PMID: 12604706
  57. Afferent vagal pathways mediating respiratory reflexes evoked by ROS in the lungs of anesthetized rats.
    J Appl Physiol (1985). 2003 May;94(5):1987-98 PMID: 12524382
  58. Ca2+ transient evoked by chemical stimulation is enhanced by PGE2 in vagal sensory neurons: role of cAMP/PKA signaling pathway.
    J Neurophysiol. 2003 Apr;89(4):1985-93 PMID: 12612039
  59. The co-expression of VR1 and VRL-1 in the rat vagal sensory ganglia.
    Brain Res. 2003 Aug 8;980(2):293-6 PMID: 12867271
  60. Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites.
    Eur J Neurosci. 1999 Mar;11(3):946-58 PMID: 10103088
  61. A capsaicin-receptor homologue with a high threshold for noxious heat.
    Nature. 1999 Apr 1;398(6726):436-41 PMID: 10201375
  62. Vanilloid (Capsaicin) receptors and mechanisms.
    Pharmacol Rev. 1999 Jun;51(2):159-212 PMID: 10353985
  63. Excitatory effect of P2X receptor activation on mesenteric afferent nerves in the anaesthetised rat.
    J Physiol. 1999 Oct 15;520 Pt 2:551-63 PMID: 10523422
  64. Bronchopulmonary afferent nerves.
    Respirology. 2003 Sep;8(3):291-301 PMID: 14528878
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2005-06-01
Epub
2005-00-31
Pages
563-78
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1464522
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]