Mediator mechanisms involved in TRPV1, TRPA1 and P2X receptor-mediated sensory transduction of pulmonary ROS by vagal lung C-fibers in rats

Respiratory Physiology and Neurobiology

Volumn 189, Issue 1, 2013, Pages 1-9

  Lin, Yu Jung ^a   Hsu, Hsao Hsun ^b   Ruan, Ting ^c,d   Kou, Yu Ru ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^d FU JEN CATHOLIC UNIVERSITY   (Taiwan)

Author keywords

ATP; Cyclooxygenase metabolites; P2X receptors; TRPA1 receptors; TRPV1 receptors; Vagal lung C fibers

Indexed keywords

ADENOSINE DEAMINASE; APYRASE; CALCIUM CHANNEL BLOCKING AGENT; CAPSAICIN; CAPSAZEPINE; DRUG METABOLITE; INDOMETACIN; N (4 ISOPROPYLPHENYL) 2 (1,2,3,6 TETRAHYDRO 1,3 DIMETHYL 2,6 DIOXO 7H PURIN 7 YL)ACETAMIDE; NORDIHYDROGUAIARETIC ACID; PROSTAGLANDIN SYNTHASE INHIBITOR; PURINERGIC P2X RECEPTOR ANTAGONIST; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; REACTIVE OXYGEN METABOLITE; VANILLOID RECEPTOR 1 ANTAGONIST;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; MALE; MEDIATOR; METABOLITE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ATP; CYCLOOXYGENASE METABOLITES; P2X RECEPTORS; TRPA1 RECEPTORS; TRPV1 RECEPTORS; VAGAL LUNG C-FIBERS;

ACTION POTENTIALS; ADENOSINE TRIPHOSPHATE; ANIMALS; ENZYME-LINKED IMMUNOSORBENT ASSAY; LUNG; MALE; MECHANOTRANSDUCTION, CELLULAR; NERVE FIBERS, UNMYELINATED; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, PURINERGIC P2X; TRPC CATION CHANNELS; TRPV CATION CHANNELS; VAGUS NERVE;

EID: 84881262357     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2013.06.021     Document Type: Article

References (34)

1. Ahmad S., Ahmad A., Ghosh M., Leslie C.C., White C.W. Extracellular ATP-mediated signaling for survival in hyperoxia-induced oxidative stress. J. Biol. Chem. 2004, 279:16317-16325.
2. Bessac B.F., Sivula M., von Hehn C.A., Escalera J., Cohn L., Jordt S.E. TRPA1 is a major oxidant sensor in murine airway sensory neurons. J. Clin. Invest. 2008, 118:1899-1910.
3. Carr M.J., Kollarik M., Meeker S.N., Undem B.J. A role for TRPV1 in bradykinin-induced excitation of vagal airway afferent nerve terminals. J. Pharmacol. Exp. Ther. 2003, 304:1275-1279.
4. 2 in pulmonary endothelium. Am. J. Physiol. 1989, 257:L430-L437.
5. Chen M.J., Chiang L.Y., Lai Y.L. Reactive oxygen species and substance P in monocrotaline-induced pulmonary hypertension. Toxicol. Appl. Pharmacol. 2001, 171:165-173.
6. Cook S.P., McCleskey E.W. Cell damage excites nociceptors through release of cytosolic ATP. Pain 2002, 95:41-47.
7. Emelyanov A., Fedoseev G., Abulimity A., Rudinski K., Fedoulov A., Karabanov A., Barnes P.J. Elevated concentrations of exhaled hydrogen peroxide in asthmatic patients. Chest 2001, 120:1136-1139.
8. Ferreira I.M., Hazari M.S., Gutierrez C., Zamel N., Chapman K.R. Exhaled nitric oxide and hydrogen peroxide in patients with chronic obstructive pulmonary disease: effects of inhaled beclomethasone. Am. J. Respir. Crit. Care Med. 2001, 164:1012-1015.
9. Franco-Cereceda A., Kallner G., Lundberg J.M. Cyclo-oxygenase products released by low pH have capsaicin-like actions on sensory nerves in the isolated guinea pig heart. Cardiovasc. Res. 1994, 28:365-369.
10. Gregus A.M., Doolen S., Dumlao D.S., Buczynski M.W., Takasusuki T., Fitzsimmons B.L., Hua X.Y., Taylor B.K., Dennis E.A., Yaksh T.L. Spinal 12-lipoxygenase-derived hepoxilin A3 contributes to inflammatory hyperalgesia via activation of TRPV1 and TRPA1 receptors. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:6721-6726.
11. Hwang S.W., Cho H., Kwak J., Lee S.Y., Kang C.J., Jung J., Cho S., Min K.H., Suh Y.G., Kim D., Oh U. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:6155-6160.
12. Irnich D., Burgstahler R., Bostock H., Grafe P. ATP affects both axons and Schwann cells of unmyelinated C fibres. Pain 2001, 92:343-350.
13. Lai C.J., Kou Y.R. Stimulation of vagal pulmonary C fibers by inhaled wood smoke in rats. J. Appl. Physiol. 1998, 84:30-36.
14. Lazarowski E.R., Boucher R.C., Harden T.K. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 2003, 64:785-795.
15. Lee L.Y., Lundberg J.M. Capsazepine abolishes pulmonary chemoreflexes induced by capsaicin in anesthetized rats. J. Appl. Physiol. 1994, 76:1848-1855.
16. Lee L.Y., Pisarri T.E. Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir. Physiol. 2001, 125:47-65.
17. Lin Y.S., Hsu C.C., Bien M.Y., Hsu H.C., Weng H.T., Kou Y.R. Activations of TRPA1 and P2X receptors are important in ROS-mediated stimulation of capsaicin-sensitive lung vagal afferents by cigarette smoke in rats. J. Appl. Physiol. 2010, 108:1293-1303.
18. Liu B.Y., Tsai T.L., Ho C.Y., Lu S.H., Lai C.J., Kou Y.R. Role of TRPA1 and TRPV1 in the ROS-dependent sensory irritation of superior laryngeal capsaicin-sensitive afferents by cigarette smoke in anesthetized rats. Pulm. Pharmacol. Ther. 2013, 26:364-372.
19. Matyas S., Pucovsky V., Bauer V. Effects of various reactive oxygen species on the guinea pig trachea and its epithelium. Jpn. J. Pharmacol. 2002, 88:270-278.
20. McCleskey E.W., Gold M.S. Ion channels of nociception. Annu. Rev. Physiol. 1999, 61:835-856.
21. Minamiya Y., Abo S., Kitamura M., Izumi K., Kimura Y., Tozawa K., Saito S. Endotoxin-induced hydrogen peroxide production in intact pulmonary circulation of rat. Am. J. Respir. Crit. Care Med. 1995, 152:348-354.
22. Nassenstein C., Kwong K., Taylor-Clark T., Kollarik M., Macglashan D.M., Braun A., Undem B.J. Expression and function of the ion channel TRPA1 in vagal afferent nerves innervating mouse lungs. J. Physiol. 2008, 586:1595-1604.
23. Rahman I., MacNee W. Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease. Am. J. Physiol. 1999, 277:L1067-L1088.
24. Ruan T., Ho C.Y., Kou Y.R. Afferent vagal pathways mediating respiratory reflexes evoked by ROS in the lungs of anesthetized rats. J. Appl. Physiol. 2003, 94:1987-1998.
25. Ruan T., Lin Y.S., Lin K.S., Kou Y.R. Sensory transduction of pulmonary reactive oxygen species by capsaicin-sensitive vagal lung afferent fibres in rats. J. Physiol. 2005, 565:563-578.
26. Ruan T., Lin Y.S., Lin K.S., Kou Y.R. Mediator mechanisms involved in TRPV1 and P2X receptor-mediated ROS-evoked bradypneic reflex in anesthetized rats. J. Appl. Physiol. 2006, 101:644-654.
27. Schwiebert E.M., Zsembery A. Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta 2003, 1615:7-32.
28. Shen M.Y., Luo Y.L., Yang C.H., Ruan T., Lai C.J. Hypersensitivity of lung vagal C fibers induced by acute intermittent hypoxia in rats: role of reactive oxygen species and TRPA1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 303:R1175-R1185.
29. Sun S.Y., Wang W., Schultz H.D. Activation of cardiac afferents by arachidonic acid: relative contributions of metabolic pathways. Am. J. Physiol. Heart Circ. Physiol. 2001, 281:H93-H104.
30. Taylor-Clark T.E., Undem B.J. Transduction mechanisms in airway sensory nerves. J. Appl. Physiol. 2006, 101:950-959.
31. Taylor-Clark T.E., Undem B.J., Macglashan D.W., Ghatta S., Carr M.J., McAlexander M.A Prostaglandin-induced activation of nociceptive neurons via direct interaction with transient receptor potential A1 (TRPA1). Mol. Pharmacol. 2008, 73:274-281.
32. Taylor-Clark T.E., Undem B.J. Ozone activates airway nerves via the selective stimulation of TRPA1 ion channels. J. Physiol. 2010, 588:423-433.
33. Taylor-Clark T.E., Undem B.J. Sensing pulmonary oxidative stress by lung vagal afferents. Respir. Physiol. Neurobiol. 2011, 178:406-413.
34. Undem B.J., Nassenstein C. Airway nerves and dyspnea associated with inflammatory airway disease. Respir. Physiol. Neurobiol. 2009, 167:36-44.