Regulation of acid signaling in rat pulmonary sensory neurons by protease-activated receptor-2

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 298, Issue 3, 2010, Pages

  Gu, Qihai ^a   Lee, Lu Yuan ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Acid sensing ion channels; Airway inflammation; Transient receptor potential vanilloid receptor 1

Indexed keywords

MESSENGER RNA; PROTEINASE ACTIVATED RECEPTOR 2; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1;

ACIDIFICATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; EVOKED RESPONSE; GENE EXPRESSION; LUNG ALVEOLUS CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SENSORY NERVE CELL;

ACIDS; ANIMALS; CALCIUM SIGNALING; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; ION CHANNEL GATING; LUNG; NERVE TISSUE PROTEINS; OLIGOPEPTIDES; PROTEIN KINASE C; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, PAR-2; RNA, MESSENGER; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SODIUM CHANNELS; TETRADECANOYLPHORBOL ACETATE; TRPV CATION CHANNELS; TYPE C PHOSPHOLIPASES; UP-REGULATION; VAGUS NERVE;

EID: 77249104011     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00381.2009     Document Type: Article

References (45)

1. Alvarez de la Rosa D, Zhang P, Shao D, White F, Canessa CM. Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc Natl Acad Sci USA 99: 2326-2331, 2002.
2. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, Manni C, Geppetti P, McRoberts JA, Ennes H, Davis JB, Mayer EA, Bunnett NW. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24: 4300-4312, 2004.
3. Asokananthan N, Graham PT, Stewart DJ, Bakker AJ, Eidne KA, Thompson PJ, Stewart GA. House dust mite allergens induce proinflammatory cytokines from respiratory epithelial cells: the cysteine protease allergen, Der p1, activates protease-activated receptor (PAR)-2 and inactivates PAR-1. J Immunol 169: 4572-4578, 2002.
4. Barrios VE, Jarosinski MA, Wright CD. Proteinase-activated receptor-2 mediates hyperresponsiveness in isolated guinea pig bronchi. Biochem Pharmacol 66: 519-525, 2003.
5. Benson CJ, Sutherland SP. Toward an understanding of the molecules that sense myocardial ischemia. Ann NY Acad Sci 940: 96-109, 2001.
6. Benson CJ, Xie J, Wemmie JA, Price MP, Henss JM, Welsh MJ, Snyder PM. Heteromultimers of DEG/ENaC subunits form H+-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA 99: 2338-2343, 2002.
7. Cadiou H, Studer M, Jones NG, Smith ES, Ballard A, McMahon SB, McNaughton PA. Modulation of acid-sensing ion channel activity by nitric oxide. J Neurosci 27: 13251-13260, 2007.
8. Caterina MJ, Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24: 487-517, 2001.
9. Chambers LS, Black JL, Poronnik P, Johnson PR. Functional effects of protease-activated receptor-2 stimulation on human airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 281: L1369-L1378, 2001.
10. Dai Y, Moriyama T, Higashi T, Togashi K, Kobayashi K, Yamanaka H, Tominaga M, Noguchi K. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 24: 4293-4299, 2004.
11. Fisher JT. The TRPV1 ion channel: implications for respiratory sensation and dyspnea. Respir Physiol Neurobiol 167: 45-52, 2009.
12. Geppetti P, Materazzi S, Nicoletti P. The transient receptor potential vanilloid 1: role in airway inflammation and disease. Eur J Pharmacol 533: 207-214, 2006.
13. Gu Q, Lee LY. Characterization of acid-signaling in rat vagal pulmonary sensory neurons. Am J Physiol Lung Cell Mol Physiol 291: L58-L65, 2006.
14. Gu Q, Lee LY. Hypersensitivity of pulmonary chemosensitive neurons induced by activation of protease-activated receptor-2 in rats. J Physiol 574: 867-876, 2006.
15. Gu Q, Lee LY. Effect of PAR2 activation on single TRPV1 channel activities in rat vagal pulmonary sensory neurons. Exp Physiol 94: 928-936, 2009.
16. Gu Q, Lim ME, Gleich GJ, Lee LY. Mechanisms of eosinophil major basic protein-evoked hyperexcitability of vagal pulmonary chemosensitive neurons. Am J Physiol Lung Cell Mol Physiol 296: L453-L461, 2009.
17. Hesselager M, Timmermann DB, Ahring PK. pH Dependency and desensitization kinetics of heterologously expressed combinations of acid-sensing ion channel subunits. J Biol Chem 279: 11006-11015, 2004.
18. Hughey RP, Bruns JB, Kinlough CL, Harkleroad KL, Tong Q, Carattino MD, Johnson JP, Stockand JD, Kleyman TR. Epithelial sodium channels are activated by furin-dependent proteolysis. J Biol Chem 279: 18111-18114, 2004.
19. Hunt JF, Fang K, Malik R, Snyder A, Malhotra N, Platts-Mills TA, Gaston B. Endogenous airway acidification. Implications for asthma pathophysiology. Am J Respir Crit Care Med 161: 694-699, 2000.
20. Jordt SE, Julius D. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108: 421-430, 2002.
21. Kawabata A, Oono Y, Yonezawa D, Hiramatsu K, Inoi N, Sekiguchi F, Honjo M, Hirofuchi M, Kanke T, Ishiwata H. 2-Furoyl-LIGRLNH2, a potent agonist for proteinase-activated receptor-2, as a gastric mucosal cytoprotective agent in mice. Br J Pharmacol 144: 212-219, 2005.
22. Kleyman TR, Carattino MD, Hughey RP. ENaC at the cutting edge: regulation of epithelial sodium channels by proteases. J Biol Chem 284: 20447-20451, 2009.
23. Knight DA, Lim S, Scaffidi AK, Roche N, Chung KF, Stewart GA, Thompson PJ. Protease-activated receptors in human airways: upregulation of PAR-2 in respiratory epithelium from patients with asthma. J Allergy Clin Immunol 108: 797-803, 2001.
24. Kodric M, Shah AN, Fabbri LM, Confalonieri M. An investigation of airway acidification in asthma using induced sputum: a study of feasibility and correlation. Am J Respir Crit Care Med 175: 905-910, 2007.
25. Kollarik M, Ru F, Undem BJ. Acid-sensitive vagal sensory pathways and cough. Pulm Pharmacol Ther 20: 402-411, 2007.
26. Kostikas K, Papatheodorou G, Ganas K, Psathakis K, Panagou P, Loukides S. pH in expired breath condensate of patients with inflammatory airways diseases. Am J Respir Crit Care Med 165: 1364-1370, 2002.
27. Krishtal O. The ASICs: signaling molecules? Modulators? Trends Neurosci 26: 477-483, 2003.
28. Lee LY. Respiratory sensations evoked by activation of bronchopulmonary C-fibers. Respir Physiol Neurobiol 167: 26-35, 2009.
29. Lee LY, Gu Q. Role of TRPV1 in inflammation-induced airway hypersensitivity. Curr Opin Pharmacol 9: 243-249, 2009.
30. Lee LY, Pisarri TE. Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir Physiol 125: 47-65, 2001.
31. Mantyh PW, Clohisy DR, Koltzenburg M, Hunt SP. Molecular mechanisms of cancer pain. Nat Rev Cancer 2: 201-209, 2002.
32. Ramachandran R, Hollenberg MD. Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br J Pharmacol 153: S263-S282, 2008.
33. Reed CE, Kita H. The role of protease activation of inflammation in allergic respiratory diseases. J Allergy Clin Immunol 114: 997-1008, 2004.
34. Reeh PW, Steen KH. Tissue acidosis in nociception and pain. Prog Brain Res 113: 143-151, 1996.
35. Ricciardolo FL, Gaston B, Hunt J. Acid stress in the pathology of asthma. J Allergy Clin Immunol 113: 610-619, 2004.
36. Ricciardolo FL, Steinhoff M, Amadesi S, Guerrini R, Tognetto M, Trevisani M, Creminon C, Bertrand C, Bunnett NW, Fabbri LM, Salvadori S, Geppetti P. Presence and bronchomotor activity of protease-activated receptor-2 in guinea pig airways. Am J Respir Crit Care Med 161: 1672-1680, 2000.
37. Schmidlin F, Amadesi S, Dabbagh K, Lewis DE, Knott P, Bunnett NW, Gater PR, Geppetti P, Bertrand C, Stevens ME. Protease-activated receptor 2 mediates eosinophil infiltration and hyperreactivity in allergic inflammation of the airway. J Immunol 169: 5315-5321, 2002.
38. Smith ES, Cadiou H, McNaughton PA. Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience 145: 686-698, 2007.
39. Sokolova E, Reiser G. A novel therapeutic target in various lung diseases: airway proteases and protease-activated receptors. Pharmacol Ther 115: 70-83, 2007.
40. Steen KH, Reeh PW, Anton F, Handwerker HO. Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci 12: 86-95, 1992.
41. Sun G, Stacey MA, Schmidt M, Mori L, Mattoli S. Interaction of mite allergens Der p3 and Der p9 with protease-activated receptor-2 expressed by lung epithelial cells. J Immunol 167: 1014-1021, 2001.
42. Waldmann R, Lazdunski M. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol 8: 418-424, 1998.
43. Welch JM, Simon SA, Reinhart PH. The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc Natl Acad Sci USA 97: 13889-13894, 2000.
44. Xie J, Price MP, Wemmie JA, Askwith CC, Welsh MJ. ASIC3 and ASIC1 mediate FMRFamide-related peptide enhancement of H+-gated currents in cultured dorsal root ganglion neurons. J Neurophysiol 89: 2459-2465, 2003.
45. Xiong ZG, Zhu XM, Chu XP, Minami M, Hey J, Wei WL, MacDonald JF, Wemmie JA, Price MP, Welsh MJ, Simon RP. Neuroprotection in ischemia: blocking calcium-permeable acid-sensing ion channels. Cell 118: 687-698, 2004.