Role of TRPV1 in inflammation-induced airway hypersensitivity

Current Opinion in Pharmacology

Volumn 9, Issue 3, 2009, Pages 243-249

  Lee, Lu Yuan ^a   Gu, Qihai ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCATION; PROTEINASE ACTIVATED RECEPTOR 2; VANILLOID RECEPTOR 1;

ACUTE DISEASE; ALLERGIC ASTHMA; BREATHING MECHANICS; CHRONIC INFLAMMATION; HUMAN; LUNG LAVAGE; MUSCLE EXCITATION; NODOSE GANGLION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; TEMPERATURE MEASUREMENT;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; NEUROFILAMENT PROTEINS; NODOSE GANGLION; RESPIRATORY HYPERSENSITIVITY; SENSORY RECEPTOR CELLS; TRPV CATION CHANNELS;

EID: 65749107679     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coph.2009.02.002     Document Type: Review

References (58)

1. Nilius B., Owsianik G., Voets T., and Peters J.A. Transient receptor potential cation channels in disease. Physiol Rev 87 (2007) 165-217
2. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
3. Caterina M.J., and Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24 (2001) 487-517
4. Geppetti P., Materazzi S., and Nicoletti P. The transient receptor potential vanilloid 1: role in airway inflammation and disease. Eur J Pharmacol 533 (2006) 207-214. This is a comprehensive review of the possible involvement of TRPV1 in various airway diseases and the putative endogenous TRPV1 activators in the airways.
5. Jia Y., and Lee L.Y. Role of TRPV receptors in respiratory diseases. Biochim Biophys Acta 1772 (2007) 915-927. A comprehensive review of the expression and activators/modulators of TRPV1 and TRPV4 in the lung, and the potential role of these channels in the pathogenesis of various acute and chronic airway diseases.
6. Gunthorpe M.J., and Szallasi A. Peripheral TRPV1 receptors as targets for drug development: new molecules and mechanisms. Curr Pharm Des 14 (2008) 32-41
7. Takemura M., Quarcoo D., Niimi A., Dinh Q.T., Geppetti P., Fischer A., Chung K.F., and Groneberg D.A. Is TRPV1 a useful target in respiratory diseases?. Pulm Pharmacol Ther 21 (2008) 833-839
8. Ho C.Y., Gu Q., Lin Y.S., and Lee L.Y. Sensitivity of vagal afferent endings to chemical irritants in the rat lung. Respir Physiol 127 (2001) 113-124
9. Watanabe N., Horie S., Michael G.J., Keir S., Spina D., Page C.P., and Priestley J.V. Immunohistochemical co-localization of transient receptor potential vanilloid (TRPV)1 and sensory neuropeptides in the guinea-pig respiratory system. Neuroscience 141 (2006) 1533-1543
10. De Swert K.O., and Joos G.F. Extending the understanding of sensory neuropeptides. Eur J Pharmacol 533 (2006) 171-181
11. Adriaensen D., Timmermans J.P., Brouns I., Berthoud H.R., Neuhuber W.L., and Scheuermann D.W. Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: an anterograde tracing and confocal microscopy study in adult rats. Cell Tissue Res 293 (1998) 395-405
12. Lee L.Y., and Pisarri T.E. Afferent properties and reflex functions of bronchopulmonary C-fibers. Respir Physiol 125 (2001) 47-65
13. Lee L.Y., and Undem B.J. Brochopulmonary vagal sensory nerves. In: Undem B.J., and Weinreich D. (Eds). Advances in Vagal Afferent Neurobiology (2005), CRC Press 279-313 (Chapter 11)
14. O'Connell F., Thomas V.E., Studham J.M., Pride N.B., and Fuller R.W. Capsaicin cough sensitivity increases during upper respiratory infection. Respir Med 90 (1996) 279-286
15. Doherty M.J., Mister R., Pearson M.G., and Calverley P.M. Capsaicin responsiveness and cough in asthma and chronic obstructive pulmonary disease. Thorax 55 (2000) 643-649
16. McLeod R.L., Fernandez X., Correll C.C., Phelps T.P., Jia Y., Wang X., and Hey J.A. TRPV1 antagonists attenuate antigen-provoked cough in ovalbumin sensitized guinea pigs. Cough 2 (2006) 10
17. Groneberg D.A., Niimi A., Dinh Q.T., Cosio B., Hew M., Fischer A., and Chung K.F. Increased expression of transient receptor potential vanilloid-1 in airway nerves of chronic cough. Am J Respir Crit Care Med 170 (2004) 1276-1280
18. Zhang G., Lin R.L., Wiggers M.E., Snow D.M., and Lee L.Y. Altered expression of TRPV1 and sensitivity to capsaicin in pulmonary myelinated afferents following chronic airway inflammation in the rat. J Physiol 586 (2008) 5771-5786. Chronic airway inflammation induced by ovalbumin sensitization generated a pronounced overexpression of TRPV1 in neurofilament-positive pulmonary sensory neurons in nodose ganglia and upregulated the capsaicin sensitivity in myelinated bronchopulmonary afferents.
19. Piacentini G.L., Peroni D., Crestani E., Zardini F., Bodini A., Costella S., and Boner A.L. Exhaled air temperature in asthma: methods and relationship with markers of disease. Clin Exp Allergy 37 (2007) 415-419. This is the first direct evidence indicating a distinctly higher airway temperature (average 2.7°C) in asthmatic patients than that in healthy individuals.
20. Paredi P., Kharitonov S.A., and Barnes P.J. Faster rise of exhaled breath temperature in asthma: a novel marker of airway inflammation?. Am J Respir Crit Care Med 165 (2002) 181-184
21. Dhaka A., Viswanath V., and Patapoutian A. TRP ion channels and temperature sensation. Annu Rev Neurosci 29 (2006) 135-161
22. Ni D., Gu Q., Hu H.Z., Gao N., Zhu M.X., and Lee L.Y. Thermal sensitivity of isolated vagal pulmonary sensory neurons: role of transient receptor potential vanilloid receptors. Am J Physiol Regul Integr Comp Physiol 291 (2006) R541-R550. This study characterized the thermal-sensitive properties of pulmonary sensory neurons, and demonstrated that increasing temperature to >34.4°C exerted a stimulatory effect on these neurons via activation of TRPVs.
23. Ni D., and Lee L.Y. Effect of increasing temperature on TRPV1-mediated responses in isolated rat pulmonary sensory neurons. Am J Physiol Lung Cell Mol Physiol 294 (2008) L563-L571. Increasing temperature within the physiological range generated a potentiating effect on the response to TRPV1 activators in pulmonary sensory neurons.
24. Ni D., and Lee L.Y. A lack of potentiating effect of increasing temperature on the responses to chemical activators in vagal sensory neurons isolated from TRPV1-null mice. Am J Physiol Lung Cell Mol Physiol 295 (2008) L897-L904
25. Vlachova V., Teisinger J., Susankova K., Lyfenko A., Ettrich R., and Vyklicky L. Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J Neurosci 23 (2003) 1340-1350. This study provided convincing evidence that the structural basis of the thermal sensitivity of the TRPV1 resides in the distal half of the COOH-terminal of the receptor.
26. Voets T., Droogmans G., Wissenbach U., Janssens A., Flockerzi V., and Nilius B. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430 (2004) 748-754. This study clearly demonstrated that an increase in temperature shifted the TRPV1 activation curve toward physiological membrane potential, and suggested that the small gating charge of the TRPV1 channel is a crucial factor for the voltage shift.
27. Nilius B., Talavera K., Owsianik G., Prenen J., Droogmans G., and Voets T. Gating of TRP channels: a voltage connection?. J Physiol 567 (2005) 35-44
28. Ossovskaya V.S., and Bunnett N.W. Protease-activated receptors: contribution to physiology and disease. Physiol Rev 84 (2004) 579-621
29. Reed C.E., and Kita H. The role of protease activation of inflammation in allergic respiratory diseases. J Allergy Clin Immunol 114 (2004) 997-1008
30. Sokolova E., and Reiser G. A novel therapeutic target in various lung diseases: airway proteases and protease-activated receptors. Pharmacol Ther 115 (2007) 70-83
31. Ramachandran R., and Hollenberg M.D. Proteinases and signalling: pathophysiological and therapeutic implications via PARs and more. Br J Pharmacol 153 Suppl 1 (2008) S263-S282
32. Oikonomopoulou K., Hansen K.K., Saifeddine M., Tea I., Blaber M., Blaber S.I., Scarisbrick I., Andrade-Gordon P., Cottrell G.S., Bunnett N.W., et al. Proteinase-activated receptors, targets for kallikrein signaling. J Biol Chem 281 (2006) 32095-32112
33. Knight D.A., Lim S., Scaffidi A.K., Roche N., Chung K.F., Stewart G.A., and Thompson P.J. Protease-activated receptors in human airways: upregulation of PAR-2 in respiratory epithelium from patients with asthma. J Allergy Clin Immunol 108 (2001) 797-803
34. Ricciardolo F.L., Steinhoff M., Amadesi S., Guerrini R., Tognetto M., Trevisani M., Creminon C., Bertrand C., Bunnett N.W., Fabbri L.M., et al. Presence and bronchomotor activity of protease-activated receptor-2 in guinea pig airways. Am J Respir Crit Care Med 161 (2000) 1672-1680
35. Barrios V.E., Jarosinski M.A., and Wright C.D. Proteinase-activated receptor-2 mediates hyperresponsiveness in isolated guinea pig bronchi. Biochem Pharmacol 66 (2003) 519-525
36. Su X., Camerer E., Hamilton J.R., Coughlin S.R., and Matthay M.A. Protease-activated receptor-2 activation induces acute lung inflammation by neuropeptide-dependent mechanisms. J Immunol 175 (2005) 2598-2605
37. Gu Q., and Lee L.Y. Hypersensitivity of pulmonary chemosensitive neurons induced by activation of protease-activated receptor-2 in rats. J Physiol 574 (2006) 867-876
38. Gatti R., Andre E., Amadesi S., Dinh T.Q., Fischer A., Bunnett N.W., Harrison S., Geppetti P., and Trevisani M. Protease-activated receptor-2 activation exaggerates TRPV1-mediated cough in guinea pigs. J Appl Physiol 101 (2006) 506-511
39. Kauffman H.F., Tomee J.F., van de Riet M.A., Timmerman A.J., and Borger P. Protease-dependent activation of epithelial cells by fungal allergens leads to morphologic changes and cytokine production. J Allergy Clin Immunol 105 (2000) 1185-1193
40. Lan R.S., Knight D.A., Stewart G.A., and Henry P.J. Role of PGE(2) in protease-activated receptor-1, -2 and -4 mediated relaxation in the mouse isolated trachea. Br J Pharmacol 132 (2001) 93-100
41. 2-induced sensitization of TRPV1.
42. Dai Y., Wang S., Tominaga M., Yamamoto S., Fukuoka T., Higashi T., Kobayashi K., Obata K., Yamanaka H., and Noguchi K. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J Clin Invest 117 (2007) 1979-1987
43. Grant A.D., Cottrell G.S., Amadesi S., Trevisani M., Nicoletti P., Materazzi S., Altier C., Cenac N., Zamponi G.W., Bautista-Cruz F., et al. Protease-activated receptor 2 sensitizes the transient receptor potential vanilloid 4 ion channel to cause mechanical hyperalgesia in mice. J Physiol 578 (2007) 715-733
44. Ahern G.P., Brooks I.M., Miyares R.L., and Wang X.B. Extracellular cations sensitize and gate capsaicin receptor TRPV1 modulating pain signaling. J Neurosci 25 (2005) 5109-5116
45. Ahern G.P., Wang X., and Miyares R.L. Polyamines are potent ligands for the capsaicin receptor TRPV1. J Biol Chem 281 (2006) 8991-8995. These authors show that polyamines directly activate TRPV1 in a charge-dependent manner and sensitize this receptor at a low concentration. Their experiments with TRPV1 mutants identified extracellular acidic residues (D646N and E648A) critical for polyamine regulation.
46. Kurosawa M., Shimizu Y., Tsukagoshi H., and Ueki M. Elevated levels of peripheral-blood, naturally occurring aliphatic polyamines in bronchial asthmatic patients with active symptoms. Allergy 47 (1992) 638-643
47. Gleich G.J. Mechanisms of eosinophil-associated inflammation. J Allergy Clin Immunol 105 (2000) 651-663
48. Bousquet J., Chanez P., Lacoste J.Y., Barneon G., Ghavanian N., Enander I., Venge P., Ahlstedt S., Simony-Lafontaine J., Godard P., et al. Eosinophilic inflammation in asthma. N Engl J Med 323 (1990) 1033-1039
49. Gu Q., Wiggers M.E., Gleich G.J., and Lee L.Y. Sensitization of isolated rat vagal pulmonary sensory neurons by eosinophil-derived cationic proteins. Am J Physiol Lung Cell Mol Physiol 294 (2008) L544-L552
50. Mitchell J.E., Campbell A.P., New N.E., Sadofsky L.R., Kastelik J.A., Mulrennan S.A., Compton S.J., and Morice A.H. Expression and characterization of the intracellular vanilloid receptor (TRPV1) in bronchi from patients with chronic cough. Exp Lung Res 31 (2005) 295-306
51. Watanabe N., Horie S., Spina D., Michael G.J., Page C.P., and Priestley J.V. Immunohistochemical localization of transient receptor potential vanilloid subtype 1 in the trachea of ovalbumin-sensitized Guinea pigs. Int Arch Allergy Immunol 146 Suppl 1 (2008) 28-32. This study demonstrated that TRPV1-immunoreactive axons were more densely stained, and increased in number in the tracheal epithelium of ovalbumin-sensitized guinea pigs.
52. Winter J. Brain derived neurotrophic factor, but not nerve growth factor, regulates capsaicin sensitivity of rat vagal ganglion neurones. Neurosci Lett 241 (1998) 21-24
53. Winston J., Toma H., Shenoy M., and Pasricha P.J. Nerve growth factor regulates VR-1 mRNA levels in cultures of adult dorsal root ganglion neurons. Pain 89 (2001) 181-186
54. Anand U., Otto W.R., Casula M.A., Day N.C., Davis J.B., Bountra C., Birch R., and Anand P. The effect of neurotrophic factors on morphology, TRPV1 expression and capsaicin responses of cultured human DRG sensory neurons. Neurosci Lett 399 (2006) 51-56
55. Zhang X., Huang J., and McNaughton P.A. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J 24 (2005) 4211-4223
56. Chuang H.H., Prescott E.D., Kong H., Shields S., Jordt S.E., Basbaum A.I., Chao M.V., and Julius D. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411 (2001) 957-962
57. Bonini S., Lambiase A., Bonini S., Angelucci F., Magrini L., Manni L., and Aloe L. Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma. Proc Natl Acad Sci U S A 93 (1996) 10955-10960
58. Lommatzsch M., Schloetcke K., Klotz J., Schuhbaeck K., Zingler D., Zingler C., Schulte-Herbruggen O., Gill H., Schuff-Werner P., and Virchow J.C. Brain-derived neurotrophic factor in platelets and airflow limitation in asthma. Am J Respir Crit Care Med 171 (2005) 115-120