Relative contributions of TRPA1 and TRPV1 channels in the activation of vagal bronchopulmonary C-fibres by the endogenous autacoid 4-oxononenal

Journal of Physiology

Volumn 586, Issue 14, 2008, Pages 3447-3459

  Taylor Clark, T E ^a   Mcalexander, M A ^b   Nassenstein, C ^a   Sheardown, S A ^c   Wilson, S ^c   Thornton, J ^c   Carr, M J ^b   Undem, B J ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GLAXOSMITHKLINE   (United States)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 OXONONENAL; AUTACOID; CALCIUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; VANILLOID RECEPTOR 1; ALKENE; AUTACOID 4 OXONONENAL; TACHYKININ; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HYPOTHESIS; INFLAMMATION; KNOCKOUT MOUSE; LUNG INNERVATION; MALE; MOUSE; NERVE ENDING; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VAGUS NERVE; ACTION POTENTIAL DURATION; BRONCHOPULMONARY C FIBER TERMINAL; CARBOXY TERMINAL SEQUENCE; CONCENTRATION (PARAMETERS); GUINEA PIG; LIPID PEROXIDATION; MOLECULAR IMAGING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE;

ACTION POTENTIALS; ALDEHYDES; ANIMALS; AUTACOIDS; CALCIUM; CALCIUM CHANNELS; CAPSAICIN; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIAL CELLS; GUINEA PIGS; HUMANS; LUNG; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS, AFFERENT; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPV CATION CHANNELS; VAGUS NERVE;

EID: 48949120476     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.153585     Document Type: Article

References (52)

1. Anderson MM, Hazen SL, Hsu FF & Heinecke JW (1997). Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to convert hydroxy-amino acids into glycolaldehyde, 2-hydroxypropanal, and acrolein. A mechanism for the generation of highly reactive α-hydroxy and α,β-unsaturated aldehydes by phagocytes at sites of inflammation. J Clin Invest 99, 424-432.
2. Andersson DA, Gentry C, Moss S & Bevan S (2008). Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J Neurosci 28, 2485-2494.
3. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ & Patapoutian A (2004). Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849-857.
4. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI & Julius D (2006). TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269-1282.
5. Blair IA (2006). Endogenous glutathione adducts. Curr Drug Metab 7, 853-872.
6. Boldogh I, Bacsi A, Choudhury BK, Dharajiya N, Alam R, Hazra TK, Mitra S, Goldblum RM & Sur S (2005). ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation. J Clin Invest 115, 2169-2179.
7. Bowler RP & Crapo JD (2002). Oxidative stress in allergic respiratory diseases. J Allergy Clin Immunol 110, 349-356.
8. Braun A, Lommatzsch M, Neuhaus-Steinmetz U, Quarcoo D, Glaab T, McGregor GP, Fischer A & Renz H (2004). Brain-derived neurotrophic factor (BDNF) contributes to neuronal dysfunction in a model of allergic airway inflammation. Br J Pharmacol 141, 431-440.
9. Carr MJ, Schechter NM & Undem BJ (2000). Trypsin-induced, neurokinin-mediated contraction of guinea pig bronchus. Am J Respir Crit Care Med 162, 1662-1667.
10. Carr MJ & Undem BJ (2001). Inflammation-induced plasticity of the afferent innervation of the airways. Environ Health Perspect 109, 567-571.
11. Carr MJ & Undem BJ (2003). Bronchopulmonary afferent nerves. Respirology 8, 291-301.
12. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD & Julius D (1997). The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 389, 816-824.
13. Coleridge JC & Coleridge HM (1984). Afferent vagal C fibre innervation of the lungs and airways and its functional significance. Rev Physiol Biochem Pharmacol 99, 1-110.
14. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P et al. (2000). Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405, 183-187.
15. Doorn JA & Petersen DR (2002). Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2-nonenal and 4-oxo-2-nonenal. Chem Res Toxicol 15, 1445-1450.
16. Ellis JL & Undem BJ (1994). Inhibition by capsazepine of resiniferatoxin- and capsaicin-induced contractions of guinea pig trachea. J Pharmacol Exp Ther 268, 85-89.
17. Esterbauer H, Schaur RJ & Zollner H (1991). Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11, 81-128.
18. Farooqui AA & Horrocks LA (2006). Phospholipase A2-generated lipid mediators in the brain: The good, the bad, and the ugly. Neuroscientist 12, 245-260.
19. Gilliland FD, Li YF, Saxon A & Diaz-Sanchez D (2004). Effect of glutathione-S-transferase M1 and P1 genotypes on xenobiotic enhancement of allergic responses: Randomised, placebo-controlled crossover study. Lancet 363, 119-125.
20. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260, 3440-3450.
21. Hayes P, Meadows HJ, Gunthorpe MJ, Harries MH, Duckworth DM, Cairns W et al. (2000). Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain 88, 205-215.
22. Hill K & Schaefer M (2007). TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine. J Biol Chem 282, 7145-7153.
23. Hinman A, Chuang HH, Bautista DM & Julius D (2006). TRP channel activation by reversible covalent modification. Proc Natl Acad Sci U S A 103, 19564-19568.
24. Imboden M, Rochat T, Brutsche MH, Schindler C, Downs SH, Gerbase MW, Berger W, Probst-Hensch NM & Sapaldia Team T (2007). Glutathione-S transferase genotype increases risk of progression from bronchial hyperresponsiveness to asthma in adults. Thorax 63, 322-328.
25. Ishii T, Matsuse T, Teramoto S, Matsui H, Miyao M, Hosoi T, Takahashi H, Fukuchi Y & Ouchi Y (1999). Glutathione S-transferase P1 (GSTP1) polymorphism in patients with chronic obstructive pulmonary disease. Thorax 54, 693-696.
26. Jian W, Lee SH, Mesaros C, Oe T, Elipe MV & Blair IA (2007). A novel 4-oxo-2(E)-nonenal-derived endogenous thiadiazabicyclo glutathione adduct formed during cellular oxidative stress. Chem Res Toxicol 20, 1008-1018.
27. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID & Julius D (2004). Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265.
28. -/- mice. J Physiol 555, 115-123.
29. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ & Corey DP (2006). TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50, 277-289.
30. Lee SH & Blair IA (2000). Characterization of 4-oxo-2-nonenal as a novel product of lipid peroxidation. Chem Res Toxicol 13, 698-702.
31. Lee SH, Oe T & Blair IA (2001). Vitamin C-induced decomposition of lipid hydroperoxides to endogenous genotoxins. Science 292, 2083-2086.
32. Lin D, Lee HG, Liu Q, Perry G, Smith MA & Sayre LM (2005). 4-Oxo-2-nonenal is both more neurotoxic and more protein reactive than 4-hydroxy-2-nonenal. Chem Res Toxicol 18, 1219-1231.
33. ++ changes in human lung mast cells: Graded vs. all-or-nothing elevations after IgE-mediated stimulation. J Cell Biol 109, 123-134.
34. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, Hayward NJ, Chong JA, Julius D, Moran MM & Fanger CM (2007). TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci U S A 104, 13525-13530.
35. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF & Patapoutian A (2007 a). Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541-545.
36. Macpherson LJ, Geierstanger BH, Viswanath V, Bandell M, Eid SR, Hwang S & Patapoutian A (2005). The pungency of garlic: Activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15, 929-934.
37. Macpherson LJ, Xiao B, Kwan KY, Petrus MJ, Dubin AE, Hwang S, Cravatt B, Corey DP & Patapoutian A (2007 b). An ion channel essential for sensing chemical damage. J Neurosci 27, 11412-11415.
38. Maher M, Ao H, Banke T, Nasser N, Wu NT, Breitenbucher JG, Chaplan SR & Wickenden AD (2008). Activation of TRPA1 by farnesyl thiosalicylic acid. Mol Pharmacol 73, 1225-1234.
39. Montell C (2005). The TRP superfamily of cation channels. Sci STKE 2005, re3.
40. Nassenstein C, Kwong KK, Taylor-Clark TE, Kollarik M, Macglashan DW, Braun A & Undem BJ (2008). TRPA1 expression and function in vagal afferent nerves innervating mouse lungs. J Physiol 586, 1595-1604.
41. Negre-Salvayre A, Coatrieux C, Ingueneau C & Salvayre R (2008). Advanced lipid peroxidation end products in oxidative damage to proteins. Potential role in diseases and therapeutic prospects for the inhibitors. Br J Pharmacol 153, 6-20.
42. Rahman I, Biswas SK & Kode A (2006 a). Oxidant and antioxidant balance in the airways and airway diseases. Eur J Pharmacol 533, 222-239.
43. Rahman I, Van Schadewijk AA, Crowther AJ, Hiemstra PS, Stolk J, MacNee W & De Boer WI (2002). 4-Hydroxy-2-nonenal, a specific lipid peroxidation product, is elevated in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 166, 490-495.
44. Rahman I, Yang SR & Biswas SK (2006 b). Current concepts of redox signaling in the lungs. Antioxid Redox Signal 8, 681-689.
45. Roberts LJ 2nd & Morrow JD (2002). Products of the isoprostane pathway: Unique bioactive compounds and markers of lipid peroxidation. Cell Mol Life Sci 59, 808-820.
46. Salazar H, Llorente I, Jara-Oseguera A, Garcia-Villegas R, Munari M, Gordon SE, Islas LD & Rosenbaum T (2008). A single N-terminal cysteine in TRPV1 determines activation by pungent compounds from onion and garlic. Nat Neurosci 11, 255-261.
47. Taylor-Clark T & Undem BJ (2006). Transduction mechanisms in airway sensory nerves. J Appl Physiol 101, 950-959.
48. Taylor-Clark TE, Undem BJ, Macglashan DW Jr, Ghatta S, Carr MJ & McAlexander MA (2008). Prostaglandin-induced activation of nociceptive neurons via direct interaction with transient receptor potential A1 (TRPA1). Mol Pharmacol 73, 274-281.
49. Trevisani M, Siemens J, Materazzi S, Bautista DM, Nassini R, Campi B et al. (2007). 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci U S A 104, 13519-13524.
50. Undem BJ, Myers AC, Barthlow H & Weinreich D (1990). Vagal innervation of guinea pig bronchial smooth muscle. J Appl Physiol 69, 1336-1346.
51. Wang H & Woolf CJ (2005). Pain TRPs. Neuron 46, 9-12.
52. Woolf CJ & Costigan M (1999). Transcriptional and posttranslational plasticity and the generation of inflammatory pain. Proc Natl Acad Sci U S A 96, 7723-7730.