Oxidative challenges sensitize the capsaicin receptor by covalent cysteine modification

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 47, 2009, Pages 20097-20102

  Chuang, Huai Hu ^a   Lin, Stephanie ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Covalent modification; Pain

Indexed keywords

CAPSAICIN; CYSTEINE; MALEIMIDE; PHOSPHOTRANSFERASE; PROTON; VANILLOID RECEPTOR 1;

ALKYLATION; AMINO ACID SUBSTITUTION; ARTICLE; CHEMOSENSITIVITY; CHEMOSENSITIZATION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MODULATION; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NOCICEPTION; NUCLEOTIDE SEQUENCE; ORTHOLOGY; OXIDATIVE STRESS; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM; CAPSAICIN; CELL LINE; CYSTEINE; HUMANS; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; OXIDANTS; OXIDATIVE STRESS; PAIN; PATCH-CLAMP TECHNIQUES; RATS; SEQUENCE ALIGNMENT; TRPV CATION CHANNELS;

EID: 73949128944     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0902675106     Document Type: Article

References (55)

1. Caterina MJ, et al. (1997) The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 389:816-824.
2. McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52-58.
3. Jordt SE, et al. (2004) Mustard oils and cannabinoids excite sensory nerve fibers through the TRP channel ANKTM1. Nature 427:260-265.
4. Peier AM, et al. (2002) A TRP channel that senses cold stimuli and menthol. Cell 108:705-715.
5. Bandell M, et al. (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849-857.
6. Hinman A, Chuang HH, Bautista DM, Julius D (2006) TRP channel activation by reversible covalent modification. Proc Natl Acad Sci USA 103:19564-19568.
7. Macpherson LJ, et al. (2007) Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445:541-545.
8. Caterina MJ, et al. (2000) Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313.
9. Davis JB, et al. (2000) Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187.
10. Bautista DM, et al. (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269-1282.
11. Kwan KY, et al. (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277-289.
12. Trevisani M, et al. (2007) 4-hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci USA 104:13519-13524.
13. 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.
14. Sawada Y, Hosokawa H, Matsumura K, Kobayashi S (2008) Activation of transient receptor potential ankyrin 1 by hydrogen peroxide. Eur J Neurosci 27:1131-1142.
15. Cruz-Orengo L, et al. (2008) Cutaneous nociception evoked by 15-delta PGJ2 via activation of ion channel TRPA1. Mol Pain 4:30.
16. Macpherson LJ, et al. (2005) The pungency of garlic: Activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15:929-934.
17. Bautista DM, et al. (2005) Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci USA 102:12248-12252.
18. Salazar H, et al. (2008) A single N-terminal cysteine in TRPV1 determines activation by pungent compounds from onion and garlic. Nat Neurosci 11:255-261.
19. Cebi M, Koert U (2007) Reactivity recognition by TRPA1 channels. Chembiochem 8:979-980.
20. Takahashi N, et al. (2008) Molecular characterization of TRPA1 channel activation by cysteine-reactive inflammatory mediators. Channels 2:287-298.
21. Yoshida T, et al. (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596-607.
22. Bessac BF, et al. (2008) TRPA1 is a major oxidant sensor in murine airway sensory neurons. J Clin Invest 118:1899-1910.
23. Keeble JE, et al. (2009) Hydrogen peroxide is a novel mediator of inflammatory hyperalgesia, acting via transient receptor potential vanilloid 1-dependent and independent mechanisms. Pain 141:135-142.
24. Filomeni G, Rotilio G, Ciriolo MR (2008) Molecular transduction mechanisms of the redox network underlying the antiproliferative effects of allyl compounds from garlic. J Nutr 138:2053-2057.
25. Ruparel NB, Patwardhan AM, Akopian AN, Hargreaves KM (2008) Homologous and heterologous desensitization of capsaicin and mustard oil responses utilize different cellular pathways in nociceptors. Pain 135:271-279.
26. Susankova K, Tousova K, Vyklicky L, Teisinger J, Vlachova V (2006) Reducing and oxidizing agents sensitize heat-activated vanilloid receptor (TRPV1) current. Mol Pharmacol 70:383-394.
27. Jin Y, et al. (2004) Thimerosal decreases TRPV1 activity by oxidation of extracellular sulfhydryl residues. Neurosci Lett 369:250-255.
28. Gitler C, Mogyoros M, Kalef E (1994) Labeling of protein vicinal dithiols: Role of protein-S2 to protein-(SH)2 conversion in metabolic regulation and oxidative stress. Methods Enzymol 233:403-415.
29. Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to ''hot'' chili peppers. Cell 108:421-430.
30. Shekels LL, Smith AJ, Van Etten RL, Bernlohr DA (1992) Identification of the adipocyte acid phosphatase as a PAO-sensitive tyrosyl phosphatase. Protein Sci 1:710-721.
31. Wiedemann C, Schafer T, Burger MM (1996) Chromaffin granule-associated phosphatidylinositol 4-kinase activity is required for stimulated secretion. EMBO J 15:2094-2101.
32. Gerhard R, John H, Aktories K, Just I (2003) Thiol-modifying phenylarsine oxide inhibits guanine nucleotide binding of rho but not of rac GTPases. Mol Pharmacol 63:1349-1355.
33. Suh BC, Hille B (2002) Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35:507-520.
34. Liu B, Zhang C, Qin F (2005) Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:4835-4843.
35. Tominaga M, et al. (1998) The cloned capsaicin receptor integrates multiple painproducing stimuli. Neuron 21:531-543.
36. Szallasi A, Blumberg PM (1996) Vanilloid receptors: New insights enhance potential as a therapeutic target. Pain 68:195-208.
37. Premkumar LS, Ahern GP (2000) Induction of vanilloid receptor channel activity by protein kinase C. Nature 408:985-990.
38. Numazaki M, Tominaga T, Toyooka H, Tominaga M (2002) Direct phosphorylation of capsaicin receptor VR1 by protein kinase cepsilon and identification of two target serine residues. J Biol Chem 277:13375-13378.
39. Salvemini D, Doyle TM, Cuzzocrea S (2006) Superoxide, peroxynitrite, and oxidative/ nitrative stress in inflammation. Biochem Soc Trans 34:965-970.
40. Chung JM (2004) The role of reactive oxygen species (ROS) in persistent pain. Mol Interv 4:248-250.
41. Gao X, Kim HK, Chung JM, Chung K (2007) Reactive oxygen species (ROS) are involved in enhancement of NMDA-receptor phosphorylation in animal models of pain. Pain 131:262-271.
42. Hacimuftuoglu A, et al. (2006) Antioxidants attenuate multiple phases of formalininduced nociceptive response in mice. Behav Brain Res 173:211-216.
43. Khattab MM (2006) TEMPOL, a membrane-permeable radical scavenger, attenuates peroxynitrite-and superoxide anion-enhanced carrageenan-induced paw edema and hyperalgesia: A key role for superoxide anion. Eur J Pharmacol 548:167-173.
44. Kim HK, et al. (2004) Reactive oxygen species (ROS) play an important role in a rat model of neuropathic pain. Pain 111:116-124.
45. Stadtman ER, Berlett BS (1998) Reactive oxygen-mediated protein oxidation in aging and disease. Drug Metab Rev 30:225-243.
46. Siniscalco D, et al. (2007) Role of reactive oxygen species and spinal cord apoptotic genes in the development of neuropathic pain. Pharmacol Res 55:158-166.
47. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272:20313-20316.
48. Herndon LA, et al. (2002) Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 419:808-814.
49. Annunziato L, et al. (2002) Modulation of ion channels by reactive oxygen and nitrogen species: A pathophysiological role in brain aging? Neurobiol Aging 23:819-834.
50. Reynolds A, Laurie C, Mosley RL, Gendelman HE (2007) Oxidative stress and the pathogenesis of neurodegenerative disorders. Int Rev Neurobiol 82:297-325.
51. Chong ZZ, Li F, Maiese K (2005) Oxidative stress in the brain: Novel cellular targets that govern survival during neurodegenerative disease. Prog Neurobiol 75:207-246.
52. Jenner P, Olanow CW (1996) Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 47:S161-S170.
53. 2+. Nat Neurosci 10:277-279.
54. Doerner JF, Gisselmann G, Hatt H, Wetzel CH (2007) Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282:13180-13189.
55. Goldin AL (1992) Maintenance of Xenopus laevis and oocyte injection. Methods Enzymol 207:266-279.