TRPA1 contributes to the acute inflammatory response and mediates carrageenan-induced paw edema in the mouse

Scientific Reports

Volumn 2, Issue , 2012, Pages

  Moilanen, Lauri J ^a   Laavola, Mirka ^a   Kukkonen, Meiju ^a   Korhonen, Riku ^a   Leppänen, Tiina ^a   Högestätt, Edward D ^b   Zygmunt, Peter M ^b   Nieminen, Riina M ^a   Moilanen, Eeva ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

2-(1,3-DIMETHYL-2,6-DIOXO-1,2,3,6-TETRAHYDRO-7H-PURIN-7-YL)-N-(4-ISOPROPYLPHENYL)ACETAMIDE; ACETANILIDE DERIVATIVE; CARRAGEENAN; IBUPROFEN; N (4 ISOPROPYLPHENYL) 2 (1,2,3,6 TETRAHYDRO 1,3 DIMETHYL 2,6 DIOXO 7H PURIN 7 YL)ACETAMIDE; PURINE DERIVATIVE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRPA1 PROTEIN, MOUSE;

ANIMAL; ARTICLE; C57BL MOUSE; CELL STRAIN HEK293; CHEMICALLY INDUCED DISORDER; DRUG POTENTIATION; EDEMA; HUMAN; MOUSE; PHYSIOLOGY;

ACETANILIDES; ANIMALS; CARRAGEENAN; EDEMA; HEK293 CELLS; HUMANS; IBUPROFEN; MICE; MICE, INBRED C57BL; PURINES; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84860249686     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep00380     Document Type: Article

References (55)

1. Jordt, S. et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265 (2004). (Pubitemid 38112043)
2. Bandell, M. et al. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41, 849-857 (2004). (Pubitemid 38429729)
3. Bautista, D. M. et al. Pungent products from garlic activate the sensory ion channel TRPA1. Proc. Natl. Acad. Sci. U. S. A. 102, 12248-12252 (2005). (Pubitemid 41291160)
4. Macpherson, L. J. et al. The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 15, 929-934 (2005). (Pubitemid 40772062)
5. Baraldi, P. G., Preti, D., Materazzi, S. & Geppetti, P. Transient Receptor Potential Ankyrin 1 (TRPA1) Channel as Emerging Target for Novel Analgesics and Anti-Inflammatory Agents. J. Med. Chem. 53, 5085-5107 (2010).
6. Bessac, B. F. & Jordt, S. E. Breathtaking TRP channels: TRPA1 and TRPV1 in airway chemosensation and reflex control. Physiology (Bethesda) 23, 360-370 (2008).
7. Andersson, K. E., Gratzke, C. & Hedlund, P. The role of the transient receptor potential (TRP) superfamily of cation-selective channels in the management of the overactive bladder. BJU Int. 106, 1114-1127 (2010).
8. Pedersen, S. F., Owsianik,G. & Nilius, B. TRP channels: an overview. Cell Calcium 38, 233-252 (2005). (Pubitemid 41283262)
9. Berridge, M. J., Lipp, P. & Bootman, M. D. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21 (2000).
10. Jaquemar, D., Schenker, T. & Trueb, B. An Ankyrin-like Protein with Transmembrane Domains Is Specifically Lost after Oncogenic Transformation of Human Fibroblasts. Journal of Biological Chemistry 274, 7325-7333 (1999).
11. Story, G. M. et al. ANKTM1, a TRP-like Channel Expressed in Nociceptive Neurons, Is Activated by Cold Temperatures. Cell 112, 819-829 (2003). (Pubitemid 36378884)
12. Hinman, A., Chuang, H., Bautista, D. M. & Julius, D. TRP channel activation by reversible covalent modification. Proceedings of the National Academy of Sciences 103, 19564-19568 (2006). (Pubitemid 46026070)
13. Sadofsky, L. R. et al. TRPA1 is activated by direct addition of cysteine residues to the N-hydroxysuccinyl esters of acrylic and cinnamic acids. Pharmacol. Res. 63, 30-36 (2011).
14. Taylor-Clark, T. E., Ghatta, S., Bettner, W. & Undem, B. J. Nitrooleic acid, an endogenous product of nitrative stress, activates nociceptive sensory nerves via the direct activation of TRPA1. Mol. Pharmacol. 75, 820-829 (2009).
15. Andersson, D. A., Gentry, C., Moss, S. & Bevan, S. Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J. Neurosci. 28, 2485-2494 (2008). (Pubitemid 351348185)
16. Eid, S. R. et al. HC-030031, a TRPA1 selective antagonist, attenuates inflammatory-and neuropathy-induced mechanical hypersensitivity. Mol. Pain 4, 48 (2008).
17. Nagata, K., Duggan, A., Kumar, G. & Garcia-Anoveros, J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25, 4052-4061 (2005). (Pubitemid 40563380)
18. Nozawa, K. et al. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc. Natl. Acad. Sci. U. S. A. 106, 3408-3413 (2009).
19. Kwan, K. Y., Glazer, J. M., Corey, D. P., Rice, F. L. & Stucky, C. L. TRPA1 modulates mechanotransduction in cutaneous sensory neurons. J. Neurosci. 29, 4808-4819 (2009).
20. Streng, T. et al.Distribution and function of the hydrogen sulfide-sensitive TRPA1 ion channel in rat urinary bladder. Eur. Urol. 53, 391-399 (2008).
21. Kochukov, M. Y., McNearney, T. A., Fu, Y. & Westlund, K. N. Thermosensitive TRP ion channels mediate cytosolic calcium response in human synoviocytes. Am. J. Physiol. Cell. Physiol. 291, C424-32 (2006). (Pubitemid 44343625)
22. El Karim, I. A. et al. Human odontoblasts express functional thermo-sensitive TRP channels: implications for dentin sensitivity. Pain 152, 2211-2223 (2011).
23. Chen, J. et al. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation. Pain 152, 1165-1172 (2011).
24. McNamara, C. R. et al. TRPA1 mediates formalin-induced pain. Proc. Natl. Acad. Sci. U. S. A. 104, 13525-13530 (2007). (Pubitemid 47293978)
25. Bautista, D. M. et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269-1282 (2006).
26. Bessac, B. F. et al. Transient receptor potential ankyrin 1 antagonists block the noxious effects of toxic industrial isocyanates and tear gases. FASEB J. 23, 1102-1114 (2009).
27. Wei, H., Koivisto, A. & Pertovaara, A. Spinal TRPA1 ion channels contribute to cutaneous neurogenic inflammation in the rat. Neurosci. Lett. 479, 253-256 (2010).
28. Nassini, R. et al. Acetaminophen, via its reactive metabolite N-acetyl-p-benzoquinoneimine and transient receptor potential ankyrin-1 stimulation, causes neurogenic inflammation in the airways and other tissues in rodents. FASEB J. (2010).
29. Caceres, A. I. et al. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proceedings of the National Academy of Sciences 106, 9099-9104 (2009).
30. da Costa, D. S. et al. The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation. Pain 148, 431-437 (2010).
31. Fernandes, E. S. et al. A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor ainduced inflammatory hyperalgesia and Freund's complete adjuvant-induced monarthritis. Arthritis & Rheumatism 63, 819-829 (2011).
32. Petrus, M. et al. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol. Pain 3, 40 (2007).
33. Kremeyer, B. et al. A Gain-of-Function Mutation in TRPA1 Causes Familial Episodic Pain Syndrome. Neuron 66, 671-680 (2010).
34. André, E. et al. Cigarette smoke-induced neurogenic inflammation is mediated by alpha,beta-unsaturated aldehydes and the TRPA1 receptor in rodents. J. Clin. Invest. 118, 2574-2582 (2008). (Pubitemid 351949784)
35. Posadas, I. et al. Carrageenan-induced mouse paw oedema is biphasic, age-weight dependent and displays differential nitric oxide cyclooxygenase-2 expression. Br. J. Pharmacol. 142, 331-338 (2004). (Pubitemid 38746169)
36. Fantone, J. C. &Ward, P. A. Role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. Am. J. Pathol. 107, 395-418 (1982).
37. Morris, C. J. Carrageenan-induced paw edema in the rat and mouse. Methods Mol. Biol. 225, 115-121 (2003).
38. Di Lorenzo, A., Fernandez-Hernando, C., Cirino, G. & Sessa, W. C. Akt1 is critical for acute inflammation and histamine-mediated vascular leakage. Proc. Natl. Acad. Sci. U. S. A. 106, 14552-14557 (2009).
39. Bucci, M. et al. Endothelial nitric oxide synthase activation is critical for vascular leakage during acute inflammation in vivo. Proc. Natl. Acad. Sci. U. S. A. 102, 904-908 (2005). (Pubitemid 40282763)
40. Rocha, A. C., Fernandes, E. S., Quintao, N. L., Campos, M. M. & Calixto, J. B. Relevance of tumour necrosis factor-alpha for the inflammatory and nociceptive responses evoked by carrageenan in the mouse paw. Br. J. Pharmacol. 148, 688-695 (2006). (Pubitemid 43993059)
41. Mazzon, E. et al. Effect of tumour necrosis factor-alpha receptor 1 genetic deletion on carrageenan-induced acute inflammation: a comparison with etanercept. Clin. Exp. Immunol. 153, 136-149 (2008). (Pubitemid 351809337)
42. Schirmer, B. C. & Langsrud, S. Evaluation of natural antimicrobials on typical meat spoilage bacteria in vitro and in vacuum-packed pork meat. J. Food Sci. 75, M98-M102 (2010).
43. Obaidat, M. M. & Frank, J. F. Inactivation of Salmonella and Escherichia coli O157:H7 on sliced and whole tomatoes by allyl isothiocyanate, carvacrol, and cinnamaldehyde in vapor phase. J. Food Prot. 72, 315-324 (2009).
44. Zhang, Y. Allyl isothiocyanate as a cancer chemopreventive phytochemical. Molecular Nutrition & Food Research 54, 127-135 (2010).
45. Holzer, P. Transient receptor potential (TRP) channels as drug targets for diseases of the digestive system. Pharmacol. Ther. 131, 142-170 (2011).
46. Henriques, M. G. et al.Mouse paw edema. Anew model for inflammation? Braz. J. Med. Biol. Res. 20, 243-249 (1987).
47. Materazzi, S. et al. Cox-dependent fatty acid metabolites cause pain through activation of the irritant receptor TRPA1. Proc. Natl. Acad. Sci. U. S. A. 105, 12045-12050 (2008).
48. Schmidt, M.,Dubin, A. E., Petrus, M. J., Earley, T. J.&Patapoutian, A. Nociceptive signals induce trafficking of TRPA1 to the plasma membrane. Neuron 64, 498-509 (2009).
49. Jakobsson, P. Pain: How macrophages mediate inflammatory pain via ATP signaling. Nat Rev Rheumatol 6, 679-681 (2010).
50. Earley, S., Gonzales, A. L. & Crnich, R. Endothelium-dependent cerebral artery dilation mediated by TRPA1 and Ca21-Activated K1 channels. Circ. Res. 104, 987-994 (2009).
51. Graepel, R. et al. 4-Oxo-2-nonenal (4-ONE): Evidence of Transient Receptor Potential Ankyrin 1-Dependent and -Independent Nociceptive and Vasoactive Responses In Vivo. Journal of Pharmacology and Experimental Therapeutics 337, 117-124 (2011).
52. Atoyan, R., Shander, D. & Botchkareva, N. V. Non-neuronal expression of transient receptor potential type A1 (TRPA1) in human skin. J. Invest. Dermatol. 129, 2312-2315 (2009).
53. Jain, A. et al. TRP-channel-specific cutaneous eicosanoid release patterns. Pain 152, 2765-2772 (2011).
54. Nieminen, R., Lahti, A., Jalonen, U., Kankaanranta, H. & Moilanen, E. JNK inhibitor SP600125 reduces COX-2 expression by attenuating mRNA in activated murine J774 macrophages. 6, 987-996 (2006).
55. Nieminen, R., Korhonen, R., Moilanen, T., Clark, A. R. & Moilanen, E. Aurothiomalate inhibits cyclooxygenase 2, matrix metalloproteinase 3, and interleukin-6 expression in chondrocytes by increasing MAPK phosphatase 1 expression and decreasing p38 phosphorylation: MAPK phosphatase 1 as a novel target for antirheumatic drugs. Arthritis Rheum. 62, 1650-1659 (2010).