TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins

Nature Communications

Volumn 5, Issue , 2014, Pages

  Meseguer, Victor ^a   Alpizar, Yeranddy A ^b   Luis, Enoch ^a   Tajada, Sendoa ^c   Denlinger, Bristol ^a   Fajardo, Otto ^a   Manenschijn, Jan Albert ^a   Fernández Peña, Carlos ^a   Talavera, Arturo ^b,d   Kichko, Tatiana ^e   Navia, Belén ^f   Sánchez, Alicia ^b   Señarís, Rosa ^f   Reeh, Peter ^e   Pérez García, María Teresa ^c   López López, José Ramón ^c   Voets, Thomas ^b   Belmonte, Carlos ^a   Talavera, Karel ^a,b   Viana, Félix ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^c UNIVERSITY OF VALLADOLID   (Spain)

^d Instituto Finlay   (Cuba)

^e UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^f Universidade de Santiago de Compostela and Instituto de Investigación Sanitaria de Santiago de Compostela   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CALCITONIN GENE RELATED PEPTIDE; TOLL LIKE RECEPTOR 4; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; LIPID A; LIPOPOLYSACCHARIDE; NEUROPEPTIDE; TLR4 PROTEIN, MOUSE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRPA1 PROTEIN, MOUSE;

BACTERIAL DISEASE; BACTERIUM; CELL ORGANELLE; DISEASE TREATMENT; LIPID; MOLECULAR ANALYSIS; NEUROLOGY; POLYSACCHARIDE; SENSORY SYSTEM; TOXIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; INFLAMMATORY PAIN; MALE; MOUSE; NEUROGENIC INFLAMMATION; NOCICEPTION; NONHUMAN; PATHOGENESIS; PROTEIN SECRETION; SENSORY NERVE CELL; AGONISTS; ANIMAL; C57BL MOUSE; CELL MEMBRANE; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; ESCHERICHIA COLI; HAMSTER; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; MEMBRANE POTENTIAL; METABOLISM; PAIN; PAIN RECEPTOR; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; ESCHERICHIA COLI; HEK293 CELLS; HUMANS; ION CHANNEL GATING; LIPID A; LIPOPOLYSACCHARIDES; MEMBRANE POTENTIALS; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGENIC INFLAMMATION; NEUROPEPTIDES; NOCICEPTORS; PAIN; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84892854661     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4125     Document Type: Article

References (67)

1. Murray, P. R., Rosenthal, K. S. & Pfaller, M. A. Medical Microbiology (Elsevier, 2009
2. Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783-801 (2006 (Pubitemid 43261452)
3. Ronald, P. C. & Beutler, B. Plant and animal sensors of conserved microbial signatures. Science 330, 1061-1064 (2010
4. Akira, S. & Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 4, 499-511 (2004 (Pubitemid 38931765)
5. Poltorak, A. et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: Mutations in Tlr4 gene. Science 282, 2085-2088 (1998 (Pubitemid 29001265)
6. Watkins, L. R. et al. Neurocircuitry of illness-induced hyperalgesia. Brain Res. 639, 283-299 (1994 (Pubitemid 24078567)
7. Yilmaz, M. S. et al. Lipopolysaccharide-induced hypotension is mediated by a neural pathway involving the vagus nerve, the nucleus tractus solitarius and alpha-Adrenergic receptors in the preoptic anterior hypothalamic area. J. Neuroimmunol. 203, 39-49 (2008
8. Romanovsky, A. A., Simons, C. T., Szekely, M. & Kulchitsky, V. A. The vagus nerve in the thermoregulatory response to systemic inflammation. Am. J. Physiol. 273, R407-R413 (1997
9. Maier, S. F., Goehler, L. E., Fleshner, M. & Watkins, L. R. The role of the vagus nerve in cytokine-To-brain communication. Ann. N. Y. Acad. Sci. 840, 289-300 (1998 (Pubitemid 28302056)
10. Diogenes, A., Ferraz, C. C., Akopian, A. N., Henry, M. A. & Hargreaves, K. M. LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J. Dent. Res. 90, 759-764 (2011
11. Ochoa-Cortes, F. et al. Bacterial cell products signal to mouse colonic nociceptive dorsal root ganglia neurons. Am. J. Physiol Gastrointest. Liver Physiol. 299, G723-G732 (2010
12. Hosoi, T., Okuma, Y., Matsuda, T. & Nomura, Y. Novel pathway for LPS-induced afferent vagus nerve activation: Possible role of nodose ganglion. Auton. Neurosci. 120, 104-107 (2005 (Pubitemid 40917314)
13. 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)
14. Jordt, S. E. et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265 (2004
15. Bautista, D. M. et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124, 1269-1282 (2006
16. Nilius, B., Appendino, G. & Owsianik, G. The transient receptor potential channel TRPA1: From gene to pathophysiology. Pflugers Arch. 464, 425-458 (2012
17. McNamara, C. R. et al. TRPA1 mediates formalin-induced pain. Proc. Natl Acad. Sci. USA 104, 13525-13530 (2007 (Pubitemid 47293978)
18. Caterina, M. J. et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313 (2000 (Pubitemid 30226186)
19. Doerner, J. F., Gisselmann, G., Hatt, H. & Wetzel, C. H. Transient receptor potential channel A1 is directly gated by calcium ions. J. Biol. Chem. 282, 13180 9 (2007 (Pubitemid 47100541)
20. Zurborg, S., Yurgionas, B., Jira, J. A., Caspani, O. & Heppenstall, P. A. Direct activation of the ion channel TRPA1 by Ca(2). Nat. Neurosci. 10, 277-279 (2007
21. Karashima, Y. et al. Bimodal action of menthol on the transient receptor potential channel TRPA1. J. Neurosci. 27, 9874-9884 (2007 (Pubitemid 47403994)
22. Fajardo, O., Meseguer, V., Belmonte, C. & Viana, F. TRPA1 channels: Novel targets of 1,4-dihydropyridines. Channels (Austin) 2, 429-438 (2008
23. Dai, Y. et al. Sensitization of TRPA1 by PAR2 contributes to the sensation of inflammatory pain. J. Clin. Invest. 117, 1979-1987 (2007 (Pubitemid 47036332)
24. Trevisani, M. et al. 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 (2007 (Pubitemid 47293977)
25. Macpherson, L. J. et al. An ion channel essential for sensing chemical damage. J. Neurosci. 27, 11412-11415 (2007 (Pubitemid 47621302)
26. Raetz, C. R. & Whitfield, C. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700 (2002 (Pubitemid 34800232)
27. Brandenburg, K., Schromm, A. B. & Gutsmann, T. Endotoxins: Relationship between structure, function, and activity. Subcell. Biochem. 53, 53-67 (2010
28. Netea, M G., van Deuren, M., Kullberg, B. J., Cavaillon, J. M. & van der Meer, J. W. Does the shape of lipid A determine the interaction of LPS with Toll-like receptors? Trends Immunol. 23, 135-139 (2002 (Pubitemid 34178295)
29. Martinac, B., Adler, J. & Kung, C. Mechanosensitive ion channels of E. coli activated by amphipaths. Nature 348, 261-263 (1990
30. Hill, K. & Schaefer, M. TRPA1 is differentially modulated by the amphipathic molecules trinitrophenol and chlorpromazine. J. Biol. Chem. 282, 7145-7153 (2007 (Pubitemid 47093678)
31. Matsunaga, N., Tsuchimori, N., Matsumoto, T. & Ii, M. TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol. Pharmacol. 79, 34-41 (2011
32. Golenbock, D. T., Hampton, R. Y., Qureshi, N., Takayama, K. & Raetz, C. R. Lipid A-like molecules that antagonize the effects of endotoxins on human monocytes. J. Biol Chem. 266, 19490-19498 (1991 (Pubitemid 21908258)
33. Morrison, D. C. & Jacobs, D. M. Binding of polymyxin B to the lipid A portion of bacterial lipopolysaccharides. Immunochemistry 13, 813-818 (1976
34. Bautista, D. M. et al. Pungent products from garlic activate the sensory ion channel TRPA1. Proc. Natl Acad. Sci. USA 102, 12248-12252 (2005 (Pubitemid 41291160)
35. Pozsgai, G. et al. Evidence for the pathophysiological relevance of TRPA1 receptors in the cardiovascular system in vivo. Cardiovasc. Res. 87, 760-768 (2010
36. Earley, S. TRPA1 channels in the vasculature. Br. J. Pharmacol. 167, 13-22 (2012
37. Caceres, A. I. et al. A sensory neuronal ion channel essential for airway inflammation and hyperreactivity in asthma. Proc. Natl Acad. Sci. USA 106, 9099-9104 (2009
38. Hua, X. Y., Chen, P., Fox, A. & Myers, R. R. Involvement of cytokines in lipopolysaccharide-induced facilitation of CGRP release from capsaicinsensitive nerves in the trachea: Studies with interleukin-1beta and tumor necrosis factor-Alpha. J. Neurosci. 16, 4742-4748 (1996 (Pubitemid 26251069)
39. Kichko, T. I. & Reeh, P. W. TRPV1 controls acid-And heat-induced calcitonin gene-related peptide release and sensitization by bradykinin in the isolated mouse trachea. Eur. J. Neurosci. 29, 1896-1904 (2009
40. Landry, D. W. & Oliver, J. A. The pathogenesis of vasodilatory shock. N. Engl. J. Med. 345, 588-595 (2001
41. Ferreira, S. H., Lorenzetti, B. B. & Poole, S. Bradykinin initiates cytokinemediated inflammatory hyperalgesia. Br. J. Pharmacol. 110, 1227-1231 (1993 (Pubitemid 24005265)
42. Kanaan, S. A. et al. Endotoxin-induced local inflammation and hyperalgesia in rats and mice: A new model for inflammatory pain. Pain 66, 373-379 (1996 (Pubitemid 26284008)
43. Andersson, D. A., Gentry, C. & Bevan, S. TRPA1 has a key role in the somatic pro-nociceptive actions of hydrogen sulfide. PLoS One 7, e46917 (2012
44. Rudaya, A. Y., Steiner, A. A., Robbins, J. R., Dragic, A. S. & Romanovsky, A. A. Thermoregulatory responses to lipopolysaccharide in the mouse: Dependence on the dose and ambient temperature. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1244-R1252 (2005 (Pubitemid 41507387)
45. Ulich, T. R., Guo, K. Z., Remick, D., Del Castillo, J. & Yin, S. M. Endotoxininduced cytokine gene expression in vivo. III. IL-6 mRNA and serum protein expression and the in vivo hematologic effects of IL-6. J. Immunol. 146, 2316-2323 (1991
46. Kim, S. H. et al. Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc. Natl Acad. Sci. USA 107, 8440-8445 (2010
47. Macpherson, L. J. et al. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445, 541-545 (2007 (Pubitemid 46197634)
48. Kang, K. et al. Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464, 597-600 (2010
49. Bosmann, M. & Ward, P. A. The inflammatory response in sepsis. Trends Immunol. 34, 129-136 (2013
50. Takahashi, N. et al. TRPA1 underlies a sensing mechanism for O2. Nat. Chem. Biol. 7, 701-711 (2011
51. Hinman, A., Chuang, H. H., Bautista, D. M. & Julius, D. TRP channel activation by reversible covalent modification. Proc. Natl Acad. Sci. USA 103, 19564-19568 (2006 (Pubitemid 46026070)
52. Brierley, S. M. et al. The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 137, 2084-2095 (2009
53. Vilceanu, D. & Stucky, C. L. TRPA1 mediates mechanical currents in the plasma membrane of mouse sensory neurons. PLoS One 5, e12177 (2010
54. 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
55. Hardie, R. C. & Franze, K. Photomechanical responses in Drosophila photoreceptors. Science 338, 260-263 (2012
56. Hurley, J. C. Endotoxemia: Methods of detection and clinical correlates. Clin. Microbiol. Rev. 8, 268-292 (1995
57. Jacinto, R. C. et al. Quantification of endotoxins in necrotic root canals from symptomatic and asymptomatic teeth. J. Med. Microbiol. 54, 777-783 (2005 (Pubitemid 41129173)
58. Basbaum, A. I., Bautista, D. M., Scherrer, G. & Julius, D. Cellular and molecular mechanisms of pain. Cell 139, 267-284 (2009
59. Derow, A., Izydorczyk, I., Kuhn, A., Reeh, P. W. & Petho, G. Prostaglandin E(2) and I(2) facilitate noxious heat-induced spike discharge but not iCGRP release from rat cutaneous nociceptors. Life Sci. 81, 1685-1693 (2007 (Pubitemid 350151446)
60. Engel, M. A. et al. TRPA1 and substance P mediate colitis in mice. Gastroenterology 141, 1346-1358 (2011
61. Hatano, N. et al. Hypoxia-inducible factor-1alpha (HIF1alpha) switches on transient receptor potential ankyrin repeat 1 (TRPA1) gene expression via a hypoxia response element-like motif to modulate cytokine release. J. Biol. Chem. 287, 31962-31972 (2012
62. Chiu, I. M. et al. Bacteria activate sensory neurons that modulate pain and inflammation. Nature 501, 52-57 (2013
63. Hoshino, K. et al. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: Evidence for TLR4 as the Lps gene product. J. Immunol. 162, 3749-3752 (1999 (Pubitemid 29314747)
64. Kwan, K. Y. et al. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50, 277-289 (2006
65. Madrid, R. et al. Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J. Neurosci. 26, 12512-12525 (2006 (Pubitemid 44864516)
66. Fajardo, O., Meseguer, V., Belmonte, C. & Viana, F. TRPA1 channels mediate cold temperature sensing in mammalian vagal sensory neurons: Pharmacological and genetic evidence. J. Neurosci. 28, 7863-7875 (2008
67. Chaplan, S. R., Bach, F. W., Pogrel, J. W., Chung, J. M. & Yaksh, T. L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53, 55-63 (1994)(Pubitemid 24238751)