Activation of TRPV1 and TRPA1 leads to muscle nociception and mechanical hyperalgesia

Pain

Volumn 144, Issue 3, 2009, Pages 270-277

  Ro, Jin Y ^a   Lee, Jong Seok ^a   Zhang, Youping ^a  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Behavior; Craniofacial; Muscle nociceptors; Rat; Trigeminal ganglia

Indexed keywords

3 (4 TERT BUTYLPHENYL) N (2,3 DIHYDROBENZO[B][1,4] DIOXIN 6 YL)ACRYLAMIDE; ALLYL ISOTHIOCYANATE; AMG 9810; AP 18; CAPSAICIN; CAPSAZEPINE; HC 030031; RECEPTOR BLOCKING AGENT; TRANSIENT RECEPTOR POTENTIAL ANKYRIN 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CRANIOFACIAL MORPHOLOGY; DRUG EFFECT; HINDLIMB; HYPERALGESIA; HYPERSENSITIVITY; IMMUNOHISTOCHEMISTRY; MALE; MASSETER MUSCLE; MASTICATORY MUSCLE; MECHANICAL HYPERALGESIA; MECHANICAL STIMULATION; MODEL; MUSCLE; MUSCLE SPINDLE AFFERENT NERVE; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; TRIGEMINUS GANGLION;

ACRYLAMIDES; AFFERENT PATHWAYS; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CALCIUM CHANNELS; CAPSAICIN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FACIAL PAIN; HYPERALGESIA; INJECTIONS, INTRAMUSCULAR; MALE; MASTICATORY MUSCLES; MUSTARD PLANT; NOCICEPTORS; PAIN MEASUREMENT; PAIN THRESHOLD; PLANT OILS; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SENSORY SYSTEM AGENTS; TRIGEMINAL GANGLION; TRPV CATION CHANNELS;

EID: 67649482336     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2009.04.021     Document Type: Article

References (57)

1. Ahluwalia J., Urban L., Capogna M., Bevan S., and Nagy I. Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience 100 (2000) 685-688
2. Ambalavanar R., Moritani M., Haines A., Hilton T., and Dessem D. Chemical phenotypes of muscle and cutaneous afferent neurons in the rat trigeminal ganglion. J Comp Neurol 460 (2003) 167-179
3. Andersson D.A., Gentry C., Moss S., and Bevan S. Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress. J Neurosci 28 (2008) 2485-2494
4. Arendt-Nielsen L., Svensson P., Sessle B.J., Cairns B.E., and Wang K. Interactions between glutamate and capsaicin in inducing muscle pain and sensitization in humans. Eur J Pain 12 (2008) 661-670
5. Arima T., Svensson P., and Arendt-Nielsen L. Capsaicin-induced muscle hyperalgesia in the exercised and non-exercised human masseter muscle. J Orofac Pain 14 (2000) 213-223
6. Arima T., Arendt-Nielsen L., Minagi S., and Svensson P. Effect of capsaicin-evoked jaw-muscle pain on intramuscular blood-flow. Arch Oral Biol 54 (2009) 241-249
7. Bandell M., Story G.M., Hwang S.W., Viswanath V., Eid S.R., Petrus M.J., Earley T.J., and Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41 (2004) 849-857
8. Bautista D.M., Movahed P., Hinman A., Axelsson H.E., Sterner O., Högestätt E.D., Julius D., Jordt S.E., and Zygmunt P.M. Pungent products from garlic activate the sensory ion channel TRPA1. Proc Natl Acad Sci 102 (2005) 12248-12252
9. Bautista D.M., Jordt S.E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., and Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124 (2006) 1269-1282
10. Bölcskei K., Helyes Z., Szabó A., Sándor K., Elekes K., Németh J., Almási R., Pintér E., Petho G., and Szolcsányi J. Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Pain 117 (2005) 368-376
11. Carlton S.M., and Hargett G.L. Stereological analysis of Ca(2+)/calmodulin-dependent protein kinase II alpha-containing dorsal root ganglion neurons in the rat: colocalization with isolectin Griffonia simplicifolia, calcitonin gene-related peptide, or vanilloid receptor 1. J Comp Neurol 448 (2002) 102-110
12. 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
13. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
14. Caterina M.J., and Julius D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24 (2001) 487-517
15. Christoph T., Gillen C., Mika J., Grünweller A., Schäfer M.K., Schiene K., Frank R., Jostock R., Bahrenberg G., Weihe E., Erdmann V.A., and Kurreck J. Antinociceptive effect of antisense oligonucleotides against the vanilloid receptor VR1/TRPV1. Neurochem Int 50 (2007) 281-290
16. 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
17. 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
18. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Clapham C., Atkinson K., Hughes S.A., Rance K., Grau E., Harper A.J., Pugh P.L., Rogers D.C., Bingham S., Randall A., and Sheardown S.A. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405 (2000) 183-187
19. Fujii Y., Ozaki N., Taguchi T., Mizumura K., Furukawa K., and Sugiura Y. TRP channels and ASICs mediate mechanical hyperalgesia in models of inflammatory muscle pain and delayed onset muscle soreness. Pain 140 (2008) 292-304
20. Gavva N.R., Tamir R., Qu Y., Klionsky L., Zhang T.J., Immke D., Wang J., Zhu D., Vanderah T.W., Porreca F., Doherty E.M., Norman M.H., Wild K.D., Bannon A.W., Louis J.C., and Treanor J.J. AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. JPET 313 (2005) 474-484
21. Gratzke C., Streng T., Waldkirch E., Sigl K., Stief C., Andersson K.E., and Hedlund P. Transient receptor potential A1 (TRPA1) activity in the human urethra-evidence for a functional role for TRPA1 in the outflow region. Eur Urol (2008) [Epub ahead of print]
22. Guo A., Vulchanova L., Wang J., Li X., and Elde R. Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11 (1999) 946-958
23. Hedenberg-Magnusson B., Ernberg M., and Kopp S. Symptoms and signs of temporomandibular disorders in patients with fibromyalgia of the temporomandibular system. Acta Odontol Scand 55 (1997) 344-349
24. Hoheisel U, Reinöhl J, Unger T, Mense S. Acidic pH and capsaicin activate mechanosensitive group IV muscle receptors in the rat. Pain 2004;110:149-57.
25. Honore P., Wismer C.T., Mikusa J., Zhu C.Z., Zhong C., Gauvin D.M., Gomtsyan A., El Kouhen R., Lee C.H., Marsh K., Sullivan J.P., Faltynek C.R., and Jarvis M.F. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. JPET 314 (2005) 410-421
26. Hu H.J., Bhave G., and Gereau IV R.W. Prostaglandin and protein kinase A-dependent modulation of vanilloid receptor function by metabotropic glutamate receptor 5: potential mechanism for thermal hyperalgesia. J Neurosci 22 (2002) 7444-7452
27. Ichikawa H., and Sugimoto T. VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res 890 (2001) 184-188
28. Jordt S.E., Bautista D.M., Chuang H.H., McKemy D.D., Zygmunt P.M., Högestätt E.D., Meng I.D., and Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427 (2004) 260-265
29. Kobayashi K., Fukuoka T., Obata K., Yamanaka H., Dai Y., Tokunaga A., and Noguchi K. Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J Comp Neurol 493 (2005) 596-606
30. Kwan K.Y., Allchorne A.J., Vollrath M.A., Christensen A.P., Zhang D.S., Woolf C.J., and Corey D.P. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50 (2006) 277-289
31. Lam D.K., Sessle B.J., and Hu J.W. Glutamate and capsaicin effects on trigeminal nociception I: activation and peripheral sensitization of deep craniofacial nociceptive afferents. Brain Res 1251 (2009) 130-139
32. Lee J.S., and Ro J.Y. Peripheral metabotropic glutamate receptor 5 mediates mechanical hypersensitivity in craniofacial muscle tissue via PKC dependent mechanisms. Neuroscience 146 (2007) 375-383
33. Lee H.J., Choi H.S., Ju J.S., Bae Y.C., Kim S.K., Yoon Y.W., and Ahn D.K. Peripheral mGluR5 antagonist attenuated craniofacial muscle pain and inflammation but not mGluR1 antagonist in lightly anesthetized rats. Brain Res Bull 70 (2006) 378-385
34. Lee J.S., Zhang Y., Haynes G., and Ro J.Y. Involvement of TRPV1, TRPV4 and TRPA1 in the development of mechanical hypersensitivity in craniofacial muscle tissue. Neuroscience meeting planner (2008), Society for Neuroscience, Washington (DC)
35. Levine J.D., and Alessandri-Haber N. TRP channels: targets for the relief of pain. Biochim Biophys Acta 1772 (2007) 989-1003
36. Lund J.P., Donga R., Widmer C.G., and Stohler C.S. The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 69 (1991) 683-694
37. Mandadi S., Tominaga T., Numazaki M., Murayama N., Saito N., Armati P.J., Roufogalis B.D., and Tominaga M. Increased sensitivity of desensitized TRPV1 by PMA occurs through PKCepsilon-mediated phosphorylation at S800. Pain 123 (2006) 106-116
38. Marchettini P., Simone D.A., Caputi G., and Ochoa J.L. Pain from excitation of identified muscle nociceptors in humans. Brain Res 740 (1996) 109-116
39. Mense S. Nociception from skeletal muscle in relation to clinical muscle pain. Pain 54 (1993) 241-289
40. Michael G.J., and Priestley J.V. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 19 (1999) 1844-1854
41. Molin C. Vertical isometric muscle forces of the mandible. A comparative study of subjects with and without manifest mandibular pain dysfunction syndrome. Acta Odontol Scand 30 (1972) 485-499
42. Obata K., Katsura H., Mizushima T., Yamanaka H., Kobayashi K., Dai Y., Fukuoka T., Tokunaga A., Tominaga M., and Noguchi K. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest 115 (2005) 2393-2401
43. Penuelas A., Tashima K., Tsuchiya S., Matsumoto K., Nakamura T., Horie S., and Yano S. Contractile effect of TRPA1 receptor agonists in the isolated mouse intestine. Eur J Pharmacol 576 (2007) 143-150
44. Petrus M., Peier A.M., Bandell M., Hwang S.W., Huynh T., Olney N., Jegla T., and Patapoutian A. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol Pain 3 (2007) 40
45. Pomonis J.D., Harrison J.E., Mark L., Bristol D.R., Valenzano K.J., and Walker K. N-(4-tertiarybutylphenyl)-4-(3-cholorphyridin-2-yl)tetrahydropyrazine-1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: II. In vivo characterization in rat models of inflammatory and neuropathic pain. JPET 306 (2003) 387-393
46. Prescott E.D., and Julius D.A. Modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300 (2003) 1284-1288
47. Ro J.Y. Functional role of peripheral glutamate receptors in craniofacial muscle pain and hyperalgesia. In: Graven-Nielsen T., Arendt-Nielsen L., and Mense S. (Eds). Fundamentals of musculoskeletal pain (2008), IASP Press, Seattle 33-45
48. Ro J.Y., and Capra N.F. Assessing mechanical sensitivity of masseter muscle in lightly anesthetized rats: a model for craniofacial muscle hyperalgesia. Neurosci Res 56 (2006) 119-123
49. Ro J.Y., Capra N., and Masri R. Development of a behavioral assessment of craniofacial muscle pain in lightly anesthetized rats. Pain 104 (2003) 179-185
50. Ro J.Y., Lee J., Capra N.F., and Zhang Y. Role of soluble guanylate cyclase in the trigeminal subnucleus caudalis in capsaicin-induced muscle hypersensitivity. Brain Res 1184 (2007) 141-148
51. Story G.M., Peier A.M., Reeve A.J., Eid S.R., Mosbacher J., Hricik T.R., Earley T.J., Hergarden A.C., Andersson D.A., Hwang S.W., McIntyre P., Jegla T., Bevan S., and Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112 (2003) 819-829
52. Story G.M., and Gereau IV R.W. Numbing the senses: role of TRPA1 in mechanical and cold sensation. Neuron 50 (2006) 177-180
53. Szabó A., Helyes Z., Sándor K., Bite A., Pintér E., Németh J., Bánvölgyi A., Bölcskei K., Elekes K., and Szolcsányi J. Role of transient receptor potential vanilloid 1 receptors in adjuvant-induced chronic arthritis: in vivo study using gene-deficient mice. JPET 314 (2005) 111-119
54. Takeda M., Tanimoto T., Ito M., Nasu M., and Matsumoto S. Role of capsaicin-sensitive primary afferent inputs from the masseter muscle in the C1 spinal neurons responding to tooth-pulp stimulation in rats. Exp Brain Res 160 (2005) 107-117
55. Trevisani M., Siemens J., Materazzi S., Bautista D.M., Nassini R., Campi B., Imamachi N., Andrè E., Patacchini R., Cottrell G.S., Gatti R., Basbaum A.I., Bunnett N.W., Julius D., and Geppetti P. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci 104 (2007) 13519-13524
56. Walker K.M., Urban L., Medhurst S.J., Patel S., Panesar M., Fox A.J., and McIntyre P. The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. JPET 304 (2003) 56-62
57. Wang S., Dai Y., Fukuoka T., Yamanaka H., Kobayashi K., Obata K., Cui X., Tominaga M., and Noguchi K. Phospholipase C and protein kinase A mediate bradykinin sensitization of TRPA1: a molecular mechanism of inflammatory pain. Brain 131 (2008) 1241-1251