Mechanisms involved in abdominal nociception induced by either TRPV1 or TRPA1 stimulation of rat peritoneum

European Journal of Pharmacology

Volumn 714, Issue 1-3, 2013, Pages 332-344

  Trevisan, Gabriela ^a   Rossato, Mateus F ^a   Hoffmeister, Carin ^a   Oliveira, Sara M ^a   Silva, Cássia R ^a   Matheus, Filipe C ^b   Mello, Gláucia C ^c   Antunes, Edson ^c   Prediger, Rui D S ^b   Ferreira, Juliano ^a,b  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^c UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Allyl isothiocyanate; Capsaicin; Mast cells; Pain; Resiniferatoxin; Substance p

Indexed keywords

ALLYL ISOTHIOCYANATE; APREPITANT; CAPSAICIN; CROMOGLYCATE DISODIUM; HISTAMINE; MYELOPEROXIDASE; NEUROKININ 1 RECEPTOR; PROMETHAZINE; PROTEIN C FOS; RESINIFERATOXIN; SUBSTANCE P; TRANSIENT RECEPTOR POTENTIAL CHANNEL A1; VANILLOID RECEPTOR 1;

ABDOMINAL PAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DESENSITIZATION; IN VITRO STUDY; MALE; MAST CELL; MAST CELL DEGRANULATION; NOCICEPTION; NONHUMAN; PERITONEAL FLUID; PERITONEUM; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSORY NERVE; SPINAL CORD DORSAL HORN;

ALLYL ISOTHIOCYANATE; CAPSAICIN; MAST CELLS; PAIN; RESINIFERATOXIN; SUBSTANCE P;

ANIMALS; CAPSAICIN; GASTROINTESTINAL TRANSIT; INTESTINES; ISOTHIOCYANATES; MACROPHAGES; MALE; MAST CELLS; NOCICEPTION; PERITONEUM; RATS; RATS, WISTAR; RECEPTORS, NEUROKININ-1; SUBSTANCE P; TRPC CATION CHANNELS; TRPV CATION CHANNELS;

EID: 84885434342     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.07.029     Document Type: Article

References (65)

1. Akbar, A., Yiangou, Y., Facer, P., Walters, J.R., Anand, P., Ghosh, S., 2008. Increased capsaicin receptor TRPV1-expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut 57, 923-929. (Pubitemid 351919527)
2. Akopian, A.N., 2011. Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Current Pharmaceutical Biotechnology 12, 89-94.
3. An, J.X., He, Y., Qian, X.Y., Wu, J.P., Xie, Y.K., Guo, Q.L., Williams, J.P., Cope, D.K., 2011. A new animal model of trigeminal neuralgia produced by administration of cobra venom to the infraorbital nerve in the rat. Anesthesia & Analgesia 113, 652-656.
4. Anaf, V., Chapron, C., El Nakadi, I., De Moor, V., Simonart, T., Noel, J.C., 2006. Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endome-triosis. Fertility and Sterility 86, 1336-1343. (Pubitemid 44740094)
5. Anand, P., Bley, K., 2011. Topical capsaicin for pain management: therapeutic potential and mechanisms of action of the new high-concentration capsaicin 8% patch. British Journal of Anaesthesia 107, 490-502.
6. Andrade, E.L., Ferreira, J., Andre, E., Calixto, J.B., 2006. Contractile mechanisms coupled to TRPA1 receptor activation in rat urinary bladder. Biochemical Pharmacology 72, 104-114. (Pubitemid 43795342)
7. Andrade, E.L., Luiz, A.P., Ferreira, J., Calixto, J.B., 2008. Pronociceptive response elicited by TRPA1 receptor activation in mice. Neuroscience 152, 511-520.
8. Andrade, E.L., Meotti, F.C., Calixto, J.B., 2012. TRPA1 antagonists as potential analgesic drugs. Pharmacology & Therapeutics 133, 189-204.
9. Ansel, J.C., Brown, J.R., Payan, D.G., Brown, M.A., 1993. Substance P selectively activates TNF-alpha gene expression in murine mast cells. The Journal of Immunology 150, 4478-4485. (Pubitemid 23133724)
10. Banvolgyi, A., Pozsgai, G., Brain, S.D., Helyes, Z.S., Szolcsanyi, J., Ghosh, M., Melegh, B., Pinter, E., 2004. Mustard oil induces a transient receptor potential vanilloid 1 receptor-independent neurogenic inflammation and a non-neuro-genic cellular inflammatory component in mice. Neuroscience 125, 449-459. (Pubitemid 38446750)
11. Bautista, D.M., Movahed, P., Hinman, A., Axelsson, H.E., Sterner, O., Hogestatt, E.D., Julius, D., Jordt, S.E., Zygmunt, P.M., 2005. Pungent products from garlic activate the sensory ion channel TRPA1. Proceedings of the National Academy of Sciences of the United States of America 102, 12248-12252. (Pubitemid 41291160)
12. Biro, T., Maurer, M., Modarres, S., Lewin, N.E., Brodie, C., Acs, G., Acs, P., Paus, R., Blumberg, P.M., 1998. Characterization of functional vanilloid receptors expressed by mast cells. Blood 91, 1332-1340. (Pubitemid 28086887)
13. Bonaz, B., Plourde, V., Tache, Y., 1994. Abdominal surgery induces fosimmunor-eactivity in the rat brain. Journal of Comparative Neurology 349, 212-222. (Pubitemid 24331249)
14. Bonaz, B., Rivière, P.J., Sinniger, V., Pascaud, X., Junien, J.L., Fournet, J., Feuerstein, C., 2000. Fedotozine, a kappa-opioid agonist, prevents spinal and supra-spinal Fos expression induced by a noxious visceral stimulus in the rat. Neurogastroen-terology and Motility 12, 135-147. (Pubitemid 30182074)
15. Brozmanova, M., Mazurova, L., Ru, F., Tatar, M., Kollarik, M., 2012. Comparison of TRPA1-versus TRPV1-mediated cough in guinea pigs. European Journal of Pharmacology 689, 211-218.
16. Caterina, M.J., Leffler, A., Malmberg, A.B., Martin, W.J., Trafton, J., Petersen-Zeitz, K.R., Koltzenburg, M., Basbaum, A.I., Julius, D., 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288, 306-313. (Pubitemid 30226186)
17. Cortright, D.N., Szallasi, A., 2009. TRP channels and pain. Current Pharmaceutical Design 15, 1736-1749.
18. Desouza, I.A., Camargo, E.A., Mariano, N.S., Optiz-Neto, J.B., Resende, J.S., Mello, G.C., Costa, S.K., De Nucci, G., Antunes, E., 2009. Role of sensory innervation in the rat pulmonary neutrophil recruitment induced by staphylococcal enterotoxins type A and B. European Journal of Pharmacology 613, 128-134.
19. Elsayes, K.M., Staveteig, P.T., Narra, V.R., Leyendecker, J.R., Lewis Jr., J.S., Brown, J.J., 2006. MRI of the peritoneum: spectrum of abnormalities. AJR American Journal of Roentgenology 186, 1368-1379. (Pubitemid 46112575)
20. Everaerts, W., Gees, M., Alpizar, Y.A., Farre, R., Leten, C., Apetrei, A., Dewachter, I., van Leuven, F., Vennekens, R., De Ridder, D., Nilius, B., Voets, T., Talavera, K., 2011. The capsaicin receptor TRPV1 is a crucial mediator of the noxious effects of mustard oil. Current Biology 21, 316-321.
21. Ferreira, J., da Silva, G.L., Calixto, J.B., 2004. Contribution of vanilloid receptors to the overt nociception induced by B2 kinin receptor activation in mice. British Journal of Pharmacology 141, 787-794. (Pubitemid 38446179)
22. Flasar, M.H., Goldberg, E., 2006. Acute abdominal pain. Medical Clinics of North America 90, 481-503. (Pubitemid 43213192)
23. Futamura, M., Goto, S., Kimura, R., Kimoto, I., Miyake, M., Ito, K., Sakamoto, T., 2009. Differential effects of topically applied formalin and aromatic compounds on neurogenic-mediated microvascular leakage in rat skin. Toxicology 255, 100-106.
24. Geppetti, P., Nassini, R., Materazzi, S., Benemei, S., 2008. The concept of neurogenic inflammation. BJU International 101 (3), 2-6. (Pubitemid 351328798)
25. Giudice, E.D., Rinaldi, L., Passarotto, M., Facchinetti, F., D'Arrigo, A., Guiotto, A., Carbonare, M.D., Battistin, L., Leon, A., 2007. Cannabidiol, unlike synthetic cannabinoids, triggers activation of RBL-2H3 mast cells. Journal of Leukocyte Biology 81, 1512-1522. (Pubitemid 46827974)
26. Holtman Jr., J.R., Crooks, P.A., Johnson-Hardy, J., Wala, E.P., 2010. Antinociceptive effects and toxicity of morphine-6-O-sulfate sodium salt in rat models of pain. European Journal of Pharmacology 648, 87-94.
27. Hsieh, Y.L., Chiang, H., Tseng, T.J., Hsieh, S.T., 2008. Enhancement of cutaneous nerve regeneration by 4-methylcatechol in resiniferatoxin-induced neuropathy. Journal of Neuropathology & Experimental Neurology 67, 93-104.
28. Ikeda, Y., Ueno, A., Naraba, H., Ohishi, S., 2001. Involvement of vanilloid receptor VR1 and prostanoids in the acid-induced writhing responses of mice. Life Science 69, 2911-2919. (Pubitemid 33030279)
29. Inoue, H., Nagata, N., Koshihara, Y., 1993. Profile of capsaicin-induced mouse ear oedema as neurogenic inflammatory model: comparison with arachidonic acid-induced ear oedema. British Journal of Pharmacology 110, 1614-1620. (Pubitemid 23361002)
30. Jakab, B., Helyes, Z., Varga, A., Bolcskei, K., Szabo, A., Sandor, K., Elekes, K., Borzsei, R., Keszthelyi, D., Pinter, E., Petho, G., Nemeth, J., Szolcsanyi, J., 2005. Pharmacological characterization of the TRPV1 receptor antagonist JYL1421 (SC0030) in vitro and in vivo in the rat. European Journal of Pharmacology 517, 35-44. (Pubitemid 40910250)
31. Jara-Oseguera, A., Simon, S.A., Rosenbaum, T., 2008. TRPV1: on the road to pain relief. Current Molecular Pharmacology 1, 255-269.
32. Jordt, S.E., Bautista, D.M., Chuang, H.H., McKemy, D.D., Zygmunt, P.M., Hogestatt, E. D., Meng, I.D., Julius, D., 2004. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427, 260-265. (Pubitemid 38112043)
33. Kamei, K., Yasuda, T., Ueda, T., Qiang, F., Takeyama, Y., Shiozaki, H., 2010. Role of triggering receptor expressed on myeloid cells-1 in experimental severe acute pancreatitis. Journal of Hepato-Biliary-Pancreatic Sciences 17, 305-312.
34. Kopczynska, B., 2008. Role of VR1 and CB1 receptors in modelling of cardio-respiratory response to arvanil, an endocannabinoid and vanilloid hybrid, in rats. Life Science 83, 85-91.
35. Lantéri-Minet, M., Isnardon, P., de Pommery, J., Menetrey, D., 1993. Spinal and hindbrain structures involved in visceroception and visceronociception as revealed by the expression of Fos, Jun and Krox-24 proteins. Neuroscience 55, 737-753. (Pubitemid 23226119)
36. Lapointe, T.K., Altier, C., 2011. The role of TRPA1 in visceral inflammation and pain. Channels (Austin) 5, 525-529.
37. Mactier, R.A., Sprosen, T.S., Gokal, R., Williams, P.F., Lindbergh, M., Naik, R.B., Wrege, U., Grontoft, K.C., Larsson, R., Berglund, J., Tranaeus, A.P., Faict, D., 1998. Bicarbonate and bicarbonate/lactate peritoneal dialysis solutions for the treatment of infusion pain. Kidney International 53, 1061-1067. (Pubitemid 28155684)
38. Malin, S., Molliver, D., Christianson, J.A., Schwartz, E.S., Cornuet, P., Albers, K.M., Davis, B.M., 2011. TRPV1 and TRPA1 function and modulation are target tissue dependent. The Journal of Neuroscience 31, 10516-10528.
39. Massaad, C.A., Safieh-Garabedian, B., Poole, S., Atweh, S.F., Jabbur, S.J., Saade, N.E., 2004. Involvement of substance P, CGRP and histamine in the hyperalgesia and cytokine upregulation induced by intraplantar injection of capsaicin in rats. Journal of Neuroimmunology 153, 171-182. (Pubitemid 38950939)
40. Millan, M.J., Dekeyne, A., Gobert, A., Mannoury la Cour, C., Brocco, M., Rivet, J.M., Di Cara, B., Lejeune, F., Cremers, T.I., Flik, G., de Jong, T.R., Olivier, B., de Nanteuil, G., 2010. S41744, a dual neurokinin (NK)1 receptor antagonist and serotonin (5-HT) reuptake inhibitor with potential antidepressant properties: a comparison to aprepitant (MK869) and paroxetine. European Neuropsychopharmacology 20, 599-621.
41. Moran, M.M., McAlexander, M.A., Biro, T., Szallasi, A., 2011. Transient receptor potential channels as therapeutic targets. Nature Reviews Drug Discovery 10, 601-620.
42. Ogawa, K., Nabe, T., Yamamura, H., Kohno, S., 1999. Nanomolar concentrations of neuropeptides induce histamine release from peritoneal mast cells of a substrain of Wistar rats. European Journal of Pharmacology 374, 285-291. (Pubitemid 29287144)
43. Ohta, Y., Kobayashi, T., Inui, K., Yoshino, J., Nakazawa, S., 2003. Protective effect of teprenone against acute gastric mucosal lesions induced by compound 48/80, a mast cell degranulator, in rats. Journal of Pharmacological Sciences 93, 337-346. (Pubitemid 37521356)
44. Okada, T., Hirayama, Y., Kishi, S., Miyayasu, K., Hiroi, J., Fujii, T., 1999. Functional neurokinin NK-1 receptor expression in rat peritoneal mast cells. Inflammation Research 48, 274-279. (Pubitemid 29257619)
45. Oliveira, S.M., Drewes, C.C., Silva, C.R., Trevisan, G., Boschen, S.L., Moreira, C.G., de Almeida Cabrini, D., Da Cunha, C., Ferreira, J., 2011. Involvement of mast cells in a mouse model of postoperative pain. European Journal of Pharmacology 672, 88-95.
46. Pecze, L., Pelsoczi, P., Kecskes, M., Winter, Z., Papp, A., Kaszas, K., Letoha, T., Vizler, C., Olah, Z., 2009. Resiniferatoxin mediated ablation of TRPV1+ neurons removes TRPA1 as well. Canadian Journal of Neurological Sciences 36, 234-241.
47. Pereira, L.M., Lima-Junior, R.C., Bem, A.X., Teixeira, C.G., Grassi, L.S., Medeiros, R.P., Marques-Neto, R.D., Callado, R.B., Aragao, K.S., Wong, D.V., Vale, M.L., Brito, G.A., Ribeiro, R.A., 2012. Blockade of TRPA1 with HC-030031 attenuates visceral nociception by a mechanism independent of inflammatory resident cells, nitric oxide and the opioid system. European Journal of Pain 2012, 1532-2149.
48. Porreca, F., Mosberg, H.I., Omnaas, J.R., Burks, T.F., Cowan, A., 1987. Supraspinal and spinal potency of selective opioid agonists in the mouse writhing test. Journal of Pharmacology and Experimental Therapeutics 240, 890-894. (Pubitemid 17043590)
49. Prasad, P., Yanagihara, A.A., Small-Howard, A.L., Turner, H., Stokes, A.J., 2008. Secretogranin III directs secretory vesicle biogenesis in mast cells in a manner dependent upon interaction with chromogranin A. The Journal of Immunology 181, 5024-5034.
50. Ribeiro, R.A., Vale, M.L., Thomazzi, S.M., Paschoalato, A.B., Poole, S., Ferreira, S.H., Cunha, F.Q., 2000. Involvement of resident macrophages and mast cells in the writhing nociceptive response induced by zymosan and acetic acid in mice. European Journal of Pharmacology 387, 111-118. (Pubitemid 30035382)
51. Richardson, J.D., Vasko, M.R., 2002. Cellular mechanisms of neurogenic inflammation. Journal of Pharmacology and Experimental Therapeutics 302, 839-845. (Pubitemid 34920202)
52. Santos, A.R., Calixto, J.B., 1997. Further evidence for the involvement of tachykinin receptor subtypes in formalin and capsaicin models of pain in mice. Neuropep-tides 31, 381-389. (Pubitemid 27394786)
53. Sauzem, P.D., Sant'Anna, Gda, S., Machado, P., Duarte, M.M., Ferreira, J., Mello, C.F., Beck, P., Bonacorso, H.G., Zanatta, N., Martins, M.A., Rubin, M.A., 2009. Effect of 5-trifluoromethyl-4,5-dihydro-1H-pyrazoles on chronic inflammatory pain model in rats. European Journal of Pharmacology 616, 91-100.
54. Schmauss, C., Yaksh, T.L., 1984. In vivo studies on spinal opiate receptor systems mediating antinociception. II. Pharmacological profiles suggesting a differential association of mu, delta and kappa receptors with visceral chemical and cutaneous thermal stimuli in the rat. Journal of Pharmacology and Experimental Therapeutics 228, 1-12. (Pubitemid 14223374)
55. Schwartz, E.S., Christianson, J.A., Chen, X., La, J.H., Davis, B.M., Albers, K.M., Gebhart, G.F., 2011. Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation. Gastroenterology 140 (1283-1291), e1281-e1282.
56. Sinniger, V., Mouchet, P., Bonaz, B., 2005. Effect of nor-trimebutine on neuronal activation induced by a noxious stimulus or an acute colonic inflammation in the rat. Life Science 77, 2927-2941. (Pubitemid 41390956)
57. Stander, S., Moormann, C., Schumacher, M., Buddenkotte, J., Artuc, M., Shpacovitch, V., Brzoska, T., Lippert, U., Henz, B.M., Luger, T.A., Metze, D., Steinhoff, M., 2004. Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Experimental Dermatology 13, 129-139. (Pubitemid 38380276)
58. Steiner, A.A., Turek, V.F., Almeida, M.C., Burmeister, J.J., Oliveira, D.L., Roberts, J.L., Bannon, A.W., Norman, M.H., Louis, J.C., Treanor, J.J., Gavva, N.R., Romanovsky, A.A., 2007. Nonthermal activation of transient receptor potential vanilloid-1 channels in abdominal viscera tonically inhibits autonomic cold-defense effectors. Journal of Neuroscience 27, 7459-7468. (Pubitemid 47066573)
59. 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., Patapoutian, A., 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112, 819-829. (Pubitemid 36378884)
60. Suzuki, H., Miura, S., Liu, Y.Y., Tsuchiya, M., Ishii, H., 1995. Substance P induces degranulation of mast cells and leukocyte adhesion to venular endothelium. Peptides 16, 1447-1452.
61. Suzuki, R., Furuno, T., McKay, D.M., Wolvers, D., Teshima, R., Nakanishi, M., Bienenstock, J., 1999. Direct neurite-mast cell communication in vitro occurs via the neuropeptide substance P. The Journal of Immunology 163, 2410-2415. (Pubitemid 29399159)
62. Tanaka, K., Matsugami, T., Chiba, T., 2002. The origin of sensory innervation of the peritoneum in the rat. Anatomy and Embryology (Berlin) 205, 307-313. (Pubitemid 34824172)
63. Weller, K., Reeh, P.W., Sauer, S.K., 2011. TRPV1, TRPA1, and CB1 in the isolated vagus nerve - axonal chemosensitivity and control of neuropeptide release. Neuro-peptides 45, 391-400.
64. Xu, H., Blair, N.T., Clapham, D.E., 2005. Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. Journal of Neuroscience 25, 8924-8937. (Pubitemid 41384461)
65. Zimmermann, M., 1983. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16, 109-110. (Pubitemid 13058546)