Bosentan, a mixed endothelin receptor antagonist, inhibits superoxide anion-induced pain and inflammation in mice

Naunyn-Schmiedeberg's Archives of Pharmacology

Volumn 388, Issue 11, 2015, Pages 1211-1221

  Serafim, Karla G G ^a   Navarro, Suelen A ^a   Zarpelon, Ana C ^a   Pinho Ribeiro, Felipe A ^a   Fattori, Victor ^a   Cunha, Thiago M ^b   Alves Filho, Jose C ^b   Cunha, Fernando Q ^b   Casagrande, Rubia ^a   Verri, Waldiceu A ^a  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Bosentan; Endothelin; Inflammation; Oxidative stress; Pain; Superoxide

Indexed keywords

BOSENTAN; ENDOTHELIN; GLUTATHIONE; INTERLEUKIN 10; INTERLEUKIN 1BETA; MYELOPEROXIDASE; POTASSIUM SUPEROXIDE; PREPROENDOTHELIN 1; SUPEROXIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANALGESIC AGENT; ANTIINFLAMMATORY AGENT; CYTOKINE; ENDOTHELIN RECEPTOR ANTAGONIST; PEROXIDASE; SULFONAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CYTOKINE PRODUCTION; ENZYME ACTIVITY; GENE EXPRESSION; HYPERALGESIA; INFLAMMATORY DISEASE; LEUKOCYTE; MALE; MECHANICAL HYPERALGESIA; MONONUCLEAR CELL; MOUSE; NEUTROPHIL; NONHUMAN; OXIDATIVE STRESS; PAIN; PAW EDEMA; PERITONEAL CAVITY; SPINAL CORD; SUPEROXIDE ANION INDUCED INFLAMMATION; SUPEROXIDE ANION INDUCED PAIN; THERMAL HYPERALGESIA; ANIMAL; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; IMMUNOLOGY; SKIN;

ANALGESICS; ANIMALS; ANTI-INFLAMMATORY AGENTS; CYTOKINES; ENDOTHELIN RECEPTOR ANTAGONISTS; HYPERALGESIA; LEUKOCYTES; MALE; MICE; PAIN; PERITONEAL CAVITY; PEROXIDASE; SKIN; SPINAL CORD; SULFONAMIDES; SUPEROXIDES;

EID: 84945489357     PISSN: 00281298     EISSN: 14321912     Source Type: Journal    
DOI: 10.1007/s00210-015-1160-z     Document Type: Article

References (80)

1. Ankier SI (1974) New hot plate tests to quantify antinociceptive and narcotic antagonist activities. Eur J Pharm 1:1-4. doi: 10.1016/0014-2999(74)90195-2
2. Avdeev SN, Tsareva NA, Nekliudova GV, Chuchalin AG (2013) First clinical experience with endothelin receptor antagonist bosentan used in patients with pulmonary hypertension: results of a one-year study. Ter Arkh 85:38-43
3. Barton M, Yanagisawa M (2008) Endothelin: 20 years from discovery to therapy. Can J Physiol Pharmacol 86:485-498. doi: 10.1139/Y08-059
4. Binshtok AM, Wang H, Zimmermann K, et al (2008) Nociceptors are interleukin-1beta sensors. J Neurosci 28:14062-14073. doi: 10.1523/JNEUROSCI.3795-08.2008
5. Bradley JR (2008) TNF-mediated inflammatory disease. J Pathol 214:149-160. doi: 10.1002/path.2287
6. Bradley PP, Christensen RD, Rothstein G (1982) Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood 60:618-622
7. Casagrande R, Georgetti SR, Verri Jr WA, et al (2006) Protective effect of topical formulations containing quercetin against UVB-induced oxidative stress in hairless mice. J Photochem Photobiol B 84:21-27. doi: 10.1016/j.jphotobiol.2006.01.006
8. Channick R, Badesch DB, Tapson VF, et al (2001) Effects of the dual endothelin receptor antagonist bosentan in patients with pulmonary hypertension: a placebo-controlled study. J Hear Lung Transpl 20:262-263
9. Conte Fde P, Barja-Fidalgo C, Verri Jr WA, et al (2008) Endothelins modulate inflammatory reaction in zymosan-induced arthritis: participation of LTB4, TNF-alpha, and CXCL-1. J Leukoc Biol 84:652-660. doi: 10.1189/jlb.1207827
10. Cunha TM, Verri WA, Silva JS, et al (2005) A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc Natl Acad Sci U S A 102:1755-1760. doi: 10.1073/pnas.0409225102
11. Cunha TM, Verri WA, Vivancos GG, et al (2004) An electronic pressure-meter nociception paw test for mice. Braz J Med Biol Res 37:401-407. doi: 10.1590/S0100-879X2004000300018
12. Davar G, Hans G, Fareed MU, et al (1998) Behavioral signs of acute pain produced by application of endothelin-1 to rat sciatic nerve. Neuroreport 9:2279-2283
13. De-Melo JD, Tonussi CR, D'Orléans-Juste P, Rae GA (1998) Articular nociception induced by endothelin-1, carrageenan and LPS in naive and previously inflamed knee-joints in the rat: inhibition by endothelin receptor antagonists. Pain 77:261-269
14. Donate PB, Cunha TM, Verri Jr WA, et al (2012) Bosentan, an endothelin receptor antagonist, ameliorates collagen-induced arthritis: the role of TNF-alpha in the induction of endothelin system genes. Inflamm Res 61:337-348. doi: 10.1007/s00011-011-0415-5
15. Dusting GJ, Selemidis S, Jiang F (2005) Mechanisms for suppressing NADPH oxidase in the vascular wall. Mem Inst Oswaldo Cruz 97-103
16. Ferreira SH, Romitelli M, de Nucci G (1989) Endothelin-1 participation in overt and inflammatory pain. J Cardiovasc Pharmacol 13(Suppl 5):S220-S222. doi: 10.1097/00005344-198900135-00065
17. Fiore G, Florio P, Micheli L, et al (2005) Endothelin-1 triggers placental oxidative stress pathways: putative role in preeclampsia. J Clin Endocrinol Metab 90:4205-4210. doi: 10.1210/jc.2004-1632
18. Fuchs J, Zollner TM, Kaufmann R, Podda M (2001) Redox-modulated pathways in inflammatory skin diseases. Free Radic Biol Med 30:337-353
19. Gabriel A, Kuddus RH, Abdul SR, et al (1998) Superoxide-induced changes in endothelin (ET) receptors in hepatic stellate cells. J Hepatol 29:614-627. doi: 10.1016/S0168-8278(98)80157-8
20. Gokin AP, Fareed MU, Pan HL, et al (2001) Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J Neurosc 14:5358-5366
21. Graido-Gonzalez E, Doherty JC, Bergreen EW, et al (1998) Plasma endothelin-1, cytokine, and prostaglandin E2 levels in sickle cell disease and acute vaso-occlusive sickle crisis. Blood 92:2551-2555
22. Guerrero AT, Verri Jr WA, Cunha TM, et al (2008) Involvement of LTB4 in zymosan-induced joint nociception in mice: participation of neutrophils and PGE2. J Leukoc Biol 83:122-130. doi: 10.1189/jlb.0207123
23. Hattori H, Subramanian KK, Sakai J, et al (2010) Small-molecule screen identifies reactive oxygen species as key regulators of neutrophil chemotaxis. Proc Natl Acad Sci U S A 107:3546-3551. doi: 10.1073/pnas.0914351107
24. Hsu J-H, Oishi P, Wiseman DA, et al (2010) Nitric oxide alterations following acute ductal constriction in the fetal lamb: a role for superoxide. Am J Physiol Lung Cell Mol Physiol 298:L880-L887. doi: 10.1152/ajplung.00384.2009
25. Hung VKL, Chen SMY, Tai LW, et al (2012) Over-expression of endothelin-1 in astrocytes, but not endothelial cells, ameliorates inflammatory pain response after formalin injection. Life Sci 618-622
26. Hung VKL, Tai LW, Qiu Q, et al (2014) Over-expression of astrocytic ET-1 attenuates neuropathic pain by inhibition of ERK1/2 and Akt(s) via activation of ETA receptor. Mol Cell Neurosci 60:26-35. doi: 10.1016/j.mcn.2014.02.007
27. Jandeleit-Dahm KA, Watson AM (2012) The endothelin system and endothelin receptor antagonists. Curr Opin Nephrol Hypertens 21:66-71. doi: 10.1097/MNH.0b013e32834dde48
28. Jarvis MF, Wessale JL, Zhu CZ, et al (2000) ABT-627, an endothelin ETA receptor-selective antagonist, attenuates tactile allodynia in a diabetic rat model of neuropathic pain. Eur J Pharmacol 388:29-35. doi: 10.1016/S0014-2999(99)00865-1
29. Jewell AN, Swamydas M, Castillo CI, et al (2010) The endothelin axis stimulates the expression of pro-inflammatory cytokines and pro-migratory molecules in breast cancer. Cancer Investig 28:932-943. doi: 10.3109/07357907.2010.496757
30. Ji R-R, Kohno T, Moore KA, Woolf CJ (2003) Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26:696-705. doi: 10.1016/j.tins.2003.09.017
31. Jin X, Gereau RW (2006) Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 26:246-255. doi: 10.1523/JNEUROSCI.3858-05.2006
32. Joosten LA, Netea MG, Kim SH, et al (2006) IL-32, a proinflammatory cytokine in rheumatoid arthritis. Proc Natl Acad Sci U S A 103:3298-3303. doi: 10.1073/pnas.0511233103
33. Katalinic V, Modun D, Music I, Boban M (2005) Gender differences in antioxidant capacity of rat tissues determined by 2,2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp Biochem Physiol C Toxicol Pharmacol 140:47-52. doi: 10.1016/j.cca.2005.01.005
34. Keles S, Halici Z, Atmaca HT, et al (2014) The ocular endothelin system: a novel target for the treatment of endotoxin-induced uveitis with bosentan. Investig Ophthalmol Vis Sci 55:3517-3524. doi: 10.1167/iovs.14-14193
35. Khodorova A, Fareed MU, Gokin A, et al (2002) Local injection of a selective endothelin-B receptor agonist inhibits endothelin-1-induced pain-like behavior and excitation of nociceptors in a naloxone-sensitive manner. J Neurosci 22:7788-7796
36. Kim YO, Kim IJ, Yoon MH (2015) Antiallodynic effect through spinal endothelin-B receptor antagonism in rat models of complex regional pain syndrome. Neurosci Lett 584:45-49. doi: 10.1016/j.neulet.2014.10.005
37. Kress M, Riedl B, Reeh PW (1995) Effects of oxygen radicals on nociceptive afferents in the rat skin in vitro. Pain 62:87-94
38. Kvietys PR, Granger DN (2012) Role of reactive oxygen and nitrogen species in the vascular responses to inflammation. Free Radic Biol Med 52:556-592. doi: 10.1016/j.freeradbiomed.2011.11.002
39. Lau D, Szöcs K, Klinke A, et al (2014) Myeloperoxidase upregulates endothelin receptor type B expression. J Mol Cell Cardiol 69:76-82. doi: 10.1016/j.yjmcc.2013.12.007
40. Letizia C, Boirivant M, De Toma G, et al (1998) Plasma levels of endothelin-1 in patients with Crohn's disease and ulcerative colitis. Ital J Gastroenterol Hepatol 30:266-269
41. Liu JQ, Erbynn EM, Folz RJ (2005) Chronic hypoxia-enhanced murine pulmonary vasoconstriction: role of superoxide and gp91phox. Chest. doi: 10.1378/chest.128.6-suppl.594S
42. López-Sepúlveda R, Gómez-Guzmán M, Zarzuelo MJ, et al (2011) Red wine polyphenols prevent endothelial dysfunction induced by endothelin-1 in rat aorta: role of NADPH oxidase. Clin Sci (Lond) 120:321-333. doi: 10.1042/CS20100311
43. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
44. Maioli NA, Zarpelon AC, Mizokami SS, et al (2015) The superoxide anion donor, potassium superoxide, induces pain and inflammation in mice through production of reactive oxygen species and cyclooxygenase-2. Braz J Med Biol Res. doi: 10.1590/1414-431X20144187
45. Martínez-Revelles S, Caracuel L, Márquez-Martín A, et al (2012) Increased endothelin-1 vasoconstriction in mesenteric resistance arteries after superior mesenteric ischaemia-reperfusion. Br J Pharmacol 165:937-950. doi: 10.1111/j.1476-5381.2011.01617.x
46. Mascia L, Fedorko L, Stewart DJ, et al (2001) Temporal relationship between endothelin-1 concentrations and cerebral vasospasm in patients with aneurysmal subarachnoid hemorrhage. Stroke 32:1185-1190
47. Matsuo J, Oku H, Kanbara Y, et al (2009) Involvement of NADPH oxidase and protein kinase C in endothelin-1-induced superoxide production in retinal microvessels. Exp Eye Res 89:693-699. doi: 10.1016/j.exer.2009.06.012
48. Miyasaka N, Hirata Y, Ando K, et al (1992) Increased production of endothelin-1 in patients with inflammatory arthritides. Arthritis Rheum 35:397-400. doi: 10.1002/art.1780350406
49. Milligan ED, Sloane EM, Langer SJ, et al (2005) Controlling neuropathic pain by adeno-associated virus driven production of the anti-inflammatory cytokine, interleukin-10. Mol Pain 1:9. doi: 10.1186/1744-8069-1-9
50. Morelli S, Ferri C, Di Francesco L, et al (1995) Plasma endothelin-1 levels in patients with systemic sclerosis: influence of pulmonary or systemic arterial hypertension. Ann Rheum Dis 54:730-734. doi: 10.1136/ard.54.9.730
51. Morgan MJ, Liu ZG (2011) Crosstalk of reactive oxygen species and NF-kappaB signaling. Cell Res 21:103-115. doi: 10.1038/cr.2010.178
52. Motte S, McEntee K, Naeije R (2006) Endothelin receptor antagonists. Pharmacol Ther 110:386-414. doi: 10.1016/j.pharmthera.2005.08.012
53. Ndengele MM, Cuzzocrea S, Esposito E, et al (2008) Cyclooxygenases 1 and 2 contribute to peroxynitrite-mediated inflammatory pain hypersensitivity. FASEB J 22:3154-3164. doi: 10.1096/fj.08-108159
54. Ohanian J, Forman SP, Katzenberg G, Ohanian V (2012) Endothelin-1 stimulates small artery VCAM-1 expression through p38MAPK-dependent neutral sphingomyelinase. J Vasc Res 49:353-362. doi: 10.1159/000336649
55. Piechota A, Polanczyk A, Goraca A (2011) Protective effects of endothelin-A receptor antagonist BQ123 against LPS-induced oxidative stress in lungs. Pharmacol Rep 63:494-500
56. Pinho-Ribeiro FA, Borghi SM, Staurengo-Ferrari L, et al (2014) Bosentan, a mixed endothelin receptor antagonist, induces antidepressant-like activity in mice. Neurosci Lett 560:57-61. doi: 10.1016/j.neulet.2013.12.018
57. Pinho-Ribeiro FA, Hohmann MSN, Borghi SM, et al (2015) Protective effects of the flavonoid hesperidin methyl chalcone in inflammation and pain in mice: role of TRPV1, oxidative stress, cytokines and NF-κB. Chem Biol Interact 228:88-99. doi: 10.1016/j.cbi.2015.01.011
58. Pomonis JD, Rogers SD, Peters CM, et al (2001) Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J Neurosci 21:999-1006
59. Poole S, Cunha FQ, Selkirk S, et al (1995) Cytokine-mediated inflammatory hyperalgesia limited by interleukin-10. Br J Pharmacol 115:684-688
60. Rachid MA, Camargos ERS, Barcellos L, et al (2006) Blockade of endothelin ETA/ETB receptors favors a role for endothelin during acute Trypanosoma cruzi infection in rats. Microbes Infect 8:2113-2119. doi: 10.1016/j.micinf.2006.03.017
61. Rancourt M-E, Rodrigue M-E, Agharazii M, et al (2010) Role of oxidative stress in erythropoietin-induced hypertension in uremic rats. Am J Hypertens 23:314-320. doi: 10.1038/ajh.2009.242
62. Re R, Pellegrini N, Proteggente A, et al (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231-1237
63. Romero M, Jimenez R, Sanchez M, et al (2010) Vascular superoxide production by endothelin-1 requires Src non-receptor protein tyrosine kinase and MAPK activation. Atherosclerosis 212:78-85. doi: 10.1016/j.atherosclerosis.2010.04.031
64. Rubin LJ, Roux S (2002) Bosentan: a dual endothelin receptor antagonist. Expert Opin Investig Drugs 11:991-1002. doi: 10.1517/13543784.11.7.991
65. Sadik CD, Noack B, Schacher B, et al (2012) Cytokine production by leukocytes of Papillon-Lefevre syndrome patients in whole blood cultures. Clin Oral Investig 16:591-597. doi: 10.1007/s00784-011-0532-0
66. Scalera F, Dittrich R, Beckmann MW, Beinder E (2002) Effect of endothelin-1 on intracellular glutathione and lipid peroxide availability and on the secretion of vasoactive substances by human umbilical vein endothelial cells. Eur J Clin Investig 32:556-562. doi: 10.1046/j.1365-2362.2002.01040.x
67. Ting E, Guerrero AT, Cunha TM, et al (2008) Role of complement C5a in mechanical inflammatory hypernociception: potential use of C5a receptor antagonists to control inflammatory pain. Br J Pharmacol 153:1043-1053. doi: 10.1038/sj.bjp.0707640
68. Verri Jr WA, Cunha TM, Ferreira SH, et al (2007) IL-15 mediates antigen-induced neutrophil migration by triggering IL-18 production. Eur J Immunol 37:3373-3380. doi: 10.1002/eji.200737488
69. Verri Jr WA, Cunha TM, Magro DA, et al (2009) Targeting endothelin ETA and ETB receptors inhibits antigen-induced neutrophil migration and mechanical hypernociception in mice. Naunyn Schmiedeberg's Arch Pharmacol 379:271-279. doi: 10.1007/s00210-008-0360-1
70. Verri Jr WA, Cunha TM, Parada CA, et al (2006a) IL-15 mediates immune inflammatory hypernociception by triggering a sequential release of IFN-gamma, endothelin, and prostaglandin. Proc Natl Acad Sci U S A 103:9721-9725. doi: 10.1073/pnas.0603286103
71. Verri Jr WA, Cunha TM, Parada CA, et al (2006b) Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 112:116-138. doi: 10.1016/j.pharmthera.2006.04.001
72. Verri Jr WA, Guerrero AT, Fukada SY, et al (2008) IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice. Proc Natl Acad Sci U S A 105:2723-2728. doi: 10.1073/pnas.0712116105
73. Verri Jr WA, Schivo IR, Cunha TM, et al (2004) Interleukin-18 induces mechanical hypernociception in rats via endothelin acting on ETB receptors in a morphine-sensitive manner. J Pharmacol Exp Ther 310:710-717. doi: 10.1124/jpet.103.063990
74. Wang T, Qin L, Liu B, et al (2004a) Role of reactive oxygen species in LPS-induced production of prostaglandin E2 in microglia. J Neurochem 88:939-947
75. Wang X, Tong M, Chinta S, et al (2006) Hypoxia-induced reactive oxygen species downregulate ETB receptor-mediated contraction of rat pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 290:L570-L578. doi: 10.1152/ajplung.00262.2005
76. Wang ZQ, Porreca F, Cuzzocrea S, et al (2004b) A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 309:869-878. doi: 10.1124/jpet.103.064154
77. Yanagisawa M, Kurihara H, Kimura S, et al (1988) A novel peptide vasoconstrictor, endothelin, is produced by vascular endothelium and modulates smooth muscle Ca2+ channels. J Hypertens Suppl 6:S188-S191
78. Yayla M, Halici Z, Unal B, et al (2014) Protective effect of Et-1 receptor antagonist bosentan on paracetamol induced acute liver toxicity in rats. Eur J Pharmacol 726:87-95. doi: 10.1016/j.ejphar.2014.01.022
79. Yoon MH, Reriani M, Mario G, et al (2013) Long-term endothelin receptor antagonism attenuates coronary plaque progression in patients with early atherosclerosis. Int J Cardiol. doi: 10.1016/j.ijcard.2012.12.001
80. Zarpelon AC, Pinto LG, Cunha TM, et al (2012) Endothelin-1 induces neutrophil recruitment in adaptive inflammation via TNFalpha and CXCL1/CXCR2 in mice. Can J Physiol Pharmacol 90:187-199. doi: 10.1139/y11-116