Peripheral P2X7 receptor-induced mechanical hyperalgesia is mediated by bradykinin

Neuroscience

Volumn 277, Issue , 2014, Pages 163-173

  Teixeira, J M ^a   de Oliveira Fusaro, M C G ^a   Parada, C A ^a   Tambeli, C H ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

BzATP; Inflammatory mediators; Mechanical hyperalgesia; P2X7 receptor; Pro inflammatory cytokines

Indexed keywords

BRADYKININ; BRADYKININ B1 RECEPTOR; BRADYKININ B2 RECEPTOR; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROSTAGLANDIN E2; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X7 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; 3'-O-(4-BENZOYL)BENZOYLADENOSINE 5'-TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CXCL1 CHEMOKINE; CXCL1 PROTEIN, RAT; CYTOKINE; IL1B PROTEIN, RAT; PURINERGIC P2X2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; HYPERALGESIA; MALE; MECHANICAL HYPERALGESIA; MOLECULAR PATHOLOGY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RECEPTOR UPREGULATION; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; HINDLIMB; IMMUNOMODULATION; METABOLISM; SUBCUTANEOUS TISSUE; TOUCH; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRADYKININ; CHEMOKINE CXCL1; CYTOKINES; DISEASE MODELS, ANIMAL; HINDLIMB; HYPERALGESIA; INTERLEUKIN-1BETA; MALE; NEUROIMMUNOMODULATION; RATS, WISTAR; RECEPTORS, PURINERGIC P2X1; RECEPTORS, PURINERGIC P2X2; RECEPTORS, PURINERGIC P2X3; RECEPTORS, PURINERGIC P2X7; SUBCUTANEOUS TISSUE; TOUCH;

EID: 84904871792     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2014.06.057     Document Type: Article

References (95)

1. Allibardi S., Merati G., Chierchia S., Samaja M. Atenolol depresses post-ischaemic recovery in the isolated rat heart. Pharmacol Res 1999, 39:431-435.
2. Barrett A.M. The pharmacology of atenolol. Postgrad Med J 1977, 53(Suppl. 3):58-64.
3. Baumann H., Gauldie J. The acute phase response. Immunol Today 1994, 15:74-80.
4. Beigi R., Kobatake E., Aizawa M., Dubyak G.R. Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase. Am J Physiol 1999, 276:C267-C278.
5. Belichard P., Landry M., Faye P., Bachvarov D.R., Bouthillier J., Pruneau D., Marceau F. Inflammatory hyperalgesia induced by zymosan in the plantar tissue of the rat: effect of kinin receptor antagonists. Immunopharmacology 2000, 46:139-147.
6. Bianchi B.R., Lynch K.J., Touma E., Niforatos W., Burgard E.C., Alexander K.M., Park H.S., Yu H., Metzger R., Kowaluk E., Jarvis M.F., van Biesen T. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 1999, 376:127-138.
7. Bilski A.J., Halliday S.E., Fitzgerald J.D., Wale J.L. The pharmacology of a beta 2-selective adrenoceptor antagonist (ICI 118,551). J Cardiovasc Pharmacol 1983, 5:430-437.
8. Bryan M.C., Biswas K., Peterkin T.A., Rzasa R.M., Arik L., Lehto S.G., Sun H., Hsieh F.Y., Xu C., Fremeau R.T., Allen J.R. Chromenones as potent bradykinin B1 antagonists. Bioorg Med Chem Lett 2012, 22:619-622.
9. Buell G., Collo G., Rassendren F. P2X receptors: an emerging channel family. Eur J Neurosci 1996, 8:2221-2228.
10. Burgess G.M., Perkins M.N., Rang H.P., Campbell E.A., Brown M.C., McIntyre P., Urban L., Dziadulewicz E.K., Ritchie T.J., Hallett A., Snell C.R., Wrigglesworth R., Lee W., Davis C., Phagoo S.B., Davis A.J., Phillips E., Drake G.S., Hughes G.A., Dunstan A., Bloomfield G.C. Bradyzide, a potent non-peptide B(2) bradykinin receptor antagonist with long-lasting oral activity in animal models of inflammatory hyperalgesia. Br J Pharmacol 2000, 129:77-86.
11. Calixto J.B., Cabrini D.A., Ferreira J., Campos M.M. Kinins in pain and inflammation. Pain 2000, 87:1-5.
12. Campwala H., Fountain S.J. Constitutive and agonist stimulated ATP secretion in leukocytes. Commun Integr Biol 2013, 6:e23631.
13. Carreira E.U., Carregaro V., Teixeira M.M., Moriconi A., Aramini A., Verri W.A., Ferreira S.H., Cunha F.Q., Cunha T.M. Neutrophils recruited by CXCR1/2 signalling mediate post-incisional pain. Eur J Pain 2013, 17:654-663.
14. Chakfe Y., Seguin R., Antel J.P., Morissette C., Malo D., Henderson D., Seguela P. ADP and AMP induce interleukin-1beta release from microglial cells through activation of ATP-primed P2X7 receptor channels. J Neurosci 2002, 22:3061-3069.
15. Cherkas P.S., Dostrovsky J.O., Sessle B.J. Activation of peripheral P2X receptors is sufficient to induce central sensitization in rat medullary dorsal horn nociceptive neurons. Neurosci Lett 2012, 526:160-163.
16. Chessell I.P., Hatcher J.P., Bountra C., Michel A.D., Hughes J.P., Green P., Egerton J., Murfin M., Richardson J., Peck W.L., Grahames C.B., Casula M.A., Yiangou Y., Birch R., Anand P., Buell G.N. Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005, 114:386-396.
17. Chiozzi P., Sanz J.M., Ferrari D., Falzoni S., Aleotti A., Buell G.N., Collo G., Di Virgilio F. Spontaneous cell fusion in macrophage cultures expressing high levels of the P2Z/P2X7 receptor. J Cell Biol 1997, 138:697-706.
18. Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology 2012, 51(Suppl 5):v3-v11.
19. Clark A.K., Staniland A.A., Marchand F., Kaan T.K., McMahon S.B., Malcangio M. P2X7-dependent release of interleukin-1beta and nociception in the spinal cord following lipopolysaccharide. J Neurosci 2010, 30:573-582.
20. Collo G., Neidhart S., Kawashima E., Kosco-Vilbois M., North R.A., Buell G. Tissue distribution of the P2X7 receptor. Neuropharmacology 1997, 36:1277-1283.
21. Colomar A., Marty V., Medina C., Combe C., Parnet P., Amedee T. Maturation and release of interleukin-1beta by lipopolysaccharide-primed mouse Schwann cells require the stimulation of P2X7 receptors. J Biol Chem 2003, 278:30732-30740.
22. Costello A.H., Hargreaves K.M. Suppression of carrageenan-induced hyperalgesia, hyperthermia and edema by a bradykinin antagonist. Eur J Pharmacol 1989, 171:259-263.
23. Couture R., Harrisson M., Vianna R.M., Cloutier F. Kinin receptors in pain and inflammation. Eur J Pharmacol 2001, 429:161-176.
24. Cunha F.Q., Lorenzetti B.B., Poole S., Ferreira S.H. Interleukin-8 as a mediator of sympathetic pain. Br J Pharmacol 1991, 104:765-767.
25. Cunha F.Q., Poole S., Lorenzetti B.B., Ferreira S.H. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol 1992, 107:660-664.
26. Cunha T.M., Verri W.A., Schivo I.R., Napimoga M.H., Parada C.A., Poole S., Teixeira M.M., Ferreira S.H., Cunha F.Q. Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J Leukoc Biol 2008, 83:824-832.
27. de Oliveira Fusaro M.C., Pelegrini-da-Silva A., Araldi D., Parada C.A., Tambeli C.H. P2X3 and P2X2/3 receptors mediate mechanical hyperalgesia induced by bradykinin, but not by pro-inflammatory cytokines, PGE(2) or dopamine. Eur J Pharmacol 2010, 649:177-182.
28. Dell'Antonio G., Quattrini A., Cin E.D., Fulgenzi A., Ferrero M.E. Relief of inflammatory pain in rats by local use of the selective P2X7 ATP receptor inhibitor, oxidized ATP. Arthritis Rheum 2002, 46:3378-3385.
29. Dell'Antonio G., Quattrini A., Dal Cin E., Fulgenzi A., Ferrero M.E. Antinociceptive effect of a new P(2Z)/P2X7 antagonist, oxidized ATP, in arthritic rats. Neurosci Lett 2002, 327:87-90.
30. Dubyak G.R., el-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol 1993, 265:C577-C606.
31. Ferrari D., Villalba M., Chiozzi P., Falzoni S., Ricciardi-Castagnoli P., Di Virgilio F. Mouse microglial cells express a plasma membrane pore gated by extracellular ATP. J Immunol 1996, 156:1531-1539.
32. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Collo G., Buell G., Di Virgilio F. ATP-mediated cytotoxicity in microglial cells. Neuropharmacology 1997, 36:1295-1301.
33. Ferrari D., Chiozzi P., Falzoni S., Dal Susino M., Melchiorri L., Baricordi O.R., Di Virgilio F. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J Immunol 1997, 159:1451-1458.
34. Ferreira S.H., Lorenzetti B.B., Cunha F.Q., Poole S. Bradykinin release of TNF-alpha plays a key role in the development of inflammatory hyperalgesia. Agents Actions 1993, 38. Spec No:C7-9.
35. Ferreira S.H., Lorenzetti B.B., Poole S. Bradykinin initiates cytokine-mediated inflammatory hyperalgesia. Br J Pharmacol 1993, 110:1227-1231.
36. Ferreira J., Campos M.M., Pesquero J.B., Araujo R.C., Bader M., Calixto J.B. Evidence for the participation of kinins in Freund's adjuvant-induced inflammatory and nociceptive responses in kinin B1 and B2 receptor knockout mice. Neuropharmacology 2001, 41:1006-1012.
37. Ferreira J., Triches K.M., Medeiros R., Cabrini D.A., Mori M.A., Pesquero J.B., Bader M., Calixto J.B. The role of kinin B1 receptors in the nociception produced by peripheral protein kinase C activation in mice. Neuropharmacology 2008, 54:597-604.
38. Filippini A., Taffs R.E., Agui T., Sitkovsky M.V. Ecto-ATPase activity in cytolytic T-lymphocytes. Protection from the cytolytic effects of extracellular ATP. J Biol Chem 1990, 265:334-340.
39. Fox A., Wotherspoon G., McNair K., Hudson L., Patel S., Gentry C., Winter J. Regulation and function of spinal and peripheral neuronal B1 bradykinin receptors in inflammatory mechanical hyperalgesia. Pain 2003, 104:683-691.
40. Fulgenzi A., Dell'Antonio G., Foglieni C., Dal Cin E., Ticozzi P., Franzone J.S., Ferrero M.E. Inhibition of chemokine expression in rat inflamed paws by systemic use of the antihyperalgesic oxidized ATP. BMC Immunol 2005, 6:18.
41. Fulgenzi A., Ticozzi P., Gabel C.A., Dell Antonio G., Quattrini A., Franzone J.S., Ferrero M.E. Periodate oxidized ATP (OATP) reduces hyperalgesia in mice: involvement of P2X7 receptors and implications for therapy. Int J Immunopathol Pharmacol 2008, 21:61-71.
42. Galli S.J., Kalesnikoff J., Grimbaldeston M.A., Piliponsky A.M., Williams C.M., Tsai M. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu Rev Immunol 2005, 23:749-786.
43. Gold M.S., Shuster M.J., Levine J.D. Role of a Ca(2+)-dependent slow after hyperpolarization in prostaglandin E2-induced sensitization of cultured rat sensory neurons. Neurosci Lett 1996, 205:161-164.
44. Gomis A., Meini S., Miralles A., Valenti C., Giuliani S., Belmonte C., Maggi C.A. Blockade of nociceptive sensory afferent activity of the rat knee joint by the bradykinin B2 receptor antagonist fasitibant. Osteoarthritis Cartilage 2013, 21:1346-1354.
45. Gourine A.V., Poputnikov D.M., Zhernosek N., Melenchuk E.V., Gerstberger R., Spyer K.M., Gourine V.N. P2 receptor blockade attenuates fever and cytokine responses induced by lipopolysaccharide in rats. Br J Pharmacol 2005, 146:139-145.
46. Greig A.V., Linge C., Terenghi G., McGrouther D.A., Burnstock G. Purinergic receptors are part of a functional signaling system for proliferation and differentiation of human epidermal keratinocytes. J Invest Dermatol 2003, 120:1007-1015.
47. Hide I., Tanaka M., Inoue A., Nakajima K., Kohsaka S., Inoue K., Nakata Y. Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. J Neurochem 2000, 75:965-972.
48. Honore P., Donnelly-Roberts D., Namovic M.T., Hsieh G., Zhu C.Z., Mikusa J.P., Hernandez G., Zhong C., Gauvin D.M., Chandran P., Harris R., Medrano A.P., Carroll W., Marsh K., Sullivan J.P., Faltynek C.R., Jarvis M.F. A-740003 [N-(1-{[(cyanoimino)(5-quinolinylamino)methyl]amino}-2,2-dimethylpropyl)-2-(3,4-dimethoxyphenyl) acetamide], a novel and selective P2X7 receptor antagonist, dose-dependently reduces neuropathic pain in the rat. J Pharmacol Exp Ther 2006, 319:1376-1385.
49. Honore P., Donnelly-Roberts D., Namovic M., Zhong C., Wade C., Chandran P., Zhu C., Carroll W., Perez-Medrano A., Iwakura Y., Jarvis M.F. The antihyperalgesic activity of a selective P2X7 receptor antagonist, A-839977, is lost in IL-1alphabeta knockout mice. Behav Brain Res 2009, 204:77-81.
50. Jacobson K.A., Jarvis M.F., Williams M. Purine and pyrimidine (P2) receptors as drug targets. J Med Chem 2002, 45:4057-4093.
51. Jain N.K., Kulkarni S.K., Singh A. Role of cysteinyl leukotrienes in nociceptive and inflammatory conditions in experimental animals. Eur J Pharmacol 2001, 423:85-92.
52. Jarvis M.F., Wismer C.T., Schweitzer E., Yu H., van Biesen T., Lynch K.J., Burgard E.C., Kowaluk E.A. Modulation of BzATP and formalin induced nociception: attenuation by the P2X receptor antagonist, TNP-ATP and enhancement by the P2X(3) allosteric modulator, cibacron blue. Br J Pharmacol 2001, 132:259-269.
53. Kahlenberg J.M., Dubyak G.R. Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am J Physiol Cell Physiol 2004, 286:C1100-C1108.
54. Khasar S.G., McCarter G., Levine J.D. Epinephrine produces a beta-adrenergic receptor-mediated mechanical hyperalgesia and in vitro sensitization of rat nociceptors. J Neurophysiol 1999, 81:1104-1112.
55. Kim M., Spelta V., Sim J., North R.A., Surprenant A. Differential assembly of rat purinergic P2X7 receptor in immune cells of the brain and periphery. J Biol Chem 2001, 276:23262-23267.
56. la Sala A., Ferrari D., Di Virgilio F., Idzko M., Norgauer J., Girolomoni G. Alerting and tuning the immune response by extracellular nucleotides. J Leukoc Biol 2003, 73:339-343.
57. Ley K., Linnemann G., Meinen M., Stoolman L.M., Gaehtgens P. Fucoidin, but not yeast polyphosphomannan PPME, inhibits leukocyte rolling in venules of the rat mesentery. Blood 1993, 81:177-185.
58. Loram L.C., Fuller A., Fick L.G., Cartmell T., Poole S., Mitchell D. Cytokine profiles during carrageenan-induced inflammatory hyperalgesia in rat muscle and hind paw. J Pain 2007, 8:127-136.
59. Marceau F., Hess J.F., Bachvarov D.R. The B1 receptors for kinins. Pharmacol Rev 1998, 50:357-386.
60. McGaraughty S., Chu K.L., Namovic M.T., Donnelly-Roberts D.L., Harris R.R., Zhang X.F., Shieh C.C., Wismer C.T., Zhu C.Z., Gauvin D.M., Fabiyi A.C., Honore P., Gregg R.J., Kort M.E., Nelson D.W., Carroll W.A., Marsh K., Faltynek C.R., Jarvis M.F. P2X7-related modulation of pathological nociception in rats. Neuroscience 2007, 146:1817-1828.
61. Mingam R., De Smedt V., Amedee T., Bluthe R.M., Kelley K.W., Dantzer R., Laye S. In vitro and in vivo evidence for a role of the P2X7 receptor in the release of IL-1 beta in the murine brain. Brain Behav Immun 2008, 22:234-244.
62. Mizumoto N., Mummert M.E., Shalhevet D., Takashima A. Keratinocyte ATP release assay for testing skin-irritating potentials of structurally diverse chemicals. J Invest Dermatol 2003, 121:1066-1072.
63. Neelands T.R., Burgard E.C., Uchic M.E., McDonald H.A., Niforatos W., Faltynek C.R., Lynch K.J., Jarvis M.F. 2', 3'-O-(2,4,6, trinitrophenyl)-ATP and A-317491 are competitive antagonists at a slowly desensitizing chimeric human P2X3 receptor. Br J Pharmacol 2003, 140:202-210.
64. Nelson D.W., Gregg R.J., Kort M.E., Perez-Medrano A., Voight E.A., Wang Y., Grayson G., Namovic M.T., Donnelly-Roberts D.L., Niforatos W., Honore P., Jarvis M.F., Faltynek C.R., Carroll W.A. Structure-activity relationship studies on a series of novel, substituted 1-benzyl-5-phenyltetrazole P2X7 antagonists. J Med Chem 2006, 49:3659-3666.
65. Oliveira M.C., Pelegrini-da-Silva A., Parada C.A., Tambeli C.H. 5-HT acts on nociceptive primary afferents through an indirect mechanism to induce hyperalgesia in the subcutaneous tissue. Neuroscience 2007, 145:708-714.
66. Oliveira M.C., Pelegrini-da-Silva A., Tambeli C.H., Parada C.A. Peripheral mechanisms underlying the essential role of P2X3,2/3 receptors in the development of inflammatory hyperalgesia. Pain 2009, 141:127-134.
67. Orita T., Kimura K., Nishida T., Sonoda K.H. Cytokine and chemokine secretion induced by poly (I:C) through NF-kappaB and phosphoinositide 3-kinase signaling pathways in human corneal fibroblasts. Curr Eye Res 2013, 38:53-59.
68. Parada C.A., Yeh J.J., Joseph E.K., Levine J.D. Tumor necrosis factor receptor type-1 in sensory neurons contributes to induction of chronic enhancement of inflammatory hyperalgesia in rat. Eur J Neurosci 2003, 17:1847-1852.
69. Pastore S., Mascia F., Girolomoni G. The contribution of keratinocytes to the pathogenesis of atopic dermatitis. Eur J Dermatol 2006, 16:125-131.
70. Poole S., Lorenzetti B.B., Cunha J.M., Cunha F.Q., Ferreira S.M. Bradykinin B1 and B2 receptors, tumor necrosis factor alpha and inflammatory hyperalgesia. Br J Pharmacol 1999, 126:649-656.
71. Preobrazhenskaya M.E., Berman A.E., Mikhailov V.I., Ushakova N.A., Mazurov A.V., Semenov A.V., Usov A.I., Nifant'ev N.E., Bovin N.V. Fucoidan inhibits leukocyte recruitment in a model peritoneal inflammation in rat and blocks interaction of P-selectin with its carbohydrate ligand. Biochem Mol Biol Int 1997, 43:443-451.
72. Randall L.O., Selitto J.J. A method for measurement of analgesic activity on inflamed tissue. Arch Int Pharmacodyn Ther 1957, 111:409-419.
73. Rosland J.H. The formalin test in mice: the influence of ambient temperature. Pain 1991, 45:211-216.
74. Rush A.M., Waxman S.G. PGE2 increases the tetrodotoxin-resistant Nav1.9 sodium current in mouse DRG neurons via G-proteins. Brain Res 2004, 1023:264-271.
75. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., Woolf C.J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol 1995, 115:1265-1275.
76. Sanz J.M., Di Virgilio F. Kinetics and mechanism of ATP-dependent IL-1 beta release from microglial cells. J Immunol 2000, 164:4893-4898.
77. Seyedi N., Maruyama R., Levi R. Bradykinin activates a cross-signaling pathway between sensory and adrenergic nerve endings in the heart: a novel mechanism of ischemic norepinephrine release?. J Pharmacol Exp Ther 1999, 290:656-663.
78. Shinoda M., Ozaki N., Asai H., Nagamine K., Sugiura Y. Changes in P2X3 receptor expression in the trigeminal ganglion following monoarthritis of the temporomandibular joint in rats. Pain 2005, 116:42-51.
79. Sikora A., Liu J., Brosnan C., Buell G., Chessel I., Bloom B.R. Cutting edge: purinergic signaling regulates radical-mediated bacterial killing mechanisms in macrophages through a P2X7-independent mechanism. J Immunol 1999, 163:558-561.
80. Solle M., Labasi J., Perregaux D.G., Stam E., Petrushova N., Koller B.H., Griffiths R.J., Gabel C.A. Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 2001, 276:125-132.
81. Spengler R.N., Allen R.M., Remick D.G., Strieter R.M., Kunkel S.L. Stimulation of alpha-adrenergic receptor augments the production of macrophage-derived tumor necrosis factor. J Immunol 1990, 145:1430-1434.
82. Summ O., Evers S. Mechanism of action of indomethacin in indomethacin-responsive headaches. Curr Pain Headache Rep 2013, 17:327.
83. Surprenant A., North R.A. Signaling at purinergic P2X receptors. Annu Rev Physiol 2009, 71:333-359.
84. Taiwo Y.O., Bjerknes L.K., Goetzl E.J., Levine J.D. Mediation of primary afferent peripheral hyperalgesia by the cAMP second messenger system. Neuroscience 1989, 32:577-580.
85. Tambeli C.H., Oliveira M.C., Clemente J.T., Pelegrini-da-Silva A., Parada C.A. A novel mechanism involved in 5-hydroxytryptamine-induced nociception: the indirect activation of primary afferents. Neuroscience 2006, 141:1517-1524.
86. Teixeira J.M., Oliveira M.C., Nociti F.H., Clemente-Napimoga J.T., Pelegrini-da-Silva A., Parada C.A., Tambeli C.H. Involvement of temporomandibular joint P2X3 and P2X2/3 receptors in carrageenan-induced inflammatory hyperalgesia in rats. Eur J Pharmacol 2010, 645:79-85.
87. Teixeira J.M., Oliveira M.C., Parada C.A., Tambeli C.H. Peripheral mechanisms underlying the essential role of P2X7 receptors in the development of inflammatory hyperalgesia. Eur J Pharmacol 2010, 644:55-60.
88. Theoharides T.C., Alysandratos K.D., Angelidou A., Delivanis D.A., Sismanopoulos N., Zhang B., Asadi S., Vasiadi M., Weng Z., Miniati A., Kalogeromitros D. Mast cells and inflammation. Biochim Biophys Acta 2012, 1822:21-33.
89. Verri W.A., Cunha T.M., Parada C.A., Poole S., Cunha F.Q., Ferreira S.H. Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development?. Pharmacol Ther 2006, 112:116-138.
90. Wankowicz Z., Megyeri P., Issekutz A. Synergy between tumour necrosis factor alpha and interleukin-1 in the induction of polymorphonuclear leukocyte migration during inflammation. J Leukoc Biol 1988, 43:349-356.
91. White F.A., Bhangoo S.K., Miller R.J. Chemokines: integrators of pain and inflammation. Nat Rev Drug Discov 2005, 4:834-844.
92. Williams M., Jarvis M.F. Purinergic and pyrimidinergic receptors as potential drug targets. Biochem Pharmacol 2000, 59:1173-1185.
93. Yalcin I., Choucair-Jaafar N., Benbouzid M., Tessier L.H., Muller A., Hein L., Freund-Mercier M.J., Barrot M. Beta(2)-adrenoceptors are critical for antidepressant treatment of neuropathic pain. Ann Neurol 2009, 65:218-225.
94. Zhang X.W., Liu Q., Thorlacius H. Inhibition of selectin function and leukocyte rolling protects against dextran sodium sulfate-induced murine colitis. Scand J Gastroenterol 2001, 36:270-275.
95. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.