Emerging role of microglial kinin B1 receptor in diabetic pain neuropathy

Experimental Neurology

Volumn 234, Issue 2, 2012, Pages 373-381

  Talbot, Sébastien ^a   Couture, Réjean ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 ALPHA AMINOADIPATE; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ACETYLLYSYLBRADYKININ[7 [3 (2 NAPHTHYL)ALANINE] 8 ISOLEUCINE 9 DEARGININE]; AMPA RECEPTOR; ANALGESIC AGENT; ANTIOXIDANT; BRADYKININ B1 RECEPTOR; BRADYKININ B1 RECEPTOR AGONIST; BRADYKININ B1 RECEPTOR ANTAGONIST; BRADYKININ B2 RECEPTOR; BRAIN DERIVED NEUROTROPHIC FACTOR; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 2 RECEPTOR AGONIST; CHEMOKINE RECEPTOR CX3CR1; CYTOKINE; DIZOCILPINE; FLUOROCITRIC ACID; G PROTEIN COUPLED RECEPTOR; GABAPENTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MINOCYCLINE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PURINERGIC P2X4 RECEPTOR; R954; SAFOTIBANT; SSR240612; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ALLODYNIA; ANALGESIC ACTIVITY; ARTICLE; BINDING AFFINITY; BIOLOGICAL MODEL; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL ACTIVITY; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL PHAGOCYTOSIS; CELL PROLIFERATION; CHEMOTAXIS; CHRONIC PAIN; CYTOKINE RELEASE; DIABETES MELLITUS; DIABETIC NEUROPATHY; DIABETIC PAIN NEUROPATHY; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; DISEASE DURATION; DRUG PENETRATION; FACILITATION; GENE DELETION; GENE EXPRESSION; GENOTYPE; GLIOSIS; GLYCEMIC CONTROL; HUMAN; HYPERALGESIA; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; LIVER TOXICITY; MICROGLIA; MICROGLIOSIS; NERVE CELL EXCITABILITY; NEUROPATHIC PAIN; NOCICEPTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STREPTOZOCIN DIABETES; SYNAPTIC TRANSMISSION; UPREGULATION;

ANIMALS; DIABETIC NEUROPATHIES; HUMANS; INFLAMMATION; KININS; MICE; MICE, KNOCKOUT; MICROGLIA; RECEPTOR, BRADYKININ B1;

EID: 84858149544     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.11.032     Document Type: Article

References (179)

1. Abbadie C., Bhangoo S., De Koninck Y., Malcangio M., Melik-Parsadaniantz S., White F.A. Chemokines and pain mechanisms. Brain Res. Rev. 2009, 60:125-134.
2. Bachvarov D.R., Houle S., Bachvarova M., Bouthillier J., Adam A., Marceau F. Bradykinin B(2) receptor endocytosis, recycling, and down-regulation assessed using green fluorescent protein conjugates. J. Pharmacol. Exp. Ther. 2001, 297:19-26.
3. Beattie E.C., Stellwagen D., Morishita W., Bresnahan J.C., Ha B.K., Von Zastrow M., Beattie M.S., Malenka R.C. Control of synaptic strength by glial TNFalpha. Science 2002, 295:2282-2285.
4. 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.
5. Besson J.M. The neurobiology of pain. Lancet 1999, 353:1610-1615.
6. Bianchi R., Kastrisianaki E., Giambanco I., Donato R. S100B protein stimulates microglia migration via RAGE-dependent up-regulation of chemokine expression and release. J. Biol. Chem. 2011, 286:7214-7226.
7. Biggs J.E., Lu V.B., Stebbing M.J., Balasubramanyan S., Smith P.A. Is BDNF sufficient for information transfer between microglia and dorsal horn neurons during the onset of central sensitization?. Mol. Pain 2010, 6:44.
8. Boulton A.J., Kirsner R.S., Vileikyte L. Clinical practice. Neuropathic diabetic foot ulcers. N. Engl. J. Med. 2004, 351:48-55.
9. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
10. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005, 54:1615-1625.
11. Bujalska M., Makulska-Nowak H. Bradykinin receptor antagonists and cyclooxygenase inhibitors in vincristine- and streptozotocin-induced hyperalgesia. Pharmacol. Rep. 2009, 61:631-640.
12. Calixto J.B., Cabrini D.A., Ferreira J., Campos M.M. Kinins in pain and inflammation. Pain 2000, 87:1-5.
13. Calixto J.B., Medeiros R., Fernandes E.S., Ferreira J., Cabrini D.A., Campos M.M. Kinin B1 receptors: key G-protein-coupled receptors and their role in inflammatory and painful processes. Br. J. Pharmacol. 2004, 143:803-818.
14. Campos M.M., Mata L.V., Calixto J.B. Expression of B1 kinin receptors mediating paw edema and formalin-induced nociception. Modulation by glucocorticoids. Can. J. Physiol. Pharmacol. 1995, 73:812-819.
15. Campos M.M., Souza G.E., Calixto J.B. In vivo B1 kinin-receptor upregulation. Evidence for involvement of protein kinases and nuclear factor kappaB pathways. Br. J. Pharmacol. 1999, 127:1851-1859.
16. Campos M.M., Leal P.C., Yunes R.A., Calixto J.B. Non-peptide antagonists for kinin B1 receptors: new insights into their therapeutic potential for the management of inflammation and pain. Trends Pharmacol. Sci. 2006, 27:646-651.
17. Candelario-Jalil E., de Oliveira A.C., Graf S., Bhatia H.S., Hull M., Munoz E., Fiebich B.L. Resveratrol potently reduces prostaglandin E2 production and free radical formation in lipopolysaccharide-activated primary rat microglia. J. Neuroinflammation 2007, 4:25.
18. Chang Y.W., Tan A., Saab C., Waxman S. Unilateral focal burn injury is followed by long-lasting bilateral allodynia and neuronal hyperexcitability in spinal cord dorsal horn. J. Pain 2010, 11:119-130.
19. Chen S., Khan Z.A., Cukiernik M., Chakrabarti S. Differential activation of NF-kappa B and AP-1 in increased fibronectin synthesis in target organs of diabetic complications. Am. J. Physiol. Endocrinol. Metab. 2003, 284:E1089-E1097.
20. Cheng H.T., Dauch J.R., Hayes J.M., Hong Y., Feldman E.L. Nerve growth factor mediates mechanical allodynia in a mouse model of type 2 diabetes. J. Neuropathol. Exp. Neurol. 2009, 68:1229-1243.
21. Chichorro J.G., Lorenzetti B.B., Zampronio A.R. Involvement of bradykinin, cytokines, sympathetic amines and prostaglandins in formalin-induced orofacial nociception in rats. Br. J. Pharmacol. 2004, 141:1175-1184.
22. Correa C.R., Calixto J.B. Evidence for participation of B1 and B2 kinin receptors in formalin-induced nociceptive response in the mouse. Br. J. Pharmacol. 1993, 110:193-198.
23. Costigan M., Mannion R.J., Kendall G., Lewis S.E., Campagna J.A., Coggeshall R.E., Meridith-Middleton J., Tate S., Woolf C.J. Heat shock protein 27: developmental regulation and expression after peripheral nerve injury. J. Neurosci. 1998, 18:5891-5900.
24. Couture R., Girolami J.P. Putative roles of kinin receptors in the therapeutic effects of angiotensin 1-converting enzyme inhibitors in diabetes mellitus. Eur. J. Pharmacol. 2004, 500:467-485.
25. Couture R., Harrisson M., Vianna R.M., Cloutier F. Kinin receptors in pain and inflammation. Eur. J. Pharmacol. 2001, 429:161-176.
26. Crofford O.B. Diabetes control and complications. Annu. Rev. Med. 1995, 46:267-279.
27. Cunha T.M., Verri W.A., Fukada S.Y., Guerrero A.T., Santodomingo-Garzon T., Poole S., Parada C.A., Ferreira S.H., Cunha F.Q. TNF-alpha and IL-1beta mediate inflammatory hypernociception in mice triggered by B1 but not B2 kinin receptor. Eur. J. Pharmacol. 2007, 573:221-229.
28. Daousi C., Benbow S.J., Woodward A., MacFarlane I.A. The natural history of chronic painful peripheral neuropathy in a community diabetes population. Diabet. Med. 2006, 23:1021-1024.
29. Daulhac L., Mallet C., Courteix C., Etienne M., Duroux E., Privat A.M., Eschalier A., Fialip J. Diabetes-induced mechanical hyperalgesia involves spinal mitogen-activated protein kinase activation in neurons and microglia via N-methyl-D-aspartate-dependent mechanisms. Mol. Pharmacol. 2006, 70:1246-1254.
30. Daulhac L., Maffre V., Mallet C., Etienne M., Privat A.M., Kowalski-Chauvel A., Seva C., Fialip J., Eschalier A. Phosphorylation of spinal N-methyl-d-aspartate receptor NR1 subunits by extracellular signal-regulated kinase in dorsal horn neurons and microglia contributes to diabetes-induced painful neuropathy. Eur. J. Pain 2011, 15:169. e161-169 e112.
31. deBlois D., Horlick R.A. Endotoxin sensitization to kinin B(1) receptor agonist in a non-human primate model: haemodynamic and pro-inflammatory effects. Br. J. Pharmacol. 2001, 132:327-335.
32. Delovitch T.L., Singh B. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 1997, 7:727-738.
33. Dias J.P., Ismael M.A., Pilon M., de Champlain J., Ferrari B., Carayon P., Couture R. The kinin B1 receptor antagonist SSR240612 reverses tactile and cold allodynia in an experimental rat model of insulin resistance. Br. J. Pharmacol. 2007, 152:280-287.
34. Dias J.P., Talbot S., Senecal J., Carayon P., Couture R. Kinin B1 receptor enhances the oxidative stress in a rat model of insulin resistance: outcome in hypertension, allodynia and metabolic complications. PLoS One 2010, 5:e12622.
35. Eisenbarth H., Rukwied R., Petersen M., Schmelz M. Sensitization to bradykinin B1 and B2 receptor activation in UV-B irradiated human skin. Pain 2004, 110:197-204.
36. El Midaoui A., de Champlain J. Prevention of hypertension, insulin resistance, and oxidative stress by alpha-lipoic acid. Hypertension 2002, 39:303-307.
37. Enquist J., Skroder C., Whistler J.L., Leeb-Lundberg L.M. Kinins promote B2 receptor endocytosis and delay constitutive B1 receptor endocytosis. Mol. Pharmacol. 2007, 71:494-507.
38. Eriksson N.P., Persson J.K., Svensson M., Arvidsson J., Molander C., Aldskogius H. A quantitative analysis of the microglial cell reaction in central primary sensory projection territories following peripheral nerve injury in the adult rat. Exp. Brain Res. 1993, 96:19-27.
39. Fernyhough P., Calcutt N.A. Abnormal calcium homeostasis in peripheral neuropathies. Cell Calcium 2010, 47:130-139.
40. 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.
41. Ferreira J., Campos M.M., Araujo R., Bader M., Pesquero J.B., Calixto J.B. The use of kinin B1 and B2 receptor knockout mice and selective antagonists to characterize the nociceptive responses caused by kinins at the spinal level. Neuropharmacology 2002, 43:1188-1197.
42. Ferreira J., Beirith A., Mori M.A., Araujo R.C., Bader M., Pesquero J.B., Calixto J.B. Reduced nerve injury-induced neuropathic pain in kinin B1 receptor knock-out mice. J. Neurosci. 2005, 25:2405-2412.
43. 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.
44. Fincham C.I., Bressan A., Paris M., Rossi C., Fattori D. Bradykinin receptor antagonists-a review of the patent literature 2005-2008. Expert Opin. Ther. Pat. 2009, 19:919-941.
45. Fischer T.Z., Waxman S.G. Neuropathic pain in diabetes-evidence for a central mechanism. Nat. Rev. Neurol. 2010, 6:462-466.
46. Fitzpatrick F., Lepault F., Homo-Delarche F., Bach J.F., Dardenne M. Influence of castration, alone or combined with thymectomy, on the development of diabetes in the nonobese diabetic mouse. Endocrinology 1991, 129:1382-1390.
47. 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.
48. Fujita M., Andoh T., Ohashi K., Akira A., Saiki I., Kuraishi Y. Roles of kinin B1 and B2 receptors in skin cancer pain produced by orthotopic melanoma inoculation in mice. Eur. J. Pain 2010, 14:588-594.
49. Gabra B.H., Sirois P. Role of bradykinin B(1) receptors in diabetes-induced hyperalgesia in streptozotocin-treated mice. Eur. J. Pharmacol. 2002, 457:115-124.
50. Gabra B.H., Sirois P. Kinin B1 receptor antagonists inhibit diabetes-induced hyperalgesia in mice. Neuropeptides 2003, 37:36-44.
51. Gabra B.H., Sirois P. Hyperalgesia in non-obese diabetic (NOD) mice: a role for the inducible bradykinin B1 receptor. Eur. J. Pharmacol. 2005, 514:61-67.
52. Gabra B.H., Merino V.F., Bader M., Pesquero J.B., Sirois P. Absence of diabetic hyperalgesia in bradykinin B1 receptor-knockout mice. Regul. Pept. 2005, 127:245-248.
53. Gao Y.J., Ji R.R. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol. Ther. 2010, 126:56-68.
54. Gerbi A., Maixent J.M., Barbey O., Jamme I., Pierlovisi M., Coste T., Pieroni G., Nouvelot A., Vague P., Raccah D. Alterations of Na, K-ATPase isoenzymes in the rat diabetic neuropathy: protective effect of dietary supplementation with n-3 fatty acids. J. Neurochem. 1998, 71:732-740.
55. Gosselin R.D., Suter M.R., Ji R.R., Decosterd I. Glial cells and chronic pain. Neuroscientist 2010, 16:519-531.
56. Gougat J., Ferrari B., Sarran L., Planchenault C., Poncelet M., Maruani J., Alonso R., Cudennec A., Croci T., Guagnini F., Urban-Szabo K., Martinolle J.P., Soubrie P., Finance O., Le Fur G. SSR240612 [(2R)-2-[((3R)-3-(1,3-benzodioxol-5-yl)-3-[[(6-methoxy-2-naphthyl)sulfonyl]amino]propanoyl)amino]-3-(4-[[2R,6S)-2,6-dimethylpiperidinyl]methyl]pheny l)-N-isopropyl-N-methylpropanamide hydrochloride], a new nonpeptide antagonist of the bradykinin B1 receptor: biochemical and pharmacological characterization. J. Pharmacol. Exp. Ther. 2004, 309:661-669.
57. Guastella V., Mick G. Strategies for the diagnosis and treatment of neuropathic pain secondary to diabetic peripheral sensory polyneuropathy. Diabetes Metab. 2009, 35:12-19.
58. Hess J.F., Hey P.J., Chen T.B., O'Brien J., Omalley S.S., Pettibone D.J., Chang R.S. Molecular cloning and pharmacological characterization of the canine B1 and B2 bradykinin receptors. Biol. Chem. 2001, 382:123-129.
59. Hickey W.F., Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 1988, 239:290-292.
60. Hutchinson M.R., Zhang Y., Brown K., Coats B.D., Shridhar M., Sholar P.W., Patel S.J., Crysdale N.Y., Harrison J.A., Maier S.F., Rice K.C., Watkins L.R. Non-stereoselective reversal of neuropathic pain by naloxone and naltrexone: involvement of toll-like receptor 4 (TLR4). Eur. J. Neurosci. 2008, 28:20-29.
61. Ifuku M., Farber K., Okuno Y., Yamakawa Y., Miyamoto T., Nolte C., Merrino V.F., Kita S., Iwamoto T., Komuro I., Wang B., Cheung G., Ishikawa E., Ooboshi H., Bader M., Wada K., Kettenmann H., Noda M. Bradykinin-induced microglial migration mediated by B1-bradykinin receptors depends on Ca2+ influx via reverse-mode activity of the Na+/Ca2+ exchanger. J. Neurosci. 2007, 27:13065-13073.
62. Inoue K. The function of microglia through purinergic receptors: neuropathic pain and cytokine release. Pharmacol. Ther. 2006, 109:210-226.
63. Inoue K. Purinergic systems in microglia. Cell. Mol. Life Sci. 2008, 65:3074-3080.
64. Ismael M.A., Talbot S., Carbonneau C.L., Beausejour C.M., Couture R. Blockade of sensory abnormalities and kinin B(1) receptor expression by N-acetyl-L-cysteine and ramipril in a rat model of insulin resistance. Eur. J. Pharmacol. 2008, 589:66-72.
65. Ji R.R., Suter M.R. p38 MAPK, microglial signaling, and neuropathic pain. Mol. Pain 2007, 3:33.
66. Ji R.R., Gereau R.W.t., Malcangio M., Strichartz G.R. MAP kinase and pain. Brain Res. Rev. 2009, 60:135-148.
67. Jin S.X., Zhuang Z.Y., Woolf C.J., Ji R.R. p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J. Neurosci. 2003, 23:4017-4022.
68. Kawasaki Y., Xu Z.Z., Wang X., Park J.Y., Zhuang Z.Y., Tan P.H., Gao Y.J., Roy K., Corfas G., Lo E.H., Ji R.R. Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat. Med. 2008, 14:331-336.
69. Kim D., Kim M.A., Cho I.H., Kim M.S., Lee S., Jo E.K., Choi S.Y., Park K., Kim J.S., Akira S., Na H.S., Oh S.B., Lee S.J. A critical role of toll-like receptor 2 in nerve injury-induced spinal cord glial cell activation and pain hypersensitivity. J. Biol. Chem. 2007, 282:14975-14983.
70. Kumar V., Abbas A.K., Fausto N., Robbins S.L., Cotran R.S. Robbins and Cotran Pathologic Basis of Disease 2005, Elsevier Saunders, Philadelphia.
71. Lassmann H., Schmied M., Vass K., Hickey W.F. Bone marrow derived elements and resident microglia in brain inflammation. Glia 1993, 7:19-24.
72. Latham J.R., Pathirathna S., Jagodic M.M., Choe W.J., Levin M.E., Nelson M.T., Lee W.Y., Krishnan K., Covey D.F., Todorovic S.M., Jevtovic-Todorovic V. Selective T-type calcium channel blockade alleviates hyperalgesia in ob/ob mice. Diabetes 2009, 58:2656-2665.
73. Leeb-Lundberg L.M., Marceau F., Muller-Esterl W., Pettibone D.J., Zuraw B.L. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol. Rev. 2005, 57:27-77.
74. Levy D.M., Terenghi G., Gu X.H., Abraham R.R., Springall D.R., Polak J.M. Immunohistochemical measurements of nerves and neuropeptides in diabetic skin: relationship to tests of neurological function. Diabetologia 1992, 35:889-897.
75. Li J., Baud O., Vartanian T., Volpe J.J., Rosenberg P.A. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9936-9941.
76. Liao Y.H., Zhang G.H., Jia D., Wang P., Qian N.S., He F., Zeng X.T., He Y., Yang Y.L., Cao D.Y., Zhang Y., Wang D.S., Tao K.S., Gao C.J., Dou K.F. Spinal astrocytic activation contributes to mechanical allodynia in a mouse model of type 2 diabetes. Brain Res. 2011, 1368:324-335.
77. Lin J.C., Talbot S., Lahjouji K., Roy J.P., Senecal J., Couture R., Morin A. Mechanism of cigarette smoke-induced kinin B(1) receptor expression in rat airways. Peptides 2010, 31:1940-1945.
78. Luiz A.P., Schroeder S.D., Chichorro J.G., Calixto J.B., Zampronio A.R., Rae G.A. Kinin B(1) and B(2) receptors contribute to orofacial heat hyperalgesia induced by infraorbital nerve constriction injury in mice and rats. Neuropeptides 2010, 44:87-92.
79. Lungu C., Dias J.P., Franca C.E., Ongali B., Regoli D., Moldovan F., Couture R. Involvement of kinin B1 receptor and oxidative stress in sensory abnormalities and arterial hypertension in an experimental rat model of insulin resistance. Neuropeptides 2007, 41:375-387.
80. Maeda T., Kiguchi N., Kobayashi Y., Ikuta T., Ozaki M., Kishioka S. Leptin derived from adipocytes in injured peripheral nerves facilitates development of neuropathic pain via macrophage stimulation. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:13076-13081.
81. Marceau F., Bachvarov D.R. Kinin receptors. Clin. Rev. Allergy Immunol. 1998, 16:385-401.
82. Marceau F., Regoli D. Bradykinin receptor ligands: therapeutic perspectives. Nat. Rev. Drug. Discov. 2004, 3:845-852.
83. Marchand F., Perretti M., McMahon S.B. Role of the immune system in chronic pain. Nat. Rev. Neurosci. 2005, 6:521-532.
84. McMahon S.B., Cafferty W.B., Marchand F. Immune and glial cell factors as pain mediators and modulators. Exp. Neurol. 2005, 192:444-462.
85. Menke J.G., Borkowski J.A., Bierilo K.K., MacNeil T., Derrick A.W., Schneck K.A., Ransom R.W., Strader C.D., Linemeyer D.L., Hess J.F. Expression cloning of a human B1 bradykinin receptor. J. Biol. Chem. 1994, 269:21583-21586.
86. Milligan E.D., Watkins L.R. Pathological and protective roles of glia in chronic pain. Nat. Rev. Neurosci. 2009, 10:23-36.
87. Milligan E.D., Zapata V., Chacur M., Schoeniger D., Biedenkapp J., O'Connor K.A., Verge G.M., Chapman G., Green P., Foster A.C., Naeve G.S., Maier S.F., Watkins L.R. Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur. J. Neurosci. 2004, 20:2294-2302.
88. Milligan E., Zapata V., Schoeniger D., Chacur M., Green P., Poole S., Martin D., Maier S.F., Watkins L.R. An initial investigation of spinal mechanisms underlying pain enhancement induced by fractalkine, a neuronally released chemokine. Eur. J. Neurosci. 2005, 22:2775-2782.
89. Milligan E.D., Sloane E.M., Watkins L.R. Glia in pathological pain: a role for fractalkine. J. Neuroimmunol. 2008, 198:113-120.
90. Molines L., Darmon P., Raccah D. Charcot's foot: newest findings on its pathophysiology, diagnosis and treatment. Diabetes Metab. 2010, 36:251-255.
91. Mosley K., Cuzner M.L. Receptor-mediated phagocytosis of myelin by macrophages and microglia: effect of opsonization and receptor blocking agents. Neurochem. Res. 1996, 21:481-487.
92. Narita M., Yoshida T., Nakajima M., Miyatake M., Takagi T., Yajima Y., Suzuki T. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J. Neurochem. 2006, 97:1337-1348.
93. Neugebauer W., Blais P.A., Halle S., Filteau C., Regoli D., Gobeil F. Kinin B1 receptor antagonists with multi-enzymatic resistance properties. Can. J. Physiol. Pharmacol. 2002, 80:287-292.
94. Ni A., Chao L., Chao J. Transcription factor nuclear factor kappaB regulates the inducible expression of the human B1 receptor gene in inflammation. J. Biol. Chem. 1998, 273:2784-2791.
95. Nishikawa T., Edelstein D., Du X.L., Yamagishi S., Matsumura T., Kaneda Y., Yorek M.A., Beebe D., Oates P.J., Hammes H.P., Giardino I., Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404:787-790.
96. Noda M., Kariura Y., Pannasch U., Nishikawa K., Wang L., Seike T., Ifuku M., Kosai Y., Wang B., Nolte C., Aoki S., Kettenmann H., Wada K. Neuroprotective role of bradykinin because of the attenuation of pro-inflammatory cytokine release from activated microglia. J. Neurochem. 2007, 101:397-410.
97. Oates P.J. Polyol pathway and diabetic peripheral neuropathy. Int. Rev. Neurobiol. 2002, 50:325-392.
98. Obrosova I.G. Diabetic painful and insensate neuropathy: pathogenesis and potential treatments. Neurotherapeutics 2009, 6:638-647.
99. Pabreja K., Dua K., Sharma S., Padi S.S., Kulkarni S.K. Minocycline attenuates the development of diabetic neuropathic pain: possible anti-inflammatory and anti-oxidant mechanisms. Eur. J. Pharmacol. 2011, 661:15-21.
100. Patel J., Iyer A., Brown L. Evaluation of the chronic complications of diabetes in a high fructose diet in rats. Indian J. Biochem. Biophys. 2009, 46:66-72.
101. Perkins M.N., Campbell E., Dray A. Antinociceptive activity of the bradykinin B1 and B2 receptor antagonists, des-Arg9, [Leu8]-BK and HOE 140, in two models of persistent hyperalgesia in the rat. Pain 1993, 53:191-197.
102. Pesquero J.B., Pesquero J.L., Oliveira S.M., Roscher A.A., Metzger R., Ganten D., Bader M. Molecular cloning and functional characterization of a mouse bradykinin B1 receptor gene. Biochem. Biophys. Res. Commun. 1996, 220:219-225.
103. Pesquero J.B., Araujo R.C., Heppenstall P.A., Stucky C.L., Silva J.A., Walther T., Oliveira S.M., Pesquero J.L., Paiva A.C., Calixto J.B., Lewin G.R., Bader M. Hypoalgesia and altered inflammatory responses in mice lacking kinin B1 receptors. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8140-8145.
104. Petcu M., Dias J.P., Ongali B., Thibault G., Neugebauer W., Couture R. Role of kinin B1 and B2 receptors in a rat model of neuropathic pain. Int. Immunopharmacol. 2008, 8:188-196.
105. Petrenko A.B., Yamakura T., Baba H., Shimoji K. The role of N-methyl-D-aspartate (NMDA) receptors in pain: a review. Anesth. Analg. 2003, 97:1108-1116.
106. Phagoo S.B., Poole S., Leeb-Lundberg L.M. Autoregulation of bradykinin receptors: agonists in the presence of interleukin-1beta shift the repertoire of receptor subtypes from B2 to B1 in human lung fibroblasts. Mol. Pharmacol. 1999, 56:325-333.
107. Phagoo S.B., Reddi K., Anderson K.D., Leeb-Lundberg L.M., Warburton D. Bradykinin B1 receptor up-regulation by interleukin-1beta and B1 agonist occurs through independent and synergistic intracellular signaling mechanisms in human lung fibroblasts. J. Pharmacol. Exp. Ther. 2001, 298:77-85.
108. Piercy V., Banner S.E., Bhattacharyya A., Parsons A.A., Sanger G.J., Smith S.A., Bingham S. Thermal, but not mechanical, nociceptive behavior is altered in the Zucker Diabetic Fatty rat and is independent of glycemic status. J. Diabetes Complications 1999, 13:163-169.
109. Pocock J.M., Kettenmann H. Neurotransmitter receptors on microglia. Trends Neurosci. 2007, 30:527-535.
110. Pop-Busui R., Sima A., Stevens M. Diabetic neuropathy and oxidative stress. Diabetes Metab. Res. Rev. 2006, 22:257-273.
111. Porreca F., Vanderah T.W., Guo W., Barth M., Dodey P., Peyrou V., Luccarini J.M., Junien J.L., Pruneau D. Antinociceptive pharmacology of N-[[4-(4,5-dihydro-1H-imidazol-2-yl)phenyl]methyl]-2-[2-[[(4-methoxy-2,6-d imethylphenyl) sulfonyl]methylamino]ethoxy]-N-methylacetamide, fumarate (LF22-0542), a novel nonpeptidic bradykinin B1 receptor antagonist. J. Pharmacol. Exp. Ther. 2006, 318:195-205.
112. Quan Y., Du J., Wang X. High glucose stimulates GRO secretion from rat microglia via ROS, PKC, and NF-kappaB pathways. J. Neurosci. Res. 2007, 85:3150-3159.
113. Quintao N.L., Passos G.F., Medeiros R., Paszcuk A.F., Motta F.L., Pesquero J.B., Campos M.M., Calixto J.B. Neuropathic pain-like behavior after brachial plexus avulsion in mice: the relevance of kinin B1 and B2 receptors. J. Neurosci. 2008, 28:2856-2863.
114. Raccah D. Physiopathology of diabetic neuropathies. Functional exploration of peripheral involvement. Diabetes Metab. 1998, 24(Suppl. 3):73-78.
115. Rajpal S., Gerovac T.A., Turner N.A., Tilghman J.I., Allcock B.K., McChesney S.L., Miranpuri G.S., Park S.W., Resnick D.K. Antihyperalgesic effects of vanilloid-1 and bradykinin-1 receptor antagonists following spinal cord injury in rats. J. Neurosurg. Spine 2007, 6:420-424.
116. Rashid M.H., Inoue M., Matsumoto M., Ueda H. Switching of bradykinin-mediated nociception following partial sciatic nerve injury in mice. J. Pharmacol. Exp. Ther. 2004, 308:1158-1164.
117. Regoli D., Rhaleb N.E., Drapeau G., Dion S. Kinin receptor subtypes. J. Cardiovasc. Pharmacol. 1990, 15(Suppl. 6):S30-S38.
118. Regoli D., Gobeil F., Nguyen Q.T., Jukic D., Seoane P.R., Salvino J.M., Sawutz D.G. Bradykinin receptor types and B2 subtypes. Life Sci. 1994, 55:735-749.
119. Regoli D., Rizzi A., Perron S.I., Gobeil F. Classification of kinin receptors. Biol. Chem. 2001, 382:31-35.
120. Roane D.S., Porter J.R. Nociception and opioid-induced analgesia in lean (Fa/-) and obese (fa/fa) Zucker rats. Physiol. Behav. 1986, 38:215-218.
121. Romagnoli M., Gomez-Cabrera M.C., Perrelli M.G., Biasi F., Pallardo F.V., Sastre J., Poli G., Vina J. Xanthine oxidase-induced oxidative stress causes activation of NF-kappaB and inflammation in the liver of type I diabetic rats. Free Radic. Biol. Med. 2010, 49:171-177.
122. Romanovsky D., Walker J.C., Dobretsov M. Pressure pain precedes development of type 2 disease in Zucker rat model of diabetes. Neurosci. Lett. 2008, 445:220-223.
123. Romero-Sandoval E.A., Horvath R.J., DeLeo J.A. Neuroimmune interactions and pain: focus on glial-modulating targets. Curr. Opin. Investig. Drugs 2008, 9:726-734.
124. Said G. Diabetic neuropathy-a review. Nat. Clin. Pract. Neurol. 2007, 3:331-340.
125. Schanstra J.P., Bataille E., Marin Castano M.E., Barascud Y., Hirtz C., Pesquero J.B., Pecher C., Gauthier F., Girolami J.P., Bascands J.L. The B1-agonist [des-Arg10]-kallidin activates transcription factor NF-kappaB and induces homologous upregulation of the bradykinin B1-receptor in cultured human lung fibroblasts. J. Clin. Invest. 1998, 101:2080-2091.
126. Schemmel K.E., Padiyara R.S., D'Souza J.J. Aldose reductase inhibitors in the treatment of diabetic peripheral neuropathy: a review. J. Diabetes Complications 2010, 24:354-360.
127. Scholz J., Woolf C.J. Can we conquer pain?. Nat. Neurosci. 2002, 5:1062-1067. Suppl.
128. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 2007, 10:1361-1368.
129. Serreze D.V., Leiter E.H. Genetic and pathogenic basis of autoimmune diabetes in NOD mice. Curr. Opin. Immunol. 1994, 6:900-906.
130. Sevcik M.A., Ghilardi J.R., Halvorson K.G., Lindsay T.H., Kubota K., Mantyh P.W. Analgesic efficacy of bradykinin B1 antagonists in a murine bone cancer pain model. J. Pain 2005, 6:771-775.
131. Stellwagen D., Malenka R.C. Synaptic scaling mediated by glial TNF-alpha. Nature 2006, 440:1054-1059.
132. Sugimoto K., Yasujima M., Yagihashi S. Role of advanced glycation end products in diabetic neuropathy. Curr. Pharm. Des. 2008, 14:953-961.
133. Sun S., Cao H., Han M., Li T.T., Pan H.L., Zhao Z.Q., Zhang Y.Q. New evidence for the involvement of spinal fractalkine receptor in pain facilitation and spinal glial activation in rat model of monoarthritis. Pain 2007, 129:64-75.
134. Suri A., Szallasi A. The emerging role of TRPV1 in diabetes and obesity. Trends Pharmacol. Sci. 2008, 29:29-36.
135. Svensson C.I., Fitzsimmons B., Azizi S., Powell H.C., Hua X.Y., Yaksh T.L. Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. J. Neurochem. 2005, 92:1508-1520.
136. Sweitzer S.M., White K.A., Dutta C., DeLeo J.A. The differential role of spinal MHC class II and cellular adhesion molecules in peripheral inflammatory versus neuropathic pain in rodents. J. Neuroimmunol. 2002, 125:82-93.
137. Talbot S., Theberge-Turmel P., Liazoghli D., Senecal J., Gaudreau P., Couture R. Cellular localization of kinin B1 receptor in the spinal cord of streptozotocin-diabetic rats with a fluorescent [Nalpha-Bodipy]-des-Arg9-bradykinin. J. Neuroinflammation 2009, 6:11.
138. Talbot S., Chahmi E., Dias J.P., Couture R. Key role for spinal dorsal horn microglial kinin B1 receptor in early diabetic pain neuropathy. J. Neuroinflammation 2010, 7:36.
139. Tanga F.Y., Raghavendra V., DeLeo J.A. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem. Int. 2004, 45:397-407.
140. Tanga F.Y., Nutile-McMenemy N., DeLeo J.A. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5856-5861.
141. Tender G.C., Li Y.Y., Cui J.G. Brain-derived neurotrophic factor redistribution in the dorsal root ganglia correlates with neuropathic pain inhibition after resiniferatoxin treatment. Spine J. 2010, 10:715-720.
142. Tesfaye S., Kempler P. Painful diabetic neuropathy. Diabetologia 2005, 48:805-807.
143. Thacker M.A., Clark A.K., Bishop T., Grist J., Yip P.K., Moon L.D., Thompson S.W., Marchand F., McMahon S.B. CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur. J. Pain 2009, 13:263-272.
144. Thornalley P.J. Cell activation by glycated proteins. AGE receptors, receptor recognition factors and functional classification of AGEs. Cell. Mol. Biol. (Noisy-le-grand) 1998, 44:1013-1023.
145. Tonussi C.R., Ferreira S.H. Bradykinin-induced knee joint incapacitation involves bradykinin B2 receptor mediated hyperalgesia and bradykinin B1 receptor-mediated nociception. Eur. J. Pharmacol. 1997, 326:61-65.
146. Torsney C., MacDermott A.B. Neuroscience: a painful factor. Nature 2005, 438:923-925.
147. Toth C.C., Jedrzejewski N.M., Ellis C.L., Frey W.H. Cannabinoid-mediated modulation of neuropathic pain and microglial accumulation in a model of murine type I diabetic peripheral neuropathic pain. Mol. Pain 2010, 6:16.
148. Tsuda M., Shigemoto-Mogami Y., Koizumi S., Mizokoshi A., Kohsaka S., Salter M.W., Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003, 424:778-783.
149. Tsuda M., Mizokoshi A., Shigemoto-Mogami Y., Koizumi S., Inoue K. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004, 45:89-95.
150. Tsuda M., Inoue K., Salter M.W. Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci. 2005, 28:101-107.
151. Tsuda M., Ueno H., Kataoka A., Tozaki-Saitoh H., Inoue K. Activation of dorsal horn microglia contributes to diabetes-induced tactile allodynia via extracellular signal-regulated protein kinase signaling. Glia 2008, 56:378-386.
152. Vague P., Dufayet D., Lamotte M.F., Mouchot C., Raccah D. Genetic factors, Na K ATPase activity and neuropathy in diabetics. Bull. Acad. Natl. Med. 1997, 181:1811-1821. discussion 1821-1813.
153. Vareniuk I., Pavlov I.A., Drel V.R., Lyzogubov V.V., Ilnytska O., Bell S.R., Tibrewala J., Groves J.T., Obrosova I.G. Nitrosative stress and peripheral diabetic neuropathy in leptin-deficient (ob/ob) mice. Exp. Neurol. 2007, 205:425-436.
154. Verge G.M., Milligan E.D., Maier S.F., Watkins L.R., Naeve G.S., Foster A.C. Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur. J. Neurosci. 2004, 20:1150-1160.
155. Viana A.F., Maciel I.S., Dornelles F.N., Figueiredo C.P., Siqueira J.M., Campos M.M., Calixto J.B. Kinin B1 receptors mediate depression-like behavior response in stressed mice treated with systemic E. coli lipopolysaccharide. J. Neuroinflammation 2010, 7:98.
156. Viviani B., Bartesaghi S., Gardoni F., Vezzani A., Behrens M.M., Bartfai T., Binaglia M., Corsini E., Di Luca M., Galli C.L., Marinovich M. Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases. J. Neurosci. 2003, 23:8692-8700.
157. Walker K., Dray A., Perkins M. Hyperalgesia in rats following intracerebroventricular administration of endotoxin: effect of bradykinin B1 and B2 receptor antagonist treatment. Pain 1996, 65:211-219.
158. Wang Z., Gleichmann H. GLUT2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 1998, 47:50-56.
159. Watkins L.R., Milligan E.D., Maier S.F. Glial activation: a driving force for pathological pain. Trends Neurosci. 2001, 24:450-455.
160. Watkins L.R., Milligan E.D., Maier S.F. Spinal cord glia: new players in pain. Pain 2001, 93:201-205.
161. Watkins L.R., Wieseler-Frank J., Milligan E.D., Johnston I., Maier S.F. Chapter 22 Contribution of glia to pain processing in health and disease. Handb. Clin. Neurol. 2006, 81:309-323.
162. Werner M.F., Kassuya C.A., Ferreira J., Zampronio A.R., Calixto J.B., Rae G.A. Peripheral kinin B(1) and B(2) receptor-operated mechanisms are implicated in neuropathic nociception induced by spinal nerve ligation in rats. Neuropharmacology 2007, 53:48-57.
163. White F.A., Jung H., Miller R.J. Chemokines and the pathophysiology of neuropathic pain. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20151-20158.
164. Wodarski R., Clark A.K., Grist J., Marchand F., Malcangio M. Gabapentin reverses microglial activation in the spinal cord of streptozotocin-induced diabetic rats. Eur. J. Pain 2009, 13:807-811.
165. Woolf C.J. Dissecting out mechanisms responsible for peripheral neuropathic pain: implications for diagnosis and therapy. Life Sci. 2004, 74:2605-2610.
166. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 2000, 288:1765-1769.
167. Yagihashi S., Yamagishi S., Wada R. Pathology and pathogenetic mechanisms of diabetic neuropathy: correlation with clinical signs and symptoms. Diabetes Res. Clin. Pract. 2007, 77(Suppl. 1):S184-S189.
168. Yasuda H., Terada M., Maeda K., Kogawa S., Sanada M., Haneda M., Kashiwagi A., Kikkawa R. Diabetic neuropathy and nerve regeneration. Prog. Neurobiol. 2003, 69:229-285.
169. Zhang J., De Koninck Y. Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury. J. Neurochem. 2006, 97:772-783.
170. Zhang R.X., Li A., Liu B., Wang L., Ren K., Zhang H., Berman B.M., Lao L. IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats. Pain 2008, 135:232-239.
171. Zhou X., Polgar P., Taylor L. Roles for interleukin-1beta, phorbol ester and a post-transcriptional regulator in the control of bradykinin B1 receptor gene expression. Biochem. J. 1998, 330(Pt 1):361-366.
172. Zhou X., Prado G.N., Taylor L., Yang X., Polgar P. Regulation of inducible bradykinin B1 receptor gene expression through absence of internalization and resensitization. J. Cell. Biochem. 2000, 78:351-362.
173. Zhou Z., Peng X., Hagshenas J., Insolera R., Fink D.J., Mata M. A novel cell-cell signaling by microglial transmembrane TNFalpha with implications for neuropathic pain. Pain 2010, 151:296-306.
174. Ziegler D. Painful diabetic neuropathy: treatment and future aspects. Diabetes Metab. Res. Rev. 2008, 24(Suppl. 1):S52-S57.
175. Ziegler D. Painful diabetic neuropathy: advantage of novel drugs over old drugs?. Diabetes Care 2009, 32(Suppl. 2):S414-S419.
176. Ziegler D., Rathmann W., Dickhaus T., Meisinger C., Mielck A. Prevalence of polyneuropathy in pre-diabetes and diabetes is associated with abdominal obesity and macroangiopathy: the MONICA/KORA Augsburg Surveys S2 and S3. Diabetes Care 2008, 31:464-469.
177. Zimmermann M. Pathobiology of neuropathic pain. Eur. J. Pharmacol. 2001, 429:23-37.
178. Zochodne D.W., Levy D. Nitric oxide in damage, disease and repair of the peripheral nervous system. Cell. Mol. Biol. (Noisy-le-grand) 2005, 51:255-267.
179. Zochodne D.W., Verge V.M., Cheng C., Hoke A., Jolley C., Thomsen K., Rubin I., Lauritzen M. Nitric oxide synthase activity and expression in experimental diabetic neuropathy. J. Neuropathol. Exp. Neurol. 2000, 59:798-807.