Suppression of vascular inflammation by kinin b1 receptor antagonism in a rat model of insulin resistance

Journal of Cardiovascular Pharmacology

Volumn 60, Issue 1, 2012, Pages 61-69

  Dias, Jenny Pena ^a   Couture, Réjean ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

adhesion molecules; bradykinin; cytokines; insulin resistance; kinin B 1 receptor; macrophage; vascular inflammation

Indexed keywords

2 [[3 (1,3 BENZODIOXOL 5 YL) 3 [[(6 METHOXY 2 NAPHTHYL)SULFONYL]AMINO]PROPANOYL]AMINO] 3 [4 [(2,6 DIMETHYLPIPERIDINYL)METHYL]PHENYL] N ISOPROPYL N METHYLPROPANAMIDE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ANTIINFLAMMATORY AGENT; CD11B ANTIGEN; CD68 ANTIGEN; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; KININ B1 RECEPTOR; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; NEUROPEPTIDE RECEPTOR; SSR 240612; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; GLUCOSE BLOOD LEVEL; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN RESISTANCE; INSULINEMIA; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; AORTA, THORACIC; BIOLOGICAL MARKERS; DIOXOLES; DISEASE MODELS, ANIMAL; GLUCOSE; INFLAMMATION; INSULIN RESISTANCE; MALE; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, BRADYKININ B1; SULFONAMIDES; UP-REGULATION;

EID: 84863783755     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3182576277     Document Type: Article

References (78)

1. Feng L, Matsumoto C, Schwartz A, et al. Chronic vascular inflammation in patients with type 2 diabetes: endothelial biopsy and RT-PCR analysis. Diabetes Care. 2005;28:379-384.
2. Liu S, Tinker L, Song Y, et al. A prospective study of inflammatory cytokines and diabetes mellitus in a multiethnic cohort of postmenopausal women. Arch Intern Med. 2007;167:1676-1685.
3. Bertoni AG, Burke GL, Owusu JA, et al. Inflammation and the incidence of type 2 diabetes: the Multi-Ethnic Study of Atherosclerosis (MESA). Diabetes Care. 2010;33:804-810.
4. Cavaillon JM, Haeffner-Cavaillon N. Cytokines and inflammation [in French]. Rev Prat. 1993;43:547-552.
5. El-seweidy MM, El-Swefy SE, Ameen RS, et al. Effect of age receptor blocker and/or anti-inflammatory coadministration in relation to glycation, oxidative stress and cytokine production in stz diabetic rats. Pharmacol Res. 2002;45:391-398.
6. Lafuente N, Matesanz N, Azcutia V, et al. The deleterious effect of high concentrations of D-glucose requires pro-inflammatory preconditioning. J Hypertens. 2008;26:478-485.
7. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
8. Ruotsalainen E, Stancakova A, Vauhkonen I, et al. Changes in cytokine levels during acute hyperinsulinemia in offspring of type 2 diabetic subjects. Atherosclerosis. 2010;210:536-541.
9. Goldberg RB. Cytokine and cytokine-like inflammation markers, endothelial dysfunction, and imbalanced coagulation in development of diabetes and its complications. J Clin Endocrinol Metab. 2009;94:3171-3182.
10. Cavaillon JM. Contribution of cytokines to inflammatory mechanisms [in French]. Pathol Biol (Paris). 1993;41:799-811.
11. Schleicher E, Friess U. Oxidative stress, AGE, and atherosclerosis. Kidney Int Suppl. 2007;106:S17-S26.
12. Toso C, Emamaullee JA, Merani S, et al. The role of macrophage migration inhibitory factor on glucose metabolism and diabetes. Diabetologia. 2008;51:1937-1946.
13. Marceau F, Sabourin T, Houle S, et al. Kinin receptors: functional aspects. Int Immunopharmacol. 2002;2:1729-1739.
14. Couture R, Girolami JP. 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.
15. Deblois D, Bouthillier J, Marceau F. Effect of glucocorticoids, monokines and growth factors on the spontaneously developing responses of the rabbit isolated aorta to des-Arg9-bradykinin. Br J Pharmacol. 1988; 93:969-977.
16. Regoli D, Nsa Allogho S, Rizzi A, et al. Bradykinin receptors and their antagonists. Eur J Pharmacol. 1998;348:1-10.
17. Emanueli C, Maestri R, Corradi D, et al. Dilated and failing cardiomyopathy in bradykinin B(2) receptor knockout mice. Circulation. 1999; 100:2359-2365.
18. Loiola RA, Reis FC, Kawamoto EM, et al. Role of vascular Kinin B1 and B2 receptors in endothelial nitric oxide metabolism. Peptides. 2011;32: 1700-1705.
19. Lungu C, Dias JP, Franca CE, et al. 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.
20. Ismael MA, Talbot S, Carbonneau CL, et al. 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.
21. Dias JP, Talbot S, Senecal J, et al. 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.
22. El-Midaoui A, de Champlain J. Effects of glucose and insulin on the development of oxidative stress and hypertension in animal models of type 1 and type 2 diabetes. J Hypertens. 2005;23:581-588.
23. Koh KK, Han SH, Quon MJ. Inflammatory markers and the metabolic syndrome: insights from therapeutic interventions. J Am Coll Cardiol. 2005;46:1978-1985.
24. Dias JP, Couture R. Blockade of kinin B(1) receptor reverses plasma fatty acids composition changes and body and tissue fat gain in a rat model of insulin resistance. Diabetes Obes Metab. 2012;14:244-253.
25. Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest. 2006;116:1793-1801.
26. Kuhr F, Lowry J, Zhang Y, et al. Differential regulation of inducible and endothelial nitric oxide synthase by kinin B1 and B2 receptors. Neuropeptides. 2010;44:145-154.
27. Gougat J, Ferrari B, Sarran L, et al. 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)-Nisopropyl-N- methylpropanamide hydrochloride], a new nonpeptide antagonist of the bradykinin B1 receptor: biochemical and pharmacological characterization. J Pharmacol Exp Ther. 2004;309:661-669.
28. Dias JP, Ismael MA, Pilon M, et al. 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.
29. Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412-419.
30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-408.
31. Pouliot M, Hetu S, Lahjouji K, et al. Modulation of retinal blood flow by kinin B(1) receptor in Streptozotocin-diabetic rats. Exp Eye Res. 2011;92: 482-489.
32. Blouet C, Mariotti F, Mathe V, et al. Nitric oxide bioavailability and not production is first altered during the onset of insulin resistance in sucrosefed rats. Exp Biol Med (Maywood). 2007;232:1458-1464.
33. Wink DA, Mitchell JB. Chemical biology of nitric oxide: Insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med. 1998;25:434-456.
34. Javanmard SH, Nematbakhsh M, Mahmoodi F, et al. l-Arginine supplementation enhances eNOS expression in experimental model of hypercholesterolemic rabbits aorta. Pathophysiology. 2009;16:9-13.
35. Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci. 2004;75:639-653.
36. Wu F, Tyml K, Wilson JX. iNOS expression requires NADPH oxidasedependent redox signaling in microvascular endothelial cells. J Cell Physiol. 2008;217:207-214.
37. Kuhlencordt PJ, Chen J, Han F, et al. Genetic deficiency of inducible nitric oxide synthase reduces atherosclerosis and lowers plasma lipid peroxides in apolipoprotein E-knockout mice. Circulation. 2001;103: 3099-3104.
38. Kuhr FK, Zhang Y, Brovkovych V, et al. Beta-arrestin 2 is required for B1 receptor-dependent post-translational activation of inducible nitric oxide synthase. FASEB J. 2010;24:2475-2483.
39. Schanstra JP, Bataille E, Marin Castano ME, et al. 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.
40. Leeb-Lundberg LM, Marceau F, Muller-Esterl W, et al. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev. 2005;57:27-77.
41. Passos GF, Fernandes ES, Campos MM, et al. Kinin B1 receptor up-regulation after lipopolysaccharide administration: role of proinflammatory cytokines and neutrophil influx. J Immunol. 2004;172:1839-1847.
42. Calixto JB, Medeiros R, Fernandes ES, et al. Kinin B1 receptors: key G-protein-coupled receptors and their role in inflammatory and painful processes. Br J Pharmacol. 2004;143:803-818.
43. Araujo RC, Kettritz R, Fichtner I, et al. Altered neutrophil homeostasis in kinin B1 receptor-deficient mice. Biol Chem. 2001;382:91-95.
44. Saxena P, Shaw OM, Misso NL, et al. Remote ischemic preconditioning stimulus decreases the expression of kinin receptors in human neutrophils. J Surg Res. 2009;171:311-316.
45. Ahluwalia A, Perretti M. Involvement of bradykinin B1 receptors in the polymorphonuclear leukocyte accumulation induced by IL-1 beta in vivo in the mouse. J Immunol. 1996;156:269-274.
46. Duchene J, Ahluwalia A. The kinin B(1) receptor and inflammation: new therapeutic target for cardiovascular disease. Curr Opin Pharmacol. 2009;9:125-131.
47. Pesquero JB, Araujo RC, Heppenstall PA, et al. Hypoalgesia and altered inflammatory responses in mice lacking kinin B1 receptors. Proc Natl Acad Sci USA. 2000;97:8140-8145.
48. Vianna RM, Ongali B, Regoli D, et al. Up-regulation of kinin B1 receptor in the lung of streptozotocin-diabetic rat: autoradiographic and functional evidence. Br J Pharmacol. 2003;138:13-22.
49. Souza DG, Lomez ES, Pinho V, et al. Role of bradykinin B2 and B1 receptors in the local, remote, and systemic inflammatory responses that follow intestinal ischemia and reperfusion injury. J Immunol. 2004;172: 2542-2548.
50. Wright HL, Moots RJ, Bucknall RC, et al. Neutrophil function in inflammation and inflammatory diseases. Rheumatology (Oxford). 2010; 49:1618-1631.
51. Burch RM, Connor JR, Tiffany CW. The kallikrein-kininogen-kinin system in chronic inflammation. Agents Actions. 1989;27:258-260.
52. Bockmann S, Paegelow I. Kinins and kinin receptors: importance for the activation of leukocytes. J Leukoc Biol. 2000;68:587-592.
53. Legedz L, Randon J, Sessa C, et al. Induction of tissue kallikrein in human carotid atheroma does not lead to kallikrein-kinins pathway activation. J Hypertens. 2005;23:359-366.
54. Tiffany CW, Burch RM. Bradykinin stimulates tumor necrosis factor and interleukin-1 release from macrophages. FEBS Lett. 1989;247:189-192.
55. Tsukagoshi H, Shimizu Y, Horie T, et al. Regulation by interleukin-1beta of gene expression of bradykinin B1 receptor in MH-S murine alveolar macrophage cell line. Biochem Biophys Res Commun. 1999;259:476-482.
56. Klein J, Gonzalez J, Decramer S, et al. Blockade of the kinin B1 receptor ameloriates glomerulonephritis. J Am Soc Nephrol. 2010;21:1157-1164.
57. Hou T, Tieu BC, Ray S, et al. Roles of IL-6-gp130 Signaling in Vascular Inflammation. Curr Cardiol Rev. 2008;4:179-192.
58. Akira S. IL-6-regulated transcription factors. Int J Biochem Cell Biol. 1997;29:1401-1418.
59. Ramar K, Caples SM. Vascular changes, cardiovascular disease and obstructive sleep apnea. Future Cardiol. 2011;7:241-249.
60. Moller DE. Potential role of TNF-alpha in the pathogenesis of insulin resistance and type 2 diabetes. Trends Endocrinol Metab. 2000;11:212-217.
61. Terra X, Pallares V, Ardevol A, et al. Modulatory effect of grape-seed procyanidins on local and systemic inflammation in diet-induced obesity rats. J Nutr Biochem. 2011;22:380-387.
62. Behr-Roussel D, Oudot A, Caisey S, et al. Daily treatment with sildenafil reverses endothelial dysfunction and oxidative stress in an animal model of insulin resistance. Eur Urol. 2008;53:1272-1280.
63. Kobayasi R, Akamine EH, Davel AP, et al. Oxidative stress and inflammatory mediators contribute to endothelial dysfunction in high-fat dietinduced obesity in mice. J Hypertens. 2010;28:2111-2119.
64. Calandra T, Bernhagen J, Mitchell RA, et al. The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med. 1994;179:1895-1902.
65. Toh ML, Aeberli D, Lacey D, et al. Regulation of IL-1 and TNF receptor expression and function by endogenous macrophage migration inhibitory factor. J Immunol. 2006;177:4818-4825.
66. Amin MA, Haas CS, Zhu K, et al. Migration inhibitory factor up-regulates vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 via Src, PI3 kinase, and NFkappaB. Blood. 2006;107:2252-2261.
67. Waeber G, Calandra T, Roduit R, et al. Insulin secretion is regulated by the glucose-dependent production of islet beta cell macrophage migration inhibitory factor. Proc Natl Acad Sci USA. 1997;94:4782-4787.
68. Atsumi T, Cho YR, Leng L, et al. The proinflammatory cytokine macrophage migration inhibitory factor regulates glucose metabolism during systemic inflammation. J Immunol. 2007;179:5399-5406.
69. Burger-Kentischer A, Gobel H, Kleemann R, et al. Reduction of the aortic inflammatory response in spontaneous atherosclerosis by blockade of macrophage migration inhibitory factor (MIF). Atherosclerosis. 2006; 184:28-38.
70. Verschuren L, Kooistra T, Bernhagen J, et al. MIF deficiency reduces chronic inflammation in white adipose tissue and impairs the development of insulin resistance, glucose intolerance, and associated atherosclerotic disease. Circ Res. 2009;105:99-107.
71. Malik AB. Endothelial cell interactions and integrins. New Horiz. 1993; 1:37-51.
72. Pober JS, Gimbrone MA Jr, Lapierre LA, et al. Overlapping patterns of activation of human endothelial cells by interleukin 1, tumor necrosis factor, and immune interferon. J Immunol. 1986;137:1893-1896.
73. Sumagin R, Sarelius IH. A role for ICAM-1 in maintenance of leukocyteendothelial cell rolling interactions in inflamed arterioles. Am J Physiol Heart Circ Physiol. 2007;293:H2786-H2798.
74. Dejana E, Breviario F, Caveda L. Leukocyte-endothelial cell adhesive receptors. Clin Exp Rheumatol. 1994;12(suppl 10):S25-S28.
75. Sligh JE Jr, Ballantyne CM, Rich SS, et al. Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc Natl Acad Sci USA. 1993;90:8529-8533.
76. Xu H, Gonzalo JA, St Pierre Y, et al. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J Exp Med. 1994;180:95-109.
77. Gobel K, Pankratz S, Schneider-Hohendorf T, et al. Blockade of the kinin receptor B1 protects from autoimmune CNS disease by reducing leukocyte trafficking. J Autoimmun. 2011;36:106-114
78. Pouliot M, Talbot S, Sénécale J, et al. Ocular application of the kinin B1 receptor antagonist LF22-0542 inhibits retinal inflammation and oxidative stress in Streptozotocin-Diabetic rats. PLoS One. 2012; 7:e33864.