Bradykinin protects against brain microvascular endothelial cell death induced by pathophysiological stimuli

Journal of Cellular Physiology

Volumn 222, Issue 1, 2010, Pages 168-176

  Bovenzi, Veronica ^a   Savard, Martin ^a   Morin, Josée ^a   Cuerrier, Charles M ^a   Grandbois, Michel ^a   Gobeil Jr , Fernand ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BRADYKININ; COPPER ZINC SUPEROXIDE DISMUTASE; CRYSTAL VIOLET; CYCLOOXYGENASE 2; HYDROGEN PEROXIDE; ICATIBANT; LIPOCORTIN 5; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN BNIP3; PROTEIN KINASE B; RADIOLIGAND; TETRAZOLIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CALCIUM TRANSPORT; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; ENDOTHELIUM CELL; EX VIVO STUDY; EXPERIMENT; EXPLANT; FLUORESCENCE ACTIVATED CELL SORTING; HEMODYNAMICS; IN VITRO STUDY; LIGAND BINDING; MICROVASCULATURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; STIMULUS RESPONSE; SWINE;

ANIMALS; BRADYKININ; BRAIN; CELL DEATH; CYTOPROTECTION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; HYDROGEN PEROXIDE; LIPOPOLYSACCHARIDES; MICROVESSELS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTECTIVE AGENTS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, BRADYKININ B2; SUS SCROFA;

RATTUS; SUIDAE;

EID: 73949137639     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21933     Document Type: Article

References (66)

1. Battegay EJ, de Miguel LS, Petrimpol M, Humar R. 2007. Effects of anti-hypertensive drugs on vessel rarefaction. Curr Opin Pharmacol 7:151-157.
2. Bauer PR. 2002. Microvascular responses to sepsis: Clinical significance. Pathophysiology 8:141-148.
3. Beauchamp MH, Martinez-Bermudez AK, Gobeil F, Jr., Marrache AM, Hou X, Speranza G, Abran D, Quiniou C, Lachapelle P, Roberts J II, Almazan G, Varma DR, Chemtob S. 2001. Role of thromboxane in retinal microvascular degeneration in oxygen-induced retinopathy. J Appl Physiol 90:2279-2288.
4. Beauchamp MH, Marrache AM, Hou X, Gobeil F, Jr., Bernier SG, Lachapelle P, Abran D, Quiniou C, Brault S, Peri KG, Roberts J II, Almazan G, Varma DR, Chemtob S. 2002. Platelet-activating factor in vasoobliteration of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 43:3327-3337.
5. Blais PA, Cote J, Morin J, Larouche A, Gendron G, FortierA, RegoliD,NeugebauerW,Gobeil F, Jr. 2005. Hypotensive effects of hemopressin and bradykinin in rabbits, rats and mice. A comparative study. Peptides 26:1317-1322.
6. Bolli R, Shinmura K, Tang XL, Kodani E, Xuan YT, Guo Y, Dawn B. 2002. Discovery of a new function of cyclooxygenase (COX)-2: COX-2 is a cardioprotective protein that alleviates ischemia/reperfusion injury and mediates the late phase of preconditioning. Cardiovasc Res 55:506-519.
7. Brasaemle DL, Attie AD. 1988. Microelisa reader quantitation of fixed, stained, solubilized cells in microtitre dishes. Biotechniques 6:418-419.
8. Brault S, Martinez-Bermudez AK, Marrache AM, Gobeil F, Jr., Hou X, Beauchamp M, Quiniou C, Almazan G, Lachance C, Roberts J II, Varma DR, Chemtob S. 2003. Selective neuromicrovascular endothelial cell death by 8-Iso-prostaglandin F2alpha: Possible role in ischemic brain injury. Stroke 34:776-782.
9. Brault S, Gobeil F, Jr., Fortier A, Honore JC, Joyal JS, Sapieha PS, Kooli A, Martin E, Hardy P, Ribeiro-da-Silva A, Peri K, Lachapelle P, VarmaD, Chemtob S. 2007. Lysophosphatidic acid induces endothelial cell death by modulating the redox environment. Am J Physiol Regul Integr Comp Physiol 292:R1174-R1183.
10. Campbell DJ, Krum H, Esler MD. 2005. Losartan increases bradykinin levels in hypertensive humans. Circulation 111:315-320.
11. Caughey GE, Cleland LG, Penglis PS, Gamble JR, James MJ. 2001. Roles of cyclooxygenase (COX)-1 and COX-2 in prostanoid production by human endothelial cells: Selective upregulation of prostacyclin synthesis by COX-2. J Immunol 167:2831-2838.
12. Ceconi C, Fox KM, Remme WJ, Simoons ML, Bertrand M, Parrinello G, Kluft C, Blann A, Cokkinos D, Ferrari R. 2007. ACE inhibition with perindopril and endothelial function. Results of a substudy of the EUROPA study: PERTINENT. Cardiovasc Res 73:237-246.
13. Chao J, Li HJ, Yao YY, Shen B, Gao L, Bledsoe G, Chao L. 2007. Kinin infusion prevents renal inflammation, apoptosis, and fibrosis via inhibition of oxidative stress and mitogenactivated protein kinase activity. Hypertension 49:490-497.
14. Choy JC,Granville DJ, HuntDW,McManus BM. 2001. Endothelial cell apoptosis: Biochemical characteristics and potential implications for atherosclerosis. J Mol Cell Cardiol 33:1673-1690.
15. Couture R, Girolami JP. 2004. Putative roles of kinin receptors in the therapeutic effects of angiotensin 1-converting enzyme inhibitors in diabetes mellitus. Eur J Pharmacol 500:467-485.
16. Cruden NL, Tse GH, Fox KA, Ludlam CA, Megson I, Newby DE. 2005. B1 kinin receptor does not contribute to vascular tone or tissue plasminogen activator release in the peripheral circulation of patients with heart failure. Arterioscler Thromb Vasc Biol 25:772-777.
17. Csordas A,Wick G, Bernhard D. 2006. Hydrogen peroxide-mediated necrosis induction in HUVECs is associated with an atypical pattern of caspase-3 cleavage. Exp Cell Res 312:1753-1764.
18. Degterev A, Yuan J. 2008. Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 9:378-390.
19. Duncan AM, Kladis A, Jennings GL, Dart AM, Esler M, Campbell DJ. 2000. Kinins in humans. Am J Physiol Regul Integr Comp Physiol 278:R897-R904.
20. Emanueli C, Salis MB, Pinna A, Stacca T, Milia AF, Spano A, Chao J, Chao L, Sciola L, Madeddu P. 2002. Prevention of diabetes-induced microangiopathy by human tissue kallikrein gene transfer. Circulation 106:993-999.
21. Feihl F, Liaudet L, Waeber B, Levy BI. 2006. Hypertension: A disease of the microcirculation? Hypertension 48:1012-1017.
22. Feletou M, Vanhoutte PM. 2006. Endothelium-derived hyperpolarizing factor: Where are we now? Arterioscler Thromb Vasc Biol 26:1215-1225.
23. Feng J, Sellke ME, Ramlawi B, Boodhwani M, Clements R, Li J, Bianchi C, Sellke FW. 2006. Bradykinin induces microvascular preconditioning through the opening of calciumactivated potassium channels. Surgery 140:192-197.
24. Fujita N, Manabe H, Yoshida N, Matsumoto N, Ochiai J, Masui Y, Uemura M, Naito Y, Yoshikawa T. 2000. Inhibition of angiotensin-converting enzyme protects endothelial cell against hypoxia/reoxygenation injury. Biofactors 11:257-266.
25. Gao XP, Anding P, Robbins RA, Rennard SI, Rubinstein I. 1994. Peptidases modulate bradykinin-induced arteriolar dilation in the hamster cheek pouch. Am J Physiol 266:H93-H98.
26. Gobeil F, Jr., Charland S, Filteau C, Perron SI, Neugebauer W, Regoli D. 1999. Kinin B1 receptor antagonists containing alpha-methyl-L-phenylalanine: In vitro and in vivo antagonistic activities. Hypertension 33:823-829.
27. Gryglewski RJ, Chlopicki S, Uracz W, Marcinkiewicz E. 2001. Significance of endothelial prostacyclin and nitric oxide in peripheral and pulmonary circulation. Med Sci Monit 7:1-16.
28. Hamdi HK, Castellon R. 2003. ACE inhibition actively promotes cell survival by altering gene expression. Biochem Biophys Res Commun 310:1227-1235.
29. Heitsch H. 2003. The therapeutic potential of bradykinin B2 receptor agonists in the treatment of cardiovascular disease. Expert Opin Investig Drugs 12:759-770.
30. Hornig B, Drexler H. 1997. Endothelial function and bradykinin in humans. Drugs 54:42-47. Jeppesen P, Aalkjaer C, Bek T. 2002. Bradykinin relaxation in small porcine retinal arterioles. Invest Ophthalmol Vis Sci 43:1891-1896.
31. Kano A, WolfgangMJ, GaoQ, Jacoby J, Chai GX, Hansen W, Iwamoto Y, Pober JS, Flavell RA, Fu XY. 2003. Endothelial cells require STAT3 for protection against endotoxin-induced inflammation. J Exp Med 198:1517-1525.
32. Karsan A, Yee E, Harlan JM. 1996. Endothelial cell death induced by tumor necrosis factoralpha is inhibited by the Bcl-2 family member, A1. J Biol Chem 271:27201-27204.
33. Kichuk MR, Seyedi N, Zhang X, Marboe CC, Michler RE, Addonizio LJ, Kaley G, Nasjletti A, Hintze TH. 1996. Regulation of nitric oxide production in human coronary microvessels and the contribution of local kinin formation. Circulation 94:44-51.
34. Knock GA, Poston L. 1996. Bradykinin-mediated relaxation of isolated maternal resistance arteries in normal pregnancy and preeclampsia.AmJ Obstet Gynecol 175:1668-1674.
35. Kobayashi N, DeLano FA, Schmid-Schonbein GW. 2005. Oxidative stress promotes endothelial cell apoptosis and loss of microvessels in the spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 25:2114-2121.
36. Kono Y, Sawada S, Kawahara T, Tsuda Y, Higaki T, Yamasaki S, Imamura H, Tada Y, Sato T, Hiranuma O, Akamatsu N, Komatsu S, Tamagaki T, Nakagawa K, Tsuji H, Nakagawa M. 2002. Bradykinin inhibits serum-depletion-induced apoptosis of human vascular endothelial cells by inducing nitric oxide via calcium ion kinetics. J Cardiovasc Pharmacol 39:251-261.
37. Leeb-Lundberg LM, Marceau F, Muller-Esterl W, Pettibone DJ, Zuraw BL. 2005. International union of pharmacology. XLV. Classification of the kinin receptor family: From molecular mechanisms to pathophysiological consequences. Pharmacol Rev 57:27-77.
38. Legos JJ, Tuma RF, Barone FC. 2002. Pharmacological interventions for stroke: Failures and future. Expert Opin Investig Drugs 11:603-614.
39. Liu YH, Yang XP, Sharov VG, Nass O, Sabbah HN, Peterson E,Carretero OA. 1997. Effects of angiotensin-converting enzyme inhibitors and angiotensin II type 1 receptor antagonists in rats with heart failure. Role of kinins and angiotensin II type 2 receptors. J Clin Invest 99:1926-1935.
40. Liuba P, Batra S, Pesonen E, Werner O. 2005. Bradykinin preconditions postischemic arterial endothelial function in humans. J Card Surg 20:420-424.
41. Malham GM, Souter MJ. 2001. Systemic inflammatory response syndrome and acute neurological disease. Br J Neurosurg 15:381-387.
42. Matsumoto N, Manabe H, Ochiai J, Fujita N, Takagi T, Uemura M, Naito Y, Yoshida N, Oka S, Yoshikawa T. 2003. An AT1-receptor antagonist and an angiotensin-converting enzyme inhibitor protect against hypoxia-induced apoptosis in human aortic endothelial cells through upregulation of endothelial cell nitric oxide synthase activity. Shock 19:547-552.
43. Michiels C, Raes M, Toussaint O, Remacle J. 1994. Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress. Free Radic Biol Med 17:235-248.
44. Mombouli JV, Vanhoutte PM. 1995. Kinins and endothelial control of vascular smooth muscle. Annu Rev Pharmacol Toxicol 35:679-705.
45. Munshi N, Fernandis AZ, Cherla RP, Park IW, Ganju RK. 2002. Lipopolysaccharide-induced apoptosis of endothelial cells and its inhibition by vascular endothelial growth factor. J Immunol 168:5860-5866.
46. Murphey LJ, Malave HA, Petro J, Biaggioni I, Byrne DW, Vaughan DE, Luther JM, PretoriusM, Brown NJ. 2006. Bradykinin and its metabolite bradykinin 1-5 inhibit thrombin-induced platelet aggregation in humans. J Pharmacol Exp Ther 318:1287-1292.
47. Oeseburg H, Iusuf D, van der Harst P, van Gilst WH, Henning RH, Roks AJ. 2009. Bradykinin protects against oxidative stress-induced endothelial cell senescence. Hypertension 53:417-422.
48. Pellacani A, Brunner HR, Nussberger J. 1994. Plasma kinins increase after angiotensinconverting enzyme inhibition in human subjects. Clin Sci (Lond) 87:567-574.
49. Ping A, Chun ZX, Xue XY. 2005. Bradykinin preconditioning induces protective effects against focal cerebral ischemia in rats. Brain Res 1059:105-112.
50. Quiniou C, Sennlaub F, Beauchamp MH, Checchin D, Lahaie I, Brault S, Gobeil F, Jr., Sirinyan M, Kooli A, Hardy P, Pshezhetsky A, Chemtob S. 2006. Dominant role for calpain in thromboxane-induced neuromicrovascular endothelial cytotoxicity. J Pharmacol Exp Ther 316:618-627.
51. Renne T, Schuh K, Muller-Esterl W. 2005. Local bradykinin formation is controlled by glycosaminoglycans. J Immunol 175:3377-3385.
52. Rhaleb NE, Rouissi N, Jukic D, Regoli D, Henke S, Breipohl G, Knolle J. 1992. Pharmacological characterization of a new highly potent B2 receptor antagonist (HOE 140: D-Arg-[Hyp3, Thi5,D-Tic7,Oic8]bradykinin). Eur J Pharmacol 210:115-120.
53. Savard M, Barbaz D, Belanger S, Muller-Esterl W, Bkaily G,D'Orleans-Juste P, Cote J, Bovenzi V, Gobeil F, Jr. 2008. Expression of endogenous nuclear bradykinin B2 receptors mediating signaling in immediate early gene activation. J Cell Physiol 216:234-244.
54. Schmaier AH, McCrae KR. 2007. The plasma kallikrein-kinin system: Its evolution from contact activation. J Thromb Haemost 5:2323-2329.
55. Shigematsu S, Yamauchi K, Nakajima K, Iijima S, Aizawa T, Hashizume K. 1999. IGF-1 regulates migration and angiogenesis of human endothelial cells. Endocr J 46:S59-S62. Sommers Smith SK, Smith DM. 2002. Beta blockade induces apoptosis in cultured capillary endothelial cells. In Vitro Cell Dev Biol Anim 38:298-304.
56. Stokes KY, Granger DN. 2005. The microcirculation:A motor for the systemic inflammatory response and large vessel disease induced by hypercholesterolaemia? J Physiol 562:647-653.
57. Strauss KI, Marini AM. 2002. Cyclooxygenase-2 inhibition protects cultured cerebellar granule neurons from glutamate-mediated cell death. J Neurotrauma 19:627-638.
58. Wang HL, Akinci IO, Baker CM, Urich D, Bellmeyer A, Jain M, Chandel NS, Mutlu GM, Budinger GR. 2007. The intrinsic apoptotic pathway is required for lipopolysaccharideinduced lung endothelial cell death. J Immunol 179:1834-1841.
59. Wang X, Wei M, Kuukasjarvi P, Laurikka J, Rinne T, Moilanen E, Tarkka M. 2009. The antiinflammatory effect of bradykinin preconditioning in coronary artery bypass grafting (bradykinin and preconditioning). Scand Cardiovasc J 43:72-79.
60. Wei M,Wang X, Kuukasjarvi P, Laurikka J, Rinne T, Honkonen EL, Tarkka M. 2004. Bradykinin preconditioning in coronary artery bypass grafting. Ann Thorac Surg 78:492-497.
61. White BC, Sullivan JM, DeGracia DJ,O'Neil BJ, Neumar RW, Grossman LI, Rafols JA, Krause GS. 2000. Brain ischemia and reperfusion: Molecular mechanisms of neuronal injury. J Neurol Sci 179:1-33.
62. Xia CF, Yin H, Yao YY, Borlongan CV, Chao L, Chao J. 2006. Kallikrein protects against ischemic stroke by inhibiting apoptosis and inflammation and promoting angiogenesis and neurogenesis. Hum Gene Ther 17:206-219.
63. Yan-Feng W, Gang L, Yan-Ting G. 2008. Bradykinin preconditioning induces protective effects on the spinal cord ischemic injury of rats. Neurosci Lett 433:114-118.
64. Yao YY, YinH, Shen B, Chao L, Chao J. 2007. Tissue kallikrein and kinin infusion rescues failing myocardium after myocardial infarction. J Card Fail 13:588-596.
65. Zhang P, Wang H, Min X,Wang Y, Tang J, Cheng J, Li D, Chen X, Cheng F, Wang N, Yang H. 2009. Pim-3 is expressed in endothelial cells and promotes vascular tube formation. J Cell Physiol 220:82-90.
66. Zhao Y, Qiu Q, Mahdi F, Shariat-Madar Z, Rojkjaer R, Schmaier AH. 2001. Assembly and activation of HK-PK complex on endothelial cells results in bradykinin liberation and NO formation. Am J Physiol Heart Circ Physiol 280:H1821-H1829.