Modulation of Kinin B2 receptor signaling controls aortic dilatation and rupture in the Angiotensin II-infused apolipoprotein E-deficient mouse

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 5, 2016, Pages 898-907

  Moran, Corey S ^a   Rush, Catherine M ^a   Dougan, Tammy ^a   Jose, Roby J ^a   Biros, Erik ^a   Norman, Paul E ^c   Gera, Lajos ^b   Golledge, Jonathan ^a,d  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d TOWNSVILLE HOSPITAL   (Australia)

Author keywords

abdominal aortic aneurysm; angiotensin II; animal model cardiovascular disease; aorta; bradykinin; kinins

Indexed keywords

ANGIOTENSIN II; APOLIPOPROTEIN E; B 9330; BRADYKININ B2 RECEPTOR; BRADYKININ B2 RECEPTOR AGONIST; BRADYKININ B2 RECEPTOR ANTAGONIST; CALCIUM PHOSPHATE; GELATINASE A; GELATINASE B; MESSENGER RNA; MYELOPEROXIDASE; OSTEOPONTIN; OSTEOPROTEGERIN; UNCLASSIFIED DRUG; B 9430; BRADYKININ; MMP2 PROTEIN, HUMAN; MMP9 PROTEIN, HUMAN; MMP9 PROTEIN, RAT; SPP1 PROTEIN, HUMAN; TNFRSF11B PROTEIN, HUMAN;

ABDOMINAL AORTA ANEURYSM; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; AORTA ARCH; AORTA DILATATION; AORTA RUPTURE; AORTA WALL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ASSOCIATION; LEUKOCYTE ACTIVATION; MODULATION; MOLECULAR PATHOLOGY; MOUSE; MOUSE MODEL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; SMOOTH MUSCLE CELL; THORACIC AORTA; VASCULAR SMOOTH MUSCLE CELL; VASODILATATION; ABDOMINAL AORTA; AGONISTS; ANALOGS AND DERIVATIVES; ANIMAL; AORTIC ANEURYSM, ABDOMINAL; AORTIC RUPTURE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENETIC PREDISPOSITION; GENETICS; HUMAN; KNOCKOUT MOUSE; LESIONS AND DEFECTS; MALE; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; TIME FACTOR; TISSUE CULTURE TECHNIQUE;

ANGIOTENSIN II; ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; AORTIC RUPTURE; APOLIPOPROTEINS E; BRADYKININ; BRADYKININ B2 RECEPTOR ANTAGONISTS; CALCIUM PHOSPHATES; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE, KNOCKOUT; NEUTROPHIL ACTIVATION; OSTEOPONTIN; OSTEOPROTEGERIN; PHENOTYPE; RATS, SPRAGUE-DAWLEY; RECEPTOR, BRADYKININ B2; SIGNAL TRANSDUCTION; TIME FACTORS; TISSUE CULTURE TECHNIQUES;

EID: 84960357523     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.306945     Document Type: Article

References (45)

1. Moll FL, Powell JT, Fraedrich G, Verzini F, Haulon S, Waltham M, van Herwaarden JA, Holt PJ, van Keulen JW, Rantner B, Schlösser FJ, Setacci F, Ricco JB, European Society for Vascular Surgery Management of abdominal aortic aneurysms clinical practice guidelines of the European society for vascular surgery. Eur J Vasc Endovasc Surg 2011 41 suppl 1 S1 S58. doi: 10.1016/j.ejvs.2010.09.011
2. Golledge J, Norman PE, Current status of medical management for abdominal aortic aneurysm. Atherosclerosis 2011 217 57 63. doi: 10.1016/j.atherosclerosis.2011.03.006
3. Rughani G, Robertson L, Clarke M, Medical treatment for small abdominal aortic aneurysms. Cochrane Database Syst Rev 2012 9 CD009536. doi: 10.1002/14651858.CD009536.pub2
4. Golledge J, Muller J, Daugherty A, Norman P, Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler Thromb Vasc Biol 2006 26 2605 2613. doi: 10.1161/01.ATV.0000245819.32762.cb
5. Moreau ME, Garbacki N, Molinaro G, Brown NJ, Marceau F, Adam A, The kallikrein-kinin system: current and future pharmacological targets. J Pharmacol Sci 2005 99 6 38
6. Quitterer U, AbdAlla S, Vasopressor meets vasodepressor: the AT1-B2 receptor heterodimer. Biochem Pharmacol 2014 88 284 290. doi: 10.1016/j.bcp.2014.01.019
7. Maestri R, Milia AF, Salis MB, Graiani G, Lagrasta C, Monica M, Corradi D, Emanueli C, Madeddu P, Cardiac hypertrophy and microvascular deficit in kinin B2 receptor knockout mice. Hypertension 2003 41 1151 1155. doi: 10.1161/01.HYP.0000064180.55222.DF
8. Couture R, Harrisson M, Vianna RM, Cloutier F, Kinin receptors in pain and inflammation. Eur J Pharmacol 2001 429 161 176
9. Ehrenfeld P, Matus CE, Pavicic F, Toledo C, Nualart F, Gonzalez CB, Burgos RA, Bhoola KD, Figueroa CD, Kinin B1 receptor activation turns on exocytosis of matrix metalloprotease-9 and myeloperoxidase in human neutrophils: involvement of mitogen-Activated protein kinase family. J Leukoc Biol 2009 86 1179 1189. doi: 10.1189/jlb.0109012
10. Dos Santos AC, Roffê E, Arantes RM, Juliano L, Pesquero JL, Pesquero JB, Bader M, Teixeira MM, Carvalho-Tavares J, Kinin B2 receptor regulates chemokines CCL2 and CCL5 expression and modulates leukocyte recruitment and pathology in experimental autoimmune encephalomyelitis (EAE) in mice. J Neuroinflammation 2008 5 49. doi: 10.1186/1742-2094-5-49
11. Shaw OM, Harper JL, Bradykinin receptor 2 extends inflammatory cell recruitment in a model of acute gouty arthritis. Biochem Biophys Res Commun 2011 416 266 269. doi: 10.1016/j.bbrc.2011.10.137
12. Böckmann S, Paegelow I, Kinins and kinin receptors: importance for the activation of leukocytes. J Leukoc Biol 2000 68 587 592
13. Tiffany CW, Burch RM, Bradykinin stimulates tumor necrosis factor and interleukin-1 release from macrophages. FEBS Lett 1989 247 189 192
14. Yogi A, Callera GE, Tostes R, Touyz RM, Bradykinin regulates calpain and proinflammatory signaling through TRPM7-sensitive pathways in vascular smooth muscle cells. Am J Physiol Regul Integr Comp Physiol 2009 296 R201 R207. doi: 10.1152/ajpregu.90602.2008
15. Kaschina E, Stoll M, Sommerfeld M, Steckelings UM, Kreutz R, Unger T, Genetic kininogen deficiency contributes to aortic aneurysm formation but not to atherosclerosis. Physiol Genomics 2004 19 41 49. doi: 10.1152/physiolgenomics.00035.2004
16. Merino VF, Todiras M, Mori MA, Sales VM, Fonseca RG, Saul V, Tenner K, Bader M, Pesquero JB, Predisposition to atherosclerosis and aortic aneurysms in mice deficient in kinin B1 receptor and apolipoprotein E. J Mol Med (Berl) 2009 87 953 963. doi: 10.1007/s00109-009-0501-0
17. Moran CS, McCann M, Karan M, Norman P, Ketheesan N, Golledge J, Association of osteoprotegerin with human abdominal aortic aneurysm progression. Circulation 2005 111 3119 3125. doi: 10.1161/CIRCULATIONAHA.104.464727
18. Golledge J, Muller J, Shephard N, Clancy P, Smallwood L, Moran C, Dear AE, Palmer LJ, Norman PE, Association between osteopontin and human abdominal aortic aneurysm. Arterioscler Thromb Vasc Biol 2007 27 655 660. doi: 10.1161/01.ATV.0000255560.49503.4e
19. Golledge J, Cullen B, Rush C, Moran CS, Secomb E, Wood F, Daugherty A, Campbell JH, Norman PE, Peroxisome proliferator-Activated receptor ligands reduce aortic dilatation in a mouse model of aortic aneurysm. Atherosclerosis 2010 210 51 56. doi: 10.1016/j.atherosclerosis.2009.10.027
20. Moran CS, Jose RJ, Biros E, Golledge J, Osteoprotegerin deficiency limits angiotensin II-induced aortic dilatation and rupture in the apolipoprotein E-knockout mouse. Arterioscler Thromb Vasc Biol 2014 34 2609 2616. doi: 10.1161/ATVBAHA.114.304587
21. Zaczynska E, Gabra BH, Sirois P, Bradykinin stimulates MMP-2 production in guinea pig tracheal smooth muscle cells. Inflammation 2003 27 307 315
22. Hsieh HL, Yen MH, Jou MJ, Yang CM, Intracellular signalings underlying bradykinin-induced matrix metalloproteinase-9 expression in rat brain astrocyte-1. Cell Signal 2004 16 1163 1176. doi: 10.1016/j.cellsig.2004.03.021
23. Ailawadi G, Moehle CW, Pei H, Walton SP, Yang Z, Kron IL, Lau CL, Owens GK, Smooth muscle phenotypic modulation is an early event in aortic aneurysms. J Thorac Cardiovasc Surg 2009 138 1392 1399. doi: 10.1016/j.jtcvs.2009.07.075
24. Mao N, Gu T, Shi E, Zhang G, Yu L, Wang C, Phenotypic switching of vascular smooth muscle cells in animal model of rat thoracic aortic aneurysm. Interact Cardiovasc Thorac Surg 2015 21 62 70. doi: 10.1093/icvts/ivv074
25. Lederle FA, The natural history of abdominal aortic aneurysm. Acta Chir Belg 2009 109 7 12
26. Saraff K, Babamusta F, Cassis LA, Daugherty A, Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2003 23 1621 1626. doi: 10.1161/01.ATV.0000085631.76095.64
27. Koike MK, de Carvalho Frimm C, de Lourdes Higuchi M, Bradykinin B2 receptor antagonism attenuates inflammation, mast cell infiltration and fibrosis in remote myocardium after infarction in rats. Clin Exp Pharmacol Physiol 2005 32 1131 1136. doi: 10.1111/j.1440-1681.2005.04309.x
28. Cassim B, Shaw OM, Mazur M, Misso NL, Naran A, Langlands DR, Thompson PJ, Bhoola KD, Kallikreins, kininogens and kinin receptors on circulating and synovial fluid neutrophils: role in kinin generation in rheumatoid arthritis. Rheumatology (Oxford) 2009 48 490 496. doi: 10.1093/rheumatology/kep016
29. Kozik A, Moore RB, Potempa J, Imamura T, Rapala-Kozik M, Travis J, A novel mechanism for bradykinin production at inflammatory sites. Diverse effects of a mixture of neutrophil elastase and mast cell tryptase versus tissue and plasma kallikreins on native and oxidized kininogens. J Biol Chem 1998 273 33224 33229
30. Eliason JL, Hannawa KK, Ailawadi G, Sinha I, Ford JW, Deogracias MP, Roelofs KJ, Woodrum DT, Ennis TL, Henke PK, Stanley JC, Thompson RW, Upchurch GR Jr, Neutrophil depletion inhibits experimental abdominal aortic aneurysm formation. Circulation 2005 112 232 240. doi: 10.1161/CIRCULATIONAHA.104.517391
31. Rzucidlo EM, Signaling pathways regulating vascular smooth muscle cell differentiation. Vascular 2009 17 suppl 1 S15 S20
32. Carrillo-Sepúlveda MA, Barreto-Chaves ML, Phenotypic modulation of cultured vascular smooth muscle cells: a functional analysis focusing on MLC and ERK1/2 phosphorylation. Mol Cell Biochem 2010 341 279 289. doi: 10.1007/s11010-010-0459-9
33. Appel S, Morgan KG, Scaffolding proteins and non-proliferative functions of ERK1/2. Commun Integr Biol 2010 3 354 356
34. Je HD, Gangopadhyay SS, Ashworth TD, Morgan KG, Calponin is required for agonist-induced signal transduction-evidence from an antisense approach in ferret smooth muscle. J Physiol 2001 537 pt 2 567 577
35. Tsakiridis T, Bergman A, Somwar R, Taha C, Aktories K, Cruz TF, Klip A, Downey GP, Actin filaments facilitate insulin activation of the src and collagen homologous/mitogen-Activated protein kinase pathway leading to DNA synthesis and c-fos expression. J Biol Chem 1998 273 28322 28331
36. Fernando AN, Fernando LP, Fukuda Y, Kaplan AP, Assembly, activation, and signaling by kinin-forming proteins on human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2005 289 H251 H257. doi: 10.1152/ajpheart.00206.2004
37. Dixon BS, Sharma RV, Dickerson T, Fortune J, Bradykinin and angiotensin II: activation of protein kinase C in arterial smooth muscle. Am J Physiol 1994 266 5 pt 1 C1406 C1420
38. AbdAlla S, Lother H, Quitterer U, AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature 2000 407 94 98. doi: 10.1038/35024095
39. Shen B, Harrison-Bernard LM, Fuller AJ, Vanderpool V, Saifudeen Z, El-Dahr SS, The Bradykinin B2 receptor gene is a target of angiotensin II type 1 receptor signaling. J Am Soc Nephrol 2007 18 1140 1149. doi: 10.1681/ASN.2006101127
40. Tan Y, Hutchison FN, Jaffa AA, Mechanisms of angiotensin II-induced expression of B2 kinin receptors. Am J Physiol Heart Circ Physiol 2004 286 H926 H932. doi: 10.1152/ajpheart.00757.2003
41. Kintsurashvili E, Duka I, Gavras I, Johns C, Farmakiotis D, Gavras H, Effects of ANG II on bradykinin receptor gene expression in cardiomyocytes and vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 2001 281 H1778 H1783
42. Baş M, Clinical efficacy of icatibant in the treatment of acute hereditary angioedema during the FAST-3 trial. Expert Rev Clin Immunol 2012 8 707 717. doi: 10.1586/eci.12.67
43. Song IH, Althoff CE, Hermann KG, Scheel AK, Knetsch T, Burmester GR, Backhaus M, Contrast-enhanced ultrasound in monitoring the efficacy of a bradykinin receptor 2 antagonist in painful knee osteoarthritis compared with MRI. Ann Rheum Dis 2009 68 75 83. doi: 10.1136/ard.2007.080382
44. Felipe SA, Rodrigues ES, Martin RP, Paiva AC, Pesquero JB, Shimuta SI, Functional expression of kinin B1 and B2 receptors in mouse abdominal aorta. Braz J Med Biol Res 2007 40 649 655
45. Stewart JM, Gera L, Hanson W, Zuzack JS, Burkard M, McCullough R, Whalley ET, A new generation of bradykinin antagonists. Immunopharmacology 1996 33 51 60