Anti-atherosclerotic effect of the angiotensin 1–7 mimetic AVE0991 is mediated by inhibition of perivascular and plaque inflammation in early atherosclerosis

British Journal of Pharmacology

Volumn 174, Issue 22, 2017, Pages 4055-4069

  Skiba, D S ^a,b   Nosalski, R ^a,b   Mikolajczyk, T P ^a,b   Siedlinski, M ^a   Rios, F J ^b   Montezano, A C ^b   Jawien, J ^a   Olszanecki, R ^a   Korbut, R ^a   Czesnikiewicz Guzik, M ^a   Touyz, R M ^b   Guzik, T J ^a,b  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; N ETHYLCARBAMOYL 3 [4 (5 FORMYL 4 METHOXY 2 PHENYL 1 IMIDAZOLYLMETHYL)PHENYL] 5 ISOBUTYL 2 THIOPHENESULFONAMIDE; TUMOR NECROSIS FACTOR; ANGIOTENSIN I; ANGIOTENSIN I (1-7); ANTIINFLAMMATORY AGENT; CYTOKINE; G PROTEIN COUPLED RECEPTOR; IMIDAZOLE DERIVATIVE; ONCOPROTEIN; PEPTIDE FRAGMENT; PROTO-ONCOGENE PROTEINS C-MAS-1;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL REACTIVITY; CELL ACTIVATION; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DESCENDING AORTA; FEMALE; IN VITRO STUDY; LYMPHOCYTIC INFILTRATION; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PERIVASCULAR ADIPOSE TISSUE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT DURATION; AGONISTS; ANIMAL; AORTA; APOLIPOPROTEIN E KNOCKOUT MOUSE; ATHEROSCLEROSIS; C57BL MOUSE; CELL LINE; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; LEUKOCYTE; PATHOLOGY; TUMOR CELL LINE;

ANGIOTENSIN I; ANIMALS; ANTI-INFLAMMATORY AGENTS; AORTA; ATHEROSCLEROSIS; CELL LINE; CELL LINE, TUMOR; CYTOKINES; FEMALE; HUMANS; IMIDAZOLES; LEUKOCYTES; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT, APOE; PEPTIDE FRAGMENTS; PLAQUE, ATHEROSCLEROTIC; PROTO-ONCOGENE PROTEINS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 85011575275     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13685     Document Type: Article

References (69)

1. Ait-Oufella H, Taleb S, Mallat Z, Tedgui A (2011). Recent advances on the role of cytokines in atherosclerosis. Arterioscler Thromb Vasc Biol 31: 969–979.
2. Alexander SP, Kelly E, Marrion N, Peters JA, Benson HE, Faccenda E et al. (2015a). The concise guide to PHARMACOLOGY 2015/16: Overview. Br J Pharmacol 172: 5729–5743.
3. Alexander SPH, Davenport AP, Kelly E, Marrion N, Peters JA, Benson HE et al. (2015b). The Concise Guide to PHARMACOLOGY 2015/16: G protein-coupled receptors. Br J Pharmacol 172: 5744–5869.
4. Antonopoulos AS, Margaritis M, Coutinho P, Shirodaria C, Psarros C, Herdman L et al. (2015). Adiponectin as a link between type 2 diabetes and vascular NADPH oxidase activity in the human arterial wall: the regulatory role of perivascular adipose tissue. Diabetes 64: 2207–2219.
5. Aubry MC, Riehle DL, Edwards WD, Maradit-Kremers H, Roger VL, Sebo TJ et al. (2004). B-Lymphocytes in plaque and adventitia of coronary arteries in two patients with rheumatoid arthritis and coronary atherosclerosis: preliminary observations. Cardiovasc Pathol 13: 233–236.
6. Back M, Hansson GK (2015). Anti-inflammatory therapies for atherosclerosis. Nat Rev Cardiol 12: 199–211.
7. Benter IF, Yousif MH, Dhaunsi GS, Kaur J, Chappell MC, Diz DI (2008). Angiotensin-(1-7) prevents activation of NADPH oxidase and renal vascular dysfunction in diabetic hypertensive rats. Am J Nephrol 28: 25–33.
8. Bonthu S, Heistad DD, Chappell DA, Lamping KG, Faraci FM (1997). Atherosclerosis, vascular remodeling, and impairment of endothelium- dependent relaxation in genetically altered hyperlipidemic mice. Arterioscler Thromb Vasc Biol 17: 2333–2340.
9. Bosnyak S, Jones ES, Christopoulos A, Aguilar MI, Thomas WG, Widdop RE (2011). Relative affinity of angiotensin peptides and novel ligands at AT1 and AT2 receptors. Clin Sci (Lond) 121: 297–303.
10. Caligiuri G, Nicoletti A, Zhou X, Tornberg I, Hansson GK (1999). Effects of sex and age on atherosclerosis and autoimmunity in apoE-deficient mice. Atherosclerosis 145: 301–308.
11. Capettini LS, Montecucco F, Mach F, Stergiopulos N, Santos RA, da Silva RF (2012). Role of renin-angiotensin system in inflammation, immunity and aging. Curr Pharm Des 18: 963–970.
12. Chalmers AD, Cohen A, Bursill CA, Myerscough MR (2015). Bifurcation and dynamics in a mathematical model of early atherosclerosis: How acute inflammation drives lesion development. J Math Biol 71: 1451–1480.
13. Chen YC, Bui AV, Diesch J, Manasseh R, Hausding C, Rivera J et al. (2013). A novel mouse model of atherosclerotic plaque instability for drug testing and mechanistic/therapeutic discoveries using gene and microRNA expression profiling. Circ Res 113: 252–265.
14. Clement M, Guedj K, Andreata F, Morvan M, Bey L, Khallou-Laschet J et al. (2015). Control of the T follicular helper-germinal center B-cell axis by CD8(+) regulatory T cells limits atherosclerosis and tertiary lymphoid organ development. Circulation 131: 560–570.
15. Curtis MJ, Bond RA, Spina D, Ahluwalia A, Alexander SPA, Giembycz MA et al. (2015). Experimental design and analysis and their reporting: new guidance for publication in BJP. Br J Pharmacol 172: 3461–3471.
16. da Silveira KD, Coelho FM, Vieira AT, Sachs D, Barroso LC, Costa VV et al. (2010). Anti-inflammatory effects of the activation of the angiotensin-(1-7) receptor, MAS, in experimental models of arthritis. J Immunol 185: 5569–5576.
17. Elhage R, Gourdy P, Brouchet L, Jawien J, Fouque M-J, Fiévet C et al. (2004). Deleting TCRαβ + or CD4+ T lymphocytes leads to opposite effects on site-specific atherosclerosis in female apolipoprotein E-deficient mice. Am J Pathol 165: 2013–2018.
18. Fraga-Silva RA, Costa-Fraga FP, Savergnini SQ, De Sousa FB, Montecucco F, da Silva D et al. (2013). An oral formulation of angiotensin-(1-7) reverses corpus cavernosum damages induced by hypercholesterolemia. J Sex Med 10: 2430–2442.
19. Fransen P, Van Assche T, Guns PJ, Van Hove CE, De Keulenaer GW, Herman AG et al. (2008). Endothelial function in aorta segments of apolipoprotein E-deficient mice before development of atherosclerotic lesions. Pflugers Arch 455: 811–818.
20. Galkina E, Kadl A, Sanders J, Varughese D, Sarembock IJ, Ley K (2006). Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially L-selectin dependent. J Exp Med 203: 1273–1282.
21. Galkina E, Ley K (2009). Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol 27: 165–197.
22. Guzik B, Sagan A, Ludew D, Mrowiecki W, Chwala M, Bujak-Gizycka B et al. (2013). Mechanisms of oxidative stress in human aortic aneurysms--association with clinical risk factors for atherosclerosis and disease severity. Int J Cardiol 168: 2389–2396.
23. Guzik TJ, Hoch NE, Brown KA, McCann LA, Rahman A, Dikalov S et al. (2007a). Role of the T cell in the genesis of angiotensin II induced hypertension and vascular dysfunction. J Exp Med 204: 2449–2460.
24. Guzik TJ, Marvar PJ, Czesnikiewicz-Guzik M, Korbut R (2007b). Perivascular adipose tissue as a messenger of the brain-vessel axis: role in vascular inflammation and dysfunction. J Physiol Pharmacol 58: 591–610.
25. Guzik TJ, Olszanecki R, Sadowski J, Kapelak B, Rudzinski P, Jopek A et al. (2005). Superoxide dismutase activity and expression in human venous and arterial bypass graft vessels. J Physiol Pharmacol 56: 313–323.
26. Guzik TJ, West NEJ, Black E, McDonald D, Ratnatunga C, Pillai R et al. (2000). Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ Res 86: e85–e90.
27. Hammer A, Yang G, Friedrich J, Kovacs A, Lee D-H, Grave K et al. (2016). Role of the receptor Mas in macrophage-mediated inflammation in vivo. Proc Natl Acad Sci 113: 14109–14114.
28. Heitzer T, Schlinzig T, Krohn K, Meinertz T, Munzel T (2001). Endothelial dysfunction, oxidative stress, and risk of cardiovascular events in patients with coronary artery disease. Circulation 104: 2673–2678.
29. Hoch NE, Guzik TJ, Chen W, Deans T, Maalouf SA, Gratze P et al. (2009). Regulation of T-cell function by endogenously produced angiotensin II. Am J Physiol Regul Integr Comp Physiol 296: R208–R216.
30. Hu D, Mohanta SK, Yin C, Peng L, Ma Z, Srikakulapu P et al. (2015). Artery tertiary lymphoid organs control aorta immunity and protect against atherosclerosis via vascular smooth muscle cell lymphotoxin beta receptors. Immunity 42: 1100–1115.
31. Jawien J, Nastalek P, Korbut R (2004). Mouse models of experimental atherosclerosis. J Physiol Pharmacol 55: 503–517.
32. Jawien J, Toton-Zuranska J, Gajda M, Niepsuj A, Gebska A, Kus K et al. (2012a). Angiotensin-(1-7) receptor Mas agonist ameliorates progress of atherosclerosis in apoE-knockout mice. J Physiol Pharmacol 63: 77–85.
33. Jawien J, Toton-Zuranska J, Kus K, Pawlowska M, Olszanecki R, Korbut R (2012b). The effect of AVE 0991, nebivolol and doxycycline on inflammatory mediators in an apoE-knockout mouse model of atherosclerosis. Med Sci Monit 18: BR389–BR393.
34. Ketelhuth DF, Hansson GK (2016). Adaptive response of T and B cells in atherosclerosis. Circ Res 118: 668–678.
35. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010). Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577–1579.
36. Kirabo A, Fontana V, de Faria AP, Loperena R, Galindo CL, Wu J et al. (2014). DC isoketal-modified proteins activate T cells and promote hypertension. J Clin Invest 124: 4642–4656.
37. Klein S, Herath CB, Schierwagen R, Grace J, Haltenhof T, Uschner FE et al. (2015). Hemodynamic effects of the non-peptidic angiotensin-(1-7) agonist AVE0991 in liver cirrhosis. PLoS One 10: e0138732.
38. Laursen JB, Somers M, Kurz S, McCann L, Warnholtz A, Freeman BA et al. (2001). Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 103: 1282–1288.
39. Lee S, Evans MA, Chu HX, Kim HA, Widdop RE, Drummond GR et al. (2015). Effect of a selective Mas Receptor agonist in cerebral ischemia in vitro and in vivo. PLoS One 10: e0142087.
40. Libby P, Ridker PM, Hansson GK (2011). Progress and challenges in translating the biology of atherosclerosis. Nature 473: 317–325.
41. Ma Y, Huang H, Jiang J, Wu L, Lin C, Tang A et al. (2016). AVE 0991 attenuates cardiac hypertrophy through reducing oxidative stress. Biochem Biophys Res Commun 474: 621–625.
42. Macritchie N, Grassia G, Sabir SR, Maddaluno M, Welsh P, Sattar N et al. (2012). Plasmacytoid dendritic cells play a key role in promoting atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 32: 2569–2579.
43. Magalhaes GS, Rodrigues-Machado MG, Motta-Santos D, Silva AR, Caliari MV, Prata LO et al. (2015). Angiotensin-(1-7) attenuates airway remodelling and hyperresponsiveness in a model of chronic allergic lung inflammation. Br J Pharmacol 172: 2330–2342.
44. Matusik P, Guzik B, Weber C, Guzik TJ (2012). Do we know enough about the immune pathogenesis of acute coronary syndromes to improve clinical practice? Thromb Haemost 108: 443–456.
45. McGrath JC, Lilley E (2015). Implementing guidelines on reporting research using animals (ARRIVE etc.): new requirements for publication in BJP. Br J Pharmacol 172: 3189–3193.
46. Mikolajczyk TP, Nosalski R, Szczepaniak P, Budzyn K, Osmenda G, Skiba D et al. (2016). Role of chemokine RANTES in the regulation of perivascular inflammation, T-cell accumulation, and vascular dysfunction in hypertension. FASEB J 30: 1987–1999.
47. Oliveira-Lima OC, Pinto MC, Duchene J, Qadri F, Souza LL, Alenina N et al. (2015). Mas receptor deficiency exacerbates lipopolysaccharide-induced cerebral and systemic inflammation in mice. Immunobiology 220: 1311–1321.
48. Passos-Silva DG, Verano-Braga T, Santos RA (2013). Angiotensin-(1-7): beyond the cardio-renal actions. Clin Sci 124: 443–456.
49. Pawlik MW, Kwiecien S, Ptak-Belowska A, Pajdo R, Olszanecki R, Suski M et al. (2016). The renin-angiotensin system and its vasoactive metabolite angiotensin-(1-7) in the mechanism of the healing of preexisting gastric ulcers. The involvement of Mas receptors, nitric oxide, prostaglandins and proinflammatory cytokines. J Physiol Pharmacol 67: 75–91.
50. Podolec J, Kopec G, Niewiara L, Komar M, Guzik B, Bartus K et al. (2016). Chemokine RANTES is increased at early stages of coronary artery disease. J Physiol Pharmacol 67: 321–328.
51. Raffai G, Durand MJ, Lombard JH (2011). Acute and chronic angiotensin-(1-7) restores vasodilation and reduces oxidative stress in mesenteric arteries of salt-fed rats. Am J Physiol Heart Circ Physiol 301: H1341–H1352.
52. Ren Y, Garvin JL, Carretero OA (2002). Vasodilator action of angiotensin-(1-7) on isolated rabbit afferent arterioles. Hypertension 39: 799–802.
53. Ridker PM, Luscher TF (2014). Anti-inflammatory therapies for cardiovascular disease. Eur Heart J 35: 1782–1791.
54. Rodrigues-Machado MG, Magalhaes GS, Cardoso JA, Kangussu LM, Murari A, Caliari MV et al. (2013). AVE 0991, a non-peptide mimic of angiotensin-(1-7) effects, attenuates pulmonary remodelling in a model of chronic asthma. Br J Pharmacol 170: 835–846.
55. Rubio-Ruiz ME, Del Valle-Mondragon L, Castrejon-Tellez V, Carreon-Torres E, Diaz-Diaz E, Guarner-Lans V (2014). Angiotensin II and 1-7 during aging in Metabolic Syndrome rats. Expression of AT1, AT2 and Mas receptors in abdominal white adipose tissue. Peptides 57: 101–108.
56. Sagan A, Mrowiecki W, Mikolajczyk TP, Urbanski K, Siedlinski M, Nosalski R et al. (2012). Local inflammation is associated with aortic thrombus formation in abdominal aortic aneurysms. Relationship to clinical risk factors. Thromb Haemost 108: 812–823.
57. Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL, Touyz RM (2006). Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension 49: 185–192.
58. Santos RAS, Simoes e Silva AC, Maric C, Silva DMR, Machado RP, de Buhr I et al. (2003). Angiotensin-(1–7) is an endogenous ligand for the G protein-coupled receptor Mas. Proc Natl Acad Sci 100: 8258–8263.
59. Silveira KD, Barroso LC, Vieira AT, Cisalpino D, Lima CX, Bader M et al. (2013). Beneficial effects of the activation of the angiotensin-(1-7) MAS receptor in a murine model of adriamycin-induced nephropathy. PLoS One 8: e66082.
60. Simoes e Silva AC, Silveira KD, Ferreira AJ, Teixeira MM (2013). ACE2, angiotensin-(1-7) and Mas receptor axis in inflammation and fibrosis. Br J Pharmacol 169: 477–492.
61. Southan C, Sharman JL, Benson HE, Faccenda E, Pawson AJ, Alexander SPH et al. (2016). The IUPHAR/BPS guide to PHARMACOLOGY in 2016: towards curated quantitative interactions between 1300 protein targets and 6000 ligands. Nucl Acids Res 44 (Database Issue): D1054–D1068.
62. Srikakulapu P, Hu D, Yin C, Mohanta SK, Bontha SV, Peng L et al. (2016). Artery tertiary lymphoid organs control multilayered territorialized atherosclerosis B-cell responses in aged ApoE−/− mice. Arterioscler Thromb Vasc Biol 36: 1174–1185.
63. Suski M, Olszanecki R, Stachowicz A, Madej J, Bujak-Gizycka B, Okon K et al. (2013). The influence of angiotensin-(1-7) Mas receptor agonist (AVE 0991) on mitochondrial proteome in kidneys of apoE knockout mice. Biochim Biophys Acta 1834: 2463–2469.
64. Tesanovic S, Vinh A, Gaspari TA, Casley D, Widdop RE (2010). Vasoprotective and atheroprotective effects of angiotensin (1-7) in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 30: 1606–1613.
65. Vinh A, Chen W, Blinder Y, Weiss D, Taylor WR, Goronzy JJ et al. (2010). Inhibition and genetic ablation of the B7/CD28 T-cell costimulation axis prevents experimental hypertension. Circulation 122: 2529–2537.
66. Vu DM, Tai A, Tatro JB, Karas RH, Huber BT, Beasley D (2014). gammadeltaT cells are prevalent in the proximal aorta and drive nascent atherosclerotic lesion progression and neutrophilia in hypercholesterolemic mice. PLoS One 9: e109416.
67. Weber C, Noels H (2011). Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 17: 1410–1422.
68. Woodward L, Akoumianakis I, Antoniades C (2016). Unravelling the adiponectin paradox: novel roles of adiponectin in the regulation of cardiovascular disease. Br J Pharmacol. doi: 10.1111/bph.13619.
69. Zimmerman MA, Baban B, Tipton AJ, O'Connor PM, Sullivan JC (2015). Chronic ANG II infusion induces sex-specific increases in renal T cells in Sprague–Dawley rats. Am J Physiol Renal Physiol 308: F706–F712.