Aliskiren limits abdominal aortic aneurysm, ventricular hypertrophy and atherosclerosis in an apolipoprotein-E-deficient mouse model

Clinical Science

Volumn 127, Issue 2, 2014, Pages 123-134

  Seto, Sai Wang ^a   Krishna, Smriti M ^a   Moran, Corey S ^a   Liu, David ^a   Golledge, Jonathan ^a,b  

^a JAMES COOK UNIVERSITY   (Australia)

^b TOWNSVILLE HOSPITAL   (Australia)

Author keywords

Abdominal aortic aneurysm; Angiotensin II; Atherosclerosis; Pro renin receptor; Ventricular hypertrophy

Indexed keywords

ALISKIREN; ANGIOTENSIN II; APOLIPOPROTEIN E; MITOGEN ACTIVATED PROTEIN KINASE; PRORENIN RECEPTOR; AMIDE; FUMARIC ACID DERIVATIVE;

ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; AORTA ARCH; ARTICLE; ATHEROSCLEROSIS; BLOOD PRESSURE; BODY WEIGHT; CONTROLLED STUDY; DISEASE COURSE; DRUG MEGADOSE; ECHOGRAPHY; ENZYME ACTIVITY; HEART MUSCLE CELL; HEART RATE; HEART VENTRICLE HYPERTROPHY; HEART WEIGHT; LOW DRUG DOSE; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TREATMENT DURATION; UPREGULATION; ABDOMINAL AORTA; ANIMAL; AORTIC ANEURYSM, ABDOMINAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; HYPERTENSION; HYPERTROPHY; KNOCKOUT MOUSE; METABOLISM;

AMIDES; ANGIOTENSIN II; ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; FUMARATES; HYPERTENSION; HYPERTROPHY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84897560702     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20130382     Document Type: Article

References (61)

1. Daugherty A., Rateri D. L., Lu H., Inagami T. and Cassis L. A. (2004) Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the AT1A receptor. Circulation 110, 3849-3857.
2. He M., Zhang L., Shao Y., Xue H., Zhou L., Wang X. F., Yu C., Yao T. and Lu L. M. (2010) Angiotensin II type 2 receptor mediated angiotensin II and high glucose induced decrease in renal prorenin/renin receptor expression. Mol. Cell. Endocrinol. 315, 188-194.
3. Singh V. P., Le B., Khode R., Baker K. M. and Kumar R. (2008) Intracellular angiotensin II production in diabetic rats is correlated with cardiomyocyte apoptosis, oxidative stress, and cardiac fibrosis. Diabetes 57, 3297-3306.
4. Wassmann S., Czech T., Van Eickels M., Fleming I., Bohm M. and Nickenig G. (2004) Inhibition of diet-induced atherosclerosis and endothelial dysfunction in apolipoprotein E/angiotensin II type 1A receptor double-knockout mice. Circulation 110, 3062-3067.
5. Golledge J. and Norman P. E. (2011) Current status of medical management for abdominal aortic aneurysm. Atherosclerosis 217, 57-63.
6. Sanoski C. A. (2009) Aliskiren: an oral direct renin inhibitor for the treatment of hypertension. Pharmacotherapy 29, 193-212.
7. Kumar R., Singh V. P. and Baker K. M. (2007) The intracellular renin-angiotensin system: a new paradigm. Trends Endocrinol. Metab. 18, 208-214.
8. Kumar R., Singh V. P. and Baker K. M. (2008) The intracellular renin-angiotensin system: implications in cardiovascular remodeling. Curr. Opin. Nephrol. Hypertens. 17, 168-173.
9. Lu H., Rateri D. L., Feldman, Jr D.L., R. J., Fukamizu A., Ishida J., Oesterling E. G., Cassis L. A. and Daugherty A. (2008) Renin inhibition reduces hypercholesterolemia-induced atherosclerosis in mice. J. Clin. Invest. 118, 984-993.
10. Poss J., Werner C., Lorenz D., Gensch C., Bohm M. and Laufs U. (2010) The renin inhibitor aliskiren upregulates pro-angiogenic cells and reduces atherogenesis in mice. Basic Res. Cardiol. 105, 725-735.
11. Deng G. G., Martin-Mcnulty B., Sukovich D. A., Freay A., Halks-Miller M., Thinnes T., Loskutoff D. J., Carmeliet P., Dole W. P. and Wang Y. X. (2003) Urokinase-type plasminogen activator plays a critical role in angiotensin II-induced abdominal aortic aneurysm. Circ. Res. 92, 510-517.
12. Ehrlichman L. K., Ford J. W., Roelofs K. J., Tedeschi-Filho W., Futchko J. S., Ramacciotti E., Eliason J. L., Henke P. K. and Upchurch, Jr G. R. (2010) Gender-dependent differential phosphorylation in the ERK signaling pathway is associated with increased MMP2 activity in rat aortic smooth muscle cells. J. Surg. Res. 160, 18-24.
13. Ghosh A., Dimusto P. D., Ehrlichman L. K., Sadiq O., Mcevoy B., Futchko J. S., Henke P. K., Eliason J. L. and Upchurch, Jr G. R. (2012) The role of extracellular signal-related kinase during abdominal aortic aneurysm formation. J. Am. Coll. Surg. 215, 668-680.
14. Habashi J. P., Doyle J. J., Holm T. M., Aziz H., Schoenhoff F., Bedja D., Chen Y., Modiri A. N., Judge D. P. and Dietz H. C. (2011) Angiotensin II type 2 receptor signaling attenuates aortic aneurysm in mice through ERK antagonism. Science 332, 361-365.
15. Kolch W. (2005) Coordinating ERK/MAPK signalling through scaffolds and inhibitors. Nat. Rev. Mol. Cell. Biol. 6, 827-837.
16. Li T., Sun M., Yin X., Wu C., Wu Q., Feng S., Li H., Luan Y., Wen J., Yan L. et al. (2013) Expression of the calcium sensing receptor in human peripheral blood T lymphocyte and its contribution to cytokine secretion through MAPKs or NF-κB pathways. Mol. Immunol. 53, 414-420.
17. Sodhi A. and Sethi G. (2003) Involvement of MAP kinase signal transduction pathway in UVB-induced activation of macrophages in vitro. Immunol. Lett. 90, 123-130.
18. Angeli F., Reboldi G., Mazzotta G., Poltronieri C. and Verdecchia P. (2012) Safety and efficacy of aliskiren in the treatment of hypertension: a systematic overview. Expert Opin. Drug Saf. 11, 659-670.
19. Nussberger J., Aubert J. F., Bouzourene K., Pellegrin M., Hayoz D. and Mazzolai L. (2008) Renin inhibition by aliskiren prevents atherosclerosis progression: comparison with irbesartan, atenolol, and amlodipine. Hypertension 51, 1306-1311.
20. Krishna S. M., Seto S. W., Moxon J. V., Rush C., Walker P. J., Norman P. E. and Golledge J. (2012) Fenofibrate increases high-density lipoprotein and sphingosine 1 phosphate concentrations limiting abdominal aortic aneurysm progression in a mouse model. Am. J. Pathol. 181, 706-718.
21. Golledge J., Cullen B., Rush C., Moran C. S., Secomb E., Wood F., Daugherty A., Campbell J. H. and Norman P. E. (2010) Peroxisome proliferator-activated receptor ligands reduce aortic dilatation in a mouse model of aortic aneurysm. Atherosclerosis 210, 51-56.
22. Shibata K., Yatera Y., Furuno Y., Sabanai K., Morisada N., Nakata S., Morishita T., Yamazaki F., Tanimoto A., Sasaguri Y. et al. (2010) Spontaneous development of left ventricular hypertrophy and diastolic dysfunction in mice lacking all nitric oxide synthases. Circ. J. 74, 2681-2692.
23. Jagadeesh G., Balakumar P. and Stockbridge N. (2012) How well do aliskiren's purported mechanisms track its effects on cardiovascular and renal disorders? Cell. Signal. 24, 1583-1591.
24. Reudelhuber T. L. (2012) The interaction between prorenin, renin and the (pro)renin receptor: time to rethink the role in hypertension. Curr. Opin. Nephrol. Hypertens. 21, 137-141.
25. Batenburg W. W., Lu X., Leijten F., Maschke U., Muller D. N. and Danser A. H. (2011) Renin- and prorenin-induced effects in rat vascular smooth muscle cells overexpressing the human (pro)renin receptor: does (pro)renin-(pro)renin receptor interaction actually occur? Hypertension 58, 1111-1119.
26. Krop M., Lu X., Danser A. H. and Meima M. E. (2013) The (pro)renin receptor. A decade of research: what have we learned? Pflugers. Arch. 465, 87-97.
27. Moilanen A. M., Rysa J., Serpi R., Mustonen E., Szabo Z., Aro J., Napankangas J., Tenhunen O., Sutinen M., Salo T. and Ruskoaho H. (2012) (Pro)renin receptor triggers distinct angiotensin II-independent extracellular matrix remodeling and deterioration of cardiac function. PLoS ONE 7, e41404.
28. Peng H., Li W., Seth D. M., Nair A. R., Francis J. and Feng Y. (2013) (Pro)renin receptor mediates both angiotensin II-dependent and -independent oxidative stress in neuronal cells. PLoS ONE 8, e58339.
29. Ichihara A., Kaneshiro Y., Takemitsu T., Sakoda M., Suzuki F., Nakagawa T., Nishiyama A., Inagami T. and Hayashi M. (2006) Nonproteolytic activation of prorenin contributes to development of cardiac fibrosis in genetic hypertension. Hypertension 47, 894-900.
30. Kaneshiro Y., Ichihara A., Sakoda M., Takemitsu T., Nabi A. H., Uddin M. N., Nakagawa T., Nishiyama A., Suzuki F., Inagami T. and Itoh H. (2007) Slowly progressive, angiotensin II-independent glomerulosclerosis in human (pro)renin receptor-transgenic rats. J. Am. Soc. Nephrol. 18, 1789-1795.
31. Ichihara A., Suzuki F., Nakagawa T., Kaneshiro Y., Takemitsu T., Sakoda M., Nabi A. H., Nishiyama A., Sugaya T., Hayashi M. and Inagami T. (2006) Prorenin receptor blockade inhibits development of glomerulosclerosis in diabetic angiotensin II type 1a receptor-deficient mice. J. Am. Soc. Nephrol. 17, 1950-1961.
32. Imanishi T., Tsujioka H., Ikejima H., Kuroi A., Takarada S., Kitabata H., Tanimoto T., Muragaki Y., Mochizuki S., Goto M. et al. (2008) Renin inhibitor aliskiren improves impaired nitric oxide bioavailability and protects against atherosclerotic changes. Hypertension 52, 563-572.
33. Ino J., Kojima C., Osaka M., Nitta K. and Yoshida M. (2009) Dynamic observation of mechanically-injured mouse femoral artery reveals an antiinflammatory effect of renin inhibitor. Arterioscler. Thromb. Vasc. Biol. 29, 1858-1863.
34. Whaley-Connell A., Habibi J., Cooper S. A., Demarco V. G., Hayden M. R., Stump C. S., Link D., Ferrario C. M. and Sowers J. R. (2008) Effect of renin inhibition and AT1R blockade on myocardial remodeling in the transgenic Ren2 rat. Am. J. Physiol. Endocrinol. Metab. 295, E103-E109.
35. Cassis L. A., Gupte M., Thayer S., Zhang X., Charnigo R., Howatt D. A., Rateri D. L. and Daugherty A. (2009) ANG II infusion promotes abdominal aortic aneurysms independent of increased blood pressure in hypercholesterolemic mice. Am. J. Physiol. Heart. Circ. Physiol. 296, H1660-H1665.
36. Weiss D., Kools J. J. and Taylor W. R. (2001) Angiotensin II-induced hypertension accelerates the development of atherosclerosis in apoE-deficient mice. Circulation 103, 448-454.
37. Lu H., Balakrishnan A., Howatt D. A., Wu C., Charnigo R., Liau G., Cassis L. A. and Daugherty A. (2012) Comparative effects of different modes of renin angiotensin system inhibition on hypercholesterolaemia-induced atherosclerosis. Br. J. Pharmacol. 165, 2000-2008.
38. Meir K. S. and Leitersdorf E. (2004) Atherosclerosis in the apolipoprotein-E-deficient mouse: a decade of progress. Arterioscler. Thromb. Vasc. Biol. 24, 1006-1014.
39. Reddick R. L., Zhang S. H. and Maeda N. (1994) Atherosclerosis in mice lacking apo E. Evaluation of lesional development and progression. Arterioscler. Thromb. 14, 141-147.
40. Sakoda M., Ichihara A., Kaneshiro Y., Takemitsu T., Nakazato Y., Nabi A. H., Nakagawa T., Suzuki F., Inagami T. and Itoh H. (2007) (Pro)renin receptor-mediated activation of mitogen-activated protein kinases in human vascular smooth muscle cells. Hypertens. Res. 30, 1139-1146.
41. Ferri N., Greco C. M., Maiocchi G. and Corsini A. (2011) Aliskiren reduces prorenin receptor expression and activity in cultured human aortic smooth muscle cells. J. Renin Angiotensin Aldosterone Syst. 12, 469-474.
42. Zheng Y. H., Tian C., Meng Y., Qin Y. W., Du Y. H., Du J. and Li H. H. (2012) Osteopontin stimulates autophagy via integrin/CD44 and p38 MAPK signaling pathways in vascular smooth muscle cells. J. Cell. Physiol. 227, 127-135.
43. Zampetaki A., Mitsialis S. A., Pfeilschifter J. and Kourembanas S. (2004) Hypoxia induces macrophage inflammatory protein-2 (MIP-2) gene expression in murine macrophages via NF-κB: the prominent role of p42/ p44 and PI3 kinase pathways. FASEB J 18, 1090-1092.
44. Izumiya Y., Araki S., Usuku H., Rokutanda T., Hanatani S. and Ogawa H. (2012) Chronic C-type natriuretic peptide infusion attenuates angiotensin II-induced myocardial superoxide production and cardiac remodeling. Int. J. Vasc. Med. 2012, 246058.
45. Li H. L., She Z. G., Li T. B., Wang A. B., Yang Q., Wei Y. S., Wang Y. G. and Liu D. P. (2007) Overexpression of myofibrillogenesis regulator-1 aggravates cardiac hypertrophy induced by angiotensin II in mice. Hypertension 49, 1399-1408.
46. Dong Y. F., Liu L., Kataoka K., Nakamura T., Fukuda M., Tokutomi Y., Nako H., Ogawa H. and Kim-Mitsuyama S. (2010) Aliskiren prevents cardiovascular complications and pancreatic injury in a mouse model of obesity and type 2 diabetes. Diabetologia 53, 180-191.
47. Pilz B., Shagdarsuren E., Wellner M., Fiebeler A., Dechend R., Gratze P., Meiners S., Feldman D. L., Webb R. L., Garrelds I. M. et al. (2005) Aliskiren, a human renin inhibitor, ameliorates cardiac and renal damage in double-transgenic rats. Hypertension 46, 569-576.
48. Rashikh A., Ahmad S. J., Pillai K. K., Kohli K. and Najmi A. K. (2012) Aliskiren attenuates myocardial apoptosis and oxidative stress in chronic murine model of cardiomyopathy. Biomed. Pharmacother. 66, 138-143.
49. Connelly K. A., Advani A., Kim S., Advani S. L., Zhang M., White K. E., Kim Y. M., Parker C., Thai K., Krum H. et al. (2011) The cardiac (pro)renin receptor is primarily expressed in myocyte transverse tubules and is increased in experimental diabetic cardiomyopathy. J. Hypertens. 29, 1175-1184.
50. Mendez M. and Lapointe M. C. (2005) PGE2-induced hypertrophy of cardiac myocytes involves EP4 receptor-dependent activation of p42/44 MAPK and EGFR transactivation. Am. J. Physiol. Heart. Circ. Physiol. 288, H2111-H2117.
51. Qian J. Y., Leung A., Harding P. and Lapointe M. C. (2006) PGE2 stimulates human brain natriuretic peptide expression via EP4 and p42/44 MAPK. Am. J. Physiol. Heart. Circ. Physiol. 290, H1740-H1746.
52. Van Deel E. D., Lu Z., Xu X., Zhu G., Hu X., Oury T. D., Bache R. J., Duncker D. J. and Chen Y. (2008) Extracellular superoxide dismutase protects the heart against oxidative stress and hypertrophy after myocardial infarction. Free Radic. Biol. Med. 44, 1305-1313.
53. Nguyen G., Delarue F., Burckle C., Bouzhir L., Giller T. and Sraer J. D. (2002) Pivotal role of the renin/prorenin receptor in angiotensin II production and cellular responses to renin. J. Clin. Invest. 109, 1417-1427.
54. Westermann D., Riad A., Lettau O., Roks A., Savvatis K., Becher P. M., Escher F., Jan Danser A. H., Schultheiss H. P. and Tschope C. (2008) Renin inhibition improves cardiac function and remodeling after myocardial infarction independent of blood pressure. Hypertension 52, 1068-1075.
55. Rateri D. L., Howatt D. A., Moorleghen J. J., Charnigo R., Cassis L. A. and Daugherty A. (2011) Prolonged infusion of angiotensin II in apoE-/- mice promotes macrophage recruitment with continued expansion of abdominal aortic aneurysm. Am. J. Pathol. 179, 1542-1548.
56. Inoue N., Muramatsu M., Jin D., Takai S., Hayashi T., Katayama H., Kitaura Y., Tamai H. and Miyazaki M. (2009) Involvement of vascular angiotensin II-forming enzymes in the progression of aortic abdominal aneurysms in angiotensin IIinfused ApoE-deficient mice. J. Atheroscler. Thromb. 16, 164-171.
57. Zhou Y., Chen R., Catanzaro S. E., Hu L., Dansky H. M. and Catanzaro D. F. (2005) Differential effects of angiotensin II on atherogenesis at the aortic sinus and descending aorta of apolipoprotein-E-deficient mice. Am. J. Hypertens. 18, 486-492.
58. Ayabe N., Babaev V. R., Tang Y. W., Tanizawa T., Fogo A. B., Linton M. F., Ichikawaa I., Fazio S. and Kon V. (2006) Transiently heightened angiotensin II has distinct effects on atherosclerosis and aneurysm formation in hyperlipidemic mice. Atherosclerosis 184, 312-321.
59. Trollope A., Moxon J. V., Moran C. S. and Golledge J. (2011) Animal models of abdominal aortic aneurysm and their role in furthering management of human disease. Cardiovasc. Pathol. 20, 114-123.
60. Saraff K., Babamusta F., Cassis L. A. and Daugherty A. (2003) Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 23, 1621-1626.
61. Weinberg P. D. and Ethier C. R. (2007) Twenty-fold difference in hemodynamic wall shear stress between murine and human aortas. J. Biomech. 40, 1594-1598.