Role of bone marrow renin-angiotensin system in the pathogenesis of atherosclerosis

Pharmacology and Therapeutics

Volumn 118, Issue 2, 2008, Pages 268-276

  Fukuda, Daiju ^a   Sata, Masataka ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Angiotensin II; Angiotensin II type I receptor; Atherosclerosis; Bone marrow; Inflammation; Vessel wall

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN RECEPTOR ANTAGONIST; CELL ADHESION MOLECULE; CHEMOKINE; CYTOKINE; DIPEPTIDYL CARBOXYPEPTIDASE; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW; BONE MARROW TRANSPLANTATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; DISEASE COURSE; DRUG EFFECT; ENDOTHELIUM CELL; GENE EXPRESSION; HEMATOPOIESIS; INFLAMMATORY CELL; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SMOOTH MUSCLE FIBER; STEM CELL; UPREGULATION; VASCULARIZATION;

ANGIOTENSIN II; ANIMALS; ATHEROSCLEROSIS; BONE MARROW; HUMANS; INFLAMMATION; MICE; MICE, KNOCKOUT; RECEPTOR, ANGIOTENSIN, TYPE 1; RENIN-ANGIOTENSIN SYSTEM;

EID: 43049168749     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2008.02.007     Document Type: Review

References (143)

1. Abali H., Haznedaroglu I.C., Goker H., Celik I., Ozatli D., Koray Z., et al. Circulating and local bone marrow renin-angiotensin system in leukemic hematopoiesis: Preliminary evidences. Hematology 7 2 (2002) 75-82
2. Arakawa K., and Urata H. Hypothesis regarding the pathophysiological role of alternative pathways of angiotensin II formation in atherosclerosis. Hypertension 36 4 (2000) 638-641
3. Asahara T., Masuda H., Takahashi T., Kalka C., Pastore C., Silver M., et al. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res 85 3 (1999) 221-228
4. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 5302 (1997) 964-967
5. Bahlmann F.H., de Groot K., Mueller O., Hertel B., Haller H., and Fliser D. Stimulation of endothelial progenitor cells: A new putative therapeutic effect of angiotensin II receptor antagonists. Hypertension 45 4 (2005) 526-529
6. Barnett A.H., Bain S.C., Bouter P., Karlberg B., Madsbad S., Jervell J., et al. Angiotensin-receptor blockade versus converting-enzyme inhibition in type 2 diabetes and nephropathy. N Engl J Med 351 19 (2004) 1952-1961
7. Barnett A.H., Bain S.C., Bouter P., Karlberg B., Madsbad S., Jervell J., et al. Angiotensin-receptor blockade versus converting-enzyme inhibition in type 2 diabetes and nephropathy. N Engl J Med 351 19 (2004) 1952-1961
8. Barry-Lane P.A., Patterson C., van der Merwe M., Hu Z., Holland S.M., Yeh E.T., et al. P47phox is required for atherosclerotic lesion progression in apoe(-/-) mice. J Clin Invest 108 10 (2001) 1513-1522
9. Batenburg W.W., Tom B., Schuijt M.P., and Danser A.H. Angiotensin ii type 2 receptor-mediated vasodilation. Focus on bradykinin, no and endothelium-derived hyperpolarizing factor(s). Vascul Pharmacol 42 3 (2005) 109-118
10. Bauters C., and Isner J.M. The biology of restenosis. Prog Cardiovasc Dis 40 2 (1997) 107-116
11. Brasier A.R., Jamaluddin M., Han Y., Patterson C., and Runge M.S. Angiotensin ii induces gene transcription through cell-type-dependent effects on the nuclear factor-kappaB (nf-kappaB) transcription factor. Mol Cell Biochem 212 1-2 (2000) 155-169
12. Brasier A.R., Recinos III A., and Eledrisi M.S. Vascular inflammation and the renin-angiotensin system. Arterioscler Thromb Vasc Biol 22 8 (2002) 1257-1266
13. Campbell D.J., and Habener J.F. Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat. J Clin Invest 78 1 (1986) 31-39
14. Carmeliet P., Moons L., Stassen J.M., De Mol M., Bouche A., van den Oord J.J., et al. Vascular wound healing and neointima formation induced by perivascular electric injury in mice. Am J Pathol 150 2 (1997) 761-776
15. Cassis L.A., Rateri D.L., Lu H., and Daugherty A. Bone marrow transplantation reveals that recipient at1a receptors are required to initiate angiotensin ii-induced atherosclerosis and aneurysms. Arterioscler Thromb Vasc Biol 27 2 (2007) 380-386
16. Cathcart M.K. Regulation of superoxide anion production by NADPH oxidase in monocytes/macrophages: Contributions to atherosclerosis. Arterioscler Thromb Vasc Biol 24 1 (2004) 23-28
17. Chapman N., Huxley R., Anderson C., Bousser M.G., Chalmers J., Colman S., et al. Effects of a perindopril-based blood pressure-lowering regimen on the risk of recurrent stroke according to stroke subtype and medical history: The progress trial. Stroke 35 1 (2004) 116-121
18. Chen J., Li D., Schaefer R.F., and Mehta J.L. Inhibitory effect of candesartan and rosuvastatin on cd40 and mmps expression in apo-e knockout mice: Novel insights into the role of ras and dyslipidemia in atherogenesis. J Cardiovasc Pharmacol 44 4 (2004) 446-452
19. Cheng C., Tempel D., van Haperen R., van der Baan A., Grosveld F., Daemen M.J., et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113 23 (2006) 2744-2753
20. Cheng H.F., Becker B.N., Burns K.D., and Harris R.C. Angiotensin II upregulates type-1 angiotensin ii receptors in renal proximal tubule. J Clin Invest 95 5 (1995) 2012-2019
21. Chisi J.E., Wdzieczak-Bakala J., and Riches A.C. Inhibitory action of the peptide acsdkp on the proliferative state of hematopoietic stem cells in the presence of captopril but not lisinopril. Stem Cells 15 6 (1997) 455-460
22. Cohn J.N., and Tognoni G. A randomized trial of the angiotensin-receptor blocker valsartan in chronic heart failure. N Engl J Med 345 23 (2001) 1667-1675
23. Comte L., Lorgeot V., Volkov L., Allegraud A., Aldigier J.C., and Praloran V. Effects of the angiotensin-converting enzyme inhibitor enalapril on blood haematopoietic progenitors and acetyl-n-ser-asp-lys-pro concentrations. Eur J Clin Invest 27 9 (1997) 788-790
24. Conlon P.J., Smith S.R., Butterly D.W., and Brennan D.C. Losartan in post-transplant erythrocytosis. Nephrol Dial Transplant 11 12 (1996) 2524-2525
25. Crosby J.R., Kaminski W.E., Schatteman G., Martin P.J., Raines E.W., Seifert R.A., et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res 87 9 (2000) 728-730
26. Daugherty A., Manning M.W., and Cassis L.A. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein e-deficient mice. J Clin Invest 105 11 (2000) 1605-1612
27. Daugherty A., Rateri D.L., Lu H., Inagami T., and Cassis L.A. Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the at1a receptor. Circulation 110 25 (2004) 3849-3857
28. Dean N.M., and Boynton A.L. Angiotensin II causes phosphatidylinositol turnover and increases 1,2-diacylglycerol mass but is not mitogenic in rat liver t51b cells. Biochem J 269 2 (1990) 347-352
29. Diet F., Pratt R.E., Berry G.J., Momose N., Gibbons G.H., and Dzau V.J. Increased accumulation of tissue ace in human atherosclerotic coronary artery disease. Circulation 94 11 (1996) 2756-2767
30. Dzau V.J. Theodore cooper lecture: Tissue angiotensin and pathobiology of vascular disease: A unifying hypothesis. Hypertension 37 4 (2001) 1047-1052
31. Dzau V.J., and Re R. Tissue angiotensin system in cardiovascular medicine. A paradigm shift?. Circulation 89 1 (1994) 493-498
32. Ezoe S., Matsumura I., Satoh Y., Tanaka H., and Kanakura Y. Cell cycle regulation in hematopoietic stem/progenitor cells. Cell Cycle 3 3 (2004) 314-318
33. Falkenhahn M., Franke F., Bohle R.M., Zhu Y.C., Stauss H.M., Bachmann S., et al. Cellular distribution of angiotensin-converting enzyme after myocardial infarction. Hypertension 25 2 (1995) 219-226
34. Fernandez-Alfonso M.S., Martorana P.A., Licka I., van Even P., Trobisch D., Scholkens B.A., et al. Early induction of angiotensin I-converting enzyme in rat carotid artery after balloon injury. Hypertension 30 2 Pt 1 (1997) 272-277
35. Ferrario C.M., Brosnihan K.B., Diz D.I., Jaiswal N., Khosla M.C., Milsted A., et al. Angiotensin-(1-7): A new hormone of the angiotensin system. Hypertension 18 5 Suppl (1991) III126-III133
36. Fukuda D., and Sata M. The renin-angiotensin system: A potential modulator of endothelial progenitor cells. Hypertens Res 30 11 (2007) 1017-1018
37. Fukuda D., Sata M., Ishizaka N., and Nagai R. Critical role of bone marrow angiotensin ii type 1 receptor in the pathogenesis of atherosclerosis in apolipoprotein e deficient mice. Arterioscler Thromb Vasc Biol 28 1 (2008) 90-96
38. Galis Z.S., and Khatri J.J. Matrix metalloproteinases in vascular remodeling and atherogenesis: The good, the bad, and the ugly. Circ Res 90 3 (2002) 251-262
39. Gill M., Dias S., Hattori K., Rivera M.L., Hicklin D., Witte L., et al. Vascular trauma induces rapid but transient mobilization of vegfr2(+)ac133(+) endothelial precursor cells. Circ Res 88 2 (2001) 167-174
40. Gomez R.A., Norling L.L., Wilfong N., Isakson P., Lynch K.R., Hock R., et al. Leukocytes synthesize angiotensinogen. Hypertension 21 (1993) 470-475
41. Griendling K.K., Sorescu D., and Ushio-Fukai M. Nad(p)h oxidase: Role in cardiovascular biology and disease. Circ Res 86 5 (2000) 494-501
42. Griendling K.K., Ushio-Fukai M., Lassegue B., and Alexander R.W. Angiotensin II signaling in vascular smooth muscle. New concepts. Hypertension 29 1 Pt 2 (1997) 366-373
43. Grossman E., Peleg E., Carroll J., Shamiss A., and Rosenthal T. Hemodynamic and humoral effects of the angiotensin ii antagonist losartan in essential hypertension. Am J Hypertens 7 12 (1994) 1041-1044
44. Gu L., Okada Y., Clinton S.K., Gerard C., Sukhova G.K., Libby P., et al. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 2 2 (1998) 275-281
45. Han Y., Runge M.S., and Brasier A.R. Angiotensin ii induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa b transcription factors. Circ Res 84 6 (1999) 695-703
46. Harrison D.G. Cellular and molecular mechanisms of endothelial cell dysfunction. J Clin Invest 100 9 (1997) 2153-2157
47. Hayek T., Attias J., Coleman R., Brodsky S., Smith J., Breslow J.L., et al. The angiotensin-converting enzyme inhibitor, fosinopril, and the angiotensin ii receptor antagonist, losartan, inhibit LDL oxidation and attenuate atherosclerosis independent of lowering blood pressure in apolipoprotein e deficient mice. Cardiovasc Res 44 3 (1999) 579-587
48. Haznedaroglu I.C., and Ozturk M.A. Towards the understanding of the local hematopoietic bone marrow renin-angiotensin system. Int J Biochem Cell Biol 35 6 (2003) 867-880
49. Haznedaroglu I.C., Tuncer S., and Gursoy M. A local renin-angiotensin system in the bone marrow. Med Hypotheses 46 6 (1996) 507-510
50. Heissig B., Ohki Y., Sato Y., Rafii S., Werb Z., and Hattori K. A role for niches in hematopoietic cell development. Hematology 10 3 (2005) 247-253
51. Hellmann W., Suzuki F., Ohkubo H., Nakanishi S., Ludwig G., and Ganten D. Angiotensinogen gene expression in extrahepatic rat tissues: Application of a solution hybridization assay. Naunyn Schmiedebergs Arch Pharmacol 338 3 (1988) 327-331
52. Hernandez-Presa M., Bustos C., Ortego M., Tunon J., Renedo G., Ruiz-Ortega M., et al. Angiotensin-converting enzyme inhibition prevents arterial nuclear factor-kappa b activation, monocyte chemoattractant protein-1 expression, and macrophage infiltration in a rabbit model of early accelerated atherosclerosis. Circulation 95 6 (1997) 1532-1541
53. Hoshida S., Kato J., Nishino M., Egami Y., Takeda T., Kawabata M., et al. Increased angiotensin-converting enzyme activity in coronary artery specimens from patients with acute coronary syndrome. Circulation 103 5 (2001) 630-633
54. Ikenaga S., Hamano K., Nishida M., Kobayashi T., Li T.S., Kobayashi S., et al. Autologous bone marrow implantation induced angiogenesis and improved deteriorated exercise capacity in a rat ischemic hindlimb model. J Surg Res 96 2 (2001) 277-283
55. Imanishi T., Hano T., and Nishio I. Angiotensin ii potentiates vascular endothelial growth factor-induced proliferation and network formation of endothelial progenitor cells. Hypertens Res 27 2 (2004) 101-108
56. Imanishi T., Hano T., and Nishio I. Angiotensin ii accelerates endothelial progenitor cell senescence through induction of oxidative stress. J Hypertens 23 1 (2005) 97-104
57. Ito K., Hirao A., Arai F., Takubo K., Matsuoka S., Miyamoto K., et al. Reactive oxygen species act through p38 mapk to limit the lifespan of hematopoietic stem cells. Nat Med 12 4 (2006) 446-451
58. Ivanova N.B., Dimos J.T., Schaniel C., Hackney J.A., Moore K.A., and Lemischka I.R. A stem cell molecular signature. Science 298 5593 (2002) 601-604
59. Iwai M., Chen R., Li Z., Shiuchi T., Suzuki J., Ide A., et al. Deletion of angiotensin ii type 2 receptor exaggerated atherosclerosis in apolipoprotein e-null mice. Circulation 112 11 (2005) 1636-1643
60. Iwai M., Chen R., Li Z., Shiuchi T., Suzuki J., Ide A., et al. Deletion of angiotensin ii type 2 receptor exaggerated atherosclerosis in apolipoprotein e-null mice. Circulation 112 11 (2005) 1636-1643
61. Iwai N., and Inagami T. Identification of two subtypes in the rat type I angiotensin II receptor. FEBS Lett 298 2-3 (1992) 257-260
62. Iwai N., Inagami T., Ohmichi N., and Kinoshita M. Renin is expressed in rat macrophage/monocyte cells. Hypertension 27 (1996) 399-403
63. Iwai N., Izumi M., Inagami T., and Kinoshita M. Induction of renin in medial smooth muscle cells by balloon injury. Hypertension 29 4 (1997) 1044-1050
64. Kawamoto A., Gwon H.C., Iwaguro H., Yamaguchi J.I., Uchida S., Masuda H., et al. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation 103 5 (2001) 634-637
65. Keidar S., Heinrich R., Kaplan M., Hayek T., and Aviram M. Angiotensin ii administration to atherosclerotic mice increases macrophage uptake of oxidized LDL: A possible role for interleukin-6. Arterioscler Thromb Vasc Biol 21 9 (2001) 1464-1469
66. Keidar S., Kaplan M., Pavlotzky E., Coleman R., Hayek T., Hamoud S., et al. Aldosterone administration to mice stimulates macrophage NADPH oxidase and increases atherosclerosis development: A possible role for angiotensin-converting enzyme and the receptors for angiotensin ii and aldosterone. Circulation 109 18 (2004) 2213-2220
67. Kim J.A., Berliner J.A., and Nadler J.L. Angiotensin ii increases monocyte binding to endothelial cells. Biochem Biophys Res Commun 226 3 (1996) 862-868
68. Lafayette R.A., Mayer G., Park S.K., and Meyer T.W. Angiotensin II receptor blockade limits glomerular injury in rats with reduced renal mass. J Clin Invest 90 3 (1992) 766-771
69. Li Z., Iwai M., Wu L., Liu H.W., Chen R., Jinno T., et al. Fluvastatin enhances the inhibitory effects of a selective at1 receptor blocker, valsartan, on atherosclerosis. Hypertension 44 5 (2004) 758-763
70. Libby P., Schwartz D., Brogi E., Tanaka H., and Clinton S.K. A cascade model for restenosis. A special case of atherosclerosis progression. Circulation 86 6 Suppl (1992) III47-III52
71. Luchtefeld M., Grote K., Grothusen C., Bley S., Bandlow N., Selle T., et al. Angiotensin II induces mmp-2 in a p47phox-dependent manner. Biochem Biophys Res Commun 328 1 (2005) 183-188
72. Lusis A.J. Atherosclerosis. Nature 407 6801 (2000) 233-241
73. MacIvor D.M., Shapiro S.D., Pham C.T., Belaaouaj A., Abraham S.N., and Ley T.J. Normal neutrophil function in cathepsin g-deficient mice. Blood 94 (1999) 4282-4293
74. Marusic-Vrsalovic M., Dominis M., Jaksic B., and Kusec R. Angiotensin i-converting enzyme is expressed by erythropoietic cells of normal and myeloproliferative bone marrow. Br J Haematol 123 (2003) 539-541
75. Moreno P.R., Purushothaman K.R., Sirol M., Levy A.P., and Fuster V. Neovascularization in human atherosclerosis. Circulation 113 18 (2006) 2245-2252
76. Morimoto S., Cassell M.D., and Sigmund C.D. The brain renin-angiotensin system in transgenic mice carrying a highly regulated human renin transgene. Circ Res 90 1 (2002) 80-86
77. Morishita R., Gibbons G.H., Ellison K.E., Nakajima M., Zhang L., Kaneda Y., et al. Single intraluminal delivery of antisense cdc2 kinase and proliferating-cell nuclear antigen oligonucleotides results in chronic inhibition of neointimal hyperplasia. Proc Natl Acad Sci U S A 90 18 (1993) 8474-8478
78. Mrug M., Stopka T., Julian B.A., Prchal J.F., and Prchal J.T. Angiotensin II stimulates proliferation of normal early erythroid progenitors. J Clin Invest 100 9 (1997) 2310-2314
79. Nakagami H., Cui T.X., Iwai M., Shiuchi T., Takeda-Matsubara Y., Wu L., et al. Tumor necrosis factor-alpha inhibits growth factor-mediated cell proliferation through shp-1 activation in endothelial cells. Arterioscler Thromb Vasc Biol 22 2 (2002) 238-242
80. Noble M., Smith J., Power J., and Mayer-Proschel M. Redox state as a central modulator of precursor cell function. Ann N Y Acad Sci 991 (2003) 251-271
81. Nomura S., Sugihara T., Tomiyama T., Kitano Y., Yawata Y., and Osawa G. Polycythaemia vera: Response to treatment with angiotensin-converting enzyme inhibitor. Eur J Haematol 57 1 (1996) 117-119
82. Nouet S., and Nahmias C. Signal transduction from the angiotensin II at2 receptor. Trends Endocrinol Metab 11 1 (2000) 1-6
83. Oparil S., and Haber E. The renin-angiotensin system (first of two parts). N Engl J Med 291 8 (1974) 389-401
84. Oparil S., and Haber E. The renin-angiotensin system (second of two parts). N Engl J Med 291 9 (1974) 446-457
85. Orlic D., Kajstura J., Chimenti S., Bodine D.M., Leri A., and Anversa P. Transplanted adult bone marrow cells repair myocardial infarcts in mice. Ann N Y Acad Sci 938 (2001) 221-229 discussion 229-230
86. Pastore L., Tessitore A., Martinotti S., Toniato E., Alesse E., Bravi M.C., et al. Angiotensin ii stimulates intercellular adhesion molecule-1 (icam-1) expression by human vascular endothelial cells and increases soluble icam-1 release in vivo. Circulation 100 15 (1999) 1646-1652
87. Petnehazy T., Stokes K.Y., Wood K.C., Russell J., and Granger D.N. Role of blood cell-associated at1 receptors in the microvascular responses to hypercholesterolemia. Arterioscler Thromb Vasc Biol 26 2 (2006) 313-318
88. Pfeffer M.A., McMurray J.J., Velazquez E.J., Rouleau J.L., Kober L., Maggioni A.P., et al. Valsartan, captopril, or both in myocardial infarction complicated by heart failure, left ventricular dysfunction, or both. N Engl J Med 349 20 (2003) 1893-1906
89. Pfeffer M.A., McMurray J.J., Velazquez E.J., Rouleau J.L., Kober L., Maggioni A.P., et al. Valsartan, captopril, or both in myocardial infarction complicated by heart failure, left ventricular dysfunction, or both. N Engl J Med 349 20 (2003) 1893-1906
90. Phillips M.I., and Kagiyama S. Angiotensin II as a pro-inflammatory mediator. Curr Opin Investig Drugs 3 4 (2002) 569-577
91. Phillips M.I., and Sumners C. Angiotensin II in central nervous system physiology. Regul Pept 78 1-3 (1998) 1-11
92. Pitt B., Segal R., Martinez F.A., Meurers G., Cowley A.J., Thomas I., et al. Randomised trial of losartan versus captopril in patients over 65 with heart failure (evaluation of losartan in the elderly study, elite). Lancet 349 9054 (1997) 747-752
93. Pueyo M.E., Gonzalez W., Nicoletti A., Savoie F., Arnal J.F., and Michel J.B. Angiotensin ii stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-kappaB activation induced by intracellular oxidative stress. Arterioscler Thromb Vasc Biol 20 3 (2000) 645-651
94. Rell K., Koziak K., Jarzyo I., Lao M., and Gaciong Z. Correction of posttransplant erythrocytosis with enalapril. Transplantation 57 7 (1994) 1059-1063
95. Rodgers K.E., DeCherney A.H., St Amand K.M., Dougherty W.R., Felix J.C., Girgis W.W., et al. Histologic alterations in dermal repair after thermal injury effects of topical angiotensin ii. J Burn Care Rehabil 18 5 (1997) 381-388
96. Rodgers K.E., Xiong S., and diZerega G.S. Accelerated recovery from irradiation injury by angiotensin peptides. Cancer Chemother Pharmacol 49 5 (2002) 403-411
97. Rodgers K., Xiong S., and DiZerega G.S. Effect of angiotensin II and angiotensin(1-7) on hematopoietic recovery after intravenous chemotherapy. Cancer Chemother Pharmacol 51 2 (2003) 97-106
98. Rodgers K.E., Xiong S., Steer R., and diZerega G.S. Effect of angiotensin II on hematopoietic progenitor cell proliferation. Stem Cells 18 4 (2000) 287-294
99. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 340 2 (1999) 115-126
100. Ruiz-Ortega M., Lorenzo O., Ruperez M., Esteban V., Suzuki Y., Mezzano S., et al. Role of the renin-angiotensin system in vascular diseases: Expanding the field. Hypertension 38 6 (2001) 1382-1387
101. Sales V.L., Sukhova G.K., Lopez-Ilasaca M.A., Libby P., Dzau V.J., and Pratt R.E. Angiotensin type 2 receptor is expressed in murine atherosclerotic lesions and modulates lesion evolution. Circulation 112 21 (2005) 3328-3336
102. Sasaki K., Murohara T., Ikeda H., Sugaya T., Shimada T., Shintani S., et al. Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis. J Clin Invest 109 5 (2002) 603-611
103. Sata M. Role of circulating vascular progenitors in angiogenesis, vascular healing, and pulmonary hypertension: Lessons from animal models. Arterioscler Thromb Vasc Biol 26 5 (2006) 1008-1014
104. Sata M., and Nagai R. Inflammation, angiogenesis, and endothelial progenitor cells: How do endothelial progenitor cells find their place?. J Mol Cell Cardiol 36 4 (2004) 459-463
105. Sayeski P.P., and Bernstein K.E. Signal transduction mechanisms of the angiotensin II type at(1)-receptor: Looking beyond the heterotrimeric g protein paradigm. J Renin Angiotensin Aldosterone Syst 2 1 (2001) 4-10
106. Schieffer B., Luchtefeld M., Braun S., Hilfiker A., Hilfiker-Kleiner D., and Drexler H. Role of nad(p)h oxidase in angiotensin ii-induced jak/stat signaling and cytokine induction. Circ Res 87 12 (2000) 1195-1201
107. Schieffer B., Schieffer E., Hilfiker-Kleiner D., Hilfiker A., Kovanen P.T., Kaartinen M., et al. Expression of angiotensin ii and interleukin 6 in human coronary atherosclerotic plaques: Potential implications for inflammation and plaque instability. Circulation 101 12 (2000) 1372-1378
108. Schiffrin E.L., Park J.B., Intengan H.D., and Touyz R.M. Correction of arterial structure and endothelial dysfunction in human essential hypertension by the angiotensin receptor antagonist losartan. Circulation 101 14 (2000) 1653-1659
109. Schmeisser A., Soehnlein O., Illmer T., Lorenz H.M., Eskafi S., Roerick O., et al. Ace inhibition lowers angiotensin II-induced chemokine expression by reduction of nf-kappaB activity and at1 receptor expression. Biochem Biophys Res Commun 325 2 (2004) 532-540
110. Schrader J., Luders S., Kulschewski A., Berger J., Zidek W., Treib J., et al. The access study: Evaluation of acute candesartan cilexetil therapy in stroke survivors. Stroke 34 7 (2003) 1699-1703
111. Schrader J., Luders S., Kulschewski A., Hammersen F., Plate K., Berger J., et al. Morbidity and mortality after stroke, eprosartan compared with nitrendipine for secondary prevention: Principal results of a prospective randomized controlled study (MOSES). Stroke 36 6 (2005) 1218-1226
112. Schwartz S.M. Perspectives series: Cell adhesion in vascular biology. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest 99 12 (1997) 2814-2816
113. Sensebe L., Deschaseaux M., Li J., Herve P., and Charbord P. The broad spectrum of cytokine gene expression by myoid cells from the human marrow microenvironment. Stem Cells 15 2 (1997) 133-143
114. Shibata H., Suzuki H., Murakami M., Sato A., and Saruta T. Angiotensin ii type 1 receptor messenger rna levels in human blood cells of patients with primary and secondary hypertension: Reference to renin profile. J Hypertens 12 (1994) 1275-1284
115. Shintani S., Murohara T., Ikeda H., Ueno T., Honma T., Katoh A., et al. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation 103 23 (2001) 2776-2779
116. Stoll M., Steckelings U.M., Paul M., Bottari S.P., Metzger R., and Unger T. The angiotensin at2-receptor mediates inhibition of cell proliferation in coronary endothelial cells. J Clin Invest 95 2 (1995) 651-657
117. Stouffer G.A., and Owens G.K. Angiotensin II-induced mitogenesis of spontaneously hypertensive rat-derived cultured smooth muscle cells is dependent on autocrine production of transforming growth factor-beta. Circ Res 70 4 (1992) 820-828
118. Strawn W.B., Chappell M.C., Dean R.H., Kivlighn S., and Ferrario C.M. Inhibition of early atherogenesis by losartan in monkeys with diet-induced hypercholesterolemia. Circulation 101 13 (2000) 1586-1593
119. Strawn W.B., Richmond R.S., Ann Tallant E., Gallagher P.E., and Ferrario C.M. Renin-angiotensin system expression in rat bone marrow haematopoietic and stromal cells. Br J Haematol 126 (2004) 120-126
120. Strippoli G.F., Craig M., Deeks J.J., Schena F.P., and Craig J.C. Effects of angiotensin converting enzyme inhibitors and angiotensin ii receptor antagonists on mortality and renal outcomes in diabetic nephropathy: Systematic review. BMJ 329 7470 (2004) 828
121. Sugaya T., Nishimatsu S., Tanimoto K., Takimoto E., Yamagishi T., Imamura K., et al. Angiotensin II type 1a receptor-deficient mice with hypotension and hyperreninemia. J Biol Chem 270 32 (1995) 18719-18722
122. Tsuchida S., Matsusaka T., Chen X., Okubo S., Niimura F., Nishimura H., et al. Murine double nullizygotes of the angiotensin type 1a and 1b receptor genes duplicate severe abnormal phenotypes of angiotensinogen nullizygotes. J Clin Invest 101 4 (1998) 755-760
123. Tummala P.E., Chen X.L., Sundell C.L., Laursen J.B., Hammes C.P., Alexander R.W., et al. Angiotensin ii induces vascular cell adhesion molecule-1 expression in rat vasculature: A potential link between the renin-angiotensin system and atherosclerosis. Circulation 100 11 (1999) 1223-1229
124. Ushio-Fukai M., Alexander R.W., Akers M., Yin Q., Fujio Y., Walsh K., et al. Reactive oxygen species mediate the activation of akt/protein kinase b by angiotensin II in vascular smooth muscle cells. J Biol Chem 274 32 (1999) 22699-22704
125. Varin R., Mulder P., Tamion F., Richard V., Henry J.P., Lallemand F., et al. Improvement of endothelial function by chronic angiotensin-converting enzyme inhibition in heart failure: Role of nitric oxide, prostanoids, oxidant stress, and bradykinin. Circulation 102 3 (2000) 351-356
126. Vasku A., Soucek M., Znojil V., Rihacek I., Cidl K., Strelcova L., et al. Does angiotensin I-converting enzyme inhibitor therapy have an antiproliferative effect on blood-forming bone marrow?. Exp Hematol 26 4 (1998) 277-279
127. Vaughan D.E., Lazos S.A., and Tong K. Angiotensin II regulates the expression of plasminogen activator inhibitor-1 in cultured endothelial cells. A potential link between the renin-angiotensin system and thrombosis. J Clin Invest 95 3 (1995) 995-1001
128. Verma S., and Strauss M. Angiotensin receptor blockers and myocardial infarction. Bmj 329 7477 (2004) 1248-1249
129. Viedt C., Soto U., Krieger-Brauer H.I., Fei J., Elsing C., Kubler W., et al. Differential activation of mitogen-activated protein kinases in smooth muscle cells by angiotensin II: Involvement of p22phox and reactive oxygen species. Arterioscler Thromb Vasc Biol 20 4 (2000) 940-948
130. Warnholtz A., Nickenig G., Schulz E., Macharzina R., Brasen J.H., Skatchkov M., et al. Increased NADH-oxidase-mediated superoxide production in the early stages of atherosclerosis: Evidence for involvement of the renin-angiotensin system. Circulation 99 15 (1999) 2027-2033
131. Wassmann S., Czech T., van Eickels M., Fleming I., Bohm M., and Nickenig G. Inhibition of diet-induced atherosclerosis and endothelial dysfunction in apolipoprotein e/angiotensin II type 1a receptor double-knockout mice. Circulation 110 19 (2004) 3062-3067
132. Williams B., Baker A.Q., Gallacher B., and Lodwick D. Angiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells. Hypertension 25 5 (1995) 913-917
133. Wilson S.K., Lynch D.R., and Snyder S.H. Angiotensin-converting enzyme labeled with [3H]captopril. Tissue localizations and changes in different models of hypertension in the rat. J Clin Invest 80 3 (1987) 841-851
134. Wintroub B.U., Klickstein L.B., Dzau V.J., and Watt K.W. Granulocyte-angiotensin system. Identification of angiotensinogen as the plasma protein substrate of leukocyte cathepsin g. Biochemistry 23 (1984) 227-232
135. Wu L., Iwai M., Nakagami H., Chen R., Suzuki J., Akishita M., et al. Effect of angiotensin ii type 1 receptor blockade on cardiac remodeling in angiotensin ii type 2 receptor null mice. Arterioscler Thromb Vasc Biol 22 1 (2002) 49-54
136. Wu L., Iwai M., Nakagami H., Li Z., Chen R., Suzuki J., et al. Roles of angiotensin II type 2 receptor stimulation associated with selective angiotensin ii type 1 receptor blockade with valsartan in the improvement of inflammation-induced vascular injury. Circulation 104 22 (2001) 2716-2721
137. Wulf G.G., Jahns-Streubel G., Nobiling R., Strutz F., Hemmerlein B., Hiddemann W., et al. Renin in acute myeloid leukaemia blasts. Br J Haematol 100 2 (1998) 335-337
138. Yamagishi H., Kim S., Nishikimi T., Takeuchi K., and Takeda T. Contribution of cardiac renin-angiotensin system to ventricular remodelling in myocardial-infarcted rats. J Mol Cell Cardiol 25 11 (1993) 1369-1380
139. Yang D., Elner S.G., Bian Z.M., Till G.O., Petty H.R., and Elner V.M. Pro-inflammatory cytokines increase reactive oxygen species through mitochondria and NADPH oxidase in cultured RPE cells. Exp Eye Res 85 4 (2007) 462-472
140. Yang R.H., Jin H., Wyss J.M., and Oparil S. Depressor effect of blocking angiotensin subtype 1 receptors in anterior hypothalamus. Hypertension 19 5 (1992) 475-481
141. Yao E.H., Yu Y., and Fukuda N. Oxidative stress on progenitor and stem cells in cardiovascular diseases. Curr Pharm Biotechnol 7 2 (2006) 101-108
142. Yusuf S., Sleight P., Pogue J., Bosch J., Davies R., and Dagenais G. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The heart outcomes prevention evaluation study investigators. N Engl J Med 342 3 (2000) 145-153
143. Zhang S.H., Reddick R.L., Piedrahita J.A., and Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein e. Science 258 5081 (1992) 468-471