Vitamin d receptor signaling in renal and cardiovascular protection

Seminars in Nephrology

Volumn 33, Issue 5, 2013, Pages 433-447

  Chun Li, Yan ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Atherosclerosis; Diabetic nephropathy; Macrophage; Podocyte; Renin angiotensin system; Vitamin D deficiency

Indexed keywords

DOXERCALCIFEROL; RAS PROTEIN; VITAMIN D RECEPTOR;

ALBUMINURIA; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; B LYMPHOCYTE; CARDIOVASCULAR DISEASE; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG EFFECT; HEART PROTECTION; HUMAN; KIDNEY DISEASE; KIDNEY INJURY; LOW DRUG DOSE; MACROPHAGE FUNCTION; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RENAL PROTECTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VITAMIN D DEFICIENCY;

ATHEROSCLEROSIS; DIABETIC NEPHROPATHY; MACROPHAGE; PODOCYTE; RENIN-ANGIOTENSIN SYSTEM; VITAMIN D DEFICIENCY;

AFRICAN AMERICANS; ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; HUMANS; KIDNEY DISEASES; MACROPHAGES; MICE; PODOCYTES; RECEPTORS, CALCITRIOL; SIGNAL TRANSDUCTION; VITAMIN D;

EID: 84885236861     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2013.07.005     Document Type: Article

References (105)

1. Haussler M.R., Whitfield G.K., Haussler C.A., Hsieh J.C., Thompson P.D., Selznick S.H., et al. The nuclear vitamin D receptor: biological and molecular regulatory properties revealed. J Bone Miner Res 1998, 13:325-349.
2. Li Y.C. Renoprotective effects of vitamin D analogs. Kidney Int 2010, 78:134-139.
3. Holick M.F. Vitamin D deficiency. N Engl J Med 2007, 357:266-281.
4. Li Y.C. Vitamin D: roles in renal and cardiovascular protection. Curr Opin Nephrol Hypertens 2012, 21:72-79.
5. Rostand S.G. Vitamin D, blood pressure, and African Americans: toward a unifying hypothesis. Clin J Am Soc Nephrol 2010, 5:1697-1703.
6. Teng M., Wolf M., Ofsthun M.N., Lazarus J.M., Hernan M.A., Camargo C.A., et al. Activated injectable vitamin D and hemodialysis survival: a historical cohort study. J Am Soc Nephrol 2005, 16:1115-1125.
7. Teng M., Wolf M., Lowrie E., Ofsthun N., Lazarus J.M., Thadhani R. Survival of patients undergoing hemodialysis with paricalcitol or calcitriol therapy. N Engl J Med 2003, 349:446-456.
8. Shoji T., Shinohara K., Kimoto E., Emoto M., Tahara H., Koyama H., et al. Lower risk for cardiovascular mortality in oral 1alpha-hydroxy vitamin D3 users in a haemodialysis population. Nephrol Dial Transplant 2004, 19:179-184.
9. Tentori F., Hunt W.C., Stidley C.A., Rohrscheib M.R., Bedrick E.J., Meyer K.B., et al. Mortality risk among hemodialysis patients receiving different vitamin D analogs. Kidney Int 2006, 70:1858-1865.
10. Shoben A.B., Rudser K.D., de Boer I.H., Young B., Kestenbaum B. Association of oral calcitriol with improved survival in nondialyzed CKD. J Am Soc Nephrol 2008, 19:1613-1619.
11. Keane W.F., Eknoyan G. Proteinuria, albuminuria, risk, assessment, detection, elimination (PARADE): a position paper of the National Kidney Foundation. Am J Kidney Dis 1999, 33:1004-1010.
12. de Boer I.H., Ioannou G.N., Kestenbaum B., Brunzell J.D., Weiss N.S. 25-Hydroxyvitamin D levels and albuminuria in the Third National Health and Nutrition Examination Survey (NHANES III). Am J Kidney Dis 2007, 50:69-77.
13. Agarwal R., Acharya M., Tian J., Hippensteel R.L., Melnick J.Z., Qiu P., et al. Antiproteinuric effect of oral paricalcitol in chronic kidney disease. Kidney Int 2005, 68:2823-2828.
14. Alborzi P., Patel N.A., Peterson C., Bills J.E., Bekele D.M., Bunaye Z., et al. Paricalcitol reduces albuminuria and inflammation in chronic kidney disease: a randomized double-blind pilot trial. Hypertension 2008, 52:249-255.
15. Fishbane S., Chittineni H., Packman M., Dutka P., Ali N., Durie N. Oral paricalcitol in the treatment of patients with CKD and proteinuria: a randomized trial. Am J Kidney Dis 2009, 54:647-652.
16. de Zeeuw D., Agarwal R., Amdahl M., Audhya P., Coyne D., Garimella T., et al. Selective vitamin D receptor activation with paricalcitol for reduction of albuminuria in patients with type 2 diabetes (VITAL study): a randomised controlled trial. Lancet 2010, 376:1543-1551.
17. Zhang Z., Sun L., Wang Y., Ning G., Minto A.W., Kong J., et al. Renoprotective role of the vitamin D receptor in diabetic nephropathy. Kidney Int 2008, 73:163-171.
18. Zhang Y., Kong J., Deb D.K., Chang A., Li Y.C. Vitamin D receptor attenuates renal fibrosis by suppressing the renin-angiotensin system. J Am Soc Nephrol 2010, 21:966-973.
19. Kuhlmann A., Haas C.S., Gross M.L., Reulbach U., Holzinger M., Schwarz U., et al. 1,25-Dihydroxyvitamin D3 decreases podocyte loss and podocyte hypertrophy in the subtotally nephrectomized rat. Am J Physiol Renal Physiol 2004, 286:F526-33.
20. Freundlich M., Quiroz Y., Zhang Z., Zhang Y., Bravo Y., Weisinger J.R., et al. Suppression of renin-angiotensin gene expression in the kidney by paricalcitol. Kidney Int 2008, 74:1394-1402.
21. Mizobuchi M., Morrissey J., Finch J.L., Martin D.R., Liapis H., Akizawa T., et al. Combination therapy with an angiotensin-converting enzyme inhibitor and a vitamin D analog suppresses the progression of renal insufficiency in uremic rats. J Am Soc Nephrol 2007, 18:1796-1806.
22. Xiao H., Shi W., Liu S., Wang W., Zhang B., Zhang Y., et al. 1,25-Dihydroxyvitamin D(3) prevents puromycin aminonucleoside-induced apoptosis of glomerular podocytes by activating the phosphatidylinositol 3-kinase/Akt-signaling pathway. Am J Nephrol 2009, 30:34-43.
23. He W., Kang Y.S., Dai C., Liu Y. Blockade of Wnt/beta-catenin signaling by paricalcitol ameliorates proteinuria and kidney injury. J Am Soc Nephrol 2011, 22:90-103.
24. Zhang Z., Zhang Y., Ning G., Deb D.K., Kong J., Li Y.C. Combination therapy with AT1 blocker and vitamin D analog markedly ameliorates diabetic nephropathy: blockade of compensatory renin increase. Proc Natl Acad Sci U S A 2008, 105:15896-15901.
25. Deb D.K., Sun T., Wong K.E., Zhang Z., Ning G., Zhang Y., et al. Combined vitamin D analog and AT1 receptor antagonist synergistically block the development of kidney disease in a model of type 2 diabetes. Kidney Int 2010, 77:1000-1009.
26. Zhang Y., Deb D.K., Kong J., Ning G., Wong Y., Li G., et al. Long-term therapeutic effect of vitamin D analog doxercalciferol on diabetic nephropathy: strong synergism with AT1 receptor antagonist. Am J Physiol Renal Physiol 2009, 297:F791-801.
27. Wang Y., Zhou J., Minto A.W., Hack B.K., Alexander J.J., Haas M., et al. Altered vitamin D metabolism in type II diabetic mouse glomeruli may provide protection from diabetic nephropathy. Kidney Int 2006, 70:882-891.
28. Deb D.K., Wang Y., Zhang Z., Nie H., Huang X., Yuan Z., et al. Molecular mechanism underlying 1,25-dihydroxyvitamin D regulation of nephrin gene expression. J Biol Chem 2011, 286:32011-32017.
29. Li Y.C. Podocytes as target of vitamin D. Curr Diabetes Rev 2011, 7:35-40.
30. Tryggvason K., Patrakka J., Wartiovaara J. Hereditary proteinuria syndromes and mechanisms of proteinuria. N Engl J Med 2006, 354:1387-1401.
31. Qi Z., Fujita H., Jin J., Davis L.S., Wang Y., Fogo A.B., et al. Characterization of susceptibility of inbred mouse strains to diabetic nephropathy. Diabetes 2005, 54:2628-2637.
32. Moeller M.J., Sanden S.K., Soofi A., Wiggins R.C., Holzman L.B. Two gene fragments that direct podocyte-specific expression in transgenic mice. J Am Soc Nephrol 2002, 13:1561-1567.
33. Wang Y., Deb D.K., Zhang Z., Sun T., Liu W., Yoon D., et al. Vitamin D receptor signaling in podocytes protects against diabetic nephropathy. J Am Soc Nephrol 2012, 23:1977-1986.
34. Stokoe D., Campbell D.G., Nakielny S., Hidaka H., Leevers S.J., Marshall C., et al. MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J 1992, 11:3985-3994.
35. Li Z., Ma J.Y., Kerr I., Chakravarty S., Dugar S., Schreiner G., et al. Selective inhibition of p38alpha MAPK improves cardiac function and reduces myocardial apoptosis in rat model of myocardial injury. Am J Physiol Heart Circ Physiol 2006, 291:H1972-H1977.
36. Carey R.M., Siragy H.M. The intrarenal renin-angiotensin system and diabetic nephropathy. Trends Endocrinol Metab 2003, 14:274-281.
37. Jia J., Ding G., Zhu J., Chen C., Liang W., Franki N., et al. Angiotensin II infusion induces nephrin expression changes and podocyte apoptosis. Am J Nephrol 2008, 28:500-507.
38. Ding G., Reddy K., Kapasi A.A., Franki N., Gibbons N., Kasinath B.S., et al. Angiotensin II induces apoptosis in rat glomerular epithelial cells. Am J Physiol Renal Physiol 2002, 283:F173-80.
39. Li Y.C., Pirro A.E., Amling M., Delling G., Baron R., Bronson R., et al. Targeted ablation of the vitamin D receptor: an animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci U S A 1997, 94:9831-9835.
40. Yoshizawa T., Handa Y., Uematsu Y., Takeda S., Sekine K., Yoshihara Y., et al. Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat Genet 1997, 16:391-396.
41. Shankland S.J. The podocyte's response to injury: role in proteinuria and glomerulosclerosis. Kidney Int 2006, 69:2131-2147.
42. Durvasula R.V., Shankland S.J. Activation of a local renin angiotensin system in podocytes by glucose. Am J Physiol Renal Physiol 2008, 294:F830-F839.
43. Yoo T.H., Li J.J., Kim J.J., Jung D.S., Kwak S.J., Ryu D.R., et al. Activation of the renin-angiotensin system within podocytes in diabetes. Kidney Int 2007, 71:1019-1027.
44. Susztak K., Raff A.C., Schiffer M., Bottinger E.P. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes 2006, 55:225-233.
45. Tsiani E., Lekas P., Fantus I.G., Dlugosz J., Whiteside C. High glucose-enhanced activation of mesangial cell p38 MAPK by ET-1, ANG II, and platelet-derived growth factor. Am J Physiol Endocrinol Metab 2002, 282:E161-E169.
46. Rostand S.G. Ultraviolet light may contribute to geographic and racial blood pressure differences. Hypertension 1997, 30:150-156.
47. He J., Klag M.J., Wu Z., Whelton P.K. Stroke in the People's Republic of China. I. Geographic variations in incidence and risk factors. Stroke 1995, 26:2222-2227.
48. Harburg E., Gleibermann L., Roeper P., Schork M.A., Schull W.J. Skin color, ethnicity, and blood pressure I: Detroit blacks. Am J Public Health 1978, 68:1177-1183.
49. Klag M.J., Whelton P.K., Coresh J., Grim C.E., Kuller L.H. The association of skin color with blood pressure in US blacks with low socioeconomic status. JAMA 1991, 265:599-602.
50. Scragg R., Sowers M., Bell C. Serum 25-hydroxyvitamin D, ethnicity, and blood pressure in the Third National Health and Nutrition Examination Survey. Am J Hypertens 2007, 20:713-719.
51. Martins D., Wolf M., Pan D., Zadshir A., Tareen N., Thadhani R., et al. Prevalence of cardiovascular risk factors and the serum levels of 25-hydroxyvitamin D in the United States: data from the Third National Health and Nutrition Examination Survey. Arch Intern Med 2007, 167:1159-1165.
52. Zittermann A., Schleithoff S.S., Tenderich G., Berthold H.K., Korfer R., Stehle P. Low vitamin D status: a contributing factor in the pathogenesis of congestive heart failure?. J Am Coll Cardiol 2003, 41:105-112.
53. Forman J.P., Giovannucci E., Holmes M.D., Bischoff-Ferrari H.A., Tworoger S.S., Willett W.C., et al. Plasma 25-hydroxyvitamin D levels and risk of incident hypertension. Hypertension 2007, 49:1063-1069.
54. Giovannucci E., Liu Y., Hollis B.W., Rimm E.B. 25-hydroxyvitamin D and risk of myocardial infarction in men: a prospective study. Arch Intern Med 2008, 168:1174-1180.
55. Wang T.J., Pencina M.J., Booth S.L., Jacques P.F., Ingelsson E., Lanier K., et al. Vitamin D deficiency and risk of cardiovascular disease. Circulation 2008, 117:503-511.
56. Glass C.K., Witztum J.L. Atherosclerosis. The road ahead. Cell 2001, 104:503-516.
57. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med 1999, 340:115-126.
58. Hynes R.O., Wagner D.D. Genetic manipulation of vascular adhesion molecules in mice. J Clin Invest 1996, 98:2193-2195.
59. Galkina E., Ley K. Vascular adhesion molecules in atherosclerosis. Arterioscler Thromb Vasc Biol 2007, 27:2292-2301.
60. Eriksson E.E. Leukocyte recruitment to atherosclerotic lesions, a complex web of dynamic cellular and molecular interactions. Curr Drug Targets Cardiovasc Haematol Disord 2003, 3:309-325.
61. Dong Z.M., Chapman S.M., Brown A.A., Frenette P.S., Hynes R.O., Wagner D.D. The combined role of P- and E-selectins in atherosclerosis. J Clin Invest 1998, 102:145-152.
62. Collins R.G., Velji R., Guevara N.V., Hicks M.J., Chan L., Beaudet A.L. P-Selectin or intercellular adhesion molecule (ICAM)-1 deficiency substantially protects against atherosclerosis in apolipoprotein E-deficient mice. J Exp Med 2000, 191:189-194.
63. Rajavashisth T., Qiao J.H., Tripathi S., Tripathi J., Mishra N., Hua M., et al. Heterozygous osteopetrotic (op) mutation reduces atherosclerosis in LDL receptor- deficient mice. J Clin Invest 1998, 101:2702-2710.
64. Smith J.D., Trogan E., Ginsberg M., Grigaux C., Tian J., Miyata M. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E. Proc Natl Acad Sci U S A 1995, 92:8264-8268.
65. Qiao J.H., Tripathi J., Mishra N.K., Cai Y., Tripathi S., Wang X.P., et al. Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am J Pathol 1997, 150:1687-1699.
66. Pennings M., Meurs I., Ye D., Out R., Hoekstra M., Van Berkel T.J., et al. Regulation of cholesterol homeostasis in macrophages and consequences for atherosclerotic lesion development. FEBS Lett 2006, 580:5588-5596.
67. Daugherty A. Atherosclerosis: cell biology and lipoproteins. Curr Opin Lipidol 2005, 16:257-259.
68. Daugherty A., Rateri D.L., Lu H., Inagami T., Cassis L.A. Hypercholesterolemia stimulates angiotensin peptide synthesis and contributes to atherosclerosis through the AT1A receptor. Circulation 2004, 110:3849-3857.
69. Potter D.D., Sobey C.G., Tompkins P.K., Rossen J.D., Heistad D.D. Evidence that macrophages in atherosclerotic lesions contain angiotensin II. Circulation 1998, 98:800-807.
70. Iwai N., Inagami T., Ohmichi N., Kinoshita M. Renin is expressed in rat macrophage/monocyte cells. Hypertension 1996, 27:399-403.
71. Okamura A., Rakugi H., Ohishi M., Yanagitani Y., Takiuchi S., Moriguchi K., et al. Upregulation of renin-angiotensin system during differentiation of monocytes to macrophages. J Hypertens 1999, 17:537-545.
72. Lu H., Rateri D.L., Feldman D.L., RJ, Fukamizu A., Ishida J., et al. Renin inhibition reduces hypercholesterolemia-induced atherosclerosis in mice. J Clin Invest 2008, 118:984-993.
73. Li Y.C. Molecular mechanism of vitamin D in the cardiovascular system. J Investig Med 2011, 59:868-871.
74. Lai H., Fishman E.K., Gerstainblith G., Brinker J.A., Tong W., Bhatia S., et al. Vitamin D deficiency is associated with significant coronary stenoses in asymptomatic African American chronic cocain users. Int J Cardiol 2012, 158:211-216.
75. Reis J.P., von Muhlen D., Michos E.D., Miller E.R., Appel L.J., Araneta M.R., et al. Serum vitamin D, parathyroid hormone levels, and carotid atherosclerosis. Atherosclerosis 2009, 207:585-590.
76. de Boer I.H., Kestenbaum B., Shoben A.B., Michos E.D., Sarnak M.J., Siscovick D.S. 25-hydroxyvitamin D levels inversely associate with risk for developing coronary artery calcification. J Am Soc Nephrol 2009, 20:1805-1812.
77. Oh J., Weng S., Felton S.K., Bhandare S., Riek A., Butler B., et al. 1,25(OH)2 vitamin d inhibits foam cell formation and suppresses macrophage cholesterol uptake in patients with type 2 diabetes mellitus. Circulation 2009, 120:687-698.
78. Takeda M., Yamashita T., Sasaki N., Nakajima K., Kita T., Shinohara M., et al. Oral administration of an active form of vitamin D3 (calcitriol) decreases atherosclerosis in mice by inducing regulatory T cells and immature dendritic cells with tolerogenic functions. Arterioscler Thromb Vasc Biol 2010, 30:2495-2503.
79. Reardon C.A., Blachowicz L., White T., Cabana V., Wang Y., Lukens J., et al. Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2001, 21:1011-1016.
80. Szeto F.L., Reardon C.A., Yoon D., Wang Y., Wong K.E., Chen Y., et al. Vitamin D receptor signaling inhibits atherosclerosis in mice. Mol Endocrinol 2012, 26:1091-1101.
81. Mombaerts P., Iacomini J., Johnson R.S., Herrup K., Tonegawa S., Papaioannou V.E. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 1992, 68:869-877.
82. Li Y.C., Kong J., Wei M., Chen Z.F., Liu S.Q., Cao L.P. 1,25-Dihydroxyvitamin D(3) is a negative endocrine regulator of the renin-angiotensin system. J Clin Invest 2002, 110:229-238.
83. Yuan W., Pan W., Kong J., Zheng W., Szeto F.L., Wong K.E., et al. 1,25-Dihydroxyvitamin D3 suppresses renin gene transcription by blocking the activity of the cyclic AMP response element in the renin gene promoter. J Biol Chem 2007, 282:29821-29830.
84. Deb D.K., Chen Y., Zhang Z., Zhang Y., Szeto F.L., Wong K.E., et al. 1,25-Dihydroxyvitamin D3 suppresses high glucose-induced angiotensinogen expression in kidney cells by blocking the NF-{kappa}B pathway. Am J Physiol Renal Physiol 2009, 296:F1212-F1218.
85. Iwai N., Izumi M., Inagami T., Kinoshita M. Induction of renin in medial smooth muscle cells by balloon injury. Hypertension 1997, 29:1044-1050.
86. Campbell D.J., Habener J.F. Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat. J Clin Invest 1986, 78:31-39.
87. Hellmann W., Suzuki F., Ohkubo H., Nakanishi S., Ludwig G., Ganten D. Angiotensinogen gene expression in extrahepatic rat tissues: application of a solution hybridization assay. Naunyn Schmiedebergs Arch Pharmacol 1988, 338:327-331.
88. 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 1995, 25:219-226.
89. 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 1997, 30:272-277.
90. Diet F., Pratt R.E., Berry G.J., Momose N., Gibbons G.H., Dzau V.J. Increased accumulation of tissue ACE in human atherosclerotic coronary artery disease. Circulation 1996, 94:2756-2767.
91. Ohishi M., Ueda M., Rakugi H., Naruko T., Kojima A., Okamura A., et al. Enhanced expression of angiotensin-converting enzyme is associated with progression of coronary atherosclerosis in humans. J Hypertens 1997, 15:1295-1302.
92. Daugherty A., Cassis L. Angiotensin II-mediated development of vascular diseases. Trends Cardiovasc Med 2004, 14:117-120.
93. Daugherty A., Manning M.W., Cassis L.A. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest 2000, 105:1605-1612.
94. Sata M., Fukuda D. Crucial role of renin-angiotensin system in the pathogenesis of atherosclerosis. J Med Invest 2010, 57:12-25.
95. Harrison D.G. Cellular and molecular mechanisms of endothelial cell dysfunction. J Clin Invest 1997, 100:2153-2157.
96. Pueyo M.E., Gonzalez W., Nicoletti A., Savoie F., Arnal J.F., 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 2000, 20:645-651.
97. 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 1999, 100:1646-1652.
98. 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 1999, 100:1223-1229.
99. 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 1997, 95:1532-1541.
100. Keidar S., Heinrich R., Kaplan M., Hayek T., Aviram M. Angiotensin II administration to atherosclerotic mice increases macrophage uptake of oxidized ldl: a possible role for interleukin-6. Arterioscler Thromb Vasc Biol 2001, 21:1464-1469.
101. Han Y., Runge M.S., 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 1999, 84:695-703.
102. Brasier A.R., Jamaluddin M., Han Y., Patterson C., 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 2000, 212:155-169.
103. Ikeda U., Ikeda M., Oohara T., Oguchi A., Kamitani T., Tsuruya Y., et al. Interleukin 6 stimulates growth of vascular smooth muscle cells in a PDGF-dependent manner. Am J Physiol 1991, 260:H1713-H1717.
104. Galis Z.S., Khatri J.J. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002, 90:251-262.
105. Chen J., Li D., Schaefer R.F., 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 2004, 44:446-452.