Aldosterone enhances IGF-I-mediated signaling and biological function in vascular smooth muscle cells

Endocrinology

Volumn 151, Issue 12, 2010, Pages 5851-5864

  Cascella, Teresa ^a   Radhakrishnan, Yashwanth ^a   Maile, Laura A ^a   Busby Jr , Walker H ^a   Gollahon, Katherine ^a   Colao, Annamaria ^b   Clemmons, David R ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ALDOSTERONE; DACTINOMYCIN; EPLERENONE; INSULIN RECEPTOR SUBSTRATE 1; MINERALOCORTICOID RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOPONTIN; P70S6 KINASE; PROTEIN KINASE; PROTEIN KINASE B; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; GENETIC TRANSCRIPTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SWINE; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ALDOSTERONE; ANIMALS; AORTA; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; INSULIN-LIKE GROWTH FACTOR I; INTEGRIN ALPHAVBETA3; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OSTEOPONTIN; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; SWINE;

EID: 78649888159     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0350     Document Type: Article

References (49)

1. Delafontaine P, Song YH, Li Y 2004 Expression, regulation, and function of IGF-1, IGF-1R, and IGF-1 binding proteins in blood vessels. Arterioscler Thromb Vasc Biol 24:435-444
2. Fath KA, Alexander RW, Delafontaine P 1993 Abdominal coarctation increases insulin-like growth factor I mRNA levels in rat aorta. Circ Res 72:271-277
3. Maile LA, Busby WH, Sitko K, Capps BE, Sergent T, Badley-Clarke J, Clemmons DR 2006 Insulin-like growth factor-I signaling in smooth muscle cells is regulated by ligand binding to the 177CYDMKTTC184 sequence of the β3-subunit of αVβ3. Mol Endocrinol 20:405-413
4. Xi G, Maile LA, Yoo SE, Clemmons DR 2008 Expression of the human β3 integrin subunit in mouse smooth muscle cells enhances IGF-I-stimulated signaling and proliferation. J Cell Physiol 214:306-315
5. Nichols TC, du Laney T, Zheng B, Bellinger DA, Nickols GA, Engleman W, Clemmons DR 1999 Reduction in atherosclerotic lesion size in pigs by αVβ3 inhibitors is associated with inhibition of insulin-like growth factor-I-mediated signaling. Circ Res 85:1040-1045
6. Pitt B, Zannad F, Remme WJ, Cody R, Castaigne A, Perez A, Palensky J, Wittes J 1999 The effect of spironolactone on morbidity and mortality in patients with severe heart failure. Randomized Aldactone Evaluation Study Investigators. N Engl J Med 341:709-717
7. Giachelli CM, Bae N, Almeida M, Denhardt DT, Alpers CE, Schwartz SM 1993 Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. J Clin Invest 92:1686-1696
8. Han M, Wen JK, Zheng B, Liu Z, Chen Y 2007 Blockade of integrin β3-FAK signaling pathway activated by osteopontin inhibits neointimal formation after balloon injury. Cardiovasc Pathol 16:283-290
9. Sodhi P, Phadke SA, Battle D, Sahai A 2001 Hypoxia stimulates osteopontin expression and proliferation of cultured vascular smooth muscle cells: proliferation by high glucose. Diabetes 50: 1482-1460
10. Isoda K, Nishikawa K, Kamezawa Y, Yoshida M, Kusuhara M, Moroi M, Tada N, Ohsuzu F 2002 Osteopontin plays and important role in the development of medial thickening and neointimal formation. Circ Res 91:77-82
11. Kurata M, Okura T, Watanabe S, Fukuoka T, Higaki J 2006 Osteopontin and carotid atherosclerosis in patients with essential hypertension. Clin Sci (Lond) 111:319-324
12. Pitt B, Williams G, Remme W, Martinez F, Lopez-Sendon J, Zannad F, Neaton J, Roniker B, Hurley S, Burns D, Bittman R, Kleiman J 2001 The EPHESUS trial: eplerenone in patients with heart failure due to systolic dysfunction complicating acute myocardial infarction. Eplerenone Post-AMI Heart Failure Efficacy and Survival Study. Cardiovasc Drugs Ther 15:79-87
13. Struthers AD 2002 Aldosterone: cardiovascular assault. Am Heart J 144:S2-S7
14. Park JB, Schiffrin EL 2002 Cardiac and vascular fibrosis and hypertrophy in aldosterone-infused rats: role of endothelin-1. Am J Hypertens 15:164-169
15. Miyata K, Hitomi H, Guo P, Zhang GX, Kimura S, Kiyomoto H, Hosomi N, Kagami S, Kohno M, Nishiyama A 2008 Possible involvement of Rho-kinase in aldosterone-induced vascular smooth muscle cell remodeling. Hypertens Res 31:1407-1413
16. Zhang A, Jia Z, Guo X, Yang T 2007 Aldosterone induces epithelial-mesenchymal transition via ROS of mitochondrial origin. Am J Physiol Renal Physiol 293:F723-F731
17. Cooper SA, Whaley-Connell A, Habibi J, Wei Y, Lastra G, Manrique C, Stas S, Sowers JR 2007 Renin-angiotensin-aldosterone system and oxidative stress in cardiovascular insulin resistance. Am J Physiol Heart Circ Physiol 293:H2009-H2023
18. Miyata K, Rahman M, Shokoji T, Nagai Y, Zhang GX, Sun GP, Kimura S, Yukimura T, Kiyomoto H, Kohno M, Abe Y, Nishiyama A 2005 Aldosterone stimulates reactive oxygen species production through activation of NADPH oxidase in rat mesangial cells. J Am Soc Nephrol 16:2906-2912
19. Dorrance AM, Osborn HL, Grekin R, Webb RC 2001 Spironolactone reduces cerebral infarct size and EGF-receptor mRNA in stroke-prone rats. Am J Physiol Regul Integr Comp Physiol 281: R944-R950
20. Grossmann C, Gekle M 2008 Nongenotropic aldosterone effects and the EGFR: interaction and biological relevance. Steroids 73: 973-978
21. Grossmann C, Krug AW, Freudinger R, Mildenberger S, Voelker K, Gekle M 2007 Aldosterone-induced EGFR expression: interaction between the human mineralocorticoid receptor and the human EGFR promoter. Am J Physiol Endocrinol Metab 292:E1790-E1800
22. Holzman JL, Liu L, Duke BJ, Kemendy AE, Eaton DC 2007 Transactivation of the IGF-1R by aldosterone. Am J Physiol Renal Physiol 292:F1219-F1228
23. Maile LA, Capps BE, Ling Y, Xi G, Clemmons DR 2007 Hyperglycemia alters the responsiveness of smooth muscle cells to insulinlike growth factor-I. Endocrinology 148:2435-2443
24. Stas S, Whaley-Connell A, Habibi J, Appesh L, Hayden MR, Karuparthi PR, Qazi M, Morris EM, Cooper SA, Link CD, Stump C, Hay M, Ferrario C, Sowers JR 2007 Mineralocorticoid receptor blockade attenuates chronic overexpression of the renin-angiotensin-aldosterone system stimulation of reduced nicotinamide adenine dinucleotide phosphate oxidase and cardiac remodeling. Endocrinology 148:3773-3780
25. Maile LA, Busby WH, Sitko K, Capps BE, Sergent T, Badley-Clarke J, Ling Y, Clemmons DR 2006 The heparin binding domain of vitronectin is the region that is required to enhance insulin-like growth factor-I signaling. Mol Endocrinol 20:881-892
26. Gockerman A, Prevette T, Jones JI, Clemmons DR 1995 Insulin-like growth factor (IGF)-binding proteins inhibit the smooth muscle cell migration responses to IGF-I and IGF-II. Endocrinology 136:4168-41473
27. Zheng B, Clemmons DR 1998 Blocking ligand occupancy of the αVβ3 integrin inhibits insulin-like growth factor I signaling in vascular smooth muscle cells. Proc Natl Acad Sci USA 95:11217-11222
28. Ling Y, Maile LA, Clemmons DR 2003 Tyrosine phosphorylation of the β3-subunit of the αVβ3 integrin is required for membrane association of the tyrosine phosphatase SHP-2 and its further recruitment to the insulin-like growth factor I receptor. Mol Endocrinol 17:1824-1833
29. Gao L, Mann GE 2009 Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling. Cardiovasc Res 82:9-20
30. Busik JV, Mohr S, Grant MB 2008 Hyperglycemia-induced reactive oxygen species toxicity to endothelial cells is dependent on paracrine mediators. Diabetes 57:1952-1965
31. Bunda S, Liu P, Wang Y, Liu K, Hinek A 2007 Aldosterone induces elastin production in cardiac fibroblasts through activation of insulin-like growth factor-I receptors in a mineralocorticoid receptorindependent manner. Am J Pathol 171:809-819
32. Wolfe BL, Rich CB, Goud HD, Terpstra AJ, Bashir M, Rosenbloom J, Sonenshein GE, Foster JA 1993 Insulin-like growth factor-I regulates transcription of the elastin gene. J Biol Chem 268:12418-12426
33. Marney AM, Brown NJ 2007 Aldosterone and end organ damage. Clin Sci 133:267-278
34. Ma Y, Zhang L, Peng T, Cheng J, Taneja S, Zhang J, Delafontaine P, Du J 2006 Angiotensin II stimulates transcription of insulin-like growth factor I receptor in vascular smooth muscle cells: role of nuclear factor-κB. Endocrinology 147:1256-1263
35. Hitomi H, Kiyomoto H, Nishiyama A, Hara T, Moriwaki K, Kaifu K, Ihara G, Fujita Y, Ugawa T, Kohno M 2007 Aldosterone suppresses insulin signaling via the downregulation of insulin receptor substrate-1 in vascular smooth muscle cells. Hypertension 50:750-755
36. Renström F, Burén J, Eriksson JW 2005 Insulin receptor substrates-1 and -2 are both depleted but via different mechanisms after down-regulation of glucose transport in rat adipocytes. Endocrinology 146:3044-3051
37. Kim B, Feldman EL 2009 Insulin receptor substrate (IRS)-2, not IRS-1, protects human neuroblastoma cells against apoptosis. Apoptosis 14:665-673
38. Radhakrishnan Y, Busby Jr WH, Shen X, Maile LA, Clemmons DR 2010 Insulin-like growth factor-1 (IGF-I) stimulated insulin receptor substrate-1 negatively regulates Src homology 2 domain-containing protein-tyrosine phosphatase substrate-1 function in vascular smooth muscle cells. J Biol Chem 285:15682-15695
39. Irita J, Okura T, Kurata M, Miyoshi K, Fukuoka T, Higaki J 2008 Osteopontin in rat renal fibroblasts: functional properties and transcriptional regulation by aldosterone. Hypertension 51:507-513
40. Sugiyama T, Yoshimoto T, Hirono Y, Suzuki N, Sakurada M, Tsuchiya K, Minami I, Iwashima F, Sakai H, Tateno T, Sato R, Hirata Y 2005 Aldosterone increases osteopontin gene expression in rat endothelial cells. Biochem Biophys Res Commun 336:163-167
41. Gauer S, Hauser IA, Obermüller N, Holzmann Y, Geiger H, Goppelt-Struebe M 2008 Synergistic induction of osteopontin by aldosterone and inflammatory cytokines in mesangial cells. J Cell Biochem 103:615-623
42. Zhang YL, Zhou SX, Lei J, Yuan GY, Wang JF 2008 Blockades of angiotensin and aldosterone reduce osteopontin expression and interstitial fibrosis infiltration in rats with myocardial infarction. Chin Med J 121:2192-2196
43. Sakurabayashi-Kitade S, Aoka Y, Nagashima H, Kasanuki H, Hagiwara N, Kawana M 2009 Aldosterone blockade by Spironolactone improves the hypertensive vascular hypertrophy and remodeling in angiotensin II overproducing transgenic mice. Atherosclerosis 206:54-60
44. Sam F, Xie Z, Ooi H, Kerstetter DL, Colucci WS, Singh M, Singh K 2004 Mice lacking osteopontin exhibit increased left ventricular dilation and reduced fibrosis after aldosterone infusion. Am J Hypertens 17:188-193
45. Irita J, Okura T, Manabe S, Kurata M, Miyoshi K, Watanabe S, Fukuoka T, Higaki J 2006 Plasma osteopontin levels are higher in patients with primary aldosteronism than in patients with essential hypertension. Am J Hypertens 19:293-297
46. Sun J, Xu Y, Dai Z, Sun Y 2009 Intermittent high glucose enhances proliferation of vascular smooth muscle cells by upregulating osteopontin. Mol Cell Endocrinol 313:64-69
47. Virdis A, Neves MF, Amiri F, Viel E, Touyz RM, Schiffrin EL 2002 Spironolactone improves angiotensin-induced vascular changes and oxidative stress. Hypertension 40:504-510
48. Keidar S, Kaplan M, Pavlotzky E, Coleman R, Hayek T, Hamoud S, Aviram M 2004 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 109:2213-2220
49. Maron BA, Zhang YY, Handy DE, Beuve A, Tang SS, Loscalzo J, Leopold JA 2009 Aldosterone increases oxidant stress to impair guanylyl cyclase activity by cysteinyl thiol oxidation in vascular smooth muscle cells. J Biol Chem 284:7665-7672