Role of Epidermal Growth Factor Receptor and Endoplasmic Reticulum Stress in Vascular Remodeling Induced by Angiotensin II

Hypertension

Volumn 65, Issue 6, 2015, Pages 1349-1355

  Takayanagi, Takehiko ^a   Kawai, Tatsuo ^a   Forrester, Steven J ^a,b   Obama, Takashi ^a   Tsuji, Toshiyuki ^a   Fukuda, Yamato ^a   Elliott, Katherine J ^a   Tilley, Douglas G ^a   Davisson, Robin L ^c   Park, Joon Young ^a,b   Eguchi, Satoru ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY   (United States)

^c Cornell University College of Veterinary Medicine ^*  (United States)

Author keywords

angiotensin II; fibrosis; hypertension; hypertrophy; muscle, smooth, vascular; signal transduction

Indexed keywords

4 PHENYLBUTYRIC ACID; ADAM PROTEIN; ADAM17 PROTEIN; ANGIOTENSIN II; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; UNCLASSIFIED DRUG; 4-PHENYLBUTYRIC ACID; ARYLBUTYRIC ACID DERIVATIVE; QUINAZOLINE DERIVATIVE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA DISEASE; AORTA HYPERTROPHY; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HEART HYPERTROPHY; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HYPERTENSION; KIDNEY HYPERTROPHY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VASCULAR REMODELING; VASCULARIZATION; ANIMAL; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; GENETICS; HYPERTROPHY; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZATION; ROLE PLAYING; SENSITIVITY AND SPECIFICITY; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

ADAM PROTEINS; ANGIOTENSIN II; ANIMALS; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; ENDOTHELIUM, VASCULAR; ERLOTINIB HYDROCHLORIDE; HYPERTENSION; HYPERTROPHY; MICE; MUSCLE, SMOOTH, VASCULAR; PHENYLBUTYRATES; QUINAZOLINES; RANDOM ALLOCATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; ROLE; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; VASCULAR REMODELING;

EID: 84937604799     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.115.05344     Document Type: Article

References (41)

1. Kang N, Walther T, Tian XL, Bohlender J, Fukamizu A, Ganten D, Bader M. Reduced hypertension-induced end-organ damage in mice lacking cardiac and renal angiotensinogen synthesis. J Mol Med (Berl). 2002;80:359-366. doi: 10.1007/s00109-002-0326-6.
2. Gibbons GH. Angiotensin-converting enzyme inhibition and vascular structure in hypertension. J Cardiovasc Pharmacol. 1991;18 Suppl 7:S19-S24.
3. Briet M, Schiffrin EL. Treatment of arterial remodeling in essential hypertension. Curr Hypertens Rep. 2013;15:3-9. doi: 10.1007/s11906-012-0325-0.
4. Kanaide H, Ichiki T, Nishimura J, Hirano K. Cellular mechanism of vasoconstriction induced by angiotensin II: it remains to be determined. Circ Res. 2003;93:1015-1017. doi: 10.1161/01.RES.0000105920.33926.60.
5. Ohtsu H, Dempsey PJ, Frank GD, Brailoiu E, Higuchi S, Suzuki H, Nakashima H, Eguchi K, Eguchi S. ADAM17 mediates epidermal growth factor receptor transactivation and vascular smooth muscle cell hypertrophy induced by angiotensin II. Arterioscler Thromb Vasc Biol. 2006;26:e133-e137. doi: 10.1161/01.ATV.0000236203.90331.d0.
6. Ohtsu H, Higuchi S, Shirai H, Eguchi K, Suzuki H, Hinoki A, Brailoiu E, Eckhart AD, Frank GD, Eguchi S. Central role of Gq in the hypertrophic signal transduction of angiotensin II in vascular smooth muscle cells. Endocrinology. 2008;149:3569-3575. doi: 10.1210/en.2007-1694.
7. Elliott KJ, Bourne AM, Takayanagi T, Takaguri A, Kobayashi T, Eguchi K, Eguchi S. ADAM17 silencing by adenovirus encoding miRNAembedded siRNA revealed essential signal transduction by angiotensin II in vascular smooth muscle cells. J Mol Cell Cardiol. 2013;62:1-7. doi: 10.1016/j.yjmcc.2013.05.005.
8. Takaguri A, Kimura K, Hinoki A, Bourne AM, Autieri MV, Eguchi S. A disintegrin and metalloprotease 17 mediates neointimal hyperplasia in vasculature. Hypertension. 2011;57:841-845. doi: 10.1161/HYPERTENSIONAHA.110.166892.
9. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res. 2002;91:406-413.
10. Kagiyama S, Eguchi S, Frank GD, Inagami T, Zhang YC, Phillips MI. Angiotensin II-induced cardiac hypertrophy and hypertension are attenuated by epidermal growth factor receptor antisense. Circulation. 2002;106:909-912.
11. Wang X, Oka T, Chow FL, Cooper SB, Odenbach J, Lopaschuk GD, Kassiri Z, Fernandez-Patron C. Tumor necrosis factor-alpha-converting enzyme is a key regulator of agonist-induced cardiac hypertrophy and fibrosis. Hypertension. 2009;54:575-582. doi: 10.1161/HYPERTENSIONAHA.108.127670.
12. Zhai P, Galeotti J, Liu J, Holle E, Yu X, Wagner T, Sadoshima J. An angiotensin II type 1 receptor mutant lacking epidermal growth factor receptor transactivation does not induce angiotensin II-mediated cardiac hypertrophy. Circ Res. 2006;99:528-536. doi: 10.1161/01. RES.0000240147.49390.61.
13. Steins M, Thomas M, Geisler M. Erlotinib. Recent Results Cancer Res. 2014;201:109-123. doi: 10.1007/978-3-642-54490-3-6.
14. Tabas I. The role of endoplasmic reticulum stress in the progression of atherosclerosis. Circ Res. 2010;107:839-850. doi: 10.1161/CIRCRESAHA.110.224766.
15. Minamino T, Komuro I, Kitakaze M. Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res. 2010;107:1071-1082. doi: 10.1161/CIRCRESAHA.110.227819.
16. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature. 2008;454:455-462. doi: 10.1038/nature07203.
17. Santos CX, Tanaka LY, Wosniak J, Laurindo FR. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal. 2009;11:2409-2427. doi: 10.1089/ARS.2009.2625.
18. Okada K, Minamino T, Tsukamoto Y, et al. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation. 2004;110:705-712. doi: 10.1161/01. CIR.0000137836.95625.D4.
19. Kassan M, Galán M, Partyka M, Saifudeen Z, Henrion D, Trebak M, Matrougui K. Endoplasmic reticulum stress is involved in cardiac damage and vascular endothelial dysfunction in hypertensive mice. Arterioscler Thromb Vasc Biol. 2012;32:1652-1661. doi: 10.1161/ATVBAHA.112.249318.
20. Young CN, Cao X, Guruju MR, Pierce JP, Morgan DA, Wang G, Iadecola C, Mark AL, Davisson RL. ER stress in the brain subfornical organ mediates angiotensin-dependent hypertension. J Clin Invest. 2012;122:3960-3964. doi: 10.1172/JCI64583.
21. Galán M, Kassan M, Choi SK, Partyka M, Trebak M, Henrion D, Matrougui K. A novel role for epidermal growth factor receptor tyrosine kinase and its downstream endoplasmic reticulum stress in cardiac damage and microvascular dysfunction in type 1 diabetes mellitus. Hypertension. 2012;60:71-80. doi: 10.1161/HYPERTENSIONAHA.112.192500.
22. Schreier B, Rabe S, Schneider B, Bretschneider M, Rupp S, Ruhs S, Neumann J, Rueckschloss U, Sibilia M, Gotthardt M, Grossmann C, Gekle M. Loss of epidermal growth factor receptor in vascular smooth muscle cells and cardiomyocytes causes arterial hypotension and cardiac hypertrophy. Hypertension. 2013;61:333-340. doi: 10.1161/HYPERTENSIONAHA.112.196543.
23. Melenhorst WB, Visser L, Timmer A, van den Heuvel MC, Stegeman CA, van Goor H. ADAM17 upregulation in human renal disease: a role in modulating TGF-alpha availability? Am J Physiol Renal Physiol. 2009;297:F781-F790. doi: 10.1152/ajprenal.90610.2008.
24. Chen J, Chen JK, Nagai K, Plieth D, Tan M, Lee TC, Threadgill DW, Neilson EG, Harris RC. EGFR signaling promotes TGFβ-dependent renal fibrosis. J Am Soc Nephrol. 2012;23:215-224. doi: 10.1681/ASN.2011070645.
25. Lian H, Ma Y, Feng J, Dong W, Yang Q, Lu D, Zhang L. Heparin-binding EGF-like growth factor induces heart interstitial fibrosis via an Akt/mTor/p70s6k pathway. PLoS One. 2012;7:e44946. doi: 10.1371/journal. pone.0044946.
26. Keys JR, Greene EA, Koch WJ, Eckhart AD. Gq-coupled receptor agonists mediate cardiac hypertrophy via the vasculature. Hypertension. 2002;40:660-666.
27. Liu X, Kwak D, Lu Z, Xu X, Fassett J, Wang H, Wei Y, Cavener DR, Hu X, Hall J, Bache RJ, Chen Y. Endoplasmic reticulum stress sensor protein kinase R-like endoplasmic reticulum kinase (PERK) protects against pressure overload-induced heart failure and lung remodeling. Hypertension. 2014;64:738-744. doi: 10.1161/HYPERTENSIONAHA.114.03811.
28. Noma T, Lemaire A, Naga Prasad SV, Barki-Harrington L, Tilley DG, Chen J, Le Corvoisier P, Violin JD, Wei H, Lefkowitz RJ, Rockman HA. Beta-arrestin-mediated beta1-adrenergic receptor transactivation of the EGFR confers cardioprotection. J Clin Invest. 2007;117:2445-2458. doi: 10.1172/JCI31901.
29. Grisanti LA, Talarico JA, Carter RL, Yu JE, Repas AA, Radcliffe SW, Tang HA, Makarewich CA, Houser SR, Tilley DG. β-Adrenergic receptor-mediated transactivation of epidermal growth factor receptor decreases cardiomyocyte apoptosis through differential subcellular activation of ERK1/2 and Akt. J Mol Cell Cardiol. 2014;72:39-51. doi: 10.1016/j. yjmcc.2014.02.009.
30. Grisanti LA, Repas AA, Talarico JA, Gold JI, Carter RL, Koch WJ, Tilley DG. Temporal and gefitinib-sensitive regulation of cardiac cytokine expression via chronic β-adrenergic receptor stimulation. Am J Physiol Heart Circ Physiol. 2015;308:H316-H330. doi: 10.1152/ajpheart.00635.2014.
31. Spitler KM, Webb RC. Endoplasmic reticulum stress contributes to aortic stiffening via proapoptotic and fibrotic signaling mechanisms. Hypertension. 2014;63:e40-e45. doi: 10.1161/HYPERTENSIONAHA.113.02558.
32. Liang B, Wang S, Wang Q, Zhang W, Viollet B, Zhu Y, Zou MH. Aberrant endoplasmic reticulum stress in vascular smooth muscle increases vascular contractility and blood pressure in mice deficient of AMP-activated protein kinase-α2 in vivo. Arterioscler Thromb Vasc Biol. 2013;33:595-604 . doi: 10.1161/ATVBAHA.112.300606.
33. Iwasaki H, Eguchi S, Ueno H, Marumo F, Hirata Y. Mechanical stretch stimulates growth of vascular smooth muscle cells via epidermal growth factor receptor. Am J Physiol Heart Circ Physiol. 2000;278:H521-H529.
34. Cheng WP, Hung HF, Wang BW, Shyu KG. The molecular regulation of GADD153 in apoptosis of cultured vascular smooth muscle cells by cyclic mechanical stretch. Cardiovasc Res. 2008;77:551-559. doi: 10.1093/cvr/cvm057.
35. Rzymski T, Petry A, Kra?un D, Ries F, Pike L, Harris AL, Görlach A. The unfolded protein response controls induction and activation of ADAM17/TACE by severe hypoxia and ER stress. Oncogene. 2012;31:3621-3634. doi: 10.1038/onc.2011.522.
36. Obama T, Tsuji T, Kobayashi T, Fukuda Y, Takayanagi T, Taro Y, Kawai T, Forrester SJ, Elliott KJ, Choi E, Daugherty A, Rizzo V, Eguchi S. Epidermal growth factor receptor inhibitor protects against abdominal aortic aneurysm in a mouse model. Clin Sci (Lond). 2015;128:559-565. doi: 10.1042/CS20140696.
37. Obama T, Takayanagi T, Kobayashi T, Bourne AM, Elliott KJ, Charbonneau M, Dubois CM, Eguchi S. Vascular induction of a disintegrin and metalloprotease 17 by angiotensin II through hypoxia inducible factor 1α. Am J Hypertens. 2015;28:10-14. doi: 10.1093/ajh/hpu094.
38. Lauzier MC, Pagé EL, Michaud MD, Richard DE. Differential regulation of hypoxia-inducible factor-1 through receptor tyrosine kinase transactivation in vascular smooth muscle cells. Endocrinology. 2007;148:4023-4031. doi: 10.1210/en.2007-0285.
39. Pereira ER, Frudd K, Awad W, Hendershot LM. Endoplasmic reticulum (ER) stress and hypoxia response pathways interact to potentiate hypoxiainducible factor 1 (HIF-1) transcriptional activity on targets like vascular endothelial growth factor (VEGF). J Biol Chem. 2014;289:3352-3364. doi: 10.1074/jbc.M113.507194.
40. Luther JM, Luo P, Wang Z, Cohen SE, Kim HS, Fogo AB, Brown NJ. Aldosterone deficiency and mineralocorticoid receptor antagonism prevent angiotensin II-induced cardiac, renal, and vascular injury. Kidney Int. 2012;82:643-651. doi: 10.1038/ki.2012.170.
41. Griol-Charhbili V, Fassot C, Messaoudi S, Perret C, Agrapart V, Jaisser F. Epidermal growth factor receptor mediates the vascular dysfunction but not the remodeling induced by aldosterone/salt. Hypertension. 2011;57:238-244. doi: 10.1161/HYPERTENSIONAHA.110.153619.