Increased epidermal growth factor-like ligands are associated with elevated vascular nicotinamide adenine dinucleotide phosphate oxidase in a primate model of atherosclerosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 10, 2012, Pages 2452-2460

  Stanic, Bojana ^a   Pandey, Deepesh ^c   Fulton, David J ^c   Miller Jr , Francis J ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

atherosclerosis; cell signaling; epidermal growth factor receptor; nicotinamide adenine dinucleotide phosphate oxidases; smooth muscle cells

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; BLOOD LEVEL; CONTROLLED STUDY; CORRELATION ANALYSIS; CYNOMOLGUS MONKEY; ENZYME ACTIVITY; MACROPHAGE; MALE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANIMALS; ARTERIES; ATHEROSCLEROSIS; CELLS, CULTURED; DIET, ATHEROGENIC; DISEASE MODELS, ANIMAL; EPIDERMAL GROWTH FACTOR; LIGANDS; MACACA FASCICULARIS; MALE; MUSCLE, SMOOTH, VASCULAR; NADPH OXIDASE; SIGNAL TRANSDUCTION;

EID: 84866610710     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.256107     Document Type: Article

References (54)

1. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
2. Prenzel N, Fischer OM, Streit S, Hart S, Ullrich A. The epidermal growth factor receptor family as a central element for cellular signal transduc-tion and diversifcation. Endocr Relat Cancer. 2001;8:11-31.
3. Dreux AC, Lamb DJ, Modjtahedi H, Ferns GA. The epidermal growth factor receptors and their family of ligands: their putative role in athero-genesis. Atherosclerosis. 2006;186:38-53.
4. Takahashi M, Hayashi K, Yoshida K, Ohkawa Y, Komurasaki T, Kitabatake A, Ogawa A, Nishida W, Yano M, Monden M, Sobue K. Epiregulin as a major autocrine/paracrine factor released from ERK-and p38MAPK-activated vascular smooth muscle cells. Circulation. 2003;108:2524-2529.
5. Matsumoto S, Kishida K, Shimomura I, Maeda N, Nagaretani H, Matsuda M, Nishizawa H, Kihara S, Funahashi T, Matsuzawa Y, Yamada A, Yamashita S, Tamura S, Kawata S. Increased plasma HB-EGF associated with obesity and coronary artery disease. Biochem Biophys Res Commun. 2002;292:781-786.
6. Sánchez-Vizcaíno E, Vehí C, Campreciós G, Morcillo C, Soley M, Ramírez I. Heparin-binding EGF-like growth factor in human serum. Association with high blood cholesterol and heart hypertrophy. Growth Factors. 2010;28:98-103.
7. Chan AK, Kalmes A, Hawkins S, Daum G, Clowes AW. Blockade of the epidermal growth factor receptor decreases intimal hyperplasia in balloon-injured rat carotid artery. J Vasc Surg. 2003;37:644-649.
8. Zhang H, Sunnarborg SW, McNaughton KK, Johns TG, Lee DC, Faber JE. Heparin-binding epidermal growth factor-like growth factor signaling in fow-induced arterial remodeling. Circ Res. 2008;102: 1275-1285.
9. Kamata H, Shibukawa Y, Oka SI, Hirata H. Epidermal growth factor receptor is modulated by redox through multiple mechanisms. Effects of reductants and H2O2. Eur J Biochem. 2000;267:1933-1944.
10. Ushio-Fukai M, Griendling KK, Becker PL, Hilenski L, Halleran S, Alexander RW. Epidermal growth factor receptor transactivation by angiotensin II requires reactive oxygen species in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2001;21:489-495.
11. Miller FJ Jr, Chu X, Stanic B, Tian X, Sharma RV, Davisson RL, Lamb FS. A differential role for endocytosis in receptor-mediated activation of Nox1. Antioxid Redox Signal. 2010;12:583-593.
12. Stocker R, Keaney JF Jr. Role of oxidative modifcations in atherosclerosis. Physiol Rev. 2004;84:1381-1478.
13. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol. 2003;91(3A): 7A-11A.
14. Irani K. Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. Circ Res. 2000;87: 179-183.
15. Lassègue B, Clempus RE. Vascular NAD(P)H oxidases: specifc features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol. 2003;285:R277-R297.
16. Azumi H, Inoue N, Takeshita S, Rikitake Y, Kawashima S, Hayashi Y, Itoh H, Yokoyama M. Expression of NADH/NADPH oxidase p22phox in human coronary arteries. Circulation. 1999;100:1494-1498.
17. Sorescu D, Weiss D, Lassègue B, Clempus RE, Szöcs K, Sorescu GP, Valppu L, Quinn MT, Lambeth JD, Vega JD, Taylor WR, Griendling KK. Superoxide production and expression of nox family proteins in human atherosclerosis. Circulation. 2002;105:1429-1435.
18. Guzik TJ, Sadowski J, Guzik B, Jopek A, Kapelak B, Przybylowski P, Wierzbicki K, Korbut R, Harrison DG, Channon KM. Coronary artery superoxide production and nox isoform expression in human coronary artery disease. Arterioscler Thromb Vasc Biol. 2006;26:333-339.
19. Azumi H, Inoue N, Ohashi Y, et al. Superoxide generation in directional coronary atherectomy specimens of patients with angina pectoris: important role of NAD(P)H oxidase. Arterioscler Thromb Vasc Biol. 2002;22:1838-1844.
20. Hathaway CA, Heistad DD, Piegors DJ, Miller FJ Jr. Regression of atherosclerosis in monkeys reduces vascular superoxide levels. Circ Res. 2002;90:277-283.
21. Lassègue B, Griendling KK. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol. 2010;30:653-661.
22. Touyz RM, Chen X, Tabet F, Yao G, He G, Quinn MT, Pagano PJ, Schiffrin EL. Expression of a functionally active gp91phox-contain-ing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res. 2002;90:1205-1213.
23. Chlopicki S, Olszanecki R, Janiszewski M, Laurindo FR, Panz T, Miedzobrodzki J. Functional role of NADPH oxidase in activation of platelets. Antioxid Redox Signal. 2004;6:691-698.
24. Lee CF, Qiao M, Schröder K, Zhao Q, Asmis R. Nox4 is a novel induc-ible source of reactive oxygen species in monocytes and macrophages and mediates oxidized low density lipoprotein-induced macrophage death. Circ Res. 2010;106:1489-1497.
25. BelAiba RS, Djordjevic T, Petry A, Diemer K, Bonello S, Banf B, Hess J, Pogrebniak A, Bickel C, Görlach A. NOX5 variants are functionally active in endothelial cells. Free Radic Biol Med. 2007;42:446-459.
26. Jay DB, Papaharalambus CA, Seidel-Rogol B, Dikalova AE, Lassègue B, Griendling KK. Nox5 mediates PDGF-induced proliferation in human aortic smooth muscle cells. Free Radic Biol Med. 2008;45:329-335.
27. Stanic B, Katsuyama M, Miller FJ Jr. An oxidized extracellular oxidation-reduction state increases Nox1 expression and proliferation in vascular smooth muscle cells via epidermal growth factor receptor activation. Arterioscler Thromb Vasc Biol. 2010;30:2234-2241.
28. Armstrong ML, Heistad DD, Marcus ML, Piegors DJ, Abboud FM. Hemodynamic sequelae of regression of experimental atherosclerosis. J Clin Invest. 1983;71:104-113.
29. Lentz SR, Miller FJ Jr, Piegors DJ, Erger RA, Fernández JA, Griffn JH, Heistad DD. Anticoagulant responses to thrombin are enhanced during regression of atherosclerosis in monkeys. Circulation. 2002;106:842-846.
30. Miller FJ Jr, Gutterman DD, Rios CD, Heistad DD, Davidson BL. Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res. 1998;82:1298-1305.
31. Takapoo M, Chamseddine AH, Bhalla RC, Miller FJ Jr. Glutathione per-oxidase-defcient smooth muscle cells cause paracrine activation of normal smooth muscle cells via cyclophilin A. Vascul Pharmacol. 2011;55:143-148.
32. Baba I, Shirasawa S, Iwamoto R, Okumura K, Tsunoda T, Nishioka M, Fukuyama K, Yamamoto K, Mekada E, Sasazuki T. Involvement of deregulated epiregulin expression in tumorigenesis in vivo through activated Ki-Ras signaling pathway in human colon cancer cells. Cancer Res. 2000;60:6886-6889.
33. Hinkle CL, Sunnarborg SW, Loiselle D, Parker CE, Stevenson M, Russell WE, Lee DC. Selective roles for tumor necrosis factor alpha-converting enzyme/ADAM17 in the shedding of the epidermal growth factor receptor ligand family: the juxtamembrane stalk determines cleavage effciency. J Biol Chem. 2004;279:24179-24188.
34. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest. 2001;108:1513-1522.
35. Judkins CP, Diep H, Broughton BR, Mast AE, Hooker EU, Miller AA, Selemidis S, Dusting GJ, Sobey CG, Drummond GR. Direct evidence of a role for Nox2 in superoxide production, reduced nitric oxide bioavail-ability, and early atherosclerotic plaque formation in ApoE-/-mice. Am J Physiol Heart Circ Physiol. 2010;298:H24-H32.
36. Sheehan AL, Carrell S, Johnson B, Stanic B, Banf B, Miller FJ Jr. Role for Nox1 NADPH oxidase in atherosclerosis. Atherosclerosis. 2011;216:321-326.
37. Lee JG, Lim EJ, Park DW, Lee SH, Kim JR, Baek SH. A combination of Lox-1 and Nox1 regulates TLR9-mediated foam cell formation. Cell Signal. 2008;20:2266-2275.
38. Singh AB, Harris RC. Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell Signal. 2005;17:1183-1193.
39. Canault M, Peiretti F, Kopp F, Bonardo B, Bonzi MF, Coudeyre JC, Alessi MC, Juhan-Vague I, Nalbone G. The TNF alpha converting enzyme (TACE/ADAM17) is expressed in the atherosclerotic lesions of apolipoprotein E-defcient mice: possible contribution to elevated plasma levels of soluble TNF alpha receptors. Atherosclerosis. 2006;187: 82-91.
40. Oksala N, Levula M, Airla N, et al. ADAM-9, ADAM-15, and ADAM-17 are upregulated in macrophages in advanced human atherosclerotic plaques in aorta and carotid and femoral arteries-Tampere vascular study. Ann Med. 2009;41:279-290.
41. Donners MM, Wolfs IM, Olieslagers S, Mohammadi-Motahhari Z, Tchaikovski V, Heeneman S, van Buul JD, Caolo V, Molin DG, Post MJ, Waltenberger J. A disintegrin and metalloprotease 10 is a novel mediator of vascular endothelial growth factor-induced endothelial cell function in angiogenesis and is associated with atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30:2188-2195.
42. Abdallah RT, Keum JS, El-Shewy HM, Lee MH, Wang B, Gooz M, Luttrell DK, Luttrell LM, Jaffa AA. Plasma kallikrein promotes epidermal growth factor receptor transactivation and signaling in vascular smooth muscle through direct activation of protease-activated receptors. J Biol Chem. 2010;285:35206-35215.
43. Schröder K, Helmcke I, Palf K, Krause KH, Busse R, Brandes RP. Nox1 mediates basic fbroblast growth factor-induced migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2007;27: 1736-1743.
44. Lee MY, San Martin A, Mehta PK, Dikalova AE, Garrido AM, Datla SR, Lyons E, Krause KH, Banf B, Lambeth JD, Lassègue B, Griendling KK. Mechanisms of vascular smooth muscle NADPH oxidase 1 (Nox1) contribution to injury-induced neointimal formation. Arterioscler Thromb Vasc Biol. 2009;29:480-487.
45. Zimmerman MC, Takapoo M, Jagadeesha DK, Stanic B, Banf B, Bhalla RC, Miller FJ Jr. Activation of NADPH oxidase 1 increases intracel-lular calcium and migration of smooth muscle cells. Hypertension. 2011;58:446-453.
46. Matsuno K, Yamada H, Iwata K, Jin D, Katsuyama M, Matsuki M, Takai S, Yamanishi K, Miyazaki M, Matsubara H, Yabe-Nishimura C. Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-defcient mice. Circulation. 2005;112:2677-2685.
47. Gavazzi G, Banf B, Deffert C, Fiette L, Schappi M, Herrmann F, Krause KH. Decreased blood pressure in NOX1-defcient mice. FEBS Lett. 2006;580:497-504.
48. Szöcs K, Lassègue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002;22:21-27.
49. Kalinina N, Agrotis A, Tararak E, Antropova Y, Kanellakis P, Ilyinskaya O, Quinn MT, Smirnov V, Bobik A. Cytochrome b558-dependent NAD(P)H oxidase-phox units in smooth muscle and macrophages of atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2002;22: 2037-2043.
50. Guzik TJ, Chen W, Gongora MC, Guzik B, Lob HE, Mangalat D, Hoch N, Dikalov S, Rudzinski P, Kapelak B, Sadowski J, Harrison DG. Calcium-dependent NOX5 nicotinamide adenine dinucleotide phosphate oxidase contributes to vascular oxidative stress in human coronary artery disease. J Am Coll Cardiol. 2008;52:1803-1809.
51. Fan C, Katsuyama M, Nishinaka T, Yabe-Nishimura C. Transactivation of the EGF receptor and a PI3 kinase-ATF-1 pathway is involved in the upregulation of NOX1, a catalytic subunit of NADPH oxidase. FEBS Lett. 2005;579:1301-1305.
52. Adachi Y, Shibai Y, Mitsushita J, Shang WH, Hirose K, Kamata T. Oncogenic Ras upregulates NADPH oxidase 1 gene expression through MEK-ERK-dependent phosphorylation of GATA-6. Oncogene. 2008;27:4921-4932.
53. Sancho P, Fabregat I. NADPH oxidase NOX1 controls autocrine growth of liver tumor cells through up-regulation of the epidermal growth factor receptor pathway. J Biol Chem. 2010;285:24815-24824.
54. Busser B, Sancey L, Brambilla E, Coll JL, Hurbin A. The multiple roles of amphiregulin in human cancer. Biochim Biophys Acta. 2011;1816:119-131.