Canonical Wnt signaling induces vascular endothelial dysfunction via p66Shc-regulated reactive oxygen species

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 34, Issue 10, 2014, Pages 2301-2309

  Vikram, Ajit ^a   Kim, Young Rae ^a   Kumar, Santosh ^a   Naqvi, Asma ^b   Hoffman, Timothy A ^c   Kumar, Ajay ^b   Miller, Francis J ^a   Kim, Cuk Seong ^d   Irani, Kaikobad ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

^d Chungnam National University   (South Korea)

Author keywords

Endothelial cells; Oxidation reduction; p66Shc protein; Reactive oxygen species; Wnt signaling pathway

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ACETYLCYSTEINE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; BETA CATENIN; CATALASE; HYDROGEN PEROXIDE; NITRIC OXIDE; NITROPRUSSIDE SODIUM; PROTEIN P66; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SHORT HAIRPIN RNA; TUMOR NECROSIS FACTOR ALPHA; WNT3A PROTEIN; CTNNB1 PROTEIN, HUMAN; CTNNB1 PROTEIN, MOUSE; PROTEIN SHC; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SHC1 PROTEIN, HUMAN; SHC1 PROTEIN, MOUSE; VASODILATOR AGENT; WNT3A PROTEIN, HUMAN; WNT3A PROTEIN, MOUSE;

ANIMAL EXPERIMENT; AORTA; ARTICLE; BIOAVAILABILITY; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LIPID DIET; MONOCYTE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; VASCULAR ENDOTHELIAL DYSFUNCTION; VASODILATATION; WNT SIGNALING PATHWAY; ANIMAL; BOVINAE; C57BL MOUSE; COCULTURE; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HEK293 CELL LINE; HYPERLIPIDEMIA; METABOLISM; PATHOPHYSIOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; TRANSGENIC MOUSE; U937 CELL LINE;

ANIMALS; AORTA; BETA CATENIN; CATTLE; COCULTURE TECHNIQUES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPERLIPIDEMIAS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NADPH OXIDASE; OXIDATIVE STRESS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SHC SIGNALING ADAPTOR PROTEINS; TRANSFECTION; U937 CELLS; VASODILATION; VASODILATOR AGENTS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84913600621     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304338     Document Type: Article

References (51)

1. Cadigan KM, Peifer M. Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol. 2009;1:a002881.
2. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol. 2004;20:781-810.
3. MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell. 2009;17:9-26.
4. Magoori K, Kang MJ, Ito MR, et al. Severe hypercholesterolemia, impaired fat tolerance, and advanced atherosclerosis in mice lacking both low density lipoprotein receptor-related protein 5 and apolipoprotein E. J Biol Chem. 2003;278:11331-11336.
5. Mani A, Radhakrishnan J, Wang H, Mani A, Mani MA, Nelson-Williams C, Carew KS, Mane S, Najmabadi H, Wu D, Lifton RP. LRP6 mutation in a family with early coronary disease and metabolic risk factors. Science. 2007;315:1278-1282.
6. Sarzani R, Salvi F, Bordicchia M, Guerra F, Battistoni I, Pagliariccio G, Carbonari L, Dessì-Fulgheri P, Rappelli A. Carotid artery atherosclerosis in hypertensive patients with a functional LDL receptor-related protein 6 gene variant. Nutr Metab Cardiovasc Dis. 2011;21:150-156.
7. Goodwin AM, Sullivan KM, D'Amore PA. Cultured endothelial cells display endogenous activation of the canonical Wnt signaling pathway and express multiple ligands, receptors, and secreted modulators of Wnt signaling. Dev Dyn. 2006;235:3110-3120.
8. Wright M, Aikawa M, Szeto W, Papkoff J. Identification of a Wntresponsive signal transduction pathway in primary endothelial cells. Biochem Biophys Res Commun. 1999;263:384-388.
9. Liu H, Fergusson MM, Castilho RM, Liu J, Cao L, Chen J, Malide D, Rovira II, Schimel D, Kuo CJ, Gutkind JS, Hwang PM, Finkel T. Augmented Wnt signaling in a mammalian model of accelerated aging. Science. 2007;317:803-806.
10. Marchand A, Atassi F, Gaaya A, Leprince P, Le Feuvre C, Soubrier F, Lompré AM, Nadaud S. The Wnt/beta-catenin pathway is activated during advanced arterial aging in humans. Aging Cell. 2011;10:220-232.
11. Funato Y, Michiue T, Asashima M, Miki H. The thioredoxin-related redoxregulating protein nucleoredoxin inhibits Wnt-beta-catenin signalling through dishevelled. Nat Cell Biol. 2006;8:501-508.
12. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L, Pelicci PG. The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature. 1999;402:309-313.
13. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science. 2002;295:2450-2452.
14. Berniakovich I, Trinei M, Stendardo M, Migliaccio E, Minucci S, Bernardi P, Pelicci PG, Giorgio M. p66Shc-generated oxidative signal promotes fat accumulation. J Biol Chem. 2008;283:34283-34293.
15. Kim CS, Jung SB, Naqvi A, Hoffman TA, DeRicco J, Yamamori T, Cole MP, Jeon BH, Irani K. p53 impairs endothelium-dependent vasomotor function through transcriptional upregulation of p66shc. Circ Res. 2008;103:1441-1450.
16. Kim CS, Kim YR, Naqvi A, Kumar S, Hoffman TA, Jung SB, Kumar A, Jeon BH, McNamara DM, Irani K. Homocysteine promotes human endothelial cell dysfunction via site-specific epigenetic regulation of p66shc. Cardiovasc Res. 2011;92:466-475.
17. Kim YR, Kim CS, Naqvi A, Kumar A, Kumar S, Hoffman TA, Irani K. Epigenetic upregulation of p66shc mediates low-density lipoprotein cholesterol- induced endothelial cell dysfunction. Am J Physiol Heart Circ Physiol. 2012;303:H189-H196.
18. Yamamori T, DeRicco J, Naqvi A, Hoffman TA, Mattagajasingh I, Kasuno K, Jung SB, Kim CS, Irani K. SIRT1 deacetylates APE1 and regulates cellular base excision repair. Nucleic Acids Res. 2010;38:832-845.
19. Zhou S, Chen HZ, Wan YZ, Zhang QJ, Wei YS, Huang S, Liu JJ, Lu YB, Zhang ZQ, Yang RF, Zhang R, Cai H, Liu DP, Liang CC. Repression of P66Shc expression by SIRT1 contributes to the prevention of hyperglycemia- induced endothelial dysfunction. Circ Res. 2011;109:639-648.
20. Martin-Padura I, de Nigris F, Migliaccio E, Mansueto G, Minardi S, Rienzo M, Lerman LO, Stendardo M, Giorgio M, De Rosa G, Pelicci PG, Napoli C. p66Shc deletion confers vascular protection in advanced atherosclerosis in hypercholesterolemic apolipoprotein E knockout mice. Endothelium. 2008;15:276-287.
21. Franzeck FC, Hof D, Spescha RD, Hasun M, Akhmedov A, Steffel J, Shi Y, Cosentino F, Tanner FC, von Eckardstein A, Maier W, Lüscher TF, Wyss CA, Camici GG. Expression of the aging gene p66Shc is increased in peripheral blood monocytes of patients with acute coronary syndrome but not with stable coronary artery disease. Atherosclerosis. 2012;220:282-286.
22. Napoli C, Martin-Padura I, de Nigris F, Giorgio M, Mansueto G, Somma P, Condorelli M, Sica G, De Rosa G, Pelicci P. Deletion of the p66Shc longevity gene reduces systemic and tissue oxidative stress, vascular cell apoptosis, and early atherogenesis in mice fed a high-fat diet. Proc Natl Acad Sci USA. 2003;100:2112-2116.
23. Jeon BH, Gupta G, Park YC, Qi B, Haile A, Khanday FA, Liu YX, Kim JM, Ozaki M, White AR, Berkowitz DE, Irani K. Apurinic/apyrimidinic endonuclease 1 regulates endothelial NO production and vascular tone. Circ Res. 2004;95:902-910.
24. Khanday FA, Santhanam L, Kasuno K, Yamamori T, Naqvi A, Dericco J, Bugayenko A, Mattagajasingh I, Disanza A, Scita G, Irani K. Sosmediated activation of rac1 by p66shc. J Cell Biol. 2006;172:817-822.
25. Hiyama A, Yokoyama K, Nukaga T, Sakai D, Mochida J. A complex interaction between Wnt signaling and TNF-α in nucleus pulposus cells. Arthritis Res Ther. 2013;15:R189.
26. Zhang YK, Huang ZJ, Liu S, Liu YP, Song AA, Song XJ. WNT signaling underlies the pathogenesis of neuropathic pain in rodents. J Clin Invest. 2013;123:2268-2286.
27. Zhou T, Hu Y, Chen Y, Zhou KK, Zhang B, Gao G, Ma JX. The pathogenic role of the canonical Wnt pathway in age-related macular degeneration. Invest Ophthalmol Vis Sci. 2010;51:4371-4379.
28. Spillmann F, Van Linthout S, Miteva K, Lorenz M, Stangl V, Schultheiss HP, Tschöpe C. LXR agonism improves TNF-α-induced endothelial dysfunction in the absence of its cholesterol-modulating effects. Atherosclerosis. 2014;232:1-9.
29. Coant N, Ben Mkaddem S, Pedruzzi E, Guichard C, Treton X, Ducroc R, Freund JN, Cazals-Hatem D, Bouhnik Y, Woerther PL, Skurnik D, Grodet A, Fay M, Biard D, Lesuffleur T, Deffert C, Moreau R, Groyer A, Krause KH, Daniel F, Ogier-Denis E. Nadph oxidase 1 modulates wnt and notch1 signaling to control the fate of proliferative progenitor cells in the colon. Mol Cell Biol. 2010;30:2636-2650
30. Kajla S, Mondol AS, Nagasawa A, Zhang Y, Kato M, Matsuno K, Yabe-Nishimura C, Kamata T. A crucial role for Nox 1 in redox-dependent regulation of Wnt-β-catenin signaling. FASEB J. 2012;26:2049-2059.
31. Liu Q, Li J, Cheng R, Chen Y, Lee K, Hu Y, Yi J, Liu Z, Ma JX. Nitrosative stress plays an important role in Wnt pathway activation in diabetic retinopathy. Antioxid Redox Signal. 2013;18:1141-1153.
32. Zhou T, Zhou KK, Lee K, Gao G, Lyons TJ, Kowluru R, Ma JX. The role of lipid peroxidation products and oxidative stress in activation of the canonical wingless-type MMTV integration site (WNT) pathway in a rat model of diabetic retinopathy. Diabetologia. 2011;54:459-468.
33. Lassègue B, San Martín A, Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res. 2012;110:1364-1390.
34. Almeida M, Ambrogini E, Han L, Manolagas SC, Jilka RL. Increased lipid oxidation causes oxidative stress, increased peroxisome proliferatoractivated receptor-gamma expression, and diminished pro-osteogenic Wnt signaling in the skeleton. J Biol Chem. 2009;284:27438-27448.
35. Tsaousi A, Williams H, Lyon CA, Taylor V, Swain A, Johnson JL, George SJ. Wnt4/β-catenin signaling induces VSMC proliferation and is associated with intimal thickening. Circ Res. 2011;108:427-436.
36. Chen J, Stahl A, Krah NM, Seaward MR, Dennison RJ, Sapieha P, Hua J, Hatton CJ, Juan AM, Aderman CM, Willett KL, Guerin KI, Mammoto A, Campbell M, Smith LE. Wnt signaling mediates pathological vascular growth in proliferative retinopathy. Circulation. 2011;124:1871-1881.
37. Tickenbrock L, Schwäble J, Strey A, Sargin B, Hehn S, Baas M, Choudhary C, Gerke V, Berdel WE, Müller-Tidow C, Serve H. Wnt signaling regulates transendothelial migration of monocytes. J Leukoc Biol. 2006;79:1306-1313.
38. Cohen ED, Ihida-Stansbury K, Lu MM, Panettieri RA, Jones PL, Morrisey EE. Wnt signaling regulates smooth muscle precursor development in the mouse lung via a tenascin C/PDGFR pathway. J Clin Invest. 2009;119:2538-2549.
39. Ueland T, Otterdal K, Lekva T, Halvorsen B, Gabrielsen A, Sandberg WJ, Paulsson-Berne G, Pedersen TM, Folkersen L, Gullestad L, Oie E, Hansson GK, Aukrust P. Dickkopf-1 enhances inflammatory interaction between platelets and endothelial cells and shows increased expression in atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:1228-1234.
40. Singh R, De Aguiar RB, Naik S, Mani S, Ostadsharif K, Wencker D, Sotoudeh M, Malekzadeh R, Sherwin RS, Mani A. LRP6 enhances glucose metabolism by promoting TCF7L2-dependent insulin receptor expression and IGF receptor stabilization in humans. Cell Metab. 2013;17:197-209.
41. Qiu W, Chen L, Kassem M. Activation of non-canonical Wnt/JNK pathway by Wnt3a is associated with differentiation fate determination of human bone marrow stromal (mesenchymal) stem cells. Biochem Biophys Res Commun. 2011;413:98-104.
42. Wu X, Tu X, Joeng KS, Hilton MJ, Williams DA, Long F. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell. 2008;133:340-353.
43. Liao G, Tao Q, Kofron M, Chen JS, Schloemer A, Davis RJ, Hsieh JC, Wylie C, Heasman J, Kuan CY. Jun NH2-terminal kinase (JNK) prevents nuclear beta-catenin accumulation and regulates axis formation in Xenopus embryos. Proc Natl Acad Sci USA. 2006;103:16313-16318.
44. Huelsken J, Behrens J. The Wnt signalling pathway. J Cell Sci. 2002;115(Pt 21):3977-3978.
45. Tu X, Joeng KS, Nakayama KI, Nakayama K, Rajagopal J, Carroll TJ, McMahon AP, Long F. Noncanonical Wnt signaling through G protein- linked PKCdelta activation promotes bone formation. Dev Cell. 2007;12:113-127.
46. Samarzija I, Sini P, Schlange T, Macdonald G, Hynes NE. Wnt3a regulates proliferation and migration of HUVEC via canonical and noncanonical Wnt signaling pathways. Biochem Biophys Res Commun. 2009;386:449-454.
47. Xu S, Jiang B, Hou X, Shi C, Bachschmid MM, Zang M, Verbeuren TJ, Cohen RA. High-fat diet increases and the polyphenol, S17834, decreases acetylation of the sirtuin-1-dependent lysine-382 on p53 and apoptotic signaling in atherosclerotic lesion-prone aortic endothelium of normal mice. J Cardiovasc Pharmacol. 2011;58:263-271.
48. Kumar A, Kim CS, Hoffman TA, Naqvi A, Dericco J, Jung SB, Lin Z, Jain MK, Irani K. p53 impairs endothelial function by transcriptionally repressing Kruppel-Like Factor 2. Arterioscler Thromb Vasc Biol. 2011;31:133-141.
49. Peng X, Yang L, Chang H, Dai G, Wang F, Duan X, Guo L, Zhang Y, Chen G. Wnt/β-catenin signaling regulates the proliferation and differentiation of mesenchymal progenitor cells through the p53 pathway. PLoS One. 2014;9:e97283.
50. Kim NH, Kim HS, Kim NG, et al. p53 and microRNA-34 are suppressors of canonical Wnt signaling. Sci Signal. 2011;4:ra71.
51. Kim TH, Xiong H, Zhang Z, Ren B. beta-Catenin activates the growth factor endothelin-1 in colon cancer cells. Oncogene. 2005;24:597-604.