Tyrosine kinase FYN negatively regulates NOX4 in cardiac remodeling

Journal of Clinical Investigation

Volumn 126, Issue 9, 2016, Pages 3403-3416

  Matsushima, Shouji ^a,b,c   Kuroda, Junya ^a   Zhai, Peiyong ^a   Liu, Tong ^d   Ikeda, Shohei ^a   Nagarajan, Narayani ^a   Oka, Shin Ichi ^a   Yokota, Takashi ^b   Kinugawa, Shintaro ^b   Hsu, Chiao Po ^e   Li, Hong ^d   Tsutsui, Hiroyuki ^b,c   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d The State University of New Jersey   (United States)

^e TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; PROTEIN KINASE FYN; PROTEIN KINASE YES; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; TUBULIN; TYROSINE; FYN PROTEIN, MOUSE; FYN PROTEIN, RAT; NOX4 PROTEIN, MOUSE; NOX4 PROTEIN, RAT; RECOMBINANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; CARDIAC MUSCLE CELL; CELL DEATH; CELL NUCLEUS; GENE DELETION; HEART FAILURE; HEART LEFT VENTRICLE; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE REMODELING; MALE; MOUSE; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; CARDIAC MUSCLE; CARDIOMEGALY; CHEMISTRY; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; PHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN PROCESSING; RAT; WISTAR RAT;

ANIMALS; APOPTOSIS; CARDIOMEGALY; CELL DEATH; CELL NUCLEUS; DOWN-REGULATION; GENE DELETION; GENE EXPRESSION REGULATION; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MYOCARDIUM; NADPH OXIDASE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN DOMAINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-FYN; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; TYROSINE; VENTRICULAR REMODELING;

EID: 84987784690     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI85624     Document Type: Article

References (40)

1. Maejima Y, Kuroda J, Matsushima S, Ago T, Sadoshima J. Regulation of myocardial growth and death by NADPH oxidase. J Mol Cell Cardiol. 2011;50(3):408-416
2. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res. 2010;106(7):1253-1264
3. Matsushima S, et al. Increased oxidative stress in the nucleus caused by Nox4 mediates oxidation of HDAC4 and cardiac hypertrophy. Circ Res. 2013;112(4):651-663
4. Sciarretta S, et al. Activation of NADPH oxidase 4 in the endoplasmic reticulum promotes cardiomyocyte autophagy and survival during energy stress through the protein kinase RNA-activatedlike endoplasmic reticulum kinase/eukaryotic initiation factor 2 and alpha/activating transcription factor 4 pathway. Circ Res. 2013;113(11):1253-1264
5. Zhao QD, et al. NADPH oxidase 4 induces cardiac fibrosis and hypertrophy through activating Akt/mTOR and NFκB signaling pathways. Circulation. 2015;131(7):643-655
6. Kuroda J, Ago T, Matsushima S, Zhai P, Schneider MD, Sadoshima J. NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proc Natl Acad Sci U S A. 2010;107(35):15565-15570
7. Zhang M, et al. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci U S A. 2010;107(42):18121-18126
8. Giordano FJ. Oxygen, oxidative stress, hypoxia, and heart failure. J Clin Invest. 2005;115(3):500-508
9. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol. 2003;15(2):247-254
10. Matsushima S, et al. Broad suppression of NADPH oxidase activity exacerbates ischemia/ reperfusion injury through inadvertent downregulation of hypoxia-inducible factor-1 and alpha and upregulation of peroxisome proliferator-activated receptor-and alpha. Circ Res. 2013;112(8):1135-1149
11. Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature. 1991;353(6345):668-670
12. Uhlinger DJ, Taylor KL, Lambeth JD. p67-phox enhances the binding of p47-phox to the human neutrophil respiratory burst oxidase complex. J Biol Chem. 1994;269(35):22095-22098
13. Geiszt M, Kopp JB, Várnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci U S A. 2000;97(14):8010-8014
14. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal. 2006;18(1):69-82
15. Löhneysen K, Noack D, Jesaitis AJ, Dinauer MC, Knaus UG. Mutational analysis reveals distinct features of the Nox4-p22 phox complex. J Biol Chem. 2008;283(50):35273-35282
16. Giannoni E, Chiarugi P. Redox circuitries driving Src regulation. Antioxid Redox Signal. 2014;20(13):2011-2025
17. Smyrnias I, et al. Nicotinamide adenine dinucleotide phosphate oxidase-4-dependent upregulation of nuclear factor erythroid-derived 2-like 2 protects the heart during chronic pressure overload. Hypertension. 2015;65(3):547-553
18. McCord JM. Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med. 1985;312(3):159-163
19. Ide T, et al. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ Res. 2000;86(2):152-157
20. Grieve DJ, et al. Involvement of the nicotinamide adenosine dinucleotide phosphate oxidase isoform Nox2 in cardiac contractile dysfunction occurring in response to pressure overload. J Am Coll Cardiol. 2006;47(4):817-826
21. Matsuno K, et al. NOX1/NADPH oxidase is involved in endotoxin-induced cardiomyocyte apoptosis. Free Radic Biol Med. 2012;53(9):1718-1728
22. Lyle AN, et al. Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ Res. 2009;105(3):249-259
23. Palomero T, et al. Recurrent mutations in epigenetic regulators, RHOA and FYN kinase in peripheral T cell lymphomas. Nat Genet. 2014;46(2):166-170
24. Um JW, et al. Alzheimer amyloid-β oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat Neurosci. 2012;15(9):1227-1235
25. Yamada E, Pessin JE, Kurland IJ, Schwartz GJ, Bastie CC. Fyn-dependent regulation of energy expenditure and body weight is mediated by tyrosine phosphorylation of LKB1. Cell Metab. 2010;11(2):113-124
26. Saito YD, Jensen AR, Salgia R, Posadas EM. Fyn: a novel molecular target in cancer. Cancer. 2010;116(7):1629-1637
27. Tang X, Feng Y, Ye K. Src-family tyrosine kinase fyn phosphorylates phosphatidylinositol 3-kinase enhancer-activating Akt, preventing its apoptotic cleavage and promoting cell survival. Cell Death Differ. 2007;14(2):368-377
28. Rosado JA, Redondo PC, Salido GM, Gómez-Arteta E, Sage SO, Pariente JA. Hydrogen peroxide generation induces pp60src activation in human platelets: evidence for the involvement of this pathway in store-mediated calcium entry. J Biol Chem. 2004;279(3):1665-1675
29. Reinehr R, Becker S, Eberle A, Grether-Beck S, Häussinger D. Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis. J Biol Chem. 2005;280(29):27179-27194
30. Cooper JA, Howell B. The when and how of Src regulation. Cell. 1993;73(6):1051-1054
31. Xu W, Harrison SC, Eck MJ. Three-dimensional structure of the tyrosine kinase c-Src. Nature. 1997;385(6617):595-602
32. Giannoni E, Buricchi F, Raugei G, Ramponi G, Chiarugi P. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol. 2005;25(15):6391-6403
33. Yadav V, Denning MF. Fyn is induced by Ras/PI3K/Akt signaling and is required for enhanced invasion/migration. Mol Carcinog. 2011;50(5):346-352
34. Ninio-Many L, Grossman H, Shomron N, Chuderland D, Shalgi R. microRNA-125a-3p reduces cell proliferation and migration by targeting Fyn. J Cell Sci. 2013;126(Pt 13):2867-2876
35. Di Bartolo BA, et al. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) promotes angiogenesis and ischemia-induced neovascularization via NADPH oxidase 4 (NOX4) and nitric oxide-dependent mechanisms. J Am Heart Assoc. 2015;4(11): e002527
36. Chen L, et al. Both hydrogen peroxide and transforming growth factor beta 1 contribute to endothelial Nox4 mediated angiogenesis in endothelial Nox4 transgenic mouse lines. Biochim Biophys Acta. 2014;1842(12 Pt A):2489-2499
37. Morisco C, Zebrowski D, Condorelli G, Tsichlis P, Vatner SF, Sadoshima J. The Akt-glycogen synthase kinase 3beta pathway regulates transcription of atrial natriuretic factor induced by beta-adrenergic receptor stimulation in cardiac myocytes. J Biol Chem. 2000;275(19):14466-14475
38. Matsuda T, et al. Distinct roles of GSK-3alpha and GSK-3beta phosphorylation in the heart under pressure overload. Proc Natl Acad Sci USA. 2008;105(52):20900-20905
39. Yamamoto S, et al. Activation of Mst1 causes dilated cardiomyopathy by stimulating apoptosis without compensatory ventricular myocyte hypertrophy. J Clin Invest. 2003;111(10):1463-1474
40. Ago T, et al. Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation. 2004;109(2):227-233