Netrin-1 abrogates ischemia/reperfusion-induced cardiac mitochondrial dysfunction via nitric oxide-dependent attenuation of NOX4 activation and recoupling of NOS

Journal of Molecular and Cellular Cardiology

Volumn 78, Issue , 2015, Pages 174-185

  Siu, Kin Lung ^a   Lotz, Christopher ^a   Ping, Peipei ^a   Cai, Hua ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ischemia reperfusion (I R) injury; Mitochondrial dysfunction; NADPH oxidase isoform 4 (NOX4); Netrin 1; NO synthase (NOS); NOS uncoupling

Indexed keywords

CYCLIC GMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NETRIN 1; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SUPEROXIDE; CARDIOTONIC AGENT; NERVE GROWTH FACTOR; NETRIN-1; NITRIC OXIDE; NOX4 PROTEIN, MOUSE; PTERIN DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SEPIAPTERIN; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MITOCHONDRIAL DYSFUNCTION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME INHIBITION; HEART DISEASE; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MALE; MOUSE; NONHUMAN; OXIDATIVE COUPLING; OXIDATIVE STRESS; PROTEIN FUNCTION; REPERFUSION INJURY; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENETICS; HEART MITOCHONDRION; KNOCKOUT MOUSE; METABOLISM; MYOCARDIAL REPERFUSION INJURY; PATHOLOGY; RNA INTERFERENCE;

ANIMALIA;

ANIMALS; CARDIOTONIC AGENTS; DISEASE MODELS, ANIMAL; HYDROGEN PEROXIDE; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCARDIAL REPERFUSION INJURY; NADPH OXIDASE; NERVE GROWTH FACTORS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; PTERINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SUPEROXIDES; TUMOR SUPPRESSOR PROTEINS;

EID: 84916602026     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2014.07.005     Document Type: Article

References (52)

1. Matsumura K., Jeremy R.W., Schaper J., Becker L.C. Progression of myocardial necrosis during reperfusion of ischemic myocardium. Circulation 1998, 97:795-804.
2. +-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 1988, 255:357-360.
3. Nazareth W., Yafei N., Crompton M. Inhibition of anoxia-induced injury in heart myocytes by cyclosporin A. J Mol Cell Cardiol 1991, 23:1351-1354.
4. +-dependent pore activated by oxidative stress in heart mitochondria. Biochem J 1987, 245:915-918.
5. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434:658-662.
6. Zweier J.L. Measurement of superoxide-derived free radicals in the reperfused heart. Evidence for a free radical mechanism of reperfusion injury. J Biol Chem 1988, 263:1353-1357.
7. Hearse D.J., Humphrey S.M., Chain E.B. Abrupt reoxygenation of the anoxic potassium-arrested perfused rat heart: a study of myocardial enzyme release. J Mol Cell Cardiol 1973, 5:395-407.
8. West M.B., Rokosh G., Obal D., Velayutham M., Xuan Y.T., Hill B.G., et al. Cardiac myocyte-specific expression of inducible nitric oxide synthase protects against ischemia/reperfusion injury by preventing mitochondrial permeability transition. Circulation 2008, 118:1970-1978.
9. Tang X.L., Takano H., Rizvi A., Turrens J.F., Qiu Y., Wu W.J., et al. Oxidant species trigger late preconditioning against myocardial stunning in conscious rabbits. Am J Physiol Heart Circ Physiol 2002, 282:H281-H291.
10. Beckman J.S., Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996, 271:C1424-C1437.
11. Turko I.V., Murad F. Protein nitration in cardiovascular diseases. Pharmacol Rev 2002, 54:619-634.
12. Zorov D.B., Filburn C.R., Klotz L.O., Zweier J.L., Sollott S.J. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 2000, 192:1001-1014.
13. Hoshida S., Yamashita N., Otsu K., Hori M. The importance of manganese superoxide dismutase in delayed preconditioning: involvement of reactive oxygen species and cytokines. Cardiovasc Res 2002, 55:495-505.
14. Sekili S., McCay P.B., Li X.Y., Zughaib M., Sun J.Z., Tang L., et al. Direct evidence that the hydroxyl radical plays a pathogenetic role in myocardial "stunning" in the conscious dog and demonstration that stunning can be markedly attenuated without subsequent adverse effects. Circ Res 1993, 73:705-723.
15. Sethi R., Takeda N., Nagano M., Dhalla N.S. Beneficial effects of vitamin E treatment in acute myocardial infarction. J Cardiovasc Pharmacol Ther 2000, 5:51-58.
16. Kennedy T.E., Serafini T., de la Torre J.R., Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 1994, 78:425-435.
17. Nguyen A., Cai H. Netrin-1 induces angiogenesis via a DCC-dependent ERK1/2-eNOS feed-forward mechanism. Proc Natl Acad Sci U S A 2006, 103:6530-6535.
18. Park K.W., Crouse D., Lee M., Karnik S.K., Sorensen L.K., Murphy K.J., et al. The axonal attractant Netrin-1 is an angiogenic factor. Proc Natl Acad Sci U S A 2004, 101:16210-16215.
19. Zhang J., Cai H. Netrin-1 prevents ischemia/reperfusion-induced myocardial infarction via a DCC/ERK1/2/eNOS s1177/NO/DCC feed-forward mechanism. J Mol Cell Cardiol 2010, 48:1060-1070.
20. Chalupsky K., Cai H. Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 2005, 102:9056-9061.
21. Oak J.H., Cai H. Attenuation of angiotensin II signaling recouples eNOS and inhibits nonendothelial NOX activity in diabetic mice. Diabetes 2007, 56:118-126.
22. Gao L., Chalupsky K., Stefani E., Cai H. Mechanistic insights into folic acid-dependent vascular protection: dihydrofolate reductase (DHFR)-mediated reduction in oxidant stress in endothelial cells and angiotensin II-infused mice: a novel HPLC-based fluorescent assay for DHFR activity. J Mol Cell Cardiol 2009, 47:752-760.
23. Gao L., Siu K.L., Chalupsky K., Nguyen A., Chen P., Weintraub N.L., et al. Role of uncoupled endothelial nitric oxide synthase in abdominal aortic aneurysm formation: treatment with folic acid. Hypertension 2012, 59:158-166.
24. Youn J.Y., Gao L., Cai H. The p47phox- and NADPH oxidase organiser 1 (NOXO1)-dependent activation of NADPH oxidase 1 (NOX1) mediates endothelial nitric oxide synthase (eNOS) uncoupling and endothelial dysfunction in a streptozotocin-induced murine model of diabetes. Diabetologia 2012, 55:2069-2079.
25. Bouhidel J.O., Wang P., Siu K.L., Li H., Youn J.Y., Cai H. Netrin-1 improves post-injury cardiac function in vivo via DCC/NO-dependent preservation of mitochondrial integrity, while attenuating autophagy. Biochim Biophys Acta Mol Basis of Dis 2014 June 10.
26. Siu K.L., Miao X.N., Cai H. Recoupling of eNOS with folic acid prevents abdominal aortic aneurysm formation in angiotensin II-infused apolipoprotein E null mice. PLoS One 2014, 9:e88899.
27. Youn J.Y., Siu K.L., Lob H., Itani H., Harrison D.G., Cai H. Role of vascular oxidative stress in obesity and metabolic syndrome. Diabetes 2014, 63:2344-2355.
28. Bhandarkar S.S., Jaconi M., Fried L.E., Bonner M.Y., Lefkove B., Govindarajan B., et al. Fulvene-5 potently inhibits NADPH oxidase 4 and blocks the growth of endothelial tumors in mice. J Clin Invest 2009, 119:2359-2365.
29. Youn J.Y., Wang T., Cai H. An ezrin/calpain/PI3K/AMPK/eNOSs1179 signaling cascade mediating VEGF-dependent endothelial nitric oxide production. Circ Res 2009, 104:50-59.
30. Sun J., Morgan M., Shen R.F., Steenbergen C., Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 2007, 101:1155-1163.
31. Kohr M.J., Evangelista A.M., Ferlito M., Steenbergen C., Murphy E. S-nitrosylation of TRIM72 at cysteine 144 is critical for protection against oxidation-induced protein degradation and cell death. J Mol Cell Cardiol 2014, 69:67-74.
32. Sun J., Kohr M.J., Nguyen T., Aponte A.M., Connelly P.S., Esfahani S.G., et al. Disruption of caveolae blocks ischemic preconditioning-mediated S-nitrosylation of mitochondrial proteins. Antioxid Redox Signal 2012, 16:45-56.
33. 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, 106:1253-1264.
34. Dikalova A.E., Gongora M.C., Harrison D.G., Lambeth J.D., Dikalov S., Griendling K.K. Upregulation of Nox1 in vascular smooth muscle leads to impaired endothelium-dependent relaxation via eNOS uncoupling. Am J Physiol Heart Circ Physiol 2010, 299:H673-H679.
35. Nam D., Ni C.W., Rezvan A., Suo J., Budzyn K., Llanos A., et al. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol 2009, 297:H1535-H1543.
36. Moens A.L., Leyton-Mange J.S., Niu X., Yang R., Cingolani O., Arkenbout E.K., et al. Adverse ventricular remodeling and exacerbated NOS uncoupling from pressure-overload in mice lacking the beta3-adrenoreceptor. J Mol Cell Cardiol 2009, 47:576-585.
37. Dixon L.J., Morgan D.R., Hughes S.M., McGrath L.T., El-Sherbeeny N.A., Plumb R.D., et al. Functional consequences of endothelial nitric oxide synthase uncoupling in congestive cardiac failure. Circulation 2003, 107:1725-1728.
38. Moens A.L., Champion H.C., Claeys M.J., Tavazzi B., Kaminski P.M., Wolin M.S., et al. High-dose folic acid pretreatment blunts cardiac dysfunction during ischemia coupled to maintenance of high-energy phosphates and reduces postreperfusion injury. Circulation 2008, 117:1810-1819.
39. Perkins K.A., Pershad S., Chen Q., McGraw S., Adams J.S., Zambrano C., et al. The effects of modulating eNOS activity and coupling in ischemia/reperfusion (I/R). Naunyn Schmiedebergs Arch Pharmacol 2012, 385:27-38.
40. An J., Du J., Wei N., Xu H., Pritchard K.A., Shi Y. Role of tetrahydrobiopterin in resistance to myocardial ischemia in Brown Norway and Dahl S rats. Am J Physiol Heart Circ Physiol 2009, 297:H1783-H1791.
41. Hoffmeyer M.R., Jones S.P., Ross C.R., Sharp B., Grisham M.B., Laroux F.S., et al. Myocardial ischemia/reperfusion injury in NADPH oxidase-deficient mice. Circ Res 2000, 87:812-817.
42. Martyn K.D., Frederick L.M., von Loehneysen K., Dinauer M.C., Knaus U.G. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 2006, 18:69-82.
43. Wan L.L., Xia J., Ye D., Liu J., Chen J., Wang G. Effects of quercetin on gene and protein expression of NOX and NOS after myocardial ischemia and reperfusion in rabbit. Cardiovasc Ther 2009, 27:28-33.
44. Calvert J.W., Condit M.E., Aragon J.P., Nicholson C.K., Moody B.F., Hood R.L., et al. Exercise protects against myocardial ischemia-reperfusion injury via stimulation of beta(3)-adrenergic receptors and increased nitric oxide signaling: role of nitrite and nitrosothiols. Circ Res 2011, 108:1448-1458.
45. Kuroda J., Ago T., Matsushima S., Zhai P., Schneider M.D., 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, 107:15565-15570.
46. Cave A.C., Brewer A.C., Narayanapanicker A., Ray R., Grieve D.J., Walker S., et al. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 2006, 8:691-728.
47. Byrne J.A., Grieve D.J., Bendall J.K., Li J.M., Gove C., Lambeth J.D., et al. Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin II-induced cardiac hypertrophy. Circ Res 2003, 93:802-805.
48. Kahles T., Kohnen A., Heumueller S., Rappert A., Bechmann I., Liebner S., et al. NADPH oxidase Nox1 contributes to ischemic injury in experimental stroke in mice. Neurobiol Dis 2010, 40:185-192.
49. Suliman H.B., Ali M., Piantadosi C.A. Superoxide dismutase-3 promotes full expression of the EPO response to hypoxia. Blood 2004, 104:43-50.
50. Vallet P., Charnay Y., Steger K., Ogier-Denis E., Kovari E., Herrmann F., et al. Neuronal expression of the NADPH oxidase NOX4, and its regulation in mouse experimental brain ischemia. Neuroscience 2005, 132:233-238.
51. Mittal M., Roth M., Konig P., Hofmann S., Dony E., Goyal P., et al. Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circ Res 2007, 101:258-267.
52. Zhang M., Brewer A.C., Schroder K., Santos C.X., Grieve D.J., Wang 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, 107:18121-18126.