Endothelial Nitric Oxide Synthase-Derived Nitric Oxide Prevents Dihydrofolate Reductase Degradation via Promoting S-Nitrosylation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 11, 2015, Pages 2366-2373

  Cai, Zhejun ^a,b   Lu, Qiulun ^a   Ding, Ye ^a   Wang, Qilong ^a   Xiao, Lei ^a   Song, Ping ^a   Zou, Ming Hui ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

human umbilical vein endothelial cells; mouse; nitric oxide; Nos3 protein; sapropterin; tetrahydrofolate dehydrogenase

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYCLOHEXIMIDE; CYSTEINE; DIHYDROFOLATE REDUCTASE; DITHIOTHREITOL; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PEROXYNITRITE; PROTEASOME; SMALL INTERFERING RNA; 7,8-DIHYDROBIOPTERIN; ATP DEPENDENT 26S PROTEASE; BIOPTERIN; NOS3 PROTEIN, HUMAN; NOS3 PROTEIN, MOUSE; PROTEASOME INHIBITOR; SCAVENGER;

AORTA; ARTICLE; CONTROLLED STUDY; ENZYME DEGRADATION; GENE MUTATION; GENE SILENCING; HALF LIFE TIME; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; NITROSYLATION; POLYUBIQUITINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING; WILD TYPE; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DRUG EFFECTS; ENDOTHELIUM CELL; ENZYME STABILITY; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; PROTEIN DEGRADATION; PROTEIN PROCESSING; RNA INTERFERENCE; THORACIC AORTA; TIME;

ANIMALS; AORTA, THORACIC; BIOPTERIN; CELLS, CULTURED; CYSTEINE; ENDOTHELIAL CELLS; ENZYME STABILITY; FREE RADICAL SCAVENGERS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RNA INTERFERENCE; TETRAHYDROFOLATE DEHYDROGENASE; TIME FACTORS; TRANSFECTION; UBIQUITINATION;

EID: 84945482894     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.305796     Document Type: Article

References (34)

1. Bendall JK, Douglas G, McNeill E, Channon KM, Crabtree MJ, Tetrahydrobiopterin in cardiovascular health and disease. Antioxid Redox Signal 2014 20 3040 3077. doi: 10.1089/ars.2013.5566
2. Münzel T, Daiber A, Ullrich V, Mülsch A, Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cGMP-dependent protein kinase. Arterioscler Thromb Vasc Biol 2005 25 1551 1557. doi: 10.1161/01.ATV.0000168896.64927.bb
3. Li H, Förstermann U, Uncoupling of endothelial NO synthase in atherosclerosis and vascular disease. Curr Opin Pharmacol 2013 13 161 167. doi: 10.1016/j.coph.2013.01.006
4. Schulz E, Jansen T, Wenzel P, Daiber A, Münzel T, Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension. Antioxid Redox Signal 2008 10 1115 1126. doi: 10.1089/ars.2007.1989
5. Abudukadier A, Fujita Y, Obara A, Ohashi A, Fukushima T, Sato Y, Ogura M, Nakamura Y, Fujimoto S, Hosokawa M, Hasegawa H, Inagaki N, Tetrahydrobiopterin has a glucose-lowering effect by suppressing hepatic gluconeogenesis in an endothelial nitric oxide synthase-dependent manner in diabetic mice. Diabetes 2013 62 3033 3043. doi: 10.2337/db12-1242
6. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG, Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003 111 1201 1209. doi: 10.1172/JCI14172
7. Crabtree MJ, Hale AB, Channon KM, Dihydrofolate reductase protects endothelial nitric oxide synthase from uncoupling in tetrahydrobiopterin deficiency. Free Radic Biol Med 2011 50 1639 1646. doi: 10.1016/j.freeradbiomed.2011.03.010
8. Kuzkaya N, Weissmann N, Harrison DG, Dikalov S, Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 2003 278 22546 22554. doi: 10.1074/jbc.M302227200
9. Crabtree MJ, Channon KM, Synthesis and recycling of tetrahydrobiopterin in endothelial function and vascular disease. Nitric Oxide 2011 25 81 88. doi: 10.1016/j.niox.2011.04.004
10. Xu J, Wu Y, Song P, Zhang M, Wang S, Zou MH, Proteasome-dependent degradation of guanosine 5'-triphosphate cyclohydrolase I causes tetrahydrobiopterin deficiency in diabetes mellitus. Circulation 2007 116 944 953. doi: 10.1161/CIRCULATIONAHA.106.684795
11. Crabtree MJ, Tatham AL, Hale AB, Alp NJ, Channon KM, Critical role for tetrahydrobiopterin recycling by dihydrofolate reductase in regulation of endothelial nitric-oxide synthase coupling: relative importance of the de novo biopterin synthesis versus salvage pathways. J Biol Chem 2009 284 28128 28136. doi: 10.1074/jbc.M109.041483
12. 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 USA 2005 102 9056 9061. doi: 10.1073/pnas.0409594102
13. Whitsett J, Rangel Filho A, Sethumadhavan S, Celinska J, Widlansky M, Vasquez-Vivar J, Human endothelial dihydrofolate reductase low activity limits vascular tetrahydrobiopterin recycling. Free Radic Biol Med 2013 63 143 150. doi: 10.1016/j.freeradbiomed.2013.04.035
14. Hess DT, Stamler JS, Regulation by S-nitrosylation of protein post-translational modification. J Biol Chem 2012 287 4411 4418. doi: 10.1074/jbc.R111.285742
15. Zhao Y, Wu J, Zhu H, Song P, Zou MH, Peroxynitrite-dependent zinc release and inactivation of guanosine 5'-triphosphate cyclohydrolase 1 instigate its ubiquitination in diabetes. Diabetes 2013 62 4247 4256. doi: 10.2337/db13-0751
16. Amici M, Sagratini D, Pettinari A, Pucciarelli S, Angeletti M, Eleuteri AM, 20S proteasome mediated degradation of DHFR: implications in neurodegenerative disorders. Arch Biochem Biophys 2004 422 168 174. doi: 10.1016/j.abb.2003.12.014
17. Shahani N, Sawa A, Nitric oxide signaling and nitrosative stress in neurons: role for S-nitrosylation. Antioxid Redox Signal 2011 14 1493 1504. doi: 10.1089/ars.2010.3580
18. Azad N, Vallyathan V, Wang L, Tantishaiyakul V, Stehlik C, Leonard SS, Rojanasakul Y, S-nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation. A novel antiapoptotic mechanism that suppresses apoptosis. J Biol Chem 2006 281 34124 34134. doi: 10.1074/jbc.M602551200
19. Kohr MJ, Evangelista AM, 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. doi: 10.1016/j.yjmcc.2014.01.010
20. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM, S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 2004 304 1328 1331. doi: 10.1126/science.1093891
21. Amaral JH, Montenegro MF, Pinheiro LC, Ferreira GC, Barroso RP, Costa-Filho AJ, Tanus-Santos JE, TEMPOL enhances the antihypertensive effects of sodium nitrite by mechanisms facilitating nitrite-derived gastric nitric oxide formation. Free Radic Biol Med 2013 65 446 455. doi: 10.1016/j.freeradbiomed.2013.07.032
22. Amm I, Sommer T, Wolf DH, Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim Biophys Acta 2014 1843 182 196. doi: 10.1016/j.bbamcr.2013.06.031
23. Peth A, Nathan JA, Goldberg AL, The ATP costs and time required to degrade ubiquitinated proteins by the 26 S proteasome. J Biol Chem 2013 288 29215 29222. doi: 10.1074/jbc.M113.482570
24. Gould N, Doulias PT, Tenopoulou M, Raju K, Ischiropoulos H, Regulation of protein function and signaling by reversible cysteine S-nitrosylation. J Biol Chem 2013 288 26473 26479. doi: 10.1074/jbc.R113.460261
25. Liu H, Yu S, Zhang H, Xu J, Identification of nitric oxide as an endogenous inhibitor of 26S proteasomes in vascular endothelial cells. PLoS One 2014 9 e98486. doi: 10.1371/journal.pone.0098486
26. Chanvorachote P, Nimmannit U, Stehlik C, Wang L, Jiang BH, Ongpipatanakul B, Rojanasakul Y, Nitric oxide regulates cell sensitivity to cisplatin-induced apoptosis through S-nitrosylation and inhibition of Bcl-2 ubiquitination. Cancer Res 2006 66 6353 6360. doi: 10.1158/0008-5472.CAN-05-4533
27. Simon JN, Duglan D, Casadei B, Carnicer R, Nitric oxide synthase regulation of cardiac excitation-contraction coupling in health and disease. J Mol Cell Cardiol 2014 73 80 91. doi: 10.1016/j.yjmcc.2014.03.004
28. Maron BA, Tang SS, Loscalzo J, S-nitrosothiols and the S-nitrosoproteome of the cardiovascular system. Antioxid Redox Signal 2013 18 270 287. doi: 10.1089/ars.2012.4744
29. Dunne KA, Allam A, McIntosh A, Houston SA, Cerovic V, Goodyear CS, Roe AJ, Beatson SA, Milling SW, Walker D, Wall DM, Increased S-nitrosylation and proteasomal degradation of caspase-3 during infection contribute to the persistence of adherent invasive Escherichia coli (AIEC) in immune cells. PLoS One 2013 8 e68386. doi: 10.1371/journal.pone.0068386
30. Qian J, Fulton D, Post-translational regulation of endothelial nitric oxide synthase in vascular endothelium. Front Physiol 2013 4 347. doi: 10.3389/fphys.2013.00347
31. -. J Biol Chem 2003 278 50949 50955. doi: 10.1074/jbc.M308317200
32. Channon KM, Tetrahydrobiopterin: a vascular redox target to improve endothelial function. Curr Vasc Pharmacol 2012 10 705 708
33. Cunnington C, Channon KM, Tetrahydrobiopterin: pleiotropic roles in cardiovascular pathophysiology. Heart 2010 96 1872 1877. doi: 10.1136/hrt.2009.180430
34. Cunnington C, Van Assche T, Shirodaria C, Systemic and vascular oxidation limits the efficacy of oral tetrahydrobiopterin treatment in patients with coronary artery disease. Circulation 2012 125 1356 1366. doi: 10.1161/CIRCULATIONAHA.111.038919