S-nitrosoglutathione and endothelial nitric oxide synthase-derived nitric oxide regulate compartmentalized ras S-nitrosylation and stimulate cell proliferation

Antioxidants and Redox Signaling

Volumn 18, Issue 3, 2013, Pages 221-238

  Batista, Wagner L ^a   Ogata, Fernando T ^a   Curcio, Marli F ^a   Miguel, Rodrigo B ^a   Arai, Roberto J ^b   Matsuo, Alisson L ^a   Moraes, Miriam S ^a   Stern, Arnold ^c   Monteiro, Hugo P ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GREEN FLUORESCENT PROTEIN; NITRIC OXIDE; PROTEIN TYROSINE KINASE; RAF PROTEIN; RAS PROTEIN; S NITROSOGLUTATHIONE;

ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; GENE ACTIVATION; GENE OVEREXPRESSION; GOLGI COMPLEX; HELA CELL; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; MOLECULAR PROBE; NITROSYLATION; ONCOGENE H RAS; PRIORITY JOURNAL; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; BRADYKININ; CALCIUM SIGNALING; CELL MEMBRANE; CELL PROLIFERATION; CERCOPITHECUS AETHIOPS; COS CELLS; CYSTEINE; ENZYME ACTIVATION; GOLGI APPARATUS; HELA CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; OXIDATION-REDUCTION; PHOSPHOLIPASE C GAMMA; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS P21(RAS); S-NITROSOGLUTATHIONE; S-NITROSOTHIOLS; SRC-FAMILY KINASES;

EID: 84870657502     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2011.4455     Document Type: Article

References (71)

1. Adachi T, Pimentel DR, Heibeck T, Hou X, Lee YJ, Jiang B, Ido Y, and Cohen RA. S-glutathiolation of Ras mediates redox-sensitive signaling by angiotensin II in vascular smooth muscle cells. J Biol Chem 279: 29857-29862, 2004. (Pubitemid 38915870)
2. Ahearn IM, Haigis K, Bar-Sagi D, and Philips MR. Regulating the regulator: post-translational modification of RAS. Nat Rev Mol Cell Biol 13: 39-51, 2012.
3. Akhand AA, Pu M, Seng T, Kato M, Suzuki H, Miyata T, Hamaguchi M, and Nakashima I. Nitric oxide controls Src kinase activity through a sulfhydryl group modificationmediated Tyr-527-independent and Tyr-416-linked mechanism. J Biol Chem 274: 25821-25826, 1999.
4. Arai RJ, Masutani H, Yodoi J, Debbas V, Laurindo FR, Stern A, and Monteiro HP. Nitric oxide induces thioredoxin-1 nuclear translocation: Possible association with the p21Ras survival pathway. Biochem Biophys Res Commun 348: 1254-1260, 2006. (Pubitemid 44291340)
5. Bae SW, Kim HS, Cha YN, Park YS, Jo SA, and Jo I. Rapid increase in endothelial nitric oxide production by bradykinin is mediated by protein kinase A signaling pathway. Biochem Biophys Res Commun. 306: 981-987, 2003. (Pubitemid 36776227)
6. Baker TL, Booden MA, and Buss JE. S-nitrosocysteine increases palmitate turnover on Ha-Ras in NIH 3T3 cells. J Biol Chem 275: 22037-22047, 2000. (Pubitemid 30621781)
7. Bivona TG, Castro IP, Ahearn IM, Grana TM, Chiu VK, Lockyer PJ, Cullen PJ, Pellicer A, Cox AD, and Philips M. R. Phospholipase Cc activates Ras on the Golgi apparatus by means of RasGRP1. Nature 424: 694-698, 2003. (Pubitemid 36987996)
8. Bivona TG and Philips MR. Analysis of Ras and Rap activation in living cells using fluorescent Ras binding domains. Methods 37: 138-145, 2005. (Pubitemid 41587422)
9. Blaukat A, Barac A, Cross MJ, Offermanns S, and Dikic I. G protein-coupled receptor-mediated mitogen-activated protein kinase activation through cooperation of Galpha(q) and Galpha(i) signals. Mol Cell Biol 20: 6837-6848, 2000.
10. Burgoyne JR, Haeussler DJ, Kumar V, Ji Y, Pimentel DR, Zee RS, Costello CE, Lin C, McComb ME, Cohen RA, and Bachschmid MM. Oxidation of HRas cysteine thiols by metabolic stress prevents palmitoylation in vivo and contributes to endothelial cell apoptosis. FASEB J 26: 832-841, 2012.
11. Caloca MG, Zugaza JL, and Bustelo XR. Exchange factors of the RasGRP family mediate Ras activation in the Golgi. J Biol Chem 278: 33465-33473, 2003. (Pubitemid 37055801)
12. Castro IP, Bivona TG, Philips MR, and Pellicer A. Ras activation in Jurkat T cells following low-grade stimulation of the T-cell receptor is specific to N-Ras and occurs only on the Golgi apparatus. Mol Cell Biol 24: 3485-3496, 2004. (Pubitemid 38452087)
13. Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL, Cox AD, and Philips MR. Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol 4: 343-350, 2002. (Pubitemid 34521029)
14. Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, Ivanov IE, and Philips MR. Endomembrane trafficking of ras: the CAAX motif targets proteins to the ER and Golgi. Cell 98: 69-80, 1999. (Pubitemid 29331197)
15. Clarke S. Protein isoprenylation and methylation at carboxyl-terminal cysteine residues. Annual Rev Biochem 61: 355-386, 1992.
16. Curcio MF, Batista WL, Linares E, Nascimento FD, Moraes MS, Borges RE, Sap J, Stern A, and Monteiro HP. Regulatory effects of nitric oxide on Src kinase, FAK, p130Cas, and receptor protein tyrosine phosphatase alpha (PTPalpha): A role for the cellular redox environment. Antiox Redox Signal 13: 109-125, 2010.
17. de Rooij J and Bos JL. Minimal Ras-binding domain of Raf1 can be used as an activation-specific probe for Ras. Oncogene 14: 623-625, 1997. (Pubitemid 27090966)
18. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, and Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605, 1999.
19. Ebinu JO, Bottorff DA, Chan EY, Stang SL, Dunn RJ, and Stone JC. RasGRP, a Ras guanyl nucleotide-releasing protein with calcium-and diacylglycerol- binding motifs. Science 280: 1082-1086, 1998 (Pubitemid 28234950)
20. Engels K, Knauer SK, Loibl S, Fetz V, Harter P, Shweitzer A, Fisseler-Eckhoff A, Kommoss F, Hanker L, Nekljudova V, Hermanns I Kleinert H, Mann W, du Bois A, and Stauber RH. NO signaling confers cytoprotectivity through surviving network in ovarian carcinomas. Cancer Res 68: 5159-5166, 2008.
21. Fehrenbacher N, Bar-Sagi D, and Philips MR. Ras/MAPK signaling from endomembranes. Mol Oncol 3: 297-307, 2009.
22. Forrester MT, Foster MW, Benhar M, and Stamler JS. Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic Biol Med 46: 119-126, 2009.
23. Fukumura D, Kashiwagi S, and Jain RK. The role of nitric oxide in tumour progression. Nat Rev Cancer 6: 521-534, 2006. (Pubitemid 43980541)
24. Fulton D, Babbitt R, Zoellner S, Fontana J, Acevedo L, McCabe TJ, Iwakiri Y, and Sessa WC. Targeting of endothelial nitric oxide synthase to the cytoplasmic face of the Golgi complex or plasma membrane regulates Akt-versus calcium-dependent mechanisms for nitric oxide release. J Biol Chem 279: 30349-30357, 2004. (Pubitemid 38937962)
25. Fulton D, Fontana J, Grzegorz S, Gratton J-P, Lin M, Li K-X, Michell B, Kemp BE, Rodman D, and Sessa WC. Localization of endothelial nitric oxide synthase phosphorylated on Serine 1179 and nitric oxide in Golgi and plasma membrane defines the existence of two pools of active enzyme. J Biol Chem 277: 4277-4284, 2002. (Pubitemid 34968692)
26. Giustarini D, Milzani A, Aldini G, Carini M, Rossi R, and Dalle-Done I. S-nitrosation versus S-glutathionylation of protein sulfhydryl groups by S-nitrosoglutathione. Antiox Redox Signal 7: 930-939, 2005. (Pubitemid 40967144)
27. Gow AJ, Buerk DG, and Ischiropoulos H. A novel reaction mechanism for the formation of S-nitrosothiols in vivo. J Biol Chem 272: 2841-2845, 1997. (Pubitemid 27053331)
28. Hancock JF, Paterson H, and Marshall CJ. A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63: 133-139, 1990.
29. Hancock JF. Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4: 373-384, 2003. (Pubitemid 36565569)
30. Hanke JH, Gardner JP, Dow RL, Changelian PS, Brissette WH, Weringer EJ, Pollok BA, and Connelly PA. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. Study of Lck-and FynT-dependent T cell activation. J Biol Chem 271: 695-701, 1996.
31. Hess DT, Matsumoto A, Kim SO, Marshall HE and Stamler JS. Protein S-nitrosylation: Purview and parameters. Nat Rev Mol Cell Biol 6: 150-166, 2005.
32. Ibiza S, Pérez-Rodr?́guez A, Ortega A, Mart?́nez-Ruiz A, Barreiro O, Garc?́a-Dom?́nguez CA, V?́ctor VM, Esplugues JV, Rojas JM, Sánchez-Madrid F, and Serrador JM. Endothelial nitric oxide synthase regulates N-Ras activation on the Golgi complex of antigen-stimulated T cells Proc Natl Acad Sci USA 105: 10507-10512, 2008.
33. Iwakiri Y, Satoh A, Chatterjee S, Toomre DK, Chalouni CM, Fulton D, Groszmann RJ, Shah VH, and Sessa WC. Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc Natl Acad Sci USA 103: 19777-19782, 2006. (Pubitemid 46037507)
34. Iwakiri Y. S-nitrosylation of proteins: a new insight into endothelial cell function regulated by eNOS-derived NO. Nitric Oxide 25: 95-101, 2011.
35. Karnoub AE and Weinberg RA. Ras oncogene: split personalities. Nat Rev Mol Cell Biol 9: 517-531, 2008.
36. Kuhr F, Lowry J, Zhang Y, Brovkovych V, and Skidgel RA. Differential regulation of inducible and endothelial nitric oxide synthase by kinin B1 and B2 receptors. Neuropeptides 44: 145-154, 2010.
37. Lander HM, Hajjar DP, Hempstead BL, Mirza UA, Chait BT, Campbell S, and Quilliam LA. A molecular redox switch on p21(ras)-Structural basis for the nitric oxide-p21(ras) interaction. J Biol Chem 272: 4323-4326, 1997. (Pubitemid 27078505)
38. Lechner M, Lirk P, and Rieder J. Inducible nitric oxide synthase (iNOS) in tumor biology: The two sides of the same coin. Sem Cancer Biol 15: 277-289, 2005. (Pubitemid 41058773)
39. Liao F, Shin HS, and Rhee SG. In vitro tyrosine phosphorylation of PLC-gamma 1 and PLC-gamma 2 by src-family protein tyrosine kinases. Biochem Biophys Res Commun 191: 1028-1033, 1993. (Pubitemid 23231593)
40. Lim K-H, Ancrile BB, Kasahtus DF, and Counter CM. Tumor maintenance is mediated by eNOS. Nature 452: 646-650, 2008.
41. Litvak KJ and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408, 2001. (Pubitemid 34164012)
42. Lorenzo PS, Kung JW, Bottorff DA, Garfield SH, Stone JC, and Blumberg PM. Phorbol esters modulate the Ras exchange factor RasGRP3 Cancer Res 61: 943-949, 2001.
43. Mallis RJ, Buss JE, and Thomas JA. Oxidative modification of H-Ras: S-thiolation and S-nitrosylation of reactive cysteines. Biochem J 355: 145-153, 2001. (Pubitemid 32304245)
44. Mallis RJ and Thomas JA. Effect of S-nitrosthiols on cellular glutathione and reaxctive protein sulfhydryls. Arch Biochem Biophys 383: 60-69, 2000.
45. Monteiro HP and Stern A. Redox modulation of tyrosine phosphorylation-dependent signal transduction pathways. Free Radic Biol Med 21: 323-333, 1996. (Pubitemid 26271722)
46. Monteiro HP, Arai RJ, and Travassos LR. Protein tyrosine phosphorylation and protein tyrosine nitration in redox signaling. Antioxid Redox Signal 10: 843-889, 2008. (Pubitemid 351301369)
47. Monteiro HP, Gruia-Gray J, Peranovich TM, de Oliveira LC, and Stern A. Nitric oxide stimulates tyrosine phosphorylation of focal adhesion kinase, Src kinase, and mitogenactivated protein kinases in murine fibroblasts. Free Radic Biol Med 28: 174-182, 2000. (Pubitemid 30084009)
48. Monteiro HP, Silva EF, and Stern A. Nitric oxide: a potential inducer of adhesion-related apoptosis-anoikis. Nitric Oxide 10: 1-10, 2004. (Pubitemid 38410889)
49. Morbidelli L, Parenti A, Giovannelli L, Granger HJ, Ledda F, and Ziche M. B1 receptor involvement in the effect of bradykinin on venular endothelial cell proliferation and potentiation of FGF-2 effects. Br J Pharmacol 124: 1286-1292, 1998. (Pubitemid 28333954)
50. Oess S, Icking A, Fulton D, Govers R, and Mü ller-Esterl W. Subcellular targeting and trafficking of nitric oxide synthases. Biochem J 396: 401-409, 2006. (Pubitemid 44228155)
51. Okayama H, Saito M, Weiss JM, Stauffer J, Takenoshita S, Wiltrout RH, Hussain SP, and Harris CC. NOS2 enhances KRas-induced lung carcinogenesis, inflammation and microRNA-21 expression. Int J Cancer 2012 [Epub ahead of print]; Doi: 10. 1002/ijc. 27644.
52. Pearce LR, Komander D, and Alessi DR. The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 11: 9-22, 2010.
53. Peranovich TM, da Silva AM, Fries DM, Stern A, and Monteiro HP. Nitric oxide stimulates tyrosine phosphorylation in murine fibroblasts in the absence and presence of epidermal growth factor. Biochem J 305: 613-619, 1995.
54. Rafikova O, Rafikov R, and Nudler E. Catalysis of s-nitrosothiols formation by serum albumin: The mechanism and implication in vascular control. Proc Natl Acad Sci USA 99: 5913-5918, 2002. (Pubitemid 34493239)
55. Rahman I, Kode A, and Biswas SK. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1: 3159-3165, 2006.
56. Rahman MA, Senga T, Ito S, Hyodo T, Hasegawa H, and Hamaguchi M. S-nitrosylation at cysteine 498 of c-Src tyrosine kinase regulates nitric oxide-mediated cell invasion. J Biol Chem 285: 3806-3814, 2010.
57. Reuter CW, Morgan MA, and Bergmann L. Targeting the Ras signaling pathway: a rational, mechanism-based treatment for hematologic malignancies? Blood 96: 1655-1669, 2000. (Pubitemid 30661043)
58. Ridnour LA, Thomas DD, Donzelli S, Espey MG, Roberts DD, Wink DA, and Isenberg JS. The biphasic nature of nitric oxide responses in tumor biology. Antioxid Redox Signal 8: 1329-1337, 2006. (Pubitemid 44182431)
59. Rocha Oliveira CJ, Curcio MF, Moraes MS, Tsujita M, Travassos LR, Stern A, and Monteiro HP. The low molecular weight s-nitrosothiol, S-nitroso-N-acetylpenicillamine, promotes cell cycle progression in rabbit aortic endothelial cells. Nitric Oxide 18: 241-255, 2008.
60. Rocha Oliveira CJ, Schindler F, Ventura AM, Moraes MS, Arai RJ, Debbas V, Stern A, and Monteiro HP. Nitric oxide and cGMP activate the Ras-MAP kinase pathwaystimulating protein tyrosine phosphorylation in rabbit aortic endothelial cells. Free Radic Biol Med 35: 381-396, 2003. (Pubitemid 37289168)
61. Rocks O, Peyker A, and Bastiaens PI. Spatio-temporal segregation of Ras signals: one ship, three anchors, many harbors. Curr Opin Cell Biol 18: 351-357, 2006. (Pubitemid 44016056)
62. Rocks O, Peyker A, Kahms M, Verveer PJ, Koerner C, Lumbierres M, Kuhlmann J, Waldmann H, Wittinghofer A, and Bastiaens PI. An acylation cycle regulates localization and activity of palmitoylated Ras isoforms. Science 307: 1746-1752, 2005. (Pubitemid 40388611)
63. Schafer FQ and Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212, 2001. (Pubitemid 32463931)
64. Schlesssinger J. Cell signaling by receptor tyrosine kinases. Cell 103: 211-225, 2000.
65. Solca FF, Baum A, Langkopf E, Dahmann G, Heider KH, Himmelsbach F, and van Meel JC Inhibition of epidermal growth factor receptor activity by two pyrimidopyrimidine derivatives. J Pharmacol Exp Ther 311: 502-509, 2004. (Pubitemid 39391534)
66. Takai Y, Sasaki T, and Matozaki T. Small GTP-binding proteins. Physiol Rev 81: 153-208, 2001. (Pubitemid 32098004)
67. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, Hussain P, Vecoli C, Paolocci N, Ambs S, Colton CA, Harris CC, Roberts DD, and Wink DA. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 45: 18-31, 2008.
68. Tsujita M, Batista WL, Ogata FT, Stern A, Monteiro HP, and Arai RJ. The nitric oxide-sensitive p21Ras-ERK pathway mediates S-nitrosoglutathione-induced apoptosis. Biochem Biophys Res Commun 369: 1001-1006, 2008.
69. van Triest M, de Rooij J, and Bos JL. Measurement of GTPbound Ras-like GTPases by activation-specific probes. Methods Enzymol 333: 343-348, 2001. (Pubitemid 32507321)
70. Villalobo A. Nitric oxide and cell proliferation. FEBS J 273: 2329-2344, 2006. (Pubitemid 43736649)
71. Zhang Y and Hogg N. Formation and stability of s-nitrosothiols in Raw 264. 7 cells. Am J Physiol Lung Cell Mol Physiol 287: L467-L474, 2004. (Pubitemid 39095899)