136
Views
8
CrossRef citations to date
0
Altmetric
Review

Proteomics insights into deregulated protein S-nitrosylation and disease

, &
Pages 59-69 | Published online: 09 Jan 2014

References

  • Hill BG, Dranka BP, Bailey SM, Lancaster JR, Darley-Usmar VM. What part of NO don’t you understand? Some answers to the cardinal questions in nitric oxide biology. J. Biol. Chem.285, 19699–19704 (2010).
  • Villanueva C, Giulivi C. Subcellular and cellular locations of nitric oxide synthase isoforms as determinants of health and disease. Free Radic. Biol. Med.49, 307–316 (2010).
  • Foster MW, Hess DT, Stamler JS. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol. Med.15, 391–404 (2009).
  • Benhar M, Forrester MT, Stamler JS. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell. Biol.10, 721–732 (2009).
  • Stamler JS, Hess DT. Nascent nitrosylases. Nat. Cell. Biol.12, 1024–1026 (2010).
  • Lima B, Forrester MT, Hess DT, Stamler JS. S-nitrosylation in cardiovascular signaling. Circ. Res.106, 633–646 (2010).
  • Ckless K, Lampert A, Reiss J et al. Inhibition of arginase activity enhances inflammation in mice with allergic airway disease, in association with increases in protein S-nitrosylation and tyrosine nitration. J. Immunol.181, 4255–4264 (2008).
  • López-Sánchez LM, Corrales FJ, Barcos M, Espejo I, Munoz-Castaneda JR, Rodríguez-Ariza A. Inhibition of nitric oxide synthesis during induced cholestasis ameliorates hepatocellular injury by facilitating S-nitrosothiol homeostasis. Lab. Invest.90, 116–127 (2010).
  • Nakamura T, Lipton SA. Redox modulation by S-nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseases. Cell Death Differ.18, 1478–1486 (2011).
  • Sarkar S, Korolchuk VI, Renna M et al. Complex inhibitory effects of nitric oxide on autophagy. Mol. Cell.43, 19–32 (2011).
  • Wei W, Li B, Hanes MA, Kakar S, Chen X, Liu L. S-nitrosylation from GSNOR deficiency impairs DNA repair and promotes hepatocarcinogenesis. Sci. Transl. Med.2, 1–9 (2010).
  • Keszler A, Zhang Y, Hogg N. Reaction between nitric oxide, glutathione, and oxygen in the presence and absence of protein: how are S-nitrosothiols formed? Free Radic. Biol. Med.48, 55–64 (2010).
  • Foster MW, Liu L, Zeng M, Hess DT, Stamler JS. A genetic analysis of nitrosative stress. Biochemistry48, 792–799 (2009).
  • Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell. Biol.6, 150–166 (2005).
  • Wu C, Parrott AM, Fu C et al. Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Antioxid. Redox Signal.15(9), 2565–2604 (2011).
  • Seth D, Stamler JS. The SNO-proteome: causation and classifications. Curr. Opin. Chem. Biol.15, 129–136 (2011).
  • Greco TM, Hodara R, Parastatidis I et al. Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc. Natl Acad. Sci. USA103, 7420–7425 (2006).
  • Doulias PT, Greene JL, Greco TM et al. Structural profiling of endogenous S-nitrosocysteine residues reveals unique features that accommodate diverse mechanisms for protein S-nitrosylation. Proc. Natl Acad. Sci. USA107, 16958–16963 (2010).
  • Marino SM, Gladyshev VN. Structural analysis of cysteine S-nitrosylation: a modified acid-based motif and the emerging role of trans-nitrosylation. J. Mol. Biol.395, 844–859 (2010).
  • Iwakiri Y, Satoh A, Chatterjee S et al. Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc. Natl Acad. Sci. USA103, 19777–19782 (2006).
  • Ibiza S, Perez-Rodriguez A, Ortega A et al. Endothelial nitric oxide synthase regulates N-Ras activation on the Golgi complex of antigen-stimulated T cells. Proc. Natl Acad. Sci. USA105, 10507–10512 (2008).
  • Xu L, Han C, Lim K, Wu T. Activation of cytosolic phospholipase A2alpha through nitric oxide-induced S-nitrosylation. Involvement of inducible nitric-oxide synthase and cyclooxygenase-2. J. Biol. Chem.283, 3077–3087 (2008).
  • Derakhshan B, Hao G, Gross SS. Balancing reactivity against selectivity: the evolution of protein S-nitrosylation as an effector of cell signaling by nitric oxide. Cardiovasc Res.75, 210–219 (2007).
  • Reynolds JD, Hess DT, Stamler JS. The transfusion problem: role of aberrant S-nitrosylation. Transfusion51, 852–858 (2011).
  • Nakamura T, Wang L, Wong CC et al. Transnitrosylation of XIAP regulates caspase-dependent neuronal cell death. Mol. Cell.39, 184–195 (2010).
  • Mitchell DA, Morton SU, Fernhoff NB, Marletta MA. Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc. Natl Acad. Sci. USA104, 11609–11614 (2007).
  • Liu L, Hausladen A, Zeng M et al. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature410, 490–494 (2001).
  • Liu L, Yan Y, Zeng M et al. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell116, 617–628 (2004).
  • Que LG, Liu L, Yan Y et al. Protection from experimental asthma by an endogenous bronchodilator. Science308, 1618–1621 (2005).
  • Lopez-Sanchez LM, Collado JA, Corrales FJ et al. S-nitrosation of proteins during D-galactosamine-induced cell death in human hepatocytes. Free Radic. Res.41, 50–61 (2007).
  • Lopez-Sanchez LM, Corrales FJ, Gonzalez R et al. Alteration of S-nitrosothiol homeostasis and targets for protein S-nitrosation in human hepatocytes. Proteomics8, 4709–4720 (2008).
  • Bateman RL, Rauh D, Tavshanjian B, Shokat KM. Human carbonyl reductase 1 is an S-nitrosoglutathione reductase. J. Biol. Chem.283, 35756–35762 (2008).
  • Sengupta R, Ryter SW, Zuckerbraun BS, Tzeng E, Billiar TR, Stoyanovsky DA. Thioredoxin catalyzes the denitrosation of low-molecular mass and protein S-nitrosothiols. Biochemistry46, 8472–8483 (2007).
  • Benhar M, Forrester MT, Hess DT, Stamler JS. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science320, 1050–1054 (2008).
  • Tello D, Tarin C, Ahicart P, Breton-Romero R, Lamas S, Martinez-Ruiz A. A ‘fluorescence switch’ technique increases the sensitivity of proteomic detection and identification of S-nitrosylated proteins. Proteomics9, 5359–5370 (2009).
  • Lopez-Sanchez LM, Corrales FJ, Lopez-Pedrera C, Aranda E, Rodriguez-Ariza A. Pharmacological impairment of S-nitrosoglutathione or thioredoxin reductases augments protein S-nitrosation in human hepatocarcinoma cells. Anticancer Res.30, 415–421 (2010).
  • Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell. Biol.3, 193–197 (2001).
  • Forrester MT, Foster MW, Benhar M, Stamler JS. Detection of protein S-nitrosylation with the biotin-switch technique. Free Radic. Biol. Med.46, 119–126 (2009).
  • Forrester MT, Foster MW, Stamler JS. Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J. Biol. Chem.282, 13977–13983 (2007).
  • Gow A, Doctor A, Mannick J, Gaston B. S-nitrosothiol measurements in biological systems. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci.851, 140–151 (2007).
  • Lopez-Sanchez LM, Muntane J, de la Mata M, Rodriguez-Ariza A. Unraveling the S-nitrosoproteome: tools and strategies. Proteomics9, 808–818 (2009).
  • Kettenhofen NJ, Broniowska KA, Keszler A, Zhang Y, Hogg N. Proteomic methods for analysis of S-nitrosation. J. Chromatogr. B. Analyt. Technol. Biomed. Life. Sci.851, 152–159 (2007).
  • Chouchani ET, Hurd TR, Nadtochiy SM et al. Identification of S-nitrosated mitochondrial proteins by S-nitrosothiol difference in gel electrophoresis (SNO-DIGE): implications for the regulation of mitochondrial function by reversible S-nitrosation. Biochem. J.430, 49–59 (2010).
  • Sun J, Morgan M, Shen RF, Steenbergen C, Murphy E. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ. Res.101, 1155–1163 (2007).
  • Lin J, Steenbergen C, Murphy E, Sun J. Estrogen receptor-beta activation results in S-nitrosylation of proteins involved in cardioprotection. Circulation120, 245–254 (2009).
  • Han P, Zhou X, Huang B, Zhang X, Chen C. On-gel fluorescent visualization and the site identification of S-nitrosylated proteins. Anal. Biochem.377, 150–155 (2008).
  • Wiktorowicz JE, Stafford S, Rea H et al. Quantification of cysteinyl S-nitrosylation by fluorescence in unbiased proteomic studies. Biochemistry50, 5601–5614 (2011).
  • Hao G, Derakhshan B, Shi L, Campagne F, Gross SS. SNOSID, a proteomic method for identification of cysteine S-nitrosylation sites in complex protein mixtures. Proc. Natl Acad. Sci. USA103, 1012–1017 (2006).
  • Camerini S, Polci ML, Restuccia U, Usuelli V, Malgaroli A, Bachi A. A novel approach to identify proteins modified by nitric oxide: the HIS-TAG switch method. J. Proteome Res.6, 3224–3231 (2007).
  • Forrester MT, Thompson JW, Foster MW, Nogueira L, Moseley MA, Stamler JS. Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat. Biotechnol.27, 557–559 (2009).
  • Benhar M, Thompson JW, Moseley MA, Stamler JS. Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry49, 6963–6969 (2010).
  • Liu M, Hou J, Huang L, Huang X et al. Site-specific proteomics approach for study protein S-nitrosylation. Anal. Chem.82, 7160–7168 (2010).
  • Sinha V, Wijewickrama GT, Chandrasena RE et al. Proteomic and mass spectroscopic quantitation of protein S-nitrosation differentiates NO-donors. ACS Chem. Biol.5, 667–680 (2010).
  • Chen YJ, Ku WC, Lin PY, Chou HC, Khoo KH, Chen YJ. S-alkylating labeling strategy for site-specific identification of the S-nitrosoproteome. J. Proteome Res.9, 6417–6439 (2010).
  • Foster MW, Forrester MT, Stamler JS. A protein microarray-based analysis of S-nitrosylation. Proc. Natl Acad. Sci. USA106, 18948–18953 (2009).
  • Numajiri N, Takasawa K, Nishiya T et al. On-off system for PI3-kinase–Akt signaling through S-nitrosylation of phosphatase with sequence homology to tensin (PTEN). Proc. Natl Acad. Sci. USA108, 10349–10354 (2011).
  • Wang Y, Liu T, Wu C, Li H. A strategy for direct identification of protein S-nitrosylation sites by quadrupole time-of-flight mass spectrometry. J. Am. Soc. Mass Spectrom.19, 1353–1360 (2008).
  • Torta F, Elviri L, Bachi A. Direct and indirect detection methods for the analysis of S-nitrosylated peptides and proteins. Methods Enzymol.473, 265–280 (2010).
  • Cook SL, Jackson GP. Characterization of tyrosine nitration and cysteine nitrosylation modifications by metastable atom-activation dissociation mass spectrometry. J. Am. Soc. Mass Spectrom.22, 221–232 (2011).
  • Jia HY, Liu Y, Zhang XJ et al. Potential oxidative stress of gold nanoparticles by induced-NO releasing in serum. J. Am. Chem. Soc.131, 40–41 (2009).
  • Faccenda A, Bonham CA, Vacratsis PO, Zhang X, Mutus B. Gold nanoparticle enrichment method for identifying S-nitrosylation and S-glutathionylation sites in proteins. J. Am. Chem. Soc.132, 11392–11394 (2010).
  • Zhang J, Li S, Zhang D, Wang H, Whorton AR, Xian M. Reductive ligation mediated one-step disulfide formation of S-nitrosothiols. Org. Lett.12, 4208–4211 (2010).
  • Bechtold E, Reisz JA, Klomsiri C et al. Water-soluble triarylphosphines as biomarkers for protein S-nitrosation. ACS Chem. Biol.5, 405–414 (2010).
  • Xue Y, Liu Z, Gao X et al. GPS-SNO: computational prediction of protein S-nitrosylation sites with a modified GPS algorithm. PLoS One5, e11290 (2010).
  • Li YX, Shao YH, Jing L, Deng NY. An efficient support vector machine approach for identifying protein S-nitrosylation sites. Protein Pept. Lett.18, 573–587 (2011).
  • Gu Z, Nakamura T, Lipton SA. Redox reactions induced by nitrosative stress mediate protein misfolding and mitochondrial dysfunction in neurodegenerative diseases. Mol. Neurobiol.41, 55–72 (2010).
  • Bizzozero OA, Zheng J. Identification of major S-nitrosylated proteins in murine experimental autoimmune encephalomyelitis. J. Neurosci. Res.87, 2881–2889 (2009).
  • Kohr MJ, Sun J, Aponte A et al. Simultaneous measurement of protein oxidation and S-nitrosylation during preconditioning and ischemia/reperfusion injury with resin-assisted capture. Circ. Res.108, 418–426 (2011).
  • Zhang HH, Wang YP, Chen DB. Analysis of nitroso-proteomes in normotensive and severe preeclamptic human placentas. Biol. Reprod.84, 966–975 (2011).

Website

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.