Quantification of cysteinyl S-nitrosylation by fluorescence in unbiased proteomic studies

Biochemistry

Volumn 50, Issue 25, 2011, Pages 5601-5614

  Wiktorowicz, John E ^a,b,c   Stafford, Susan ^b   Rea, Harriet ^a   Urvil, Petri ^c   Soman, Kizhake ^a,b,c   Kurosky, Alexander ^a,b,c   Perez Polo, J Regino ^a,c   Savidge, Tor C ^c  

^a University of Texas Medical Branch School of Medicine   (United States)

^b National Heart Lung   (United States)

^c UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL APPLICATIONS; BRANCHING MORPHOGENESIS; CALCIUM SIGNALING; CELLULAR DEVELOPMENT; CORTICAL NEURONS; FIBRILLAR PROTEINS; HOST RESPONSE; HYPOXIA-ISCHEMIA; IN-VIVO; MICROBIAL PATHOGENS; NEURITES; NEUROGENESIS; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN FUNCTIONS; PROTEOMIC STUDIES; QUANTITATIVE APPROACH; S-NITROSYLATION;

AMINO ACIDS; CELL DEATH; ELECTROPHORETIC MOBILITY; FLUORESCENCE; MICROORGANISMS; NEURONS;

PROTEINS;

CELL PROTEIN; CYSTEINE; NITRIC OXIDE SYNTHASE; NITROSOPROTEOME; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEOME; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL VIRULENCE; BRAIN CELL; BRAIN EDEMA; CALCIUM SIGNALING; CELL STRUCTURE; CONTROLLED STUDY; FEMALE; FLUORESCENCE; GLIA; HYPOXIA; ISCHEMIA; MICROBIAL ACTIVITY; NERVE CELL; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEURITE; NEWBORN; NITROSYLATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT;

ANIMALS; ANOXIA; BORON COMPOUNDS; CALORIMETRY; CYSTEINE; FEMALE; FLUORESCENCE; ISCHEMIA; LUMINESCENCE; MALEIMIDES; NITRIC OXIDE; PERFUSION; PHOSPHORYLATION; PROTEOMICS; RANDOM ALLOCATION; RATS; RATS, WISTAR;

RATTUS;

EID: 79959423082     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200008b     Document Type: Article

References (55)

1. Torta, F., Usuelli, V., Malgaroli, A., and Bachi, A. (2008) Proteomic analysis of protein S-nitrosylation Proteomics 8, 4484-4494
2. Foster, M. W., Hess, D. T., and Stamler, J. S. (2009) Protein S-nitrosylation in health and disease: A current perspective Trends Mol. Med. 15, 391-404
3. Lopez-Sanchez, L. M., Muntane, J., de la Mata, M., and Rodriguez-Ariza, A. (2009) Unraveling the S-nitrosoproteome: Tools and strategies Proteomics 9, 808-818
4. Lima, B., Forrester, M. T., Hess, D. T., and Stamler, J. S. (2010) S-nitrosylation in cardiovascular signaling Circ. Res. 106, 633-646
5. Mannick, J. B., Hausladen, A., Liu, L., Hess, D. T., Zeng, M., Miao, Q. X., Kane, L. S., Gow, A. J., and Stamler, J. S. (1999) Fas-induced caspase denitrosylation Science 284, 651-654 (Pubitemid 29289591)
6. Gow, A., Doctor, A., Mannick, J., and Gaston, B. (2007) S-Nitrosothiol measurements in biological systems J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 851, 140-151 (Pubitemid 46720150)
7. Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P., and Snyder, S. H. (2001) Protein S-nitrosylation: A physiological signal for neuronal nitric oxide Nat. Cell Biol. 3, 193-197 (Pubitemid 32118373)
8. Jaffrey, S. R., Fang, M., and Snyder, S. H. (2002) Nitrosopeptide mapping: A novel methodology reveals S-nitrosylation of dexras1 on a single cysteine residue Chem. Biol. 9, 1329-1335 (Pubitemid 36010689)
9. Sun, J., Morgan, M., Shen, R. F., Steenbergen, C., and Murphy, E. (2007) Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport Circ. Res. 101, 1155-1163 (Pubitemid 350146442)
10. Kettenhofen, N. J., Broniowska, K. A., Keszler, A., Zhang, Y., and Hogg, N. (2007) Proteomic methods for analysis of S-nitrosation J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 851, 152-159 (Pubitemid 46720147)
11. Pretzer, E. and Wiktorowicz, J. E. (2008) Saturation fluorescence labeling of proteins for proteomic analyses Anal. Biochem. 374, 250-262
12. Tyagarajan, K., Pretzer, E. L., and Wiktorowicz, J. E. (2003) Thiol-reactive dyes for fluorescence labeling of proteomic samples Electrophoresis 24, 2348-2358 (Pubitemid 38089020)
13. Jamaluddin, M., Wiktorowicz, J. E., Soman, K. V., Boldogh, I., Forbus, J. D., Spratt, H., Garofalo, R. P., and Brasier, A. R. (2010) Role of Peroxiredoxin-1 and -4 in Protection of RSV-induced Cysteinyl-oxidation of Nuclear Cytoskeletal Proteins J. Virol. 84, 9533-9545
14. Rice, J. E., III, Vannucci, R. C., and Brierley, J. B. (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat Ann. Neurol. 9, 131-141 (Pubitemid 11191192)
15. Grafe, M. R. (1994) Developmental changes in the sensitivity of the neonatal rat brain to hypoxic/ischemic injury Brain Res. 653, 161-166 (Pubitemid 24252834)
16. Hu, X., Qiu, J., Grafe, M. R., Rea, H. C., Rassin, D. K., and Perez-Polo, J. R. (2003) Bcl-2 family members make different contributions to cell death in hypoxia and/or hyperoxia in rat cerebral cortex Int. J. Dev. Neurosci. 21, 371-377 (Pubitemid 37346401)
17. Hu, X., Rea, H. C., Wiktorowicz, J. E., and Perez-Polo, J. R. (2006) Proteomic analysis of hypoxia/ischemia-induced alteration of cortical development and dopamine neurotransmission in neonatal rat J. Proteome Res. 5, 2396-2404 (Pubitemid 44330833)
18. Gill, M. B., Bockhorst, K., Narayana, P., and Perez-Polo, J. R. (2008) Bax shuttling after neonatal hypoxia-ischemia: Hyperoxia effects J. Neurosci. Res. 86, 3584-3604
19. Ferrari, D. C., Nesic, O. B., and Perez-Polo, J. R. (2010) Oxygen resuscitation does not ameliorate neonatal hypoxia/ischemia-induced cerebral edema J. Neurosci. Res. 88, 2056-2065
20. Iguchi, A., Thomson, N. R., Ogura, Y., Saunders, D., Ooka, T., Henderson, I. R., Harris, D., Asadulghani, M., Kurokawa, K., Dean, P., Kenny, B., Quail, M. A., Thurston, S., Dougan, G., Hayashi, T., Parkhill, J., and Frankel, G. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69 J. Bacteriol. 191, 347-354
21. Ames, G. F.-L., Brody, C., and Kustu, S. (1984) Simple, rapid, and quantitative release of periplasmic proteins by chloroform J. Bacteriol. 160, 1181-1183 (Pubitemid 15222722)
22. Jaffrey, S. R. and Snyder, S. H. (2001) The Biotin Switch Method for the detection of S-nitrosylated proteins Sci. STKE 86, 1-10
23. Turck, C. W., Falick, A. M., Kowalek, J. A., Lane, W. S., Lilley, K. S., Phinney, B. S., Weintraub, S. T., Witkowska, H. E., and Yates, N. A. (2006) ABRF-PRG06: Relative Protein Quantification. In Association of Biomolecular Resource Facilities 2006, Long Beach, CA.
24. Storey, J. D. and Tibshirani, R. (2003) Statistical significance for genomewide studies Proc. Natl. Acad. Sci. U.S.A. 100, 9440-9445 (Pubitemid 37033947)
25. Pei, D. S., Sun, Y. F., and Song, Y. J. (2009) S-Nitrosylation of PTEN involved in ischemic brain injury in rat hippocampal CA1 region Neurochem. Res. 34, 1507-1512
26. Duan, S., Wan, L., Fu, W. J., Pan, H., Ding, Q., Chen, C., Han, P., Zhu, X., Du, L., Liu, H., Chen, Y., Liu, X., Yan, X., Deng, M., and Qian, M. (2009) Nonlinear cooperation of p53-ING1-induced bax expression and protein S-nitrosylation in GSNO-induced thymocyte apoptosis: A quantitative approach with cross-platform validation Apoptosis 14, 236-245
27. Kolb, J. P. (2001) Pro- and anti-apoptotic role of nitric oxide, NO C. R. Acad. Sci., Ser. III 324, 413-424
28. Boichot, C., Walker, P. M., Durand, C., Grimaldi, M., Chapuis, S., Gouyon, J. B., and Brunotte, F. (2006) Term neonate prognoses after perinatal asphyxia: Contributions of MR imaging, MR spectroscopy, relaxation times, and apparent diffusion coefficients Radiology 239, 839-848 (Pubitemid 43830621)
29. Zanelli, S. A., Stanley, D. P., and Kaufman, D. A. (2008) Hypoxic-Ischemic Encephalopathy. http://emedicine.medscape.com/article/973501- overview.
30. Calvert, J. W. and Zhang, J. H. (2005) Pathophysiology of an hypoxic-ischemic insult during the perinatal period Neurol. Res. 27, 246-260 (Pubitemid 40523796)
31. Deulofeut, R., Critz, A., Adams-Chapman, I., and Sola, A. (2006) Avoiding hyperoxia in infants < or = 1250 g is associated with improved short- and long-term outcomes J. Perinatol. 26, 700-705 (Pubitemid 44650189)
32. Koch, J. D., Miles, D. K., Gilley, J. A., Yang, C. P., and Kernie, S. G. (2008) Brief exposure to hyperoxia depletes the glial progenitor pool and impairs functional recovery after hypoxic-ischemic brain injury J. Cereb. Blood Flow Metab. 28, 1294-1306 (Pubitemid 351896643)
33. Wang, C. L., Anderson, C., Leone, T. A., Rich, W., Govindaswami, B., and Finer, N. N. (2008) Resuscitation of preterm neonates by using room air or 100% oxygen Pediatrics 121, 1083-1089
34. Klinger, G., Beyene, J., Shah, P., and Perlman, M. (2005) Do hyperoxaemia and hypocapnia add to the risk of brain injury after intrapartum asphyxia? Arch. Dis. Child. 90 (Fetal Neonatal Edition) F49-F52
35. Ahn, E. S., Robertson, C. L., Vereczki, V., Hoffman, G. E., and Fiskum, G. (2008) Normoxic ventilatory resuscitation following controlled cortical impact reduces peroxynitrite-mediated protein nitration in the hippocampus J. Neurosurg. 108, 124-131
36. Savidge, T. C., Newman, P., Pothoulakis, C., Ruhl, A., Neunlist, M., Bourreille, A., Hurst, R., and Sofroniew, M. V. (2007) Enteric glia regulate intestinal barrier function and inflammation via release of S-nitrosoglutathione Gastroenterology 132, 1344-1358 (Pubitemid 46656255)
37. Stamler, J. S., Toone, E. J., Lipton, S. A., and Sucher, N. J. (1997) (S)NO signals: Translocation, regulation, and a consensus motif Neuron 18, 691-696
38. Miseta, A. and Csutora, P. (2000) Relationship between the Occurrence of Cysteine in Proteins and the Complexity of Organisms Mol. Biol. Evol. 17, 1232-1239 (Pubitemid 30617150)
39. Monteiro, G., Horta, B. B., Pimenta, D. C., Augusto, O., and Netto, L. E. (2007) Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C Proc. Natl. Acad. Sci. U.S.A. 104, 4886-4891 (Pubitemid 47186146)
40. Huang, B. and Chen, C. (2006) An ascorbate-dependent artifact that interferes with the interpretation of the biotin switch assay Free Radical Biol. Med. 41, 562-567 (Pubitemid 44080503)
41. Giustarini, D., Dalle-Donne, I., Colombo, R., Milzani, A., and Rossi, R. (2008) Is ascorbate able to reduce disulfide bridges? A cautionary note Nitric Oxide 19, 252-258
42. Dahm, C. C., Moore, K., and Murphy, M. P. (2006) Persistent S-nitrosation of complex I and other mitochondrial membrane proteins by S-nitrosothiols but not nitric oxide or peroxynitrite: Implications for the interaction of nitric oxide with mitochondria J. Biol. Chem. 281, 10056-10065 (Pubitemid 43864540)
43. Forrester, M. T., Foster, M. W., and Stamler, J. S. (2007) 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 (Pubitemid 47100466)
44. Paige, J. S., Xu, G., Stancevic, B., and Jaffrey, S. R. (2008) Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability Chem. Biol. 15, 1307-1316 (Pubitemid 352841468)
45. Chouchani, E. T., Hurd, T. R., Nadtochiy, S. M., Brookes, P. S., Fearnley, I. M., Lilley, K. S., Smith, R. A., and Murphy, M. P. (2010) 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
46. Nadtochiy, S. M., Burwell, L. S., Ingraham, C. A., Spencer, C. M., Friedman, A. E., Pinkert, C. A., and Brookes, P. S. (2009) In vivo cardioprotection by S-nitroso-2-mercaptopropionyl glycine J. Mol. Cell. Cardiol. 46, 960-968
47. Sanghani, P. C., Davis, W. I., Fears, S. L., Green, S. L., Zhai, L., Tang, Y., Martin, E., Bryan, N. S., and Sanghani, S. P. (2009) Kinetic and cellular characterization of novel inhibitors of S-nitrosoglutathione reductase J. Biol. Chem. 284, 24354-24362
48. Straub, A. C., Billaud, M., Johnstone, S. R., Best, A. K., Yemen, S., Dwyer, S. T., Looft-Wilson, R., Lysiak, J. J., Gaston, B., Palmer, L., and Isakson, B. E. (2011) Compartmentalized connexin 43 S-nitrosylation/ denitrosylation regulates heterocellular communication in the vessel wall Arterioscler., Thromb., Vasc. Biol. 31, 399-407
49. Wang, X., Kettenhofen, N. J., Shiva, S., Hogg, N., and Gladwin, M. T. (2008) Copper dependence of the biotin switch assay: Modified assay for measuring cellular and blood nitrosated proteins Free Radical Biol. Med. 44, 1362-1372
50. Kallakunta, V. M., Staruch, A., and Mutus, B. (2010) Sinapinic acid can replace ascorbate in the biotin switch assay Biochim. Biophys. Acta 1800, 23-30
51. Krucker, T., Siggins, G. R., McNamara, R. K., Lindsley, K. A., Dao, A., Allison, D. W., De Lecea, L., Lovenberg, T. W., Sutcliffe, J. G., and Gerendasy, D. D. (2002) Targeted disruption of RC3 reveals a calmodulin-based mechanism for regulating metaplasticity in the hippocampus J. Neurosci. 22, 5525-5535 (Pubitemid 35386474)
52. Li, J., Huang, F. L., and Huang, K. P. (2001) Glutathiolation of proteins by glutathione disulfide S-oxide derived from S-nitrosoglutathione. Modifications of rat brain neurogranin/RC3 and neuromodulin/GAP-43 J. Biol. Chem. 276, 3098-3105
53. Sliskovic, I., Raturi, A., and Mutus, B. (2005) Characterization of the S-denitrosation activity of protein disulfide isomerase J. Biol. Chem. 280, 8733-8741 (Pubitemid 40409560)
54. Ramachandran, N., Root, P., Jiang, X. M., Hogg, P. J., and Mutus, B. (2001) Mechanism of transfer of NO from extracellular S-nitrosothiols into the cytosol by cell-surface protein disulfide isomerase Proc. Natl. Acad. Sci. U.S.A. 98, 9539-9544 (Pubitemid 32769339)
55. Tu, B. P. and Weissman, J. S. (2004) Oxidative protein folding in eukaryotes: Mechanisms and consequences J. Cell Biol. 164, 341-346 (Pubitemid 38174761)