2ifq › Citations

Buried S-nitrosocysteine revealed in crystal structures of human thioredoxin.

Weichsel A, Brailey JL, Montfort WR
Biochemistry 46 1219-27 (2007)
Related entries: 2hsh, 2hxk, 2iiy

Cited: 45 times
EuropePMC logo PMID: 17260951

Abstract

We have determined the 1.65 A crystal structure of human thioredoxin-1 after treatment with S-nitrosoglutathione, providing a high-resolution view of this important protein modification and mechanistic insight into protein transnitrosation. Thioredoxin-1 appears to play an intermediary role in cellular S-nitrosylation and is important in numerous biological and pathobiological activities. S-Nitroso modifications of cysteines 62 and 69 are clearly visible in the structure and display planar cis geometries, whereas cysteines 32, 35, and 73 form intra- and intermolecular disulfide bonds. Surprisingly, the Cys 62 nitroso group is completely buried and pointing to the protein interior yet is the most readily formed at neutral pH. The Cys 69 nitroso group is also protected but requires a higher pH for stable formation. The helix intervening between residues 62 and 69 shifts by approximately 0.5 A to accommodate the SNO groups. The crystallographic asymmetric unit contains three independent molecules of thioredoxin, providing three views of the nitrosated protein. The three molecules are in general agreement but display subtle differences, including both cis and trans conformers for Cys 69 SNO in molecule C, and greater disorder in the Cys 62-Cys 69 helix in molecule B. Possible mechanisms for protein transnitrosation with specific geometric requirements and charge stabilization of the nitroxyl disulfide reaction intermediate are discussed.

Reviews - 2ifq mentioned but not cited (1)

  1. Protein crystallography for non-crystallographers, or how to get the best (but not more) from published macromolecular structures. Wlodawer A, Minor W, Dauter Z, Jaskolski M. FEBS J 275 1-21 (2008)

Articles - 2ifq mentioned but not cited (2)

  1. A rational blueprint for the design of chemically-controlled protein switches. Shui S, Gainza P, Scheller L, Yang C, Kurumida Y, Rosset S, Georgeon S, Di Roberto RB, Castellanos-Rueda R, Reddy ST, Correia BE. Nat Commun 12 5754 (2021)
  2. PTM-Psi: A python package to facilitate the computational investigation of post-translational modification on protein structures and their impacts on dynamics and functions. Mejia-Rodriguez D, Kim H, Sadler N, Li X, Bohutskyi P, Valiev M, Qian WJ, Cheung MS. Protein Sci 32 e4822 (2023)


Reviews citing this publication (11)

  1. Protein denitrosylation: enzymatic mechanisms and cellular functions. Benhar M, Forrester MT, Stamler JS. Nat Rev Mol Cell Biol 10 721-732 (2009)
  2. The thioredoxin system as a therapeutic target in human health and disease. Mahmood DF, Abderrazak A, El Hadri K, Simmet T, Rouis M. Antioxid Redox Signal 19 1266-1303 (2013)
  3. Redox Signaling Mediated by Thioredoxin and Glutathione Systems in the Central Nervous System. Ren X, Zou L, Zhang X, Branco V, Wang J, Carvalho C, Holmgren A, Lu J. Antioxid Redox Signal 27 989-1010 (2017)
  4. Emerging role of protein-protein transnitrosylation in cell signaling pathways. Nakamura T, Lipton SA. Antioxid Redox Signal 18 239-249 (2013)
  5. Thioredoxin 1-mediated post-translational modifications: reduction, transnitrosylation, denitrosylation, and related proteomics methodologies. Wu C, Parrott AM, Fu C, Liu T, Marino SM, Gladyshev VN, Jain MR, Baykal AT, Li Q, Oka S, Sadoshima J, Beuve A, Simmons WJ, Li H. Antioxid Redox Signal 15 2565-2604 (2011)
  6. NADPH-dependent and -independent disulfide reductase systems. Miller CG, Holmgren A, Arnér ESJ, Schmidt EE. Free Radic Biol Med 127 248-261 (2018)
  7. Methodologies for the characterization, identification and quantification of S-nitrosylated proteins. Foster MW. Biochim Biophys Acta 1820 675-683 (2012)
  8. Modulation of signaling mechanisms in the heart by thioredoxin 1. Nagarajan N, Oka S, Sadoshima J. Free Radic Biol Med 109 125-131 (2017)
  9. Chemical methods for the direct detection and labeling of S-nitrosothiols. Bechtold E, King SB. Antioxid Redox Signal 17 981-991 (2012)
  10. Computational Structural Biology of S-nitrosylation of Cancer Targets. Bignon E, Allega MF, Lucchetta M, Tiberti M, Papaleo E. Front Oncol 8 272 (2018)
  11. Protein Transnitrosylation Signaling Networks Contribute to Inflammaging and Neurodegenerative Disorders. Nakamura T, Oh CK, Zhang X, Tannenbaum SR, Lipton SA. Antioxid Redox Signal 35 531-550 (2021)

Articles citing this publication (31)

  1. Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation. Sayed N, Baskaran P, Ma X, van den Akker F, Beuve A. Proc Natl Acad Sci U S A 104 12312-12317 (2007)
  2. Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Paige JS, Xu G, Stancevic B, Jaffrey SR. Chem Biol 15 1307-1316 (2008)
  3. Regulation of the catalytic activity and structure of human thioredoxin 1 via oxidation and S-nitrosylation of cysteine residues. Hashemy SI, Holmgren A. J Biol Chem 283 21890-21898 (2008)
  4. Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Mitchell DA, Morton SU, Fernhoff NB, Marletta MA. Proc Natl Acad Sci U S A 104 11609-11614 (2007)
  5. Redox regulatory mechanism of transnitrosylation by thioredoxin. Wu C, Liu T, Chen W, Oka S, Fu C, Jain MR, Parrott AM, Baykal AT, Sadoshima J, Li H. Mol Cell Proteomics 9 2262-2275 (2010)
  6. A protein microarray-based analysis of S-nitrosylation. Foster MW, Forrester MT, Stamler JS. Proc Natl Acad Sci U S A 106 18948-18953 (2009)
  7. Crystal structure of the human thioredoxin reductase-thioredoxin complex. Fritz-Wolf K, Kehr S, Stumpf M, Rahlfs S, Becker K. Nat Commun 2 383 (2011)
  8. A strategy for direct identification of protein S-nitrosylation sites by quadrupole time-of-flight mass spectrometry. Wang Y, Liu T, Wu C, Li H. J Am Soc Mass Spectrom 19 1353-1360 (2008)
  9. Myosin is reversibly inhibited by S-nitrosylation. Nogueira L, Figueiredo-Freitas C, Casimiro-Lopes G, Magdesian MH, Assreuy J, Sorenson MM. Biochem J 424 221-231 (2009)
  10. Distinction of thioredoxin transnitrosylation and denitrosylation target proteins by the ICAT quantitative approach. Wu C, Parrott AM, Liu T, Jain MR, Yang Y, Sadoshima J, Li H. J Proteomics 74 2498-2509 (2011)
  11. Site-specific and redox-controlled S-nitrosation of thioredoxin. Barglow KT, Knutson CG, Wishnok JS, Tannenbaum SR, Marletta MA. Proc Natl Acad Sci U S A 108 E600-6 (2011)
  12. S-nitrosylation-induced conformational change in blackfin tuna myoglobin. Schreiter ER, Rodríguez MM, Weichsel A, Montfort WR, Bonaventura J. J Biol Chem 282 19773-19780 (2007)
  13. Proteome-wide detection of S-nitrosylation targets and motifs using bioorthogonal cleavable-linker-based enrichment and switch technique. Mnatsakanyan R, Markoutsa S, Walbrunn K, Roos A, Verhelst SHL, Zahedi RP. Nat Commun 10 2195 (2019)
  14. Studies on the reaction of nitric oxide with the hypoxia-inducible factor prolyl hydroxylase domain 2 (EGLN1). Chowdhury R, Flashman E, Mecinović J, Kramer HB, Kessler BM, Frapart YM, Boucher JL, Clifton IJ, McDonough MA, Schofield CJ. J Mol Biol 410 268-279 (2011)
  15. Insights into BAY 60-2770 activation and S-nitrosylation-dependent desensitization of soluble guanylyl cyclase via crystal structures of homologous nostoc H-NOX domain complexes. Kumar V, Martin F, Hahn MG, Schaefer M, Stamler JS, Stasch JP, van den Akker F. Biochemistry 52 3601-3608 (2013)
  16. Allostery in recombinant soluble guanylyl cyclase from Manduca sexta. Hu X, Murata LB, Weichsel A, Brailey JL, Roberts SA, Nighorn A, Montfort WR. J Biol Chem 283 20968-20977 (2008)
  17. Shrimp thioredoxin is a potent antioxidant protein. Aispuro-Hernandez E, Garcia-Orozco KD, Muhlia-Almazan A, Del-Toro-Sanchez L, Robles-Sanchez RM, Hernandez J, Gonzalez-Aguilar G, Yepiz-Plascencia G, Sotelo-Mundo RR. Comp Biochem Physiol C Toxicol Pharmacol 148 94-99 (2008)
  18. Force field parameters for S-nitrosocysteine and molecular dynamics simulations of S-nitrosated thioredoxin. Han S. Biochem Biophys Res Commun 377 612-616 (2008)
  19. Crystal structure of human thioredoxin revealing an unraveled helix and exposed S-nitrosation site. Weichsel A, Kem M, Montfort WR. Protein Sci 19 1801-1806 (2010)
  20. Post-translational S-nitrosylation is an endogenous factor fine tuning the properties of human S100A1 protein. Lenarčič Živković M, Zaręba-Kozioł M, Zhukova L, Poznański J, Zhukov I, Wysłouch-Cieszyńska A. J Biol Chem 287 40457-40470 (2012)
  21. Crystal structure of fully oxidized human thioredoxin. Hwang J, Nguyen LT, Jeon YH, Lee CY, Kim MH. Biochem Biophys Res Commun 467 218-222 (2015)
  22. A zinc-finger like metal binding site in the nucleosome. Adamczyk M, Poznański J, Kopera E, Bal W. FEBS Lett 581 1409-1416 (2007)
  23. Master redox regulator Trx1 upregulates SMYD1 & modulates lysine methylation. Liu T, Wu C, Jain MR, Nagarajan N, Yan L, Dai H, Cui C, Baykal A, Pan S, Ago T, Sadoshima J, Li H. Biochim Biophys Acta 1854 1816-1822 (2015)
  24. Slight Deuterium Enrichment in Water Acts as an Antioxidant: Is Deuterium a Cell Growth Regulator? Zhang X, Wang J, Zubarev RA. Mol Cell Proteomics 19 1790-1804 (2020)
  25. S-nitrosylation of Mycobacterium tuberculosis tyrosine phosphatase A (PtpA) induces its structural instability. Matiollo C, Ecco G, Menegatti AC, Razzera G, Vernal J, Terenzi H. Biochim Biophys Acta 1834 191-196 (2013)
  26. Molecular dynamics simulations of thioredoxin with S-glutathiolated cysteine-73. Han S. Biochem Biophys Res Commun 362 532-537 (2007)
  27. New insights into the posttranslational regulation of human cytosolic thioredoxin by S-palmitoylation. Xu Z, Zhong L. Biochem Biophys Res Commun 460 949-956 (2015)
  28. Deciphering the Path of S-nitrosation of Human Thioredoxin: Evidence of an Internal NO Transfer and Implication for the Cellular Responses to NO. Almeida VS, Miller LL, Delia JPG, Magalhães AV, Caruso IP, Iqbal A, Almeida FCL. Antioxidants (Basel) 11 1236 (2022)
  29. SP3-Enabled Rapid and High Coverage Chemoproteomic Identification of Cell-State-Dependent Redox-Sensitive Cysteines. Desai HS, Yan T, Yu F, Sun AW, Villanueva M, Nesvizhskii AI, Backus KM. Mol Cell Proteomics 21 100218 (2022)
  30. Nitric oxide delivery and heme-assisted S-nitrosation by the bedbug nitrophorin. Badgandi HB, Weichsel A, Montfort WR. J Inorg Biochem 246 112263 (2023)
  31. Oxidation is an underappreciated post-translational modification in the regulation of immune responses associated with changes in phosphorylation. Karkossa I, Fürst S, Großkopf H, von Bergen M, Schubert K. Front Immunol 14 1244431 (2023)


Related citations provided by authors (1)

  1. Crystal structures of reduced, oxidized, and mutated human thioredoxin: evidence for a regulatory homodimer. Weichsel A, Gasdaska JR, Powis G, Montfort WR Structure 4 735-751 (1996)

Quick links