Thioredoxin-mimetic peptides as catalysts of S-denitrosylation and anti-nitrosative stress agents

Free Radical Biology and Medicine

Volumn 79, Issue , 2015, Pages 138-146

  Kronenfeld, Gali ^a   Engelman, Rotem ^a   Weisman Shomer, Pnina ^a   Atlas, Daphne ^b   Benhar, Moran ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Denitrosylation; Free radicals; Nitrosative stress; Thiols; Thioredoxin mimetic peptides

Indexed keywords

AMIDE; CELL PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; S NITROSOGLUTATHIONE; THIOREDOXIN; THIOREDOXIN REDUCTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATALYST; CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CELLS BY BODY ANATOMY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULINOMA; MOLECULE; NEUROBLASTOMA; NITROSATIVE STRESS; NITROSYLATION; NONHUMAN; RAT; CATALYSIS; CELL LINE; CHEMISTRY; METABOLISM; MOLECULAR MIMICRY; MOLECULAR WEIGHT; NITROSATION;

RATTUS;

CATALYSIS; CELL LINE; HUMANS; MOLECULAR MIMICRY; MOLECULAR WEIGHT; NITROSATION; THIOREDOXINS;

EID: 84920072830     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.11.021     Document Type: Article

References (36)

1. Hess, D. T.; Matsumoto, A.; Kim, S. O.; Marshall, H. E.; Stamler, J. S. Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6:150-166; 2005.
2. Gould, N.; Doulias, P. T.; Tenopoulou, M.; Raju, K.; Ischiropoulos, H. Regulation of protein function and signaling by reversible cysteine S-nitrosylation. J. Biol. Chem. 288:26473-26479; 2013.
3. Foster, M. W.; Hess, D. T.; Stamler, J. S. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol. Med. 15:391-404; 2009.
4. Nakamura, T.; Tu, S.; Akhtar, M. W.; Sunico, C. R.; Okamoto, S.; Lipton, S. A. Aberrant protein S-nitrosylation in neurodegenerative diseases. Neuron 78:596-614; 2013.
5. Shahani, N.; Sawa, A. Nitric oxide signaling and nitrosative stress in neurons: role for S-nitrosylation. Antioxid. Redox Signaling 14:1493-1504; 2011.
6. Lima, B.; Forrester, M. T.; Hess, D. T.; Stamler, J. S. S-nitrosylation in cardiovascular signaling. Circ. Res. 106: 633-646; 2010.
7. Ovadia, H.; Haim, Y.; Nov, O.; Almog, O.; Kovsan, J.; Bashan, N.; Benhar, M.; Rudich, A. Increased adipocyte S-nitrosylation targets anti-lipolytic action of insulin: relevance to adipose tissue dysfunction in obesity. J. Biol. Chem. 286:30433-30443; 2011.
8. - donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch. Biochem. Biophys. 318: 279-285; 1995.
9. Haendeler, J.; Weiland, U.; Zeiher, A. M.; Dimmeler, S. Effects of redox-related congeners of NO on apoptosis and caspase-3 activity. Nitric Oxide 1:282-293; 1997.
10. Stoyanovsky, D. A.; Tyurina, Y. Y.; Tyurin, V. A.; Anand, D.; Mandavia, D. N.; Gius, D.; Ivanova, J.; Pitt, B.; Billiar, T. R.; Kagan, V. E. Thioredoxin and lipoic acid catalyze the denitrosation of low molecular weight and protein S-nitrosothiols. J. Am. Chem. Soc. 127:15815-15823; 2005.
11. Benhar, M.; Forrester, M. T.; Stamler, J. S. Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 10:721-732; 2009.
12. Benhar, M.; Forrester, M. T.; Hess, D. T.; Stamler, J. S. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050-1054; 2008.
13. Benhar, M.; Thompson, J. W.; Moseley, M. A.; Stamler, J. S. Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49:6963-6969; 2010.
14. Sengupta, R.; Holmgren, A. The role of thioredoxin in the regulation of cellular processes by S-nitrosylation. Biochim. Biophys. Acta 1820: 689-700; 2012.
15. Ben-Lulu, S.; Ziv, T.; Admon, A.; Weisman-Shomer, P.; Benhar, M. A substrate trapping approach identifies proteins regulated by reversible S-nitrosylation. Mol. Cell. Proteomics 13:2573-2583; 2014.
16. Kneeshaw, S.; Gelineau, S.; Tada, Y.; Loake, G. J.; Spoel, S. H. Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol. Cell 56:153-162; 2014.
17. Forrester, M. T.; Seth, D.; Hausladen, A.; Eyler, C. E.; Foster, M. W.; Matsumoto, A.; Benhar, M.; Marshall, H. E.; Stamler, J. S. Thioredoxin-interacting protein (Txnip) is a feedback regulator of S-nitrosylation. J. Biol. Chem. 284:36160-36166; 2009.
18. Kelleher, Z. T.; Sha, Y.; Foster, M. W.; Foster, W. M.; Forrester, M. T.; Marshall, H. E. Thioredoxin-mediated denitrosylation regulates cytokine-induced nuclear factor kappaB (NF-kappaB) activation. J. Biol. Chem. 289:3066-3072; 2014.
19. Bartov, O. Sultana, R.; Butterfield, D. A.; Atlas, D. Low molecular weight thiol amides attenuate MAPK activity and protect primary neurons from Abeta(1-42) toxicity. Brain Res. 1069: 198-206; 2006.
20. Bachnoff, N.; Trus, M.; Atlas, D. Alleviation of oxidative stress by potent and selective thioredoxin-mimetic peptides. Free Radic. Biol. Med. 50:1355-1367; 2011.
21. Cohen-Kutner, M.; Khomsky, L.; Trus, M.; Aisner, Y.; Niv, M. Y.; Benhar, M.; Atlas, D. Thioredoxin-mimetic peptides (TXM) reverse auranofin induced apoptosis and restore insulin secretion in insulinoma cells. Biochem. Pharmacol. 85:977-990; 2013.
22. Kim, S. R.; Lee, K. S.; Park, S. J.; Min, K. H.; Lee, M. H.; Lee, K. A.; Bartov, O.; Atlas, D.; Lee, Y. C. A novel dithiol amide CB3 attenuates allergic airway disease through negative regulation of p38 mitogen-activated protein kinase. Am. J. Respir Crit. Care Med. 183:1015-1024; 2011.
23. Cohen-Kutner, M.; Khomsky, L.; Trus, M.; Ben-Yehuda, H.; Lenhard, J. M.; Liang, Y.; Martin, T.; Atlas, D. Thioredoxin-mimetic peptide CB3 lowers MAPKinase activity in the Zucker rat brain. Redox Biol. 2:447-456; 2014.
24. Engelman, R.; Weisman-Shomer, P.; Ziv, T.; Xu, J.; Arner, E. S.; Benhar, M. Multilevel regulation of 2-Cys peroxiredoxin reaction cycle by S-nitrosylation. J. Biol. Chem. 288: 11312-11324; 2013.
25. Nelson, K. J.; Parsonage, D. Measurement of peroxiredoxin activity. Curr. Protoc. Toxicol :10; 2011. (Chap. 7:Unit 7).
26. Arner, E. S.; Holmgren, A. Measurement of thioredoxin and thioredoxin reductase. Curr. Protoc. Toxicol :4; 2001. (Chap. 7:Unit 7).
27. Forrester, M. T.; Thompson, J. W.; Foster, M. W.; Nogueira, L.; Moseley, M. A.; Stamler, J. S. Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture. Nat. Biotechnol. 27:557-559; 2009.
28. Nikitovic, D.; Holmgren, A. S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J. Biol. Chem. 271:19180-19185; 1996.
29. Fang, J.; Nakamura, T.; Cho, D. H.; Gu, Z.; Lipton, S. A. S-nitrosylation of peroxiredoxin 2 promotes oxidative stress-induced neuronal cell death in Parkinson's disease. Proc. Natl. Acad. Sci. USA 104: 18742-18747; 2007.
30. Zareba-Koziol, M.; Szwajda, A.; Dadlez, M.; Wyslouch-Cieszynska, A.; Lalowski, M. Global analysis of S-nitrosylation sites in the wild type (APP) transgenic mouse brain-clues for synaptic pathology. Mol. Cell. Proteomics 13:2288-2305; 2014.
31. Sen, N.; Hara, M. R.; Kornberg, M. D.; Cascio, M. B.; Bae, B. I.; Shahani, N.; Thomas, B.; Dawson, T. M.; Dawson, V. L.; Snyder, S. H.; Sawa, A. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat. Cell Biol. 10:866-873; 2008.
32. Benhar, M.; Stamler, J. S. A central role for S-nitrosylation in apoptosis. Nat. Cell Biol. 7:645-646; 2005.
33. Banci, L.; Bertini, I.; Cefaro, C.; Ciofi-Baffoni, S.; Gallo, A.; Martinelli, M.; Sideris, D. P.; Katrakili, N.; Tokatlidis, K. MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat. Struct. Mol. Biol. 16:198-206; 2009.
34. Zahid, S.; Khan, R.; Oellerich, M.; Ahmed, N.; Asif, A. R. Differential S-nitrosylation of proteins in Alzheimer's disease. Neuroscience 256:126-136; 2014.
35. Lillig, C. H.; Holmgren, A. Thioredoxin and related molecules-from biology to health and disease. Antioxid. Redox Signaling 9:25-47; 2007.
36. Arnér, E. S. Focus on mammalian thioredoxin reductases-important selenoproteins with versatile functions. Biochim. Biophys. Acta 1790:495-526; 2009.