Thioredoxin-1 regulates cellular heme insertion by controlling S-nitrosation of glyceraldehyde-3-phosphate dehydrogenase

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16179-16186

  Chakravarti, Ritu ^a   Stuehr, Dennis J ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL EXPRESSION; CYTOKINE ACTIVATION; DENITROSATION; DYNAMIC PROCESS; EXPRESSION LEVELS; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; HEME PROTEINS; MACROPHAGE-LIKE CELLS; NO DONOR; OVER-EXPRESSION; RECOVERY TIME; S-NITROSATION; S-NITROSOGLUTATHIONE; SLOW RELEASE;

CELLS; CHEMICAL REACTIONS; CYTOLOGY; PORPHYRINS; PROTEINS; RECOVERY; RESPIRATORY MECHANICS;

MOLECULAR BIOLOGY;

GLUTATHIONE REDUCTASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEME; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE; S NITROSOGLUTATHIONE; S NITROSOGLUTATHIONE REDUCTASE; THIOREDOXIN 1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; MACROPHAGE; NITROSATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING;

ALDEHYDE OXIDOREDUCTASES; AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; GENE KNOCKDOWN TECHNIQUES; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HEME; MACROPHAGES; MICE; MUTATION, MISSENSE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; THIOREDOXINS;

EID: 84860875546     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.342758     Document Type: Article

References (38)

1. Benhar, M., Forrester, M. T., and Stamler, J. S. (2009) Protein denitrosylation: enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 10, 721-732
2. Guikema, B., Lu, Q., and Jourd'heuil, D. (2005) Chemical considerations and biological selectivity of protein nitrosation: implications for NO-mediated signal transduction. Antioxid. Redox Signal. 7, 593-606 (Pubitemid 40563197)
3. Lima, B., Lam, G. K., Xie, L., Diesen, D. L., Villamizar, N., Nienaber, J., Messina, E., Bowles, D., Kontos, C. D., Hare, J. M., Stamler, J. S., and Rockman, H. A. (2009) Endogenous S-nitrosothiols protect against myocardial injury. Proc. Natl. Acad. Sci. U.S.A. 106, 6297-6302
4. Thomas, D. D., Ridnour, L. A., Isenberg, J. S., Flores-Santana, W., Switzer, C. H., Donzelli, S., Hussain, P., Vecoli, C., Paolocci, N., Ambs, S., Colton, C. A., Harris, C. C., Roberts, D. D., and Wink, D. A. (2008) The chemical biology of nitric oxide: implications in cellular signaling. Free Radic. Biol. Med. 45, 18-31
5. 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
6. Kornberg, M. D., Sen, N., Hara, M. R., Juluri, K. R., Nguyen, J. V., Snowman, A. M., Law, L., Hester, L. D., and Snyder, S. H. (2010) GAPDH mediates nitrosylation of nuclear proteins. Nat. Cell Biol. 12, 1094-1100
7. Benhar, M., Thompson, J. W., Moseley, M. A., and Stamler, J. S. (2010) Identification of S-nitrosylated targets of thioredoxin using a quantitative proteomic approach. Biochemistry 49, 6963-6969
8. Sengupta, R., and Holmgren, A. (2012) The role of thioredoxin in the regulation of cellular processes by S-nitrosylation. Biochim. Biophys. Acta doi: 10.1016/j.bbagen.2011.08/012
9. Mitchell, D. A., and Marletta, M. A. (2005) Thioredoxin catalyzes the S-nitrosation of the caspase-3 active site cysteine. Nat. Chem. Biol. 1, 154-158
10. Benhar, M., Forrester, M. T., Hess, D. T., and Stamler, J. S. (2008) Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320, 1050-1054 (Pubitemid 351929542)
11. Kim, Y. M., Kim, T. H., Chung, H. T., Talanian, R. V., Yin, X. M., and Billiar, T. R. (2000) Nitric oxide prevents tumor necrosis factor α-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology 32, 770-778
12. Sengupta, R., Billiar, T. R., Kagan, V. E., and Stoyanovsky, D. A. (2010) Nitric oxide and thioredoxin type 1 modulate the activity of caspase-8 in HepG2 cells. Biochem. Biophys. Res. Commun. 391, 1127-1130
13. Ecco, G., Vernal, J., Razzera, G., Martins, P. A., Matiollo, C., and Terenzi, H. (2010) Mycobacterium tuberculosis tyrosine phosphatase A (PtpA) activity is modulated by S-nitrosylation. Chem. Commun. 46, 7501-7503
14. Whalen, E. J., Foster, M. W., Matsumoto, A., Ozawa, K., Violin, J. D., Que, L. G., Nelson, C. D., Benhar, M., Keys, J. R., Rockman, H. A., Koch, W. J., Daaka, Y., Lefkowitz, R. J., and Stamler, J. S. (2007) Regulation of β-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell 129, 511-522 (Pubitemid 46660966)
15. Moore, P. E., Ryckman, K. K., Williams, S. M., Patel, N., Summar, M. L., and Sheller, J. R. (2009) Genetic variants of GSNOR and ADRB2 influence response to albuterol in African-American children with severe asthma. Pediatr. Pulmonol. 44, 649-654
16. Waheed, S. M., Ghosh, A., Chakravarti, R., Biswas, A., Haque, M. M., Panda, K., and Stuehr, D. J. (2010) Nitric oxide blocks cellular heme insertion into a broad range of heme proteins. Free Radic. Biol. Med. 48, 1548-1558
17. Albakri, Q. A., and Stuehr, D. J. (1996) Intracellular assembly of inducible NO synthase is limited by nitric oxide-mediated changes in heme insertion and availability. J. Biol. Chem. 271, 5414-5421 (Pubitemid 26084448)
18. Chakravarti, R., Aulak, K. S., Fox, P. L., and Stuehr, D. J. (2010) GAPDH regulates cellular heme insertion into inducible nitric-oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 107, 18004-18009
19. Hara, M. R., Cascio, M. B., and Sawa, A. (2006) GAPDH as a sensor of NO stress. Biochim. Biophys. Acta 1762, 502-509
20. Sirover, M. A. (1999) New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim. Biophys. Acta 1432, 159-184
21. Padgett, C. M., and Whorton, A. R. (1995) S-Nitrosoglutathione reversibly inhibits GAPDH by S-nitrosylation. Am. J. Physiol. 269, C739-C749
22. Padgett, C. M., and Whorton, A. R. (1997) Glutathione redox cycle regulates nitric oxide-mediated glyceraldehyde-3-phosphate dehydrogenase inhibition. Am. J. Physiol. 272, C99-C108
23. Koenitzer, J. R., and Freeman, B. A. (2010) Redox signaling in inflammation: interactions of endogenous electrophiles and mitochondria in cardiovascular disease. Ann. N.Y. Acad. Sci. 1203, 45-52
24. Liu, L., Hausladen, A., Zeng, M., Que, L., Heitman, J., and Stamler, J. S. (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410, 490-494 (Pubitemid 32240051)
25. Tang, C. H., Wei, W., and Liu, L. (2011) Regulation of DNA repair by S-nitrosylation. Biochim. Biophys. Acta, doi:10.1016/j.bbagen.2011.04.014
26. Ito, T., Yamakuchi, M., and Lowenstein, C. J. (2011) Thioredoxin increases exocytosis by denitrosylating N-ethylmaleimide-sensitive factor. J. Biol. Chem. 286, 11179-11184
27. 6-alkylguanine-DNA alkyltransferase and increased sensitivity to genotoxic diethylnitrosamine. Carcinogenesis 32, 973-977
28. Yang, Z., Wang, Z. E., Doulias, P. T., Wei, W., Ischiropoulos, H., Locksley, R. M., and Liu, L. (2010) Lymphocyte development requires S-nitrosoglutathione reductase. J. Immunol. 185, 6664-6669
29. Panda, K., Chawla-Sarkar, M., Santos, C., Koeck, T., Erzurum, S. C., Parkinson, J. F., and Stuehr, D. J. (2005) Visualizing inducible nitric-oxide synthase in living cells with a heme-binding fluorescent inhibitor. Proc. Natl. Acad. Sci. U.S.A. 102, 10117-10122 (Pubitemid 41023335)
30. Jaffrey, S. R., and Snyder, S. H. (2001) The biotin switch method for the detection of S-nitrosylated proteins. Sci. STKE 2001, pl1
31. Molina y Vedia, L., McDonald, B., Reep, B., Brüne, B., Di Silvio, M., Billiar, T. R., and Lapetina, E. G. (1992) Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation. J. Biol. Chem. 267, 24929-24932
32. Mooradian, D. L., Hutsell, T. C., and Keefer, L. K. (1995) Nitric oxide (NO) donor molecules: effect of NO release rate on vascular smooth muscle cell proliferation in vitro. J. Cardiovasc. Pharmacol. 25, 674-678
33. Hara, M. R., Agrawal, N., Kim, S. F., Cascio, M. B., Fujimuro, M., Ozeki, Y., Takahashi, M., Cheah, J. H., Tankou, S. K., Hester, L. D., Ferris, C. D., Hayward, S. D., Snyder, S. H., and Sawa, A. (2005) S-Nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat. Cell Biol. 7, 665-674 (Pubitemid 40975747)
34. Barglow, K. T., Knutson, C. G., Wishnok, J. S., Tannenbaum, S. R., and Marletta, M. A. (2011) Site-specific and redox-controlled S-nitrosation of thioredoxin. Proc. Natl. Acad. Sci. U.S.A. 108, E600-E606
35. Que, L. G., Liu, L., Yan, Y., Whitehead, G. S., Gavett, S. H., Schwartz, D. A., and Stamler, J. S. (2005) Protection from experimental asthma by an endogenous bronchodilator. Science 308, 1618-1621 (Pubitemid 40807509)
36. Sengupta, R., Ryter, S. W., Zuckerbraun, B. S., Tzeng, E., Billiar, T. R., and Stoyanovsky, D. A. (2007) Thioredoxin catalyzes the denitrosation of low molecular mass and protein S-nitrosothiols. Biochemistry 46, 8472-8483 (Pubitemid 47075984)
37. Xu, W., Zheng, S., Dweik, R. A., and Erzurum, S. C. (2006) Role of epithelial nitric oxide in airway viral infection. Free Radic. Biol. Med. 41, 19-28 (Pubitemid 43884780)
38. Hara, M. R., Thomas, B., Cascio, M. B., Bae, B. I., Hester, L. D., Dawson, V. L., Dawson, T. M., Sawa, A., and Snyder, S. H. (2006) Neuroprotection by pharmacologic blockade of the GAPDH death cascade. Proc. Natl. Acad. Sci. U.S.A. 103, 3887-3889 (Pubitemid 43376650)