Studies on the reaction of nitric oxide with the hypoxia-inducible factor prolyl hydroxylase domain 2 (EGLN1)

Journal of Molecular Biology

Volumn 410, Issue 2, 2011, Pages 268-279

  Chowdhury, Rasheduzzaman ^a   Flashman, Emily ^a   Mecinović, Jasmin ^a   Kramer, Holger B ^b   Kessler, Benedikt M ^b   Frapart, Yves M ^c   Boucher, Jean Luc ^c   Clifton, Ian J ^a   McDonough, Michael A ^a   Schofield, Christopher J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

2 oxoglutarate; hypoxia inducible factor; nitric oxide; oxygen dependent degradation domain; prolyl hydroxylase domain containing enzyme

Indexed keywords

CYSTEINE; HYPOXIA INDUCIBLE FACTOR; ISOENZYME; NITRIC OXIDE; NITRIC OXIDE DONOR; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE;

ARTICLE; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; MOLECULAR CLONING; OXYGEN SENSING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

ANIMALIA;

EID: 79958716098     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.04.075     Document Type: Article

References (67)

1. Chowdhury, R., Hardy, A. & Schofield, C. J. (2008). The human oxygen sensing machinery and its manipulation. Chem. Soc. Rev. 37, 1308-1319.
2. Kaelin, W. G., Jr & Ratcliffe, P. J. (2008). Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell, 30, 393-402.
3. Loenarz, C. & Schofield, C. J. (2008). Expanding chemical biology of 2-oxoglutarate oxygenases. Nat. Chem. Biol. 4, 152-156.
4. Semenza, G. L. (2009). Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda), 24, 97-106.
5. Moncada, S. & Higgs, A. (1993). The L-arginine-nitric oxide pathway. N. Engl. J. Med. 329, 2002-2012.
6. Xu, W., Charles, I. G. & Moncada, S. (2005). Nitric oxide: orchestrating hypoxia regulation through mitochondrial respiration and the endoplasmic reticulum stress response. Cell Res. 15, 63-65. (Pubitemid 41653968)
7. Berchner-Pfannschmidt, U., Tug, S., Kirsch, M. & Fandrey, J. (2010). Oxygen-sensing under the influence of nitric oxide. Cell. Signalling, 22, 349-356.
8. Metzen, E., Zhou, J., Jelkmann, W., Fandrey, J. & Brune, B. (2003). Nitric oxide impairs normoxic degradation of HIF-1α by inhibition of prolyl hydroxylases. Mol. Biol. Cell, 14, 3470-3481.
9. Peyssonnaux, C., Datta, V., Cramer, T., Doedens, A., Theodorakis, E. A., Gallo, R. L. et al. (2005). HIF-1α expression regulates the bactericidal capacity of phagocytes. J. Clin. Invest. 115, 1806-1815.
10. Hagen, T., Taylor, C. T., Lam, F. & Moncada, S. (2003). Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1α. Science, 302, 1975-1978. (Pubitemid 37523507)
11. Huang, L. E., Willmore, W. G., Gu, J., Goldberg, M. A. & Bunn, H. F. (1999). Inhibition of hypoxia-inducible factor 1 activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling. J. Biol. Chem. 274, 9038-9044.
12. Berchner-Pfannschmidt, U., Tug, S., Hu, J., Delos Reyes, B., Fandrey, J. & Kirsch, M. (2010). Role of N-acetyl-N-nitroso-tryptophan as nitric oxide donor in the modulation of HIF-1-dependent signaling. Biol. Chem. 391, 533-540.
13. Roach, P. L., Clifton, I. J., Hensgens, C. M., Shibata, N., Schofield, C. J., Hajdu, J. et al. (1997). Structure of isopenicillin N synthase complexed with substrate and the mechanism of penicillin formation. Nature, 387, 827-830. (Pubitemid 27270911)
14. Zhang, Z., Ren, J., Harlos, K., McKinnon, C. H., Clifton, I. J. & Schofield, C. J. (2002). Crystal structure of a clavaminate synthase-Fe(II)-2- oxoglutarate-substrate-NO complex: evidence for metal centered rearrangements. FEBS Lett. 517, 7-12. (Pubitemid 34327621)
15. McNeill, L. A., Flashman, E., Buck, M. R., Hewitson, K. S., Clifton, I. J., Jeschke, G. et al. (2005). Hypoxia-inducible factor prolyl hydroxylase 2 has a high affinity for ferrous iron and 2-oxoglutarate. Mol. Biosyst. 1, 321-324.
16. 2 activation by nonheme iron enzyme active sites. J. Am. Chem. Soc. 117, 715-732.
17. Gaffney, B. J. (2009). EPR of mononuclear non-heme iron proteins. Biol. Magn. Reson. 28, 233-268.
18. Galpin, J. R., Veldink, G. A., Vliegenthart, J. F. & Boldingh, J. (1978). The interaction of nitric oxide with soybean lipoxygenase-1. Biochim. Biophys. Acta, 536, 356-362.
19. McDonough, M. A., Li, V., Flashman, E., Chowdhury, R., Mohr, C., Lienard, B. M. et al. (2006). Cellular oxygen sensing: crystal structure of hypoxia-inducible factor prolyl hydroxylase (PHD2). Proc. Natl Acad. Sci. USA, 103, 9814-9819.
20. Schreiter, E. R., Rodriguez, M. M., Weichsel, A., Montfort, W. R. & Bonaventura, J. (2007). S-Nitrosylation-induced conformational change in blackfin tuna myoglobin. J. Biol. Chem. 282, 19773-19780.
21. Chan, N. L., Kavanaugh, J. S., Rogers, P. H. & Arnone, A. (2004). Crystallographic analysis of the interaction of nitric oxide with quaternary-T human hemoglobin. Biochemistry, 43, 118-132. (Pubitemid 38055947)
22. Zhao, Y. L. & Houk, K. N. (2006). Thionitroxides, RSNHO*: the structure of the SNO moiety in "S-nitrosohemoglobin", a possible NO reservoir and transporter. J. Am. Chem. Soc. 128, 1422-1423.
23. Chan, N. L., Rogers, P. H. & Arnone, A. (1998). Crystal structure of the S-nitroso form of liganded human hemoglobin. Biochemistry, 37, 16459-16464. (Pubitemid 28543903)
24. Chen, Y. Y., Chu, H. M., Pan, K. T., Teng, C. H., Wang, D. L., Wang, A. H. et al. (2008). Cysteine S-nitrosylation protects protein-tyrosine phosphatase 1B against oxidation-induced permanent inactivation. J. Biol. Chem. 283, 35265-35272.
25. Frey, D., Braun, O., Briand, C., Vasak, M. & Grutter, M. G. (2006). Structure of the mammalian NOS regulator dimethylarginine dimethylaminohydrolase: a basis for the design of specific inhibitors. Structure, 14, 901-911. (Pubitemid 43674095)
26. Hubbard, S. J., Campbell, S. F. & Thornton, J. M. (1991). Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors. J. Mol. Biol. 220, 507-530.
27. Weichsel, A., Brailey, J. L. & Montfort, W. R. (2007). Buried S-nitrosocysteine revealed in crystal structures of human thioredoxin. Biochemistry, 46, 1219-1227. (Pubitemid 46208470)
28. Weichsel, A., Maes, E. M., Andersen, J. F., Valenzuela, J. G., Shokhireva, T., Walker, F. A. et al. (2005). Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein. Proc. Natl Acad. Sci. USA, 102, 594-599.
29. Flashman, E., Davies, S. L., Yeoh, K.K.&Schofield, C. J. (2010). Investigating the dependence of the hypoxia-inducible factor hydroxylases (factor inhibiting HIF and prolyl hydroxylase domain 2) on ascorbate and other reducing agents. Biochem. J. 427, 135-142.
30. Jaffrey, S. R., Erdjument-Bromage, H., Ferris, C. D., Tempst, P. & Snyder, S. H. (2001). Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3, 193-197.
31. Chen, Y. Y., Huang, Y. F., Khoo, K. H. & Meng, T. C. (2007). Mass spectrometry-based analyses for identifying and characterizing S-nitrosylation of protein tyrosine phosphatases. Methods, 42, 243-249.
32. Jorge, I., Casas, E. M., Villar, M., Ortega-Perez, I., Lopez-Ferrer, D., Martinez-Ruiz, A. et al. (2007). High-sensitivity analysis of specific peptides in complex samples by selected MS/MS ion monitoring and linear ion trap mass spectrometry: application to biological studies. J. Mass Spectrom. 42, 1391-1403. (Pubitemid 350113456)
33. Zech, B., Wilm, M., van Eldik, R. & Brune, B. (1999). Mass spectrometric analysis of nitric oxide-modified caspase-3. J. Biol. Chem. 274, 20931-20936.
34. Kaneko, R. & Wada, Y. (2003). Decomposition of protein nitrosothiolsin matrix-assisted laser desorption/ ionization and electrospray ionization mass spectrometry. J. Mass Spectrom. 38, 526-530. (Pubitemid 36665539)
35. Choi, S., Jeong, J., Na, S., Lee, H. S., Kim, H. Y., Lee, K. J. et al. (2010). New algorithm for the identification of intact disulfide linkages based on fragmentation characteristics in tandem mass spectra. J. Proteome Res. 9, 626-635.
36. Burg, A., Cohen, H. & Meyerstein, D. (2000). The reaction mechanism of nitrosothiols with copper(I). J. Biol. Inorg. Chem. 5, 213-217.
37. Noble, D. R. & Williams, D. L. (2000). Structure-reactivity studies of the Cu2+-catalyzed decomposition of four S-nitrosothiols based around the S-nitrosocysteine/S-nitrosoglutathione structures. Nitric Oxide, 4, 392-398. (Pubitemid 30664033)
38. Martin, F., Linden, T., Katschinski, D. M., Oehme, F., Flamme, I., Mukhopadhyay, C. K. et al. (2005). Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation. Blood, 105, 4613-4619. (Pubitemid 40807279)
39. Brune, B. & Zhou, J. (2007). Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc. Res. 75, 275-282.
40. Hall, C. N. & Garthwaite, J. (2009). What is the real physiological NO concentration in vivo? Nitric Oxide, 21, 92-103.
41. Privett, B. J., Shin, J. H. & Schoenfisch, M. H. (2010). Electrochemical nitric oxide sensors for physiological measurements. Chem. Soc. Rev. 39, 1925-1935.
42. Thomas, D. D., Ridnour, L. A., Isenberg, J. S., Flores-Santana, W., Switzer, C. H., Donzelli, S. et al. (2008). The chemical biology of nitric oxide: implications in cellular signaling. Free Radical Biol. Med. 45, 18-31.
43. Tuckerman, J. R., Zhao, Y., Hewitson, K. S., Tian, Y. M., Pugh, C. W., Ratcliffe, P. J. et al. (2004). Determination and comparison of specific activity of the HIF-prolyl hydroxylases. FEBS Lett. 576, 145-150. (Pubitemid 39330473)
44. D'Angelo, G., Duplan, E., Boyer, N., Vigne, P. & Frelin, C. (2003). Hypoxia up-regulates prolyl hydroxylase activity: a feedback mechanism that limits HIF-1 responses during reoxygenation. J. Biol. Chem. 278, 38183-38187.
45. Marxsen, J. H., Stengel, P., Doege, K., Heikkinen, P., Jokilehto, T., Wagner, T. et al. (2004). Hypoxia-inducible factor-1 (HIF-1) promotes its degradation by induction of HIF-alpha-prolyl-4-hydroxylases. Biochem. J. 381, 761-767. (Pubitemid 39120486)
46. Cesareo, E., Parker, L. J., Pedersen, J. Z., Nuccetelli, M., Mazzetti, A. P., Pastore, A. et al. (2005). Nitrosylation of human glutathione transferase P1-1 with dinitrosyl diglutathionyl iron complex in vitro and in vivo. J. Biol. Chem. 280, 42172-42180.
47. Karlsson, A., Parales, J. V., Parales, R. E., Gibson, D. T., Eklund, H. & Ramaswamy, S. (2005). NO binding to naphthalene dioxygenase. J. Biol. Inorg. Chem. 10, 483-489.
48. Nagashima, S., Nakasako, M., Dohmae, N., Tsujimura, M., Takio, K., Odaka, M. et al. (1998). Novel non-heme iron center of nitrile hydratase with a claw setting of oxygen atoms. Nat. Struct. Biol. 5, 347-351.
49. Sato, N., Uragami, Y., Nishizaki, T., Takahashi, Y., Sazaki, G., Sugimoto, K. et al. (2002). Crystal structures of the reaction intermediate and its homologue of an extradiol-cleaving catecholic dioxygenase. J. Mol. Biol. 321, 621-636.
50. Dang, L., Jin, S. & Su, S. M. (2010). IDH mutations in glioma and acute myeloid leukemia. Trends Mol. Med. 16, 387-397.
51. Chowdhury, R., McDonough, M. A., Mecinovic, J., Loenarz, C., Flashman, E., Hewitson, K. S. et al. (2009). Structural basis for binding of hypoxia-inducible factor to the oxygen-sensing prolyl hydroxylases. Structure, 17, 981-989.
52. Loenarz, C., Coleman, M. L., Boleininger, A., Schierwater, B., Holland, P. W., Ratcliffe, P. J. et al. (2011). The hypoxia-inducible transcription factor pathway regulates oxygen sensing in the simplest animal, Trichoplax adhaerens. EMBO Rep. 12, 63-70.
53. Mecinovic, J., Chowdhury, R., Flashman, E. & Schofield, C. J. (2009). Use of mass spectrometry to probe the nucleophilicity of cysteinyl residues of prolyl hydroxylase domain 2. Anal. Biochem. 393, 215-221.
54. Singh, S. P., Wishnok, J. S., Keshive, M., Deen, W. M. & Tannenbaum, S. R. (1996). The chemistry of the S-nitrosoglutathione/glutathione system. Proc. Natl Acad. Sci. USA, 93, 14428-14433.
55. Stamler, J. S. & Toone, E. J. (2002). The decomposition of thionitrites. Curr. Opin. Chem. Biol. 6, 779-785.
56. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E. &Stamler, J. S. (2005). Protein S-nitrosylation: purview and parameters. Nat. Rev., Mol. Cell Biol. 6, 150-166.
57. Meister, A. & Anderson, M. E. (1983). Glutathione. Annu. Rev. Biochem. 52, 711-760.
58. Mirza, U. A., Chait, B. T. & Lander, H. M. (1995). Monitoring reactions of nitric oxide with peptides and proteins by electrospray ionization-mass spectrometry. J. Biol. Chem. 270, 17185-17188.
59. Flashman, E., Bagg, E. A., Chowdhury, R., Mecinovic, J., Loenarz, C., McDonough, M. A. et al. (2008). Kinetic rationale for selectivity toward N- and C-terminal oxygen-dependent degradation domain substrates mediated by a loop region of hypoxia-inducible factor prolyl hydroxylases. J. Biol. Chem. 283, 3808-3815.
60. Xu, D., Suenaga, N., Edelmann, M. J., Fridman, R., Muschel, R. J. & Kessler, B. M. (2008). Novel MMP-9 substrates in cancer cells revealed by a label-free quantitative proteomics approach. Mol. Cell. Proteomics, 7, 2215-2228.
61. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326. (Pubitemid 27085611)
62. Bailey, S. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 50, 760-763.
63. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. & Read, R. J. (2007). Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674.
64. Schuttelkopf, A. W. & van Aalten, D. M. (2004). PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 1355-1363. (Pubitemid 41079731)
65. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W. et al. (1998). Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
66. Emsley, P. & Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132. (Pubitemid 41742764)
67. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.