Molecular insights of p47phox phosphorylation dynamics in the regulation of NADPH oxidase activation and superoxide production

Journal of Biological Chemistry

Volumn 289, Issue 33, 2014, Pages 22759-22770

  Meijles, Daniel N ^a   Fan, Lampson M ^b   Howlin, Brendan J ^a   Li, Jian Mei ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL ACTIVATION; ENDOTHELIAL CELLS; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; OXYGEN; PROTEINS;

CONFORMATIONAL CHANGE; INTRAMOLECULAR INTERACTIONS; MEMBRANE TRANSLOCATION; MOLECULAR DYNAMICS SIMULATIONS; SITE DIRECTED MUTAGENESIS; STRUCTURAL INFORMATION; STRUCTURAL MODELING; SUPEROXIDE PRODUCTION;

PHOSPHORYLATION;

ALANINE; PROTEIN P22; PROTEIN P47; PROTEIN SH3; PROTEIN TYROSINE KINASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERINE; SUPEROXIDE; NEUTROPHIL CYTOSOLIC FACTOR 1;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME REGULATION; HOST RESISTANCE; HUMAN; HYDROGEN BOND; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; AMINO ACID SUBSTITUTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MISSENSE MUTATION; MOUSE; PHOSPHORYLATION; PHYSIOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; ANIMALS; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ENZYME ACTIVATION; HYDROGEN BONDING; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTATION, MISSENSE; NADPH OXIDASE; PHOSPHORYLATION; SUPEROXIDES;

EID: 84905979611     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.561159     Document Type: Article

References (38)

1. Bedard, K., and Krause, K.-H. (2007) The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol. Rev. 87, 245-313 (Pubitemid 46209993)
2. Babior, B. M., Lambeth, J. D., and Nauseef, W. (2002) The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397, 342-344 (Pubitemid 34852301)
3. Li, J.-M., and Shah, A. M. (2004) Endothelial cell superoxide generation: Regulation and relevance for cardiovascular pathophysiology. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R1014-R1030 (Pubitemid 39391043)
4. Drummond, G. R., Selemidis, S., Griendling, K. K., and Sobey, C. G. (2011) Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 10, 453-471
5. Lambeth, J. D., Cheng, G., Arnold, R. S., and Edens, W. A. (2000) Novel homologs of gp91phox. Trends Biochem. Sci. 25, 459-461
6. Nauseef, W. M. (2004) Assembly of the phagocyte NADPH oxidase. Histochem. Cell Biol. 122, 277-291
7. Perisic, O., Wilson, M. I., Karathanassis, D., Bravo, J., Pacold, M. E., Ellson, C. D., Hawkins, P. T., Stephens, L., and Williams, R. L. (2004) The role of phosphoinositides and phosphorylation in regulation of NADPH oxidase. Adv. Enzyme Regul. 44, 279-298 (Pubitemid 39568177)
8. Sumimoto, H., Miyano, K., and Takeya, R. (2005) Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem. Biophys. Res. Commun. 338, 677-686 (Pubitemid 41540615)
9. El-Benna, J., Dang, P. M.-C., and Gougerot-Pocidalo, M.-A. (2008) Priming of the neutrophil NADPH oxidase activation: Role of p47phox phosphorylation and NOX2 mobilization to the plasma membrane. Semin. Immunopathol. 30, 279-289
10. phox and on NADPH oxidase activation. Biochemistry 41, 7743-7750
11. Li, J.-M., Fan, L. M., Christie, M. R., and Shah, A. M. (2005) Acute tumor necrosis factor alpha signaling via NADPH oxidase in microvascular endothelial cells: role of p47phox phosphorylation and binding to TRAF4. Mol. Cell. Biol 25, 2320-2330 (Pubitemid 40354628)
12. Li, J.-M., and Shah, A. M. (2003) Mechanism of endothelial cell NADPH oxidase activation by angiotensin II: Role of the p47phox subunit. J. Biol. Chem. 278, 12094-12100 (Pubitemid 36800187)
13. McPhail, L. C. (1994) SH3-dependent assembly of the phagocyte NADPH oxidase. J. Exp. Med. 180, 2011-2015
14. Groemping, Y., Lapouge, K., Smerdon, S. J., and Rittinger, K. (2003) Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell 113, 343-355 (Pubitemid 36556116)
15. phox: Insights into the mechanism of activation. Biophys. J. 99, 3716-3725
16. phox SH3 domains. J. Biol. Chem. 280, 13752-13761
17. phox, a subunit of the respiratory burst oxidase. J. Clin. Invest. 96, 1499-1505
18. phox phosphorylation at S303-4 or S379 on tumor necrosis factor-α signaling via TRAF4 and MAPK in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 32, 1488-1496
19. phox, Grb2 and Pex13p. EMBO J. 21, 4268-4276
20. Jefferys, B. R., Kelley, L. A., and Sternberg, M. J. (2010) Protein folding requires crowd control in a simulated cell. J. Mol. Biol. 397, 1329-1338
21. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
22. Shen, H. D., Tam, M. F., Huang, C. H., Chou, H., Tai, H. Y., Chen, Y. S., Sheu, S. Y., and Thomas, W. R. (2011) Homology modeling and monoclonal antibody binding of the Der f 7 dust mite allergen. Immunol. Cell Biol. 89, 225-230
23. Schwede, T., Kopp, J., Guex, N., and Peitsch, M. C. (2003) SWISSMODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31, 3381-3385 (Pubitemid 37442164)
24. Rost, B., and Sander, C. (1994) Conservation and prediction of solvent accessibility in protein families. Proteins 20, 216-226 (Pubitemid 24378913)
25. phox subunit of the NADPH oxidase. Comput. Biol. Chem. 39, 6-13
26. Wass, M. N., Fuentes, G., Pons, C., Pazos, F., and Valencia, A. (2012) Towards the prediction of protein interaction partners using physical docking. Mol. Syst. Biol. 7, 469-doi:10.1038/msb.2011.3
27. Li, J.-M., Mullen, A. M., and Shah, A. M. (2001) Phenotypic properties and characteristics of superoxide production by mouse coronary microvascular endothelial cells. J. Mol. Cell. Cardiol. 33, 1119-1131 (Pubitemid 32579279)
28. Fan, L. M., and Li, J. M. (2014) Evaluation of methods of detecting cell reactive oxygen species production for drug screening and cell cycle studies. J. Pharmacol. Toxicol. Methods 70, 40-47
29. phox in reactive oxygen species production in microvascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 29, 1651-1656
30. Du, J., Fan, L. M., Mai, A., and Li, J.-M. (2013) Crucial roles of Nox2- derived oxidative stress in deteriorating the function of insulin receptor and endothelium in dietary obesity of middle-aged mice. Br. J. Pharmacol. 170, 1064-1077
31. Durand, D., Cannella, D., Dubosclard, V., Pebay-Peyroula, E., Vachette, P., and Fieschi, F. (2006) Small-angle X-ray scattering reveals an extended organization for the autoinhibitory resting state of the p47(phox) modular protein. Biochemistry 45, 7185-7193 (Pubitemid 43877407)
32. Lambeth, J. D. (2007) Nox enzymes, ROS, and chronic disease: An example of antagonistic pleiotropy. Free Rad. Biol. Med. 43, 332-347
33. phox-derived proline-rich peptide. J. Biol. Chem. 281, 3660-3668
34. .- production, vascular tone, and mitogen-activated protein kinase activation. Circulation 109, 1307-1313
35. El-Benna, J., Dang, P. M., Gougerot-Pocidalo, M. A., Marie, J. C., and Braut-Boucher, F. (2009) p47phox, the phagocyte NADPH oxidase/Nox2 organizer: structure, phosphorylation and implication in diseases. Exp. Mol. Med. 41, 217-225
36. Burritt, J. B., DeLeo, F. R., McDonald, C. L., Prigge, J. R., Dinauer, M. C., Nakamura, M., Nauseef, W. M., and Jesaitis, A. J. (2001) Phage display epitope mapping of human neutrophil flavocytochrome b558. Identification of two juxtaposed extracellular domains. J. Biol. Chem. 276, 2053-2061 (Pubitemid 32109686)
37. Watanabe, Y., Tsuboi, H., Koyama, M., Kubo, M., Del Carpio, C. A., Broclawik, E., Ichiishi, E., Kohno, M., and Miyamoto, A. (2006) Molecular dynamics study on the ligand recognition by tandem SH3 domains of p47phox, regulating NADPH oxidase activity. Comput. Biol. Chem. 30, 303-312 (Pubitemid 44118833)
38. Li, J.-M., and Shah, A. M. (2002) Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277, 19952-19960 (Pubitemid 34967517)