Divergent effects of p47 phox phosphorylation at S303-4 or S379 on tumor necrosis factor-α signaling via TRAF4 and MAPK in endothelial cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 6, 2012, Pages 1488-1496

  Teng, Lei ^a   Fan, Lampson M ^a   Meijles, Daniel ^a   Li, Jian Mei ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Endothelial cells; Extracellular signal Cregulated kinase 1 2; P47 phox; Phosphorylation; Tumor necrosis factor

Indexed keywords

ALANINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; OXIDE; PROTEIN P47; SERINE; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 4; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE INACTIVATION; GENE SILENCING; GENETIC VARIABILITY; HUMAN; KNOCKOUT GENE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SUBUNIT; SIGNAL TRANSDUCTION;

ANIMALS; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MUTAGENESIS, SITE-DIRECTED; NADPH OXIDASE; PHOSPHORYLATION; PROTEIN TRANSPORT; RNA INTERFERENCE; SERINE; SUPEROXIDES; TIME FACTORS; TNF RECEPTOR-ASSOCIATED FACTOR 4; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84861529165     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.247775     Document Type: Article

References (29)

1. Pagano PJ. Vascular gp91(phox): beyond the endothelium. Circ Res. 2000;87:1-3.
2. El-Benna J, Dang PM, Gougerot-Pocidalo MA, Marie JC, Braut-Boucher F. p47phox, the phagocyte NADPH oxidase/NOX2 organizer: structure, phosphorylation and implication in diseases. Exp Mol Med. 2009;41:217-225.
3. Li JM, Mullen AM, Yun S, Wientjes F, Brouns GY, Thrasher AJ, Shah AM. Essential role of the NADPH oxidase subunit p47(phox) in endothelial cell superoxide production in response to phorbol ester and tumor necrosis factor-alpha. Circ Res. 2002;90:143-150.
4. Park L, Anrather J, Zhou P, Frys K, Wang G, Iadecola C. Exogenous NADPH increases cerebral blood flow through NADPH oxidase-dependent and-independent mechanisms. Arterioscler Thromb Vasc Biol. 2004;24:1860-1865.
5. Ago T, Nunoi H, Ito T, Sumimoto H. Mechanism for phosphorylation-induced activation of the phagocyte NADPH oxidase protein p47(phox). Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47(phox), thereby activating the oxidase. J Biol Chem. 1999;274:33644-33653.
6. Groemping Y, Lapouge K, Smerdon SJ, Rittinger K. Molecular basis of phosphorylation-induced activation of the NADPH oxidase. Cell. 2003;113:343-355.
7. Autore F, Pagano B, Fornili A, Rittinger K, Fraternali F. In silico phosphorylation of the autoinhibited form of p47(phox): insights into the mechanism of activation. Biophys J. 2010;99:3716-3725.
8. Kleinbongard P, Heusch G, Schulz R. TNFalpha in atherosclerosis, myocardial ischemia/reperfusion and heart failure. Pharmacol Ther. 2010;127:295-314.
9. Mathew SJ, Haubert D, Krönke M, Leptin M. Looking beyond death: a morphogenetic role for the TNF signalling pathway. J Cell Sci. 2009;122(Pt 12):1939-1946.
10. Li JM, Fan LM, Christie MR, Shah AM. Acute tumor necrosis factor alpha signaling via NADPH oxidase in microvascular endothelial cells: role of p47phox phosphorylation and binding to TRAF4. Mol Cell Biol. 2005;25:2320-2330.
11. Xu YC, Wu RF, Gu Y, Yang YS, Yang MC, Nwariaku FE, Terada LS. Involvement of TRAF4 in oxidative activation of c-Jun N-terminal kinase. J Biol Chem. 2002;277:28051-28057.
12. Li JM, Mullen AM, Shah AM. Phenotypic properties and characteristics of superoxide production by mouse coronary microvascular endothelial cells. J Mol Cell Cardiol. 2001;33:1119-1131.
13. Price MO, McPhail LC, Lambeth JD, Han CH, Knaus UG, Dinauer MC. Creation of a genetic system for analysis of the phagocyte respiratory burst: high-level reconstitution of the NADPH oxidase in a nonhematopoietic system. Blood. 2002;99:2653-2661.
14. Tickner J, Fan LM, Du J, Meijles D, Li JM. Nox2-derived ROS in PPAR? signaling and cell-cycle progression of lung alveolar epithelial cells. Free Radic Biol Med. 2011;51:763-772.
15. Fernandes DC, Wosniak J Jr, Pescatore LA, Bertoline MA, Liberman M, Laurindo FR, Santos CX. Analysis of DHE-derived oxidation products by HPLC in the assessment of superoxide production and NADPH oxidase activity in vascular systems. Am J Physiol, Cell Physiol. 2007;292:C413-C422.
16. Zhao H, Joseph J, Fales HM, Sokoloski EA, Levine RL, Vasquez-Vivar J, Kalyanaraman B. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc Natl Acad Sci USA. 2005;102:5727-5732.
17. Fan LM, Teng L, Li JM. Knockout of p47 phox uncovers a critical role of p40 phox in reactive oxygen species production in microvascular endothelial cells. Arterioscler Thromb Vasc Biol. 2009;29:1651-1656.
18. Li JM, Shah AM. Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J Biol Chem. 2002;277:19952- 19960.
19. Fontayne A, Dang PM, Gougerot-Pocidalo MA, El-Benna J. Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry. 2002;41:7743-7750.
20. Garg AK, Aggarwal BB. Reactive oxygen intermediates in TNF signaling. Mol Immunol. 2002;39:509-517.
21. Wajant H, Henkler F, Scheurich P. The TNF-receptor-associated factor family: scaffold molecules for cytokine receptors, kinases and their regulators. Cell Signal. 2001;13:389-400.
22. Chandel NS, Schumacker PT, Arch RH. Reactive oxygen species are downstream products of TRAF-mediated signal transduction. J Biol Chem. 2001;276:42728-42736.
23. Glauner H, Siegmund D, Motejadded H, Scheurich P, Henkler F, Janssen O, Wajant H. Intracellular localization and transcriptional regulation of tumor necrosis factor (TNF) receptor-associated factor 4 (TRAF4). Eur J Biochem. 2002;269:4819-4829.
24. Kédinger V, Alpy F, Baguet A, Polette M, Stoll I, Chenard MP, Tomasetto C, Rio MC. Tumor necrosis factor receptor-associated factor 4 is a dynamic tight junction-related shuttle protein involved in epithelium homeostasis. PLoS ONE. 2008;3:e3518.
25. Massenet C, Chenavas S, Cohen-Addad C, Dagher MC, Brandolin G, Pebay-Peyroula E, Fieschi F. Effects of p47phox C terminus phosphorylations on binding interactions with p40phox and p67phox. Structural and functional comparison of p40phox and p67phox SH3 domains. J Biol Chem. 2005;280:13752- 13761.
26. Faust LR, el Benna J, Babior BM, Chanock SJ. The phosphorylation targets of p47phox, a subunit of the respiratory burst oxidase. Functions of the individual target serines as evaluated by site-directed mutagenesis. J Clin Invest. 1995;96:1499-1505.
27. Liang C-J, Wang S-H, Chen Y-H, Chang S-S, Hwang T-L, Leu Y-L, Tseng Y-C, Li C-Y, Chen Y-L. Viscolin reduced VCAM-1 expression in TNF-a-treated endothelial cells via the JNK/NF-κB and ROS pathway. Free Rad Biol Med. 2011;51:1337-1346.
28. Inanami O, Johnson JL, McAdara JK, Benna JE, Faust LR, Newburger PE, Babior BM. Activation of the leukocyte NADPH oxidase by phorbol ester requires the phosphorylation of p47PHOX on serine 303 or 304. J Biol Chem. 1998;273:9539-9543.
29. Johnson JL, Park JW, Benna JE, Faust LP, Inanami O, Babior BM. Activation of p47(PHOX), a cytosolic subunit of the leukocyte NADPH oxidase. Phosphorylation of ser-359 or ser-370 precedes phosphorylation at other sites and is required for activity. J Biol Chem. 1998;273:35147-35152.