Phosphorylation of threonine 154 in p40phox is an important physiological signal for activation of the neutrophil NADPH oxidase

Blood

Volumn 116, Issue 26, 2010, Pages 6027-6036

  Chessa, Tamara A M ^a   Anderson, Karen E ^a   Hu, Yanhua ^b   Xu, Qingbo ^b   Rausch, Oliver ^c   Stephens, Len R ^a   Hawkins, Phillip T ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c UCB PHARMA   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

FORMYLMETHIONYLLEUCYLPHENYLALANINE; IMMUNOGLOBULIN; PROTEIN KINASE C DELTA; PROTEIN P22; PROTEIN P40; PROTEIN P47; PROTEIN P67; PROTEIN SH3; RAC PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERINE; THREONINE; WORTMANNIN;

ANIMAL CELL; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; ENZYME ACTIVATION; ERYTHROCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIATION CHIMERA; SHEEP; STAPHYLOCOCCUS AUREUS; VIRAL GENE DELIVERY SYSTEM;

EID: 78650667827     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-08-300889     Document Type: Article

References (51)

1. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006;6(3):173-182.
2. Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood. 1998;92(9):3007-3017.
3. Abo A, Webb MR, Grogan A, Segal AW. Activation of NADPH oxidase involves the dissociation of p21rac from its inhibitory GDP/GTP exchange protein (rhoGDI) followed by its translocation to the plasma membrane. Biochem J. 1994;298(Pt 3):585-591.
4. Bourmeyster N, Vignais PV. Phosphorylation of Rho GDI stabilizes the Rho A-Rho GDI complex in neutrophil cytosol. Biochem Biophys Res Commun. 1996;218(1):54-60.
5. Brown GE, Stewart MQ, Liu H, Ha VL, Yaffe MB. A novel assay system implicates PtdIns (3, 4) P (2), PtdIns (3) P, and PKC delta in intracellular production of reactive oxygen species by the NADPH oxidase. Mol Cell. 2003;11(1):35-47.
6. Ginsel LA, Onderwater JJ, Fransen JA, Verhoeven AJ, Roos D. Localization of the low-Mr subunit of cytochrome b558 in human blood phagocytes by immunoelectron microscopy. Blood. 1990;76(10):2105-2116.
7. Cross AR, Segal AW. The NADPH oxidase of professional phagocytes-prototype of the NOX electron transport chain systems. Biochim Biophys Acta. 2004;1657(1):1-22.
8. Groemping Y, Rittinger K. Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J. 2005;386(Pt 3):401-416.
9. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol. 2004;76(4):760-781.
10. Sheppard FR, Kelher MR, Moore EE, McLaughlin NJ, Banerjee A, Silliman CC. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J Leukoc Biol. 2005;78(5):1025- 1042.
11. Dinauer MC. Chronic granulomatous disease and other disorders of phagocyte function. Hematol Am Soc Hematol Educ Program. 2005:89-95.
12. Diebold BA, Bokoch GM. Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat Immunol. 2001;2(3):211-215.
13. Lapouge K, Smith SJ, Walker PA, Gamblin SJ, Smerdon SJ, Rittinger K. Structure of the TPR domain of p67phox in complex with Rac. GTP. Mol Cell. 2000;6(4):899-907.
14. Kanai F, Liu H, Field SJ, et al. The PX domains of p47phox and p40phox bind to lipid products of PI (3) K. Nat Cell Biol. 2001;3(7):675-678.
15. Karathanassis D, Stahelin RV, Bravo J, et al. Binding of the PX domain of p47 (phox) to phosphatidylinositol 3, 4-bisphosphateand phosphatidic acid is masked by an intramolecular interaction. EmboJ. 2002;21(19):5057-5068.
16. Ueyama T, Tatsuno T, Kawasaki T, et al. A regulated adaptor function of p40phox: distinct p67phox membrane targeting by p40phox and by p47phox. Mol Biol Cell. 2007;18(2):441-454.
17. Kuribayashi F, Nunoi H, Wakamatsu K, et al. The adaptor protein p40 (phox) as a positive regulator of thesuperoxide-producing phagocyte oxidase. EMBOJ. 2002;21(23):6312-6320.
18. Sathyamoorthy M, de Mendez I, Adams AG, Leto TL. p40 (phox) down-regulates NADPH oxidase activity through interactions with its SH3 domain. J Biol Chem. 1997;272(14):9141-9146.
19. -/- mice exhibit severe defects in NADPH oxidase regulation and oxidant-dependent bacterial killing. J Exp Med. 2006;203(8):1927-1937.
20. Ellson C, Davidson K, Anderson K, Stephens LR, Hawkins PT. PtdIns3P binding to the PX domain of p40phox is a physiological signal in NADPH oxidase activation. EMBOJ. 2006;25(19):4468-4478.
21. Matute JD, Arias AA, Wright NA, et al. A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity. Blood. 2009;114(15):3309-3315.
22. Bouin AP, Grandvaux N, Vignais PV, Fuchs A. p40 (phox) is phosphorylated on threonine 154 and serine 315 during activation of the phagocyte NADPH oxidase. Implication of a protein kinase c-type kinase in the phosphorylation process. J Biol Chem. 1998;273(46):30097-30103.
23. Someya A, Nunoi H, Hasebe T, Nagaoka I. Phosphorylation of p40-phox during activation of neutrophil NADPH oxidase. J Leukoc Biol. 1999;66(5):851-857.
24. Utomo A, Cullere X, Glogauer M, Swat W, Mayadas TN. Vav proteins in neutrophils are required for FcgammaR-mediated signaling to Rac GTPases and nicotinamide adenine dinucleotide phosphate oxidase component p40 (phox). J Immunol. 2006;177(9):6388-6397.
25. Lopes LR, Dagher MC, Gutierrez A, et al. Phosphorylated p40PHOX as a negative regulator of NADPH oxidase. Biochemistry. 2004;43(12):3723-3730.
26. Massenet C, Chenavas S, Cohen-Addad C, et al. 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(14):13752-13761.
27. Bissonnette SA, Glazier CM, Stewart MQ, Brown GE, Ellson CD, Yaffe MB. Phosphatidylinositol 3-phosphate-dependent and-independent functions of p40phox in activation of the neutrophil NADPH oxidase. J Biol Chem. 2008;283(4):2108- 2119.
28. Suh CI, Stull ND, Li XJ, et al. The phosphoinositide-binding protein p40phox activates the NADPH oxidase during FcgammaIIA receptorinduced phagocytosis. J Exp Med. 2006;203(8):1915-1925.
29. Tamura M, Shiozaki I, Ono S, Miyano K, Kunihiro S, Sasaki T. p40phox as an alternative organizer to p47phox in Nox2 activation: a new mechanism involving an interaction with p22phox. FEBS Lett. 2007;581(23):4533-4538.
30. Leitges M, Mayr M, Braun U, et al. Exacerbated vein graft arteriosclerosis in protein kinase Cdelta-null mice. J Clin Invest. 2001;108(10):1505-1512.
31. Colucci F, Soudais C, Rosmaraki E, Vanes L, Tybulewicz VL, Di Santo JP. Dissecting NK cell development using a novel alymphoid mouse model: investigating the role of the c-abl protooncogene in murine NK cell differentiation. J Immunol. 1999;162(5):2761-2765.
32. Anderson KE, Boyle KB, Davidson K, et al. CD18-dependent activation of the neutrophil NADPH oxidase during phagocytosis of Escherichia coli or Staphylococcus aureus is regulated by class III but not class I or II PI3Ks. Blood. 2008;112(13):5202-5211.
33. Morita S, Kojima T, Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 2000;7(12):1063-1066.
34. Feng B, Cheng S, Pear WS, Liou HC. NF-kB inhibitor blocks B cell development at two checkpoints. Med Immunol. 2004;3(1):1.
35. Tan SL, Parker PJ. Emerging and diverse roles of protein kinase C in immune cell signalling. Biochem J. 2003;376(Pt 3):545-552.
36. Chang LC, Wang JP. Examination of the signal transduction pathways leading to activation of extracellular signal-regulated kinase by formylmethionyl-leucyl-phenylalanine in rat neutrophils. FEBS Lett. 454 (1-2): 165-168, 1999.
37. Cheng N, He R, Tian J, Dinauer MC, Ye RD. A critical role of protein kinase C delta activation loop phosphorylation in formyl-methionyl- leucylphenylalanine-induced phosphorylation of p47 (phox) and rapid activation of nicotinamide adenine dinucleotide phosphate oxidase. J Immunol. 2007;179(11):7720-7728.
38. Dang PM, Fontayne A, Hakim J, El Benna J, Perianin A. Protein kinase C zeta phosphorylates a subset of selective sites of the NADPH oxidase component p47phox and participates in formyl peptide-mediated neutrophil respiratory burst. J Immunol. 2001;166(2):1206-1213.
39. 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(24):7743-7750.
40. Kim C, Dinauer MC. Impaired NADPH oxidase activity in Rac2-deficient murine neutrophils does not result from defective translocation of p47phox and p67phox and can be rescued by exogenous arachidonic acid. J Leukoc Biol. 2006;79(1):223-234.
41. Dusi S, Donini M, Rossi F. Mechanisms of NADPH oxidase activation: translocation of p40phox, Rac1 and Rac2 from the cytosol to the membranes in human neutrophils lacking p47phox or p67phox. Biochem J. 1996;314(Pt 2):409-412.
42. Ellson CD, Gobert-Gosse S, Anderson KE, et al. PtdIns (3) P regulates the neutrophil oxidase complex by binding to the PX domain of p40 (phox). Nat Cell Biol. 2001;3(7):679-682.
43. Wientjes FB, Hsuan JJ, Totty NF, Segal AW. p40phox, a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains. Biochem J. 1993;296(Pt 3):557-561.
44. Yamamori T, Inanami O, Nagahata H, Kuwabara M. Phosphoinositide 3-kinase regulates the phosphorylation of NADPH oxidase component p47 (phox) by controlling cPKC/PKCdelta but not Akt. Biochem Biophys Res Commun. 2004;316(3):720-730.
45. Honbou K, Minakami R, Yuzawa S, et al. Fulllength p40phox structure suggests a basis for regulation mechanism of its membrane binding. EMBO J. 2007;26(4):1176-1186.
46. Anderson KE, Chessa TAM, Davidson K, et al. PtdIns3P and Rac direct the assembly of the NADPH oxidase on a novel, pre-phagosomal compartment during FcR-mediated phagocytosis in primary mouse neutrophils. Blood. 2010; DOI 10.1182/blood-2010-03-275602.
47. Dekker LV, Leitges M, Altschuler G, et al. Protein kinase C-beta contributes to NADPH oxidase activation in neutrophils. Biochem J. 2000;347(Pt 1):285-289.
48. Gschwendt M, Dieterich S, Rennecke J, Kittstein W, Mueller HJ, Johannes FJ. Inhibition of protein kinase C mu by various inhibitors. Differentiation from protein kinase c isoenzymes. FEBS Lett. 1996;392(2):77-80.
49. Martiny-Baron G, Kazanietz MG, Mischak H, et al. Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem. 1993;268(13):9194-9197.
50. Toullec D, Pianetti P, Coste H, et al. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem. 1991;266(24):15771-15781.
51. Keenan C, Goode N, Pears C. Isoform specificity of activators and inhibitors of protein kinase C gamma and delta. FEBS Lett. 1997;415(1):101-108. (Pubitemid 27402058)