Properties of phagocyte NADPH oxidase p47-phox mutants with unmasked SH3 (Src homolooy 3) domains: Full reconstitution of oxidase activity in a semi-recombinant cell-free system lacking arachidonic acid

Biochemical Journal

Volumn 373, Issue 1, 2003, Pages 221-229

  Peng, Guihong ^a   Huang, Jin ^a   Boyd, Mellonie ^a   Kleinberg, Michael E ^a,b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

Author keywords

NADPH oxidase; p47 phox; Phox homology domain; Proline rich region; SH3 domain

Indexed keywords

BIOLOGICAL MEMBRANES; PHOSPHOLIPIDS; PROTEINS;

OXIDASE ACTIVITY;

BIOCHEMISTRY;

ARACHIDONIC ACID; ARGININE; ASPARTIC ACID; GLUTAMIC ACID; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); LYSINE; OXIDOREDUCTASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLINOSITOL; PHOSPHOLIPID; PROLINE; PROTEIN P47; PROTEIN P47 PHOX; RAC1 GUANOSINE 5' (GAMMA THIO)TRIPHOSPHATE; RAC1 PROTEIN; RECOMBINANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SERINE; SUPEROXIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL FREE SYSTEM; CELL MEMBRANE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; NEUTROPHIL; PHAGOCYTE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE HOMOLOGY; SRC HOMOLOGY DOMAIN; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARACHIDONIC ACID; CELL-FREE SYSTEM; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NADPH OXIDASE; PHOSPHOPROTEINS; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE DELETION; SRC HOMOLOGY DOMAINS;

EID: 0038005797     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021629     Document Type: Article

References (31)

1. Babior, B. M. (1994) Activation of the respiratory burst oxidase. Environ Health Perspect. 102, 53-56
2. Nathan, C. and Shiloh, M. U. (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. U.S.A. 97, 8841-8848
3. Clark, R. A. (1999) Activation of the neutrophil respiratory burst oxidase. J. Infect. Dis. 179, S309-S317
4. Babior, B. M., Lambeth, J. D. and Nauseef, W. (2002) The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397, 342-344
5. Huang, J., Hitt, N. D. and Kleinberg, M. E. (1995) Stoichiometry of p22-phox and gp91-phox in phagocyte cytochrome b558. Biochemistry 34, 16753-16757
6. Wallach, T. M. and Segal, A. W. (1996) Stoichiometry of the subunits of flavocytochrome b558 of the NADPH oxidase of phagocytes. Biochem. J. 320, 33-38
7. Segal, A. W., West, I., Wientjes, F., Nugent, J. H. A., Chavan, A. J., Haley, B., Garcia, R. C., Rosens, H. and Scrace, G. (1992) Cytochrome b -245 is a flavocytochrome containing FAD and the NADPH-binding site of the microbicidal oxidase of phagocytes. Biochem. J. 284, 781-788
8. Cross, A. R., Rae, J. and Curnutte, J. T. (1995) Cytochrome b -245 of the neutrophil superoxide-generating system contains two nonidentical hemes: potentiometric studies of a mutant form of gp91-phox. J. Biol. Chem. 270, 17075-17077
9. Prigmore, E., Ahmed, S., Best, A., Kozma, R., Manser, E., Segal, A. W. and Lim, L. (1995) A 68-kDa kinase and NADPH oxidase component p67 phox are targets for Cdc42Hs and Rac1 in neutrophils. J. Biol. Chem. 270, 10717-10722
10. Dang, P. M.-C., Cross, A. R. and Babior, B. M. (2001) Assembly of the neutrophil respiratory burst oxidase: a direct interaction between p67phox and cytochrome b558. Proc. Natl. Acad Sci. U.S.A. 98, 3001-3005
11. Sumimoto, H., Hata, K., Mizuki, K., Ito, T., Kage, Y., Sakaki, Y., Fukumaki, Y., Nakamura, M. and Takeshige, K. (1996) Assembly and activation of the phagocyte NADPH oxidase: specific interaction of the N-terminal Src homology 3 domain of p47 phox with p22phox is required for activation of the NADPH oxidase. J. Biol. Chem. 271, 22152-22158
12. Hiroaki, H., Ago, T., Ito, T., Sumimoto, H. and Kohda, D. (2001) Solution structure of the PX domain, a target of the SH3 domain. Nat. Struct. Biol. 8, 526-530
13. phox to phosphatidylinositol 3,4-bisphosphate and phosphatidic acid is masked by an intramolecular interaction. EMBO J. 21, 5057-5068
14. Zhan, Y., Virbasius, J. V., Song, X., Pomerleau, D. P. and Zhou, G. W. (2002) The p40 phox and p47 phox PX domains of NADPH oxidase target cell membranes via direct and indirect recruitment by phosphoinositides. J. Biol. Chem. 277, 4512-4518
15. Finan, P., Shimizu, Y., Gout, I., Hsuan, J., Truong, O., Butcher, C., Bennett, P., Waterfield, M. D. and Kellie, S. (1994) An SH3 domain and proline-rich sequence mediate an interaction between two components of the phagocyte NADPH oxidase complex. J. Biol. Chem. 269, 13752-13755
16. phox as a positive regulator of the superoxide-producing phagocyte oxidase. EMBO J. 21, 6312-6320
17. Wientjes, F. B., Hsuan, J., Totty, N. F. and Segal, A. W. (1993) p40phox, a third cytosolic component of the activation complex of the NADPH oxidase to contain src homology 3 domains. Biochem. J. 296, 557-561
18. El Benna, J., Faust, L. P. and Babior, B. M. (1994) The phosphorylation of the respiratory burst oxidase component p47 phox during neutrophil activation: phosphorylation of sites recognized by protein kinase C and by proline-directed kinases. J. Biol. Chem. 269, 23431-23436
19. Rotrosen, D. and Leto, T. L. (1990) Phosphorylation of neutrophil p47-kDa cytosolic oxidase factor: translocation to membrane is associated with distinct phosphorylation events. J. Biol. Chem. 265, 19910-19915
20. Fontayne, A., Dang, P. M.-C., Gougerot-Pocidalo, M.-A. and El Benna, J. (2002) Phosphorylation of p47 phox sites by PKC α, β11, δ and ζ: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 41, 7743-7750
21. Ago, T., Nunoi, H., Ito, T. and Sumimoto, H. (1999) 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. 274, 33644-33653
22. Huang, J. and Kleinberg, M. E. (1999) Activation of the phagocyte NADPH oxidase protein p47phox: phosphorylation controls SH3 domain-dependent binding to p22phox. J. Biol. Chem. 274, 19731-19737
23. Golemis, E. A., Gyuris, J. and Brent, R. (1994) In Current Protocols in Molecular Biology (Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D. and Seigman, J. G., eds.), pp. 13.14.1-13.14.17, John Wiley and Sons, New York
24. Leto, T. L., Garrett, M. C., Fujii, H. and Nunoi, H. (1991) Characterization of neutrophil NADPH oxidase factors p47-phox and p67-phox from recombinant baculoviruses. J. Biol. Chem. 266, 19812-19818
25. Kleinberg, M. E., Mital, D., Rotrosen, D. and Malech, H. L. (1992) Characterization of a phagocyte cytochrome b558 91-kilodalton subunit functional domain: identification of peptide sequence and amino acids essential for activity. Biochemistry 31, 2686-2690
26. Palicz, A., Foubert, T. R., Jesaitis, A. J., Marodi, L. and McPhail, L. C. (2001) Phosphatidic acid and diacylglycerol directly activate NADPH oxidase by interacting with enzyme components. J. Biol. Chem. 276, 3090-3097
27. Sumimoto, H., Kage, Y., Nunoi, H., Sasaki, H., Nose, T., Fukumaki, Y., Ohno, M., Minamaki, S. and Tageshige, K. (1994) Role of Src homology 3 domains in assembly and activation of the phagocyte NADPH oxidase. Proc. Natl. Acad. Sci. U.S.A. 91, 5345-5349
28. Hata, K., Ito, T., Takeshige, K. and Sumimoto, H. (1998) Anionic amphiphile-independent activation of the phagocyte NADPH oxidase in a cell-free system by p47 phox and p67 phox, both in C terminarry truncated forms: implication for regulatory Src homology 3 domain-mediated interactions. J. Biol. Chem. 273, 4232-4236
29. Lopes, L. R., Hoyal, C. R., Knaus, U. G. and Babior, B. M. (1999) Activation of the leukocyte NADPH oxidase by protein kinase C in a partially recombinant cell-free system. J. Biol. Chem 274, 15533-15537
30. Shiose, A. and Sumimoto, H. (2000) Arachidonic acid and phosphorylation synergistically induce a conformational change of p47 phox to activate the phagocyte NADPH oxidase. J. Biol. Chem. 275, 13793-13801
31. de Mendez, I., Garrett, M. C., Adams, A. G. and Leto, T. L. (1994) Role of p67-phox SH3 domains in assembly of the NADPH oxidase system. J. Biol. Chem. 269, 16326-16332