The NAD(P)H Oxidase Homolog Nox4 Modulates Insulin-Stimulated Generation of H2O2 and Plays an Integral Role in Insulin Signal Transduction

Molecular and Cellular Biology

Volumn 24, Issue 5, 2004, Pages 1844-1854

  Mahadev, Kalyankar ^a   Motoshima, Hiroyuki ^a   Wu, Xiangdong ^a   Ruddy, Jean Marie ^a   Arnold, Rebecca S ^b   Cheng, Guangjie ^b   Lambeth, J David ^b   Goldstein, Barry J ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CELL PROTEIN; FLAVINE ADENINE NUCLEOTIDE; GLUCOSE; HYDROGEN PEROXIDE; INSULIN; INSULIN RECEPTOR; INSULIN RECEPTOR SUBSTRATE 1; NOX4 PROTEIN; OLIGONUCLEOTIDE; PROTEIN; PROTEIN SERINE KINASE; PROTEIN TYROSINE PHOSPHATASE; PTP1B PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL STRAIN; CELL STRAIN 3T3 L1; DELETION MUTANT; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME SUBSTRATE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; GLUCOSE TRANSPORT; HORMONE ACTION; INSULIN SENSITIVITY; MODULATION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OXIDATION; PEROXIDATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

3T3-L1 CELLS; ADENOVIRIDAE; ADIPOCYTES; ANIMALS; ENZYME ACTIVATION; GLUCOSE; HUMANS; HYDROGEN PEROXIDE; INSULIN; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NADPH OXIDASE; OXIDANTS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

ADENOVIRIDAE; ANIMALIA;

EID: 1342304048     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.5.1844-1854.2004     Document Type: Article

References (47)

1. Babior, B. M., J. D. Lambeth, and W. Nauseef. 2002. The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397:342-344.
2. Bae, Y. S., S. W. Kang, M. S. Seo, I. C. Baines, E. Tekle, P. B. Chock, and S. G. Rhee. 1997. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272:217-221.
3. 2 production requires the activation of phosphatidylinositol 3-kinase. J. Biol. Chem. 275:10527-10531.
4. Banfi, B., R. A. Clark, K. Steger, and K. H. Krause. 2003. Two novel proteins activate superoxide generation by the NADPH oxidase NOX1. J. Biol. Chem. 278:3510-3513.
5. Barrett, W. C., J. P. DeGnore, Y. F. Keng, Z. Y. Zhang, M. B. Yim, and P. B. Chock. 1999. Roles of superoxide radical anion in signal transduction mediated by reversible regulation of protein-tyrosine phosphatase 1B. J. Biol. Chem. 274:34543-34546.
6. Bose, A., A. Guilherme, S. I. Robida, S. M. Nicoloro, Q. L. Zhou, Z. Y. Jiang, D. P. Pomerleau, and M. P. Czech. 2002. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420:821-824.
7. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
8. Cheng, G., Z. Cao, X. Xu, E. G. Van Meir, and J. D. Lambeth. 2001. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269:131-140.
9. Cross, A. R., J. Rae, and J. T. Curnutte. 1995. Cytochrome b-245 of the neutrophil superoxide-generating system contains two nonidentical hemes. Potentiometric studies of a mutant form of gp91phox. J. Biol. Chem. 270:17075-17077.
10. 2+-dependent thiol activation of fat cell glucose utilization. J Biol. Chem. 249:1001-1006.
11. Czech, M. P., J. C. Lawrence, Jr., and W. S. Lynn. 1974. Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin. Proc. Natl. Acad. Sci. USA 71:4173-4177.
12. Dadke, S., and J. Chernoff. 2002. Interaction of protein tyrosine phosphatase (PTP) 1B with its substrates is influenced by two distinct binding domains. Biochem. J. 364:377-383.
13. Elchebly, M., P. Payette, E. Michaliszyn, W. Cromlish, S. Collins, A. L. Loy, D. Normandin, A. Cheng, J. Himms-Hagen, C. C. Chan, C. Ramachandran, M, J. Gresser, M. L. Tremblay, and B. P. Kennedy. 1999. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science 283:1544-1548.
14. Fingar, D. C., S. F. Hausdorff, J. Blenis, and M. J. Birnbaum. 1993. Dissociation of pp70 ribosomal protein S6 kinase from insulin-stimulated glucose transport in 3T3-L1 adipocytes. J. Biol. Chem. 268:3005-3008.
15. Finkel, T. 2000. Redox-dependent signal transduction. FEBS Lett. 476:52-54.
16. Flynn, J. T., M. Westbrooks, and K. A. Lucas, 1997. Establishment and characterization of a line of adipose-derived human microvascular endothelial cells (HADMEC-5) transformed by simian virus 40 large T antigen expression: application to endotoxin research. Shock 8:45-54.
17. Galic, S., M. Klingler-Hoffmann, M. T. Fodero-Tavoletti, M. A. Puryer, T. C. Meng, N. K. Tonks, and T. Tiganis. 2003. Regulation of insulin receptor signaling by the protein tyrosine phosphatase TCPTP. Mol. Cell. Biol. 23:2096-2108.
18. Goldstein, B. J. 2001. Protein-tyrosine phosphatase 1B (PTP1B): a novel therapeutic target for type 2 diabetes mellitus, obesity and related states of insulin resistance. Curr. Drug Targets Immune Endocr. Metabol. Disorders 1:265-275.
19. Goldstein, B. J. 2002. Protein-tyrosine phosphatases: emerging targets for therapeutic intervention in type 2 diabetes and related states of insulin resistance. J. Clin. Endocrinol. Metab. 87:2474-2480.
20. Griendling, K. K., and M. Ushio-Fukai. 2000. Reactive oxygen species as mediators of angiotensin II signaling. Regul. Peptides 91:21-27.
21. Herriich, P., and F. D. Bohmer. 2000. Redox regulation of signal transduction in mammalian cells. Biochem. Pharmacol. 59:35-41.
22. 2+ in TGF-beta 1-induced IL-6 expression. J. Immunol. 165:2190-2197.
23. Kido, Y., J. Nakae, and D. Accili. 2001. The insulin receptor and its cellular targets. J. Clin. Endocrinol. Metab. 86:972-979.
24. Kim, J. R., H. W. Yoon, K. S. Kwon, S. R. Lee, and S. G. Rhee. 2000. Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal. Biochem. 283:214-221.
25. Klaman, L. D., O. Boss, O. D. Peroni, J. K. Kim, J. L. Martino, J. M. Zabolotny, N. Moghal, M. Lubkin, Y. B. Kim, A. H. Sharpe, A. Stricker-Krongrad, G. I. Shulman, B. G. Neel, and B. B. Kahn. 2000. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol. Cell. Biol. 20:5479-5489.
26. 2-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J. Clin. Investig. 89:1006-1013.
27. 2 generation in 3T3-L1 cells. Biochem. J. 307:549-556.
28. 2-generating system present in human fat-cell plasma membranes is multireceptor-linked and under antagonistic control by hormones and cytokines. Biochem. J. 307:543-548.
29. αi2. J. Biol. Chem. 272:10135-10143.
30. Lambeth, J. D. 2002. Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases. Curr. Opin. Hematol. 9:11-17.
31. Lee, S. R., K. S. Kwon, S. R. Kim, and S. G. Rhee. 1998. Reversible inactivation of protein-tyrosine phosphatase 1b in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273:15366-15372.
32. 2. J. Biol. Chem. 277:20336-20342.
33. 2 formation. J. Biol. Chem. 252:560-562.
34. Mahadev, K., X. Wu, A. Zilbering, L. Zhu, J. T. R. Lawrence, and B. J. Goldstein. 2001. Hydrogen peroxide generated during cellular insulin stimulation is integral to activation of the distal insulin signaling cascade in 3T3-L1 adipocytes. J. Biol. Chem. 276:48662-48669.
35. Mahadev, K., A. Zilbering, L. Zhu, and B. J. Goldstein. 2001. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1B in vivo and enhances the early insulin action cascade. J. Biol. Chem. 276:21938-21942.
36. May, J. M., and C. de Haen. 1979. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J. Biol. Chem. 254:2214-2220.
37. Meng, T. C., T. Fukada, and N. K. Tonks. 2002. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9:387-399.
38. Mukherjee, S. P., and W. S. Lynn. 1977. Reduced nicotinamide adenine dinucleotide phosphate oxidase in adipocyte plasma membrane and its activation by insulin. Possible role in the hormone's effects on adenylate cyclase and the hexose monophosphate shunt. Arch. Biochem. Biophys. 184:69-76.
39. 558 with 8-mercapto-FAD and characterization of the flavin-reconstituted enzyme. J. Biol. Chem. 270:16428-16434.
40. Orlicky, D. J., and J. Schaack. 2001. Adenovirus transduction of 3T3-L1 cells. J. Lipid Res. 42:460-466.
41. Rhee, S. G., Y. S. Bae, S. R. Lee, and J. Kwon. 2000. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci. STKE 2000:E1.
42. Saltiel, A. R., and C. R. Kahn. 2001. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799-806.
43. 2 or heat shock is mediated by phosphoinositide 3-kinase and not by mitogen-activated protein kinase-activated protein kinase-2. Biochem. J. 336:241-246.
44. Tonks, N. K. 2003. PTP1B: from the sidelines to the front lines! FEBS Lett. 546:140-148.
45. White, M. F. 2002. IRS proteins and the common path to diabetes. Am. J. Physiol. Endocrinol. Metab. 283:E413-E422.
46. Woo, H. A., H. Z. Chae, S. C. Hwang, K. S. Yang, S. W. Kang, K. Kim, and S. G. Rhee. 2003. Reversing the inactivation of peroxiredoxins caused by cysteine sulfinic acid formation. Science 300:653-656.
47. Zhu, L., A. Zilbering, X. Wu, K. Mahadev, J. I. Joseph, S. Jabbour, W. Deeb, and B. J. Goldstein. 2001. Use of an anaerobic environment to preserve the endogenous activity of protein-tyrosine phosphatases isolated from intact cells. FASEB J. 15:1637-1639.