Inhibition of insulin-stimulated hydrogen peroxide production prevents stimulation of sodium transport in A6 cell monolayers

American Journal of Physiology - Renal Physiology

Volumn 296, Issue 6, 2009, Pages

  Markadieu, Nicolas ^a   Crutzen, Raphaël ^a   Boom, Alain ^a   Erneux, Christophe ^a   Beauwens, Renaud ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Dichlorodihydrofluorescein; ENaC; H2O2; PI 3 kinase; ROS

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ARTICLE; CELL LINE; CELL STRAIN A6; IMMUNOPRECIPITATION; INCUBATION TIME; MONOLAYER CULTURE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SODIUM TRANSPORT;

EID: 66449111593     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.90397.2008     Document Type: Article

References (61)

1. Ago T, Kitazono T, Ooboshi H, Iyama T, Han YH, Takada J, Wakisaka M, Ibayashi S, Utsumi H, Iida M. Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation 109: 227-233, 2004. (Pubitemid 38114144)
2. Bae YS, Kang SW, Seo MS, Baines IC, Tekle E, Chock PB, Rhee SG. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 272: 217-221, 1997. (Pubitemid 27021147)
3. 2 production requires the activation of phosphatidylinositol 3-kinase. J Biol Chem 275: 10527-10531, 2000.
4. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007. (Pubitemid 46209993)
5. Blazer-Yost BL, Esterman MA, Vlahos CJ. Insulin-stimulated trafficking of ENaC in renal cells requires PI 3-kinase activity. Am J Physiol Cell Physiol 284: C1645-C1653, 2003. (Pubitemid 36583406)
6. Blazer-Yost BL, Liu X, Helman SI. Hormonal regulation of ENaCs: insulin and aldosterone. Am J Physiol Cell Physiol 274: C1373-C1379, 1998. (Pubitemid 28255788)
7. Blazer-Yost BL, Nofziger C. Phosphoinositide lipid second messengers: new paradigms for transepithelial signal transduction. Pflügers Arch 450: 75-82, 2005. (Pubitemid 40674731)
8. Blazer-Yost BL, Pǎunescu TG, Helman SI, Lee KD, Vlahos CJ. Phosphoinositide 3-kinase is required for aldosterone-regulated sodium transport. Am J Physiol Cell Physiol 277: C531-C536, 1999. (Pubitemid 29458187)
9. Blazer-Yost BL, Vahle JC, Byars JM, Bacallao R. Real-time three dimensional imaging of lipid signal transduction: apical membrane insertion of epithelial Na+ channels. Am J Physiol Cell Physiol 287: C1569-C1576, 2004. (Pubitemid 39507674)
10. de la Rosa DA, Li H, Canessa CM. Effects of aldosterone on biosynthesis, traffic, and functional expression of epithelial sodium channels in A6 cells. J Gen Physiol 119: 427-442, 2002. (Pubitemid 34522289)
11. Ding Y, Chen ZJ, Liu S, Che D, Vetter M, Chang CH. Inhibition of Nox-4 activity by plumbagin, a plant-derived bioactive naphthoquinone. J Pharm Pharmacol 57: 111-116, 2005. (Pubitemid 40030109)
12. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002. (Pubitemid 34654215)
13. Frost SC, Lane MD. Evidence for the involvement of vicinal sulfhydryl groups in insulin-activated hexose transport by 3T3-L1 adipocytes. J Biol Chem 260: 2646-2652, 1985. (Pubitemid 15139315)
14. Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci USA 97: 8010-18004, 2000. (Pubitemid 30460764)
15. Gill PS, Wilcox CS. NADPH oxidases in the kidney. Antioxid Redox Signal 8: 1597-1607, 2006. (Pubitemid 44726334)
16. Goldstein BJ, Mahadev K, Wu X. Redox paradox: insulin action is facilitated by insulin-stimulated reactive oxygen species with multiple potential signaling targets. Diabetes 54: 311-321, 2005.
17. Goldstein BJ, Mahadev K, Wu X, Zhu L, Motoshima H. Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxid Redox Signal 7: 1021-1031, 2005. (Pubitemid 40973798)
18. 2+: studies with phenylarsine oxide in thyroid plasma membrane. Biochem J 321: 383-388, 1997.
19. Grasberger H, Refetoff S. Identification of the maturation factor for dual oxidase. Evolution of an eukaryotic operon equivalent. J Biol Chem 281: 18269-18272, 2006. (Pubitemid 44035482)
20. Harper RW, Xu C, McManus M, Heidersbach A, Eiserich JP. Duox2 exhibits potent heme peroxidase activity in human respiratory tract epithelium. FEBS Lett 580: 5150-5154, 2006. (Pubitemid 44419566)
21. Helms MN, Liu L, Liang YY, Al-Khalili O, Vandewalle A, Saxena S, Eaton DC, Ma HP. Phosphatidylinositol 3,4,5-trisphosphate mediates aldosterone stimulation of epithelial sodium channel (ENaC) and interacts with gamma-ENaC. J Biol Chem 280: 40885-40891, 2005. (Pubitemid 41780581)
22. Kawahara T, Lambeth JD. Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evol Biol 27: 178, 2007. (Pubitemid 47218714)
23. Kawahara BT, Quinn MT, Lambeth JD. Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol Biol 7: 109, 2007. (Pubitemid 47218714)
24. Knight ZA, Gonzalez B, Feldman ME, Zunder ER, Goldenberg DD, Williams O, Loewith R, Stokoe D, Balla A, Toth B, Balla T, Weiss WA, Williams RL, Shokat KM. A pharmacological map of the PI3-K family defines a role for p110α in insulin signaling. Cell 125: 733-747, 2006.
25. Krause KH. Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn J Infect Dis 57: S28-S29, 2004. (Pubitemid 39545724)
26. Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, Rhee SG. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci USA 101: 16419-16424, 2004. (Pubitemid 39557728)
27. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189, 2004. (Pubitemid 38339084)
28. 2. J Biol Chem 277: 20336-20342, 2002.
29. Leslie NR. The redox regulation of PI3-kinase dependent signaling. Antioxid Redox Signal 8: f1-f10, 2006. (Pubitemid 44726350)
30. Leto TL, Geiszt M. Role of Nox family NADPH oxidases in host defense. Antioxid Redox Signal 8: 1549-1561, 2006. (Pubitemid 44726330)
31. 2 formation. Free Radic Biol Med 42: 1465-1469, 2007.
32. Ma HP, Chou CF, Wei SP, Eaton DC. Regulation of the epithelial sodium channel by phosphatidylinositides: experiments, implications, and speculations. Pflügers Arch 455: 169-180, 2007. (Pubitemid 47403987)
33. Ma HP, Eaton DC. Acute regulation of epithelial sodium channels by anionic phospholipids. J Am Soc Nephrol 16: 3182-3187, 2005. (Pubitemid 46179324)
34. 2 and plays an integral role in insulin signal transduction. Mol Cell Biol 24: 1844-1854, 2004.
35. Mahadev K, Wu X, Zilbering A, Zhu L, Lawrence JTR, Goldstein BJ. 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, 2001. (Pubitemid 37370561)
36. Mahadev K, Zilbering A, Zhu L, Goldstein BJ. 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, 2001. (Pubitemid 37413200)
37. Markadieu N, Blero D, Boom A, Erneux C, Beauwens R. Phosphatidylinositol 3,4,5-trisphosphate: an early mediator of insulin-stimulated sodium transport in A6 cells. Am J Physiol Renal Physiol 287: F319-F328, 2004. (Pubitemid 38943949)
38. Markadieu N, Crutzen R, Blero D, Erneux C, Beauwens R. Hydrogen peroxide and epidermal growth factor activate phosphatidylinositol 3-kinase and increase sodium transport in A6 cell monolayers. Am J Physiol Renal Physiol 288: F1201-F1212, 2005. (Pubitemid 40677090)
39. + channels in a distal nephron cell line (A6). Am J Physiol Renal Fluid Electrolyte Physiol 263: F392-F400, 1992.
40. May JM, de Haën C. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J Biol Chem 254: 2214-2220, 1979. (Pubitemid 9160038)
41. May JM, de Haën C. The insulin-like effect of hydrogen peroxide on pathways of lipid synthesis in rat adipocytes. J Biol Chem 254: 9017-9021, 1979. (Pubitemid 10239442)
42. Park HS, Lee SH, Park D, Lee JS, Ryu SH, Lee WJ, Rhee SG, Bae YS. Sequential activation of phosphatidylinositol 3-kinase, beta Pix, Rac1, and NOX1 in growth factor-induced production of H2O2. Mol Cell Biol 24: 4384-4394, 2004. (Pubitemid 41071008)
43. Pearce D. SGK1 regulation of epithelial sodium transport. Cell Physiol Biochem 13: 13-20, 2003. (Pubitemid 36359377)
44. Pochynyuk O, Staruschenko A, Tong Q, Medina J, Stockand JD. Identification of a functional phosphatidylinositol 3,4,5-trisphosphate binding site in the epithelial Na+ channel. J Biol Chem 280: 37565-37571, 2005. (Pubitemid 41642365)
45. + channel (ENaC) by phosphatidylinositides. Am J Physiol Renal Physiol 290: F949-F957, 2006.
46. Qin S, Chock PB. Implication of phosphatidylinositol 3-kinase membrane recruitment in hydrogen peroxide-induced activation of PI3K and Akt. Biochemistry 42: 2995-3003, 2003. (Pubitemid 36331543)
47. Ris-Stalpers C. Physiology and pathophysiology of the DUOxes. Antioxid Redox Signal 89: 1563-1572, 2006. (Pubitemid 44726331)
48. Rossary A, Arab K, Steghens JP. Polyunsaturated fatty acids modulate NOX4 anion superoxide production in human fibroblasts. Biochem J 406: 77-83, 2007. (Pubitemid 47264737)
49. Rossier BC, Canessa CM, Schild L, Horisberger JD. Epithelial sodium channels. Curr Opin Nephrol Hypertens 3: 487-496, 1994. (Pubitemid 2138428)
50. Schrader M, Fahimi HD. Peroxisomes and oxidative stress. Biochim Biophys Acta 1763: 1755-1766, 2006. (Pubitemid 44880480)
51. Seo JH, Ahn Y, Lee SR, Yeol Yeo C, Chung, Hur K. The major target of the endogenously generated reactive oxygen species in response to insulin stimulation is phosphatase and tensin homolog and not phosphoinositide-3 kinase (PI-3 kinase) in the PI-3 kinase/Akt pathway. Mol Biol Cell 16: 348-357, 2005. (Pubitemid 40024316)
52. Serrander L, Cartier L, Bedard K, Banfi B, Lardy B, Plastre O, Sienkiewicz A, Forro L, Schlegel W, Krause KH. Nox4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J 406: 105-114, 2007. (Pubitemid 47264740)
53. Serrander L, Jaquet V, Bedard K, Plastre O, Hartley O, Arnaudeau S, Demaurex N, Schlegel W, Krause KH. Nox5 is expressed at the plasma membrane and generates superoxide in response to protein kinase C activation. Biochem J 89: 1159-1167, 2007. (Pubitemid 47248008)
54. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniayama Y, Griendling KK. Angiotensin II estimation of NAD(P)H oxidase activity: upstream mediators. Circ Res 91: 406-413, 2002.
55. 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, 1998.
56. + homeostasis and hypertension. Endocr Rev 23: 258-275, 2002.
57. Stolk J, Hiltermann TJN, Dijkman JH, Verhoeven AJ. Characteristics of the inhibition of NADPH oxidase activation in neutrophils by Apocynin, a methoxy-substituted catechol. Am J Respir Cell Mol Biol 11: 95-102, 1994.
58. + channel by phosphatidylinositol 3,4,5-trisphosphate and phosphatidylinositol 3,4-bisphosphate produced by phosphoinositide 3-OH kinase. J Biol Chem 279: 22654-22663, 2004.
59. Vlahos CJ, Matter WF, Hui KY, Brown F. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY-294002). J Biol Chem 269: 5241-5248, 1994. (Pubitemid 2045363)
60. Yu L, Bao HF, Self JL, Eaton DC, Helms MN. Aldosterone-induced increases in superoxide production counters nitric oxide inhibition of epithelial Na channel activity in A6 distal nephron cells. Am J Physiol Renal Physiol 293: F1666-F1677, 2007. (Pubitemid 350086004)
61. Wang J, Knight ZA, Fiedler D, Williams O, Shokat KM, Pearce D. Activity of the p110-α subunit of phosphatidylinositol-3-kinase is required for activation of epithelial sodium transport. Am J Physiol Renal Physiol 295: F843-F850, 2008.