Mitochondrial respiratory chain complex i is inactivated by NADPH oxidase Nox4

Biochemical Journal

Volumn 452, Issue 2, 2013, Pages 231-239

  Kozieł, Rafał ^a   Pircher, Haymo ^a   Kratochwil, Manuela ^b   Lener, Barbara ^c   Hermann, Martin ^d   Dencher, Norbert A ^b   Jansen Dürr, Pidder ^c  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^c TYROLEAN CANCER RESEARCH INSTITUTE   (Austria)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

Complex I; Electron transport chain; Mitochondrion; Nox4; Oxidative stress; Senescence

Indexed keywords

HYDROGEN PEROXIDE; MEMBRANE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SHORT HAIRPIN RNA;

ARTICLE; CELL STRESS; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN ANALYSIS; RESPIRATORY CHAIN; RESPIROMETRY; SOLUBILIZATION; STRESS;

ELECTRON TRANSPORT COMPLEX I; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NADPH OXIDASE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROTEIN SUBUNITS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84877756855     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121778     Document Type: Article

References (48)

1. Bedard, K. and Krause, K. H. (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313
2. Krause, K. H. (2004) Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn. J. Infect. Dis. 57, S28-S29
3. Nisimoto, Y., Jackson, H. M., Ogawa, H., Kawahara, T. and Lambeth, J. D. (2010) Constitutive NADPH-dependent electron transferase activity of the Nox4 dehydrogenase domain. Biochemistry 49, 2433-2442
4. Blanchetot, C. and Boonstra, J. (2008) The ROS-NOX connection in cancer and angiogenesis. Crit. Rev. Eukaryotic Gene Expression 18, 35-45
5. Serrander, L., Cartier, L., Bedard, K., Banfi, B., Lardy, B., Plastre, O., Sienkiewicz, A., Forro, L., Schlegel, W. and Krause, K. H. (2007) NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem. J. 406, 105-114
6. Chen, K., Craige, S. E. and Keaney, Jr, J. F. (2009) Downstream targets and intracellular compartmentalization in Nox signaling. Antioxid. Redox Signaling 11, 2467-2480
7. Schroder, K., Wandzioch, K., Helmcke, I. and Brandes, R. P. (2008) Nox4 acts as a switch between differentiation and proliferation in preadipocytes. Arterioscler. Thromb. Vasc. Biol. 29, 239-245
8. Chan, E. C., Jiang, F., Peshavariya, H. M. and Dusting, G. J. (2009) Regulation of cell proliferation by NADPH oxidase-mediated signaling: potential roles in tissue repair, regenerative medicine and tissue engineering. Pharmacol. Ther. 122, 97-108
9. Lassegue, B. and Griendling, K. K. (2010) NADPH oxidases: functions and pathologies in the vasculature. Arterioscler. Thromb. Vasc. Biol. 30, 653-661
10. Meng, D., Lv, D. D. and Fang, J. (2008) Insulin-like growth factor-I induces reactive oxygen species production and cell migration through Nox4 and Rac1 in vascular smooth muscle cells. Cardiovasc. Res. 80, 299-308
11. Lyle, A. N., Deshpande, N. N., Taniyama, Y., Seidel-Rogol, B., Pounkova, L., Du, P., Papaharalambus, C., Lassegue, B. and Griendling, K. K. (2009) Poldip2, a novel regulator of Nox4 and cytoskeletal integrity in vascular smooth muscle cells. Circ. Res. 105, 249-259
12. Van Buul, J. D., Fernandez-Borja, M., Anthony, E. C. and Hordijk, P. L. (2005) Expression and localization of NOX2 and NOX4 in primary human endothelial cells. Antioxid. Redox Signaling 7, 308-317
13. Brandes, R. P. and Schroder, K. (2008) Differential vascular functions of Nox family NADPH oxidases. Curr. Opin. Lipidol. 19, 513-518
14. Chen, K., Kirber, M. T., Xiao, H., Yang, Y. and Keaney, Jr, J. F. (2008) Regulation of ROS signal transduction by NADPH oxidase 4 localization. J. Cell Biol. 181, 1129-1139
15. Hilenski, L. L., Clempus, R. E., Quinn, M. T., Lambeth, J. D. and Griendling, K. K. (2004) Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24, 677-683
16. Block, K., Gorin, Y. and Abboud, H. E. (2009) Subcellular localization of Nox4 and regulation in diabetes. Proc. Natl. Acad. Sci. U.S.A. 106, 14385-14390
17. Kuroda, J., Nakagawa, K., Yamasaki, T., Nakamura, K., Takeya, R., Kuribayashi, F., Imajoh-Ohmi, S., Igarashi, K., Shibata, Y., Sueishi, K. and Sumimoto, H. (2005) The superoxide-producing NAD(P)H oxidase Nox4 in the nucleus of human vascular endothelial cells. Genes Cells 10, 1139-1151
18. Lener, B., Koziel, R., Pircher, H., Hutter, E., Greussing, R., Herndler-Brandstetter, D., Hermann, M., Unterluggauer, H. and Jansen-Dürr, P. (2009) The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells. Biochem. J. 423, 363-374
19. Weyemi, U., Lagente-Chevallier, O., Boufraqech, M., Prenois, F., Courtin, F., Caillou, B., Talbot, M., Dardalhon, M., Al Ghuzlan, A., Bidart, J. M. et al. (2012) ROS-generating NADPH oxidase NOX4 is a critical mediator in oncogenic H-Ras-induced DNA damage and subsequent senescence. Oncogene 31, 1117-1129
20. Wagner, M., Hampel, B., Bernhard, D., Hala, M., Zwerschke, W. and Jansen-Dürr, P. (2001) Replicative senescence of human endothelial cells in vitro involves G1 arrest, polyploidization and senescence-associated apoptosis. Exp. Gerontol. 36, 1327-1347
21. Cossarizza, A., Baccarani-Contri, M., Kalashnikova, G. and Franceschi, C. (1993) A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6, 6′-tetrachloro-1,1′,3,3′-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem. Biophys. Res. Commun. 197, 40-45
22. Hutter, E., Renner, K., Pfister, G., Stockl, P., Jansen-Dürr, P. and Gnaiger, E. (2004) Senescence-associated changes in respiration and oxidative phosphorylation in primary human fibroblasts. Biochem. J. 380, 919-928
23. Hutter, E., Skovbro, M., Lener, B., Prats, C., Rabol, R., Dela, F. and Jansen-Dürr, P. (2007) Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 6, 245-256
24. Schagger, H. (2001) Blue-native gels to isolate protein complexes from mitochondria. Methods Cell Biol. 65, 231-244
25. Reifschneider, N. H., Goto, S., Nakamoto, H., Takahashi, R., Sugawa, M., Dencher, N. A. and Krause, F. (2006) Defining the mitochondrial proteomes from five rat organs in a physiologically significant context using 2D blue-native/SDS-PAGE. J. Proteome Res. 5, 1117-1132
26. Frenzel, M., Rommelspacher, H., Sugawa, M. D. and Dencher, N. A. (2010) Ageing alters the supramolecular architecture of OxPhos complexes in rat brain cortex. Exp. Gerontol. 45, 563-572
27. Hausenloy, D. J., Yellon, D. M., Mani-Babu, S. and Duchen, M. R. (2004) Preconditioning protects by inhibiting the mitochondrial permeability transition. Am. J. Physiol. Heart Circ. Physiol. 287, H841-H849
28. Lundberg, J. O., Weitzberg, E. and Gladwin, M. T. (2008) The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discovery 7, 156-167
29. Shiva, S., Huang, Z., Grubina, R., Sun, J., Ringwood, L. A., MacArthur, P. H., Xu, X., Murphy, E., Darley-Usmar, V. M. and Gladwin, M. T. (2007) Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ. Res. 100, 654-661
30. Wasilewski, M. and Scorrano, L. (2009) The changing shape of mitochondrial apoptosis. Trends Endocrinol. Metab. 20, 287-294
31. Galloway, C. A., Lee, H. and Yoon, Y. (2012) Mitochondrial morphology-emerging role in bioenergetics. Free Radical Biol. Med. 53, 2218-2228
32. Parone, P. A., Da Cruz, S., Tondera, D., Mattenberger, Y., James, D. I., Maechler, P., Barja, F. and Martinou, J. C. (2008) Preventing mitochondrial fission impairs mitochondrial function and leads to loss of mitochondrial DNA. PLoS ONE 3, e3257
33. Kuznetsov, A. V., Kehrer, I., Kozlov, A. V., Haller, M., Redl, H., Hermann, M., Grimm, M. and Troppmair, J. (2011) Mitochondrial ROS production under cellular stress: comparison of different detection methods. Anal. Bioanal. Chem. 400, 2383-2390
34. Graham, K. A., Kulawiec, M., Owens, K. M., Li, X., Desouki, M. M., Chandra, D. and Singh, K. K. (2010) NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol. Ther. 10, 223-231
35. Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V. and Lukyanov, S. (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat. Methods 3, 281-286
36. Stump, C. S., Short, K. R., Bigelow, M. L., Schimke, J. M. and Nair, K. S. (2003) Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc. Natl. Acad. Sci. U.S.A. 100, 7996-8001
37. Yu, T., Robotham, J. L. and Yoon, Y. (2006) Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. U.S.A. 103, 2653-2658
38. Arachiche, A., Augereau, O., Decossas, M., Pertuiset, C., Gontier, E., Letellier, T. and Dachary-Prigent, J. (2008) Localization of PTP-1B, SHP-2, and Src exclusively in rat brain mitochondria and functional consequences. J. Biol. Chem. 283, 24406-24411
39. Lai, H. C., Liu, T. J., Ting, C. T., Sharma, P. M. and Wang, P. H. (2003) Insulin-like growth factor-1 prevents loss of electrochemical gradient in cardiac muscle mitochondria via activation of PI 3 kinase/Akt pathway. Mol. Cell. Endocrinol. 205, 99-106
40. Block, K., Eid, A., Griendling, K. K., Lee, D. Y., Wittrant, Y. and Gorin, Y. (2008) Nox4 NAD(P)H oxidase mediates Src-dependent tyrosine phosphorylation of PDK-1 in response to angiotensin II: role in mesangial cell hypertrophy and fibronectin expression. J. Biol. Chem. 283, 24061-24076
41. Schafer, E., Seelert, H., Reifschneider, N. H., Krause, F., Dencher, N. A. and Vonck, J. (2006) Architecture of active mammalian respiratory chain supercomplexes. J. Biol. Chem. 281, 15370-15375
42. Wosniak, Jr, J., Santos, C. X., Kowaltowski, A. J. and Laurindo, F. R. (2009) Cross-talk between mitochondria and NADPH oxidase: effects of mild mitochondrial dysfunction on angiotensin II-mediated increase in Nox isoform expression and activity in vascular smooth muscle cells. Antioxid. Redox Signaling 11, 1265-1278
43. Ago, T., Kuroda, J., Pain, J., Fu, C., Li, H. and Sadoshima, J. (2010) Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ. Res. 106, 1253-1264
44. Lenaz, G. and Genova, M. L. (2012) Supramolecular organisation of the mitochondrial respiratory chain: a new challenge for the mechanism and control of oxidative phosphorylation. Adv. Exp. Med. Biol. 748, 107-144
45. Calvaruso, M. A., Willems, P., van den Brand, M., Valsecchi, F., Kruse, S., Palmiter, R., Smeitink, J. and Nijtmans, L. (2012) Mitochondrial complex III stabilizes complex I in the absence of NDUFS4 to provide partial activity. Hum. Mol. Genet. 21, 115-120
46. Leshinsky-Silver, E., Lev, D., Tzofi-Berman, Z., Cohen, S., Saada, A., Yanoov-Sharav, M., Gilad, E. and Lerman-Sagie, T. (2005) Fulminant neurological deterioration in a neonate with Leigh syndrome due to a maternally transmitted missense mutation in the mitochondrial ND3 gene. Biochem. Biophys. Res. Commun. 334, 582-587
47. Lener, B., Koziel, R., Pircher, H., Hutter, E., Greussing, R., Herndler-Brandstetter, D., Hermann, M., Unterluggauer, H. and Jansen-Dürr, P. (2009) The NADPH oxidase Nox4 restricts the replicative lifespan of human endothelial cells. Biochem. J. 423, 363-374
48. Hutter, E., Renner, K., Pfister, G., Stockl, P., Jansen-Dürr, P. and Gnaiger, E. (2004) Senescence-associated changes in respiration and oxidative phosphorylation in primary human fibroblasts. Biochem. J. 380, 919-928