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BioMed Research International
Volume 2013 (2013), Article ID 839761, 7 pages
Role of NADPH Oxidase-Mediated Reactive Oxygen Species in Podocyte Injury
1Department of Nephrology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology,
Wuhan 430022, China
2Department of Neurobiology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
Received 10 June 2013; Revised 16 September 2013; Accepted 4 October 2013
Academic Editor: Maha Zaki Rizk
Copyright © 2013 Shan Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- S. J. Shankland, “The podocyte's response to injury: role in proteinuria and glomerulosclerosis,” Kidney International, vol. 69, no. 12, pp. 2131–2147, 2006.
- K. Tryggvason, J. Patrakka, and J. Wartiovaara, “Hereditary proteinuria syndromes and mechanisms of proteinuria,” The New England Journal of Medicine, vol. 354, no. 13, pp. 1387–1401, 2006.
- S. V. Shah, R. Baliga, M. Rajapurkar, and V. A. Fonseca, “Oxidants in chronic kidney disease,” Journal of the American Society of Nephrology, vol. 18, no. 1, pp. 16–28, 2007.
- K. Bedard and K.-H. Krause, “The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology,” Physiological Reviews, vol. 87, no. 1, pp. 245–313, 2007.
- D. Wang, Y. Chen, T. Chabrashvili et al., “Role of oxidative stress in endothelial dysfunction and enhanced responses to angiotensin II of afferent arterioles from rabbits infused with angiotensin II,” Journal of the American Society of Nephrology, vol. 14, no. 11, pp. 2783–2789, 2003.
- S. Altenhofer, P. W. Kleikers, K. A. Radermacher et al., “The NOX toolbox: validating the role of NADPH oxidases in physiology and disease,” Cellular and Molecular Life Sciences, vol. 69, pp. 2327–2343, 2012.
- P. Modlinger, T. Chabrashvili, P. S. Gill et al., “RNA silencing in vivo reveals role of p2 in rat angiotensin slow pressor response,” Hypertension, vol. 47, no. 2, pp. 238–244, 2006.
- S. Greiber, T. Münzel, S. Kästner, B. Müller, P. Schollmeyer, and H. Pavenstädt, “NAD(P)H oxidase activity in cultured human podocytes: effects of adenosine triphosphate,” Kidney International, vol. 53, no. 3, pp. 654–663, 1998.
- A. Whaley-Connell, J. Habibi, R. Nistala et al., “Attenuation of NADPH oxidase activation and glomerular filtration barrier remodeling with statin treatment,” Hypertension, vol. 51, no. 2, pp. 474–480, 2008.
- C. Zhang, F. Yi, M. Xia et al., “NMDA receptor-mediated activation of NADPH oxidase and glomerulosclerosis in hyperhomocysteinemic rats,” Antioxidants and Redox Signaling, vol. 13, no. 7, pp. 975–986, 2010.
- T. B. Huber, H. C. Reinhardt, M. Exner et al., “Expression of functional CCR and CXCR chemokine receptors in podocytes,” Journal of Immunology, vol. 168, no. 12, pp. 6244–6252, 2002.
- S. Shibata, M. Nagase, S. Yoshida, H. Kawachi, and T. Fujita, “Podocyte as the target for aldosterone: roles of oxidative stress and Sgk1,” Hypertension, vol. 49, no. 2, pp. 355–364, 2007.
- J. Xu, Z. Li, P. Xu, and Z. Yang, “Protective effects of leukemia inhibitory factor against oxidative stress during high glucose-induced apoptosis in podocytes,” Cell Stress Chaperones, vol. 17, pp. 485–493, 2012.
- J. Toyonaga, K. Tsuruya, H. Ikeda et al., “Spironolactone inhibits hyperglycemia-induced podocyte injury by attenuating ROS production,” Nephrology Dialysis Transplantation, vol. 26, no. 8, pp. 2475–2484, 2011.
- A. A. Eid, B. M. Ford, K. Block et al., “AMP-activated Protein Kinase (AMPK) negatively regulates Nox4-dependent activation of p53 and epithelial cell apoptosis in diabetes,” The Journal of Biological Chemistry, vol. 285, no. 48, pp. 37503–37512, 2010.
- A. Piwkowska, D. Rogacka, M. Jankowski, M. H. Dominiczak, J. K. Stepiński, and S. Angielski, “Metformin induces suppression of NAD(P)H oxidase activity in podocytes,” Biochemical and Biophysical Research Communications, vol. 393, no. 2, pp. 268–273, 2010.
- K. Susztak, A. C. Raff, M. Schiffer, and E. P. Böttinger, “Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy,” Diabetes, vol. 55, no. 1, pp. 225–233, 2006.
- Z.-H. Chen, W.-S. Qin, C.-H. Zeng et al., “Triptolide reduces proteinuria in experimental membranous nephropathy and protects against C5b-9-induced podocyte injury in vitro,” Kidney International, vol. 77, no. 11, pp. 974–988, 2010.
- C. Zhang, M. Xia, K. M. Boini et al., “Epithelial-to-mesenchymal transition in podocytes mediated by activation of NADPH oxidase in hyperhomocysteinemia,” Pflügers Archiv—European Journal of Physiology, vol. 462, no. 3, pp. 455–467, 2011.
- C.-X. Li, M. Xia, W.-Q. Han et al., “Reversal by growth hormone of homocysteine-induced epithelial-to- mesenchymal transition through membrane raft-redox signaling in podocytes,” Cellular Physiology and Biochemistry, vol. 27, no. 6, pp. 691–702, 2011.
- C. Zhang, J.-J. Hu, M. Xia, K. M. Boini, C. Brimson, and P.-L. Li, “Redox signaling via lipid raft clustering in homocysteine-induced injury of podocytes,” Biochimica et Biophysica Acta, vol. 1803, no. 4, pp. 482–491, 2010.
- E. Y. Kim, M. Anderson, and S. E. Dryer, “Insulin increases surface expression of TRPC6 channels in podocytes: role of NADPH oxidases and reactive oxygen species,” American Journal of Physiology—Renal Physiology, vol. 302, no. 3, pp. F298–F307, 2012.
- Q. Yan, K. Gao, Y. Chi et al., “NADPH oxidase-mediated upregulation of connexin43 contributes to podocyte injury,” Free Radical Biology and Medicine, vol. 53, pp. 1286–1297, 2012.
- Z. Wang, X. Wei, Y. Zhang et al., “NADPH oxidase-derived ROS contributes to upregulation of TRPC6 expression in puromycin aminonucleoside-induced podocyte injury,” Cellular Physiology and Biochemistry, vol. 24, no. 5-6, pp. 619–626, 2009.
- E. Y. Kim, M. Anderson, and S. E. Dryer, “Sustained activation of N-methyl-D-aspartate receptors in podoctyes leads to oxidative stress, mobilization of transient receptor potential canonical 6 channels, nuclear factor of activated T cells activation, and apoptotic cell death,” Molecular Pharmacology, vol. 82, no. 4, pp. 728–737, 2012.
- C. Ponticelli, “Membranous nephropathy,” Journal of Nephrology, vol. 20, no. 3, pp. 268–287, 2007.
- T. Etoh, T. Inoguchi, M. Kakimoto et al., “Increased expression of NAD(P)H oxidase subunits, NOX4 and p2, in the kidney of streptozotocin-induced diabetic rats and its reversibity by interventive insulin treatment,” Diabetologia, vol. 46, no. 10, pp. 1428–1437, 2003.
- A. A. Eid, Y. Gorin, B. M. Fagg et al., “Mechanisms of podocyte injury in diabetes role of cytochrome P450 and NADPH oxidases,” Diabetes, vol. 58, no. 5, pp. 1201–1211, 2009.
- L. L. Zhou, F. F. Hou, G. B. Wang et al., “Accumulation of advanced oxidation protein products induces podocyte apoptosis and deletion through NADPH-dependent mechanisms,” Kidney International, vol. 76, no. 11, pp. 1148–1160, 2009.
- A. M. Johnson and J. M. Olefsky, “The origins and drivers of insulin resistance,” Cell, vol. 152, pp. 673–684, 2013.
- F. Yi, M. Xia, N. Li, C. Zhang, L. Tang, and P.-L. Li, “Contribution of guanine nucleotide exchange factor Vav2 to hyperhomocysteinemic glomerulosclerosis in rats,” Hypertension, vol. 53, no. 1, pp. 90–96, 2009.
- Z.-Z. Yang and A.-P. Zou, “Homocysteine enhances TIMP-1 expression and cell proliferation associated with NADH oxidase in rat mesangial cells,” Kidney International, vol. 63, no. 3, pp. 1012–1020, 2003.
- C. Zhang, J.-J. Hu, M. Xia et al., “Protection of podocytes from hyperhomocysteinemia-induced injury by deletion of the gp9 gene,” Free Radical Biology and Medicine, vol. 48, no. 8, pp. 1109–1117, 2010.
- K. M. Boini, M. Xia, C. Li et al., “Acid sphingomyelinase gene deficiency ameliorates the hyperhomocysteinemia- induced glomerular injury in mice,” American Journal of Pathology, vol. 179, no. 5, pp. 2210–2219, 2011.
- A. M. Brennan, S. W. Suh, S. J. Won et al., “NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation,” Nature Neuroscience, vol. 12, no. 7, pp. 857–863, 2009.
- S. Chen, F.-F. He, H. Wang et al., “Calcium entry via TRPC6 mediates albumin overload-induced endoplasmic reticulum stress and apoptosis in podocytes,” Cell Calcium, vol. 50, no. 6, pp. 523–529, 2011.
- J. C. Q. Velez, A. M. Bland, J. M. Arthur, J. R. Raymond, and M. G. Janech, “Characterization of renin-angiotensin system enzyme activities in cultured mouse podocytes,” American Journal of Physiology—Renal Physiology, vol. 293, no. 1, pp. F398–F407, 2007.
- K. K. Griendling and M. Ushio-Fukai, “Reactive oxygen species as mediators of angiotensin II signaling,” Regulatory Peptides, vol. 91, no. 1–3, pp. 21–27, 2000.
- A. T. Whaley-Connell, N. A. Chowdhury, M. R. Hayden et al., “Oxidative stress and glomerular filtration barrier injury: role of the renin-angiotensin system in the Ren2 transgenic rat,” American Journal of Physiology—Renal Physiology, vol. 291, no. 6, pp. F1308–F1314, 2006.
- M. C. Blendea, D. Jacobs, C. S. Stump et al., “Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression,” American Journal of Physiology—Endocrinology and Metabolism, vol. 288, no. 2, pp. E353–E359, 2005.
- D. J. Campbell, P. Rong, A. Kladis, B. Rees, D. Ganten, and S. L. Skinner, “Angiotensin and bradykinin peptides in the TGR(mRen-2)27 rat,” Hypertension, vol. 25, no. 5, pp. 1014–1020, 1995.
- A. Whaley-Connell, J. Habibi, M. Johnson et al., “Nebivolol reduces proteinuria and renal NADPH oxidase-generated reactive oxygen species in the transgenic Ren2 rat,” American Journal of Nephrology, vol. 30, no. 4, pp. 354–360, 2009.
- A. Whaley-Connell, R. Nistala, J. Habibi et al., “Comparative effect of direct renin inhibition and AT1R blockade on glomerular filtration barrier injury in the transgenic Ren2 rat,” American Journal of Physiology—Renal Physiology, vol. 298, no. 3, pp. F655–F661, 2010.
- A. Whaley-Connell, J. Habibi, Y. Wei et al., “Mineralocorticoid receptor antagonism attenuates glomerular filtration barrier remodeling in the transgenic Ren2 rat,” American Journal of Physiology—Renal Physiology, vol. 296, no. 5, pp. F1013–F1022, 2009.
- M. Nagase, H. Matsui, S. Shibata, T. Gotoda, and T. Fujita, “Salt-induced nephropathy in obese spontaneously hypertensive rats via paradoxical activation of the mineralocorticoid receptor: role of oxidative stress,” Hypertension, vol. 50, no. 5, pp. 877–883, 2007.
- M. Nagase and T. Fujita, “Aldosterone and glomerular podocyte injury,” Clinical and Experimental Nephrology, vol. 12, no. 4, pp. 233–242, 2008.
- Y. S. Kang, Y. Li, C. Dai, L. P. Kiss, C. Wu, and Y. Liu, “Inhibition of integrin-linked kinase blocks podocyte epithelial-mesenchymal transition and ameliorates proteinuria,” Kidney International, vol. 78, no. 4, pp. 363–373, 2010.
- R. Sam, L. Wanna, K. P. Gudehithlu et al., “Glomerular epithelial cells transform to myofibroblasts: early but not late removal of TGF-β1 reverses transformation,” Translational Research, vol. 148, no. 3, pp. 142–148, 2006.
- H.-Y. Dai, M. Zheng, L.-L. Lv et al., “The roles of connective tissue growth factor and integrin-linked kinase in high glucose-induced phenotypic alterations of podocytes,” Journal of Cellular Biochemistry, vol. 113, no. 1, pp. 293–301, 2012.
- C. Wang, X. Liu, Z. Ke et al., “Mesangial medium from IgA nephropathy patients induces podocyte epithelial-to-mesenchymal transition through activation of the phosphatidyl inositol-3-kinase/Akt signaling pathway,” Cellular Physiology and Biochemistry, vol. 29, pp. 743–752, 2012.
- A. Djamali, S. Reese, O. Hafez et al., “Nox2 is a mediator of chronic CsA nephrotoxicity,” American Journal of Transplantation, vol. 12, no. 8, pp. 1997–2007, 2012.
- F. Liu, A. M. Gomez Garcia, and F. L. Meyskens Jr., “NADPH oxidase 1 overexpression enhances invasion via matrix metalloproteinase-2 and epithelial-mesenchymal transition in melanoma cells,” Journal of Investigative Dermatology, vol. 132, pp. 2033–2041, 2012.
- H. E. Boudreau, B. W. Casterline, B. Rada, A. Korzeniowska, and T. L. Leto, “Nox4 involvement in TGF-beta and SMAD3-driven induction of the epithelial-to-mesenchymal transition and migration of breast epithelial cells,” Free Radical Biology and Medicine, vol. 53, pp. 1489–1499, 2012.
- K. Lee, Q. K. Chen, C. Lui, M. A. Cichon, D. C. Radisky, and C. M. Nelson, “Matrix compliance regulates Rac1b localization, NADPH oxidase assembly, and epithelial-mesenchymal transition,” Molecular Biology of the Cell, vol. 23, no. 20, pp. 4097–4108, 2012.
- W.-J. Zhang, H. Wei, and B. Frei, “Genetic deficiency of NADPH oxidase does not diminish, but rather enhances, LPS-induced acute inflammatory responses in vivo,” Free Radical Biology and Medicine, vol. 46, no. 6, pp. 791–798, 2009.
- Z. Hu, L. Ren, C. Wang, B. Liu, and G. Song, “Effect of chenodeoxycholic acid on fibrosis, inflammation and oxidative stress in kidney in high-fructose-fed Wistar rats,” Kidney & Blood Pressure Research, vol. 36, no. 1, pp. 85–97, 2012.
- S. Greiber, B. Müller, P. Daemisch, and H. Pavenstädt, “Reactive oxygen species alter gene expression in podocytes: induction of granulocyte macrophage-colony-stimulating factor,” Journal of the American Society of Nephrology, vol. 13, no. 1, pp. 86–95, 2002.
- C. Zhang, K. M. Boini, M. Xia et al., “Activation of Nod-like receptor protein 3 inflammasomes turns on podocyte injury and glomerular sclerosis in hyperhomocysteinemia,” Hypertension, vol. 60, pp. 154–162, 2012.
- J. M. Abais, C. Zhang, M. Xia et al., “NADPH oxidase-mediated triggering of inflammasome activation in mouse podocytes and glomeruli during hyperhomocysteinemia,” Antioxidants & Redox Signaling, vol. 18, no. 13, pp. 1537–1548, 2013.
- S. Kinugasa, A. Tojo, T. Sakai et al., “Selective albuminuria via podocyte albumin transport in puromycin nephrotic rats is attenuated by an inhibitor of NADPH oxidase,” Kidney International, vol. 80, no. 12, pp. 1328–1338, 2011.
- S. Wind, K. Beuerlein, T. Eucker et al., “Comparative pharmacology of chemically distinct NADPH oxidase inhibitors,” British Journal of Pharmacology, vol. 161, no. 4, pp. 885–898, 2010.
- D. Gianni, N. Taulet, H. Zhang et al., “A novel and specific NADPH oxidase-1 (Nox1) small-molecule inhibitor blocks the formation of functional invadopodia in human colon cancer cells,” ACS Chemical Biology, vol. 5, no. 10, pp. 981–993, 2010.
- S. S. Bhandarkar, M. Jaconi, L. E. Fried et al., “Fulvene-5 potently inhibits NADPH oxidase 4 and blocks the growth of endothelial tumors in mice,” The Journal of Clinical Investigation, vol. 119, no. 8, pp. 2359–2365, 2009.
- A. E. Vendrov, N. R. Madamanchi, X.-L. Niu et al., “NADPH oxidases regulate CD44 and hyaluronic acid expression in thrombin-treated vascular smooth muscle cells and in atherosclerosis,” The Journal of Biological Chemistry, vol. 285, no. 34, pp. 26545–26557, 2010.
- B. Laleu, F. Gaggini, M. Orchard et al., “First in class, potent, and orally bioavailable NADPH oxidase isoform 4 (Nox4) inhibitors for the treatment of idiopathic pulmonary fibrosis,” Journal of Medicinal Chemistry, vol. 53, no. 21, pp. 7715–7730, 2010.
- A. Manea, “NADPH oxidase-derived reactive oxygen species: involvement in vascular physiology and pathology,” Cell and Tissue Research, vol. 342, no. 3, pp. 325–339, 2010.
- A. Whaley-Connell, V. G. Demarco, G. Lastra et al., “Insulin resistance, oxidative stress, and podocyte injury: role of rosuvastatin modulation of filtration barrier injury,” American Journal of Nephrology, vol. 28, no. 1, pp. 67–75, 2007.
- X. W. Cheng, M. Kuzuya, T. Sasaki et al., “Inhibition of mineralocorticoid receptor is a renoprotective effect of the 3-hydroxy-3-methylglutaryl-coenzyme A reductase inhibitor pitavastatin,” Journal of Hypertension, vol. 29, no. 3, pp. 542–552, 2011.
- A. Fortuno, J. Bidegain, P. A. Robador et al., “Losartan metabolite EXP3179 blocks NADPH oxidase-mediated superoxide production by inhibiting protein kinase C: potential clinical implications in hypertension,” Hypertension, vol. 54, pp. 744–750, 2009.
- D. Qui and P. N. Kao, “Immunosuppressive and anti-inflammatory mechanisms of triptolide, the principal active diterpenoid from the Chinese medicinal herb Tripterygium wilfordii Hook. f,” Drugs in R and D, vol. 4, no. 1, pp. 1–18, 2003.
- C.-X. Zheng, Z.-H. Chen, C.-H. Zeng, W.-S. Qin, L.-S. Li, and Z.-H. Liu, “Triptolide protects podocytes from puromycin aminonucleoside induced injury in vivo and in vitro,” Kidney International, vol. 74, no. 5, pp. 596–612, 2008.
- N. D. Vaziri, “Roles of oxidative stress and antioxidant therapy in chronic kidney disease and hypertension,” Current Opinion in Nephrology and Hypertension, vol. 13, no. 1, pp. 93–99, 2004.