175
Views
12
CrossRef citations to date
0
Altmetric
Original Article

N-acetylcysteine with apocynin prevents hyperoxaluria-induced mitochondrial protein perturbations in nephrolithiasis

, , , &
Pages 1032-1044 | Received 26 May 2016, Accepted 03 Aug 2016, Published online: 25 Aug 2016

References

  • Glew RH, Sun Y, Horowitz BL, Konstantinov KN, Barry M, Fair JR, et al. Nephropathy in dietary hyperoxaluria: a potentially preventable acute or chronic kidney disease. World J Nephrol 2014;3:122–142.
  • Khan SR. Hyperoxaluria-induced oxidative stress and antioxidants for renal protection. Urol Res 2005;33:349–357.
  • Bijarnia RK, Bachtler M, Chandak PG, van Goor H, Pasch A. Sodium thiosulfate ameliorates oxidative stress and preserves renal function in hyperoxaluric rats. PLoS One 2015;10:e0124881.
  • Schepers MS, van Ballegooijen ES, Bangma CH, Verkoelen CF. Crystals cause acute necrotic cell death in renal proximal tubule cells, but not in collecting tubule cells. Kidney Int 2005;68:1543–1553.
  • McMartin KE, Wallace KB. Calcium oxalate monohydrate, a metabolite of ethylene glycol, is toxic for rat renal mitochondrial function. Toxicol Sci 2005;84:195–200.
  • McMartin K. Are calcium oxalate crystals involved in the mechanism of acute renal failure in ethylene glycol poisoning? Clin Toxicol (Phila) 2009;47:859–869.
  • Khan SR. Role of renal epithelial cells in the initiation of calcium oxalate stones. Nephron Exp Nephrol 2004;98:e55–e60.
  • Sharma M, Kaur T, Singla SK. Protective effects of N-acetylcysteine against hyperoxaluria induced mitochondrial dysfunction in male wistar rats. Mol Cell Biochem 2015;405:105–114.
  • Veena CK, Josephine A, Preetha SP, Rajesh NG, Varalakshmi P. Mitochondrial dysfunction in an animal model of hyperoxaluria: a prophylactic approach with fucoidan. Eur J Pharmacol 2008;579:330–336.
  • Zhang CY, Kong T, Wu WH, Lan MB. The protection of polysaccharide from the Brown Seaweed Sargassum graminifolium against ethylene glycol-induced mitochondrial damage. Mar Drugs 2013;11:870–880.
  • Jonassen JA, Kohjimoto Y, Scheid CR, Schmidt M. Oxalate toxicity in renal cells. Urol Res 2005;33:329–339.
  • Muthukumar A, Selvam R. Role of glutathione on renal mitochondrial status in hyperoxaluria. Mol Cell Biochem 1998;185:77–84.
  • Cao LC, Honeyman TW, Cooney R, Kennington L, Scheid CR, Jonassen JA. Mitochondrial dysfunction is a primary event in renal cell oxalate toxicity. Kidney Int 2004;66:1890–1900.
  • Gregersen N, Hansen J, Palmfeldt J. Mitochondrial proteomics – a tool for the study of metabolic disorders. J Inherit Metab Dis 2012;35:715–726.
  • Semangoen T, Sinchaikul S, Chen ST, Thongboonkerd V. Altered proteins in MDCK renal tubular cells in response to calcium oxalate dihydrate crystal adhesion: a proteomics approach. J Proteome Res 2008;7:2889–2896.
  • Hernandez-Fernaud JR, Salido E. Differential expression of liver and kidney proteins in a mouse model for primary hyperoxaluria type I. FEBS J 2010;277:4766–4774.
  • Chaiyarit S, Thongboonkerd V. Changes in mitochondrial proteome of renal tubular cells induced by calcium oxalate monohydrate crystal adhesion and internalization are related to mitochondrial dysfunction. J Proteome Res 2012;11:3269–3280.
  • Dhouib IE, Annabi A, Jallouli M, Elfazaa S, Lasram MM. A minireview on N-acetylcysteine: an old drug with new approaches. Life Sci 2016;151:359–363.
  • Li X, Lu J, Shang P, Bao J, Yue Z. The selective NADPH oxidase inhibitor apocynin has potential prophylactic effects on melamine-related nephrolithiasis in vitro and in vivo. Mol Cell Biochem 2015;399:167–178.
  • Joshi S, Wang W, Peck AB, Khan SR. Activation of the NLRP3 inflammasome in association with calcium oxalate crystal induced reactive oxygen species in kidneys. J Urol 2015;193:1684–1691.
  • Sharma M, Kaur T, Singla SK. Role of mitochondria and NADPH oxidase derived reactive oxygen species in hyperoxaluria induced nephrolithiasis: therapeutic intervention with combinatorial therapy of N-acetyl cysteine and apocynin. Mitochondrion 2016;27:15–24.
  • Hodgkinson A, Williams A. An improved colorimetric procedure for urine oxalate. Clin Chim Acta 1972;36:127–132.
  • Mattiasson G. Flow cytometric analysis of isolated liver mitochondria to detect changes relevant to cell death. Cytometry A 2004;60:145–154.
  • Kim N, Lee Y, Kim H, Joo H, Youm JB, Park WS, et al. Potential biomarkers for ischemic heart damage identified in mitochondrial proteins by comparative proteomics. Proteomics 2006;6:1237–1249.
  • Sottocasa GL, Kuylenstierna B, Ernster L, Bergstrand A. An electron-transport system associated with the outer membrane of liver mitochondria. A biochemical and morphological study. J Cell Biol 1967;32:415–438.
  • Kirby DM, Thorburn DR, Turnbull DM, Taylor RW. Biochemical assays of respiratory chain complex activity. Methods Cell Biol 2007;80:93–119.
  • Wessel D, Flügge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 1984;138:141–143.
  • Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, et al. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004;25:1327–1333.
  • Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006;1:2856–2860.
  • Lim AI, Tang SC, Lai KN, Leung JC. Kidney injury molecule-1: more than just an injury marker of tubular epithelial cells? J Cell Physiol 2013;228:917–924.
  • Niimi K, Yasui T, Okada A, Hirose Y, Kubota Y, Umemoto Y, et al. Novel effect of the inhibitor of mitochondrial cyclophilin D activation, N-methyl-4-isoleucine cyclosporin, on renal calcium crystallization. Int J Urol 2014;21:707–713.
  • Zhai W, Zheng J, Yao X, Peng B, Liu M, Huang J, et al. Catechin prevents the calcium oxalate monohydrate induced renal calcium crystallization in NRK-52E cells and the ethylene glycol induced renal stone formation in rat. BMC Complement Altern Med 2013;13:228.
  • Wan XY, Liu JY. Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Mol Cell Proteomics 2008;7:1469–1488.
  • Bhattacharyya D, Sinha R, Ghanta S, Chakraborty A, Hazra S, Chattopadhyay S. Proteins differentially expressed in elicited cell suspension culture of Podophyllum hexandrum with enhanced podophyllotoxin content. Proteome Sci 2012;10:34.
  • Niimi K, Yasui T, Hirose M, Hamamoto S, Itoh Y, Okada A, et al. Mitochondrial permeability transition pore opening induces the initial process of renal calcium crystallization. Free Radic Biol Med 2012;52:1207–1217.
  • Raza H. Dual localization of glutathione S-transferase in the cytosol and mitochondria: implications in oxidative stress, toxicity and disease. FEBS J 2011;278:4243–4251.
  • Raza H, Robin MA, Fang JK, Avadhani NG. Multiple isoforms of mitochondrial glutathione S-transferases and their differential induction under oxidative stress. Biochem J 2002;366:45–55.
  • Akeno N, Matsunuma A, Maeda T, Kawane T, Horiuchi N. Regulation of vitamin D-1alpha-hydroxylase and -24-hydroxylase expression by dexamethasone in mouse kidney. J Endocrinol 2000;164:339–348.
  • Sakaki T, Kagawa N, Yamamoto K, Inouye K. Metabolism of vitamin D3 by cytochromes P450. Front Biosci 2005;10:119–134.
  • Achouri Y, Noël G, Vertommen D, Rider MH, Veiga-Da-Cunha M, Van Schaftingen E. Identification of a dehydrogenase acting on D-2-hydroxyglutarate. Biochem J 2004;381:35–42.
  • Struys EA, Salomons GS, Achouri Y, Van Schaftingen E, Grosso S, Craigen WJ, et al. Mutations in the D-2-hydroxyglutarate dehydrogenase gene cause D-2-hydroxyglutaric aciduria. Am J Hum Genet 2005;76:358–360.
  • Van Schaftingen E, Rzem R, Veiga-da-Cunha M. L: -2-Hydroxyglutaric aciduria, a disorder of metabolite repair. J Inherit Metab Dis 2009;32:135–142.
  • Shim EH, Sudarshan S. Another small molecule in the oncometabolite mix: L-2-Hydroxyglutarate in kidney cancer. Oncoscience 2015;2:483–486.
  • Van Schaftingen E, Rzem R, Marbaix A, Collard F, Veiga-da-Cunha M, Linster CL. Metabolite proofreading, a neglected aspect of intermediary metabolism. J Inherit Metab Dis 2013;36:427–434.
  • Neckelmann N, Warner CK, Chung A, Kudoh J, Minoshima S, Fukuyama R, et al. The human ATP synthase beta subunit gene: sequence analysis, chromosome assignment, and differential expression. Genomics 1989;5:829–843.
  • Ohta S, Tomura H, Matsuda K, Kagawa Y. Gene structure of the human mitochondrial adenosine triphosphate synthase beta subunit. J Biol Chem 1988;263:11257–11262.
  • Whitaker RM, Korrapati MC, Stallons LJ, Jesinkey SR, Arthur JM, Beeson CC, et al. Urinary ATP synthase subunit beta is a novel biomarker of renal mitochondrial dysfunction in acute kidney injury. Toxicol Sci 2015;145:108–117.
  • Funk JA, Schnellmann RG. Persistent disruption of mitochondrial homeostasis after acute kidney injury. Am J Physiol Renal Physiol 2012;302:F853–F864.
  • Jesinkey SR, Funk JA, Stallons LJ, Wills LP, Megyesi JK, Beeson CC, Schnellmann RG. Formoterol restores mitochondrial and renal function after ischemia-reperfusion injury. J Am Soc Nephrol 2014;25:1157–1162.
  • Das KC, Lewis-Molock Y, White CW. Elevation of manganese superoxide dismutase gene expression by thioredoxin. Am J Respir Cell Mol Biol 1997;17:713–726.
  • Marine A, Krager KJ, Aykin-Burns N, Macmillan-Crow LA. Peroxynitrite induced mitochondrial biogenesis following MnSOD knockdown in normal rat kidney (NRK) cells. Redox Biol 2014;2:348–357.
  • Roesch K, Hynds PJ, Varga R, Tranebjaerg L, Koehler CM. The calcium-binding aspartate/glutamate carriers, citrin and aralar1, are new substrates for the DDP1/TIMM8a-TIMM13 complex. Hum Mol Genet 2004;13:2101–2111.
  • Curran SP, Leuenberger D, Schmidt E, Koehler CM. The role of the Tim8p-Tim13p complex in a conserved import pathway for mitochondrial polytopic inner membrane proteins. J Cell Biol 2002;158:1017–1027.
  • Paschen SA, Neupert W. Protein import into mitochondria. IUBMB Life 2001;52:101–112.
  • Gerhard DS, Wagner L, Feingold EA, Shenmen CM, Grouse LH, Schuler G, et al. The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res 2004;14:2121–2127.
  • Sugiana C, Pagliarini DJ, McKenzie M, Kirby DM, Salemi R, Abu-Amero KK, et al. Mutation of C20orf7 disrupts complex I assembly and causes lethal neonatal mitochondrial disease. Am J Hum Genet 2008;83:468–478.
  • Saad, II, Saha SB, Thomas G. The RAS subfamily evolution – tracing evolution for its utmost exploitation. Bioinformation 2014;10:293–298.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.