N-acetyl-cysteine increases cellular dysfunction in progressive chronic kidney damage after acute kidney injury by dampening endogenous antioxidant responses.

Oxidative stress and mitochondrial dysfunction exacerbate acute kidney injury (AKI), but their role in any associated progress to chronic kidney disease (CKD) remains unclear. Antioxidant therapies often benefit AKI, but their benefits in CKD are controversial since clinical and preclinical investigations often conflict. Here we examined the influence of the antioxidant N-acetyl-cysteine (NAC) on oxidative stress and mitochondrial function during AKI (20-min bilateral renal ischemia plus reperfusion/IR) and progression to chronic kidney pathologies in mice. NAC (5% in diet) was given to mice 7 days prior and up to 21 days post-IR (21d-IR). NAC treatment resulted in the following: prevented proximal tubular epithelial cell apoptosis at early IR (40-min postischemia), yet enhanced interstitial cell proliferation at 21d-IR; increased transforming growth factor-β1 expression independent of IR time; and significantly dampened nuclear factor-like 2-initiated cytoprotective signaling at early IR. In the long term, NAC enhanced cellular metabolic impairment demonstrated by increased peroxisome proliferator activator-γ serine-112 phosphorylation at 21d-IR. Intravital multiphoton microscopy revealed increased endogenous fluorescence of nicotinamide adenine dinucleotide (NADH) in cortical tubular epithelial cells during ischemia, and at 21d-IR that was not attenuated with NAC. Fluorescence lifetime imaging microscopy demonstrated persistent metabolic impairment by increased free/bound NADH in the cortex at 21d-IR that was enhanced by NAC. Increased mitochondrial dysfunction in remnant tubular cells was demonstrated at 21d-IR by tetramethylrhodamine methyl ester fluorimetry. In summary, NAC enhanced progression to CKD following AKI not only by dampening endogenous cellular antioxidant responses at time of injury but also by enhancing persistent kidney mitochondrial and metabolic dysfunction.

[1]  M. Duchen,et al.  Investigating mitochondrial redox state using NADH and NADPH autofluorescence , 2016, Free radical biology & medicine.

[2]  M. Salahshoor,et al.  The effect of time and temperature on viability and performance of Langerhans islets separated from Balb/c mouse after death , 2015, Advanced biomedical research.

[3]  G. Canaud,et al.  Cell cycle arrest and the evolution of chronic kidney disease from acute kidney injury. , 2015, Nephrology, Dialysis and Transplantation.

[4]  David W. Johnson,et al.  Oxidative stress-induced alterations in PPAR-γ and associated mitochondrial destabilization contribute to kidney cell apoptosis. , 2014, American journal of physiology. Renal physiology.

[5]  A. J. Bain,et al.  Separating NADH and NADPH fluorescence in live cells and tissues using FLIM , 2014, Nature Communications.

[6]  M. Shimizu,et al.  High dose of N-acetylcystein prevents acute kidney injury in chronic kidney disease patients undergoing myocardial revascularization. , 2014, The Annals of thoracic surgery.

[7]  In-geun Ryoo,et al.  Inhibitory Role of the KEAP1-NRF2 Pathway in TGFβ1-Stimulated Renal Epithelial Transition to Fibroblastic Cells: A Modulatory Effect on SMAD Signaling , 2014, PloS one.

[8]  Charles D. Ellis,et al.  Provision of antioxidant therapy in hemodialysis (PATH): a randomized clinical trial. , 2014, Journal of the American Society of Nephrology : JASN.

[9]  Washington Y. Sanchez,et al.  Multiphoton fluorescence microscopy of the live kidney in health and disease , 2014, Journal of biomedical optics.

[10]  Wachirasek Peerapanyasut,et al.  Ubiquinol supplementation protects against renal ischemia and reperfusion injury in rats , 2014, Free radical research.

[11]  J. K. Kundu,et al.  Keap1 Cysteine 288 as a Potential Target for Diallyl Trisulfide-Induced Nrf2 Activation , 2014, PloS one.

[12]  J. McMurray,et al.  Bardoxolone methyl in type 2 diabetes and stage 4 chronic kidney disease. , 2013, The New England journal of medicine.

[13]  Rafael Kramann,et al.  Differentiated kidney epithelial cells repair injured proximal tubule , 2013, Proceedings of the National Academy of Sciences.

[14]  M. Jun Antioxidants for chronic kidney disease , 2013, Nephrology.

[15]  F. Thaiss,et al.  Effects of Everolimus on Oxidative Stress in Kidney Model of Ischemia/Reperfusion Injury , 2013, American Journal of Nephrology.

[16]  K. Kalantar-Zadeh,et al.  The Extinguished BEACON of Bardoxolone: Not a Monday Morning Quarterback Story , 2013, American Journal of Nephrology.

[17]  A. Tasanarong,et al.  Protective effect of alpha tocopherol on contrast-induced nephropathy in rats. , 2013, Nefrologia : publicacion oficial de la Sociedad Espanola Nefrologia.

[18]  Michael S Roberts,et al.  Changes in the redox state and endogenous fluorescence of in vivo human skin due to intrinsic and photo-aging, measured by multiphoton tomography with fluorescence lifetime imaging , 2012, Journal of biomedical optics.

[19]  G. Camussi,et al.  Protective effects of peroxisome proliferator‐activated receptor agonists on human podocytes: proposed mechanisms of action , 2012, British journal of pharmacology.

[20]  M. Shimizu,et al.  N-acetylcysteine (NAC) protects against acute kidney injury (AKI) following prolonged pneumoperitoneum in the rat. , 2012, The Journal of surgical research.

[21]  R. Zager,et al.  Plasma and urinary heme oxygenase-1 in AKI. , 2012, Journal of the American Society of Nephrology : JASN.

[22]  H. Drummond,et al.  Expression of heme oxygenase-1 in thick ascending loop of henle attenuates angiotensin II-dependent hypertension. , 2012, Journal of the American Society of Nephrology : JASN.

[23]  David W. Johnson,et al.  Oxidative stress, anti‐oxidant therapies and chronic kidney disease , 2012, Nephrology.

[24]  J. Bonventre,et al.  Cellular pathophysiology of ischemic acute kidney injury. , 2011, The Journal of clinical investigation.

[25]  Ronghua Chen,et al.  Cardiovascular , Pulmonary , and Renal Pathology Mitochondrial Dysfunction Mediates Aldosterone-Induced Podocyte Damage A Therapeutic Target of PPAR , 2011 .

[26]  T. Monks,et al.  The cytoprotective effect of N-acetyl-L-cysteine against ROS-induced cytotoxicity is independent of its ability to enhance glutathione synthesis. , 2011, Toxicological sciences : an official journal of the Society of Toxicology.

[27]  A. Landar,et al.  Heme oxygenase-1 inhibits renal tubular macroautophagy in acute kidney injury. , 2010, Journal of the American Society of Nephrology : JASN.

[28]  V. Fung,et al.  A double‐blind, placebo‐controlled study to assess the mitochondria‐targeted antioxidant MitoQ as a disease‐modifying therapy in Parkinson's disease , 2010, Movement disorders : official journal of the Movement Disorder Society.

[29]  Shih‐Ping Hsu,et al.  N-Acetylcysteine for the Management of Anemia and Oxidative Stress in Hemodialysis Patients , 2010, Nephron Clinical Practice.

[30]  Michael S Roberts,et al.  Analysis of the metabolic deterioration of ex vivo skin from ischemic necrosis through the imaging of intracellular NAD(P)H by multiphoton tomography and fluorescence lifetime imaging microscopy. , 2010, Journal of biomedical optics.

[31]  S. Achilefu,et al.  Fluorescence lifetime measurements and biological imaging. , 2010, Chemical reviews.

[32]  Li Yang,et al.  Epithelial cell cycle arrest in G2/M mediates kidney fibrosis after injury , 2010, Nature Medicine.

[33]  B. Lindholm,et al.  EFFECT OF ORAL N-ACETYLCYSTEINE TREATMENT ON PLASMA INFLAMMATORY AND OXIDATIVE STRESS MARKERS IN PERITONEAL DIALYSIS PATIENTS: A PLACEBO-CONTROLLED STUDY , 2010, Peritoneal Dialysis International.

[34]  Jean-Philippe Lafrance,et al.  Acute kidney injury associates with increased long-term mortality. , 2010, Journal of the American Society of Nephrology : JASN.

[35]  A. Heikal,et al.  Two-photon autofluorescence dynamics imaging reveals sensitivity of intracellular NADH concentration and conformation to cell physiology at the single-cell level. , 2009, Journal of photochemistry and photobiology. B, Biology.

[36]  D. Power,et al.  Obesity and hypertension have differing oxidant handling molecular pathways in age-related chronic kidney disease , 2009, Mechanisms of Ageing and Development.

[37]  Fu-Jen Kao,et al.  Differentiation of apoptosis from necrosis by dynamic changes of reduced nicotinamide adenine dinucleotide fluorescence lifetime in live cells. , 2008, Journal of biomedical optics.

[38]  D. Zorov,et al.  The role of mitochondria in oxidative and nitrosative stress during ischemia/reperfusion in the rat kidney. , 2007, Kidney international.

[39]  F. Gaunitz,et al.  Heme Oxygenase-1 Protein Localizes to the Nucleus and Activates Transcription Factors Important in Oxidative Stress* , 2007, Journal of Biological Chemistry.

[40]  M. Mahdavi-Mazdeh,et al.  Antioxidant vitamins preserve superoxide dismutase activities in gentamicin-induced nephrotoxicity. , 2007, Transplantation proceedings.

[41]  Jens Eickhoff,et al.  In vivo multiphoton fluorescence lifetime imaging of protein-bound and free nicotinamide adenine dinucleotide in normal and precancerous epithelia. , 2007, Journal of biomedical optics.

[42]  S. Dooley,et al.  N-Acetyl-L-Cysteine abrogates fibrogenic properties of fibroblasts isolated from Dupuytren's disease by blunting TGF-β signalling , 2006, Journal of cellular and molecular medicine.

[43]  A. Gressner,et al.  Disruption of intermolecular disulfide bonds in PDGF-BB dimers by N-acetyl-L-cysteine does not prevent PDGF signaling in cultured hepatic stellate cells. , 2005, Biochemical and biophysical research communications.

[44]  A. Gressner,et al.  N-acetyl-L-cysteine suppresses TGF-beta signaling at distinct molecular steps: the biochemical and biological efficacy of a multifunctional, antifibrotic drug. , 2005, Biochemical pharmacology.

[45]  N. Ramanujam,et al.  Metabolic mapping of MCF10A human breast cells via multiphoton fluorescence lifetime imaging of the coenzyme NADH. , 2005, Cancer research.

[46]  W. Hauswirth,et al.  Interleukin 10 attenuates neointimal proliferation and inflammation in aortic allografts by a heme oxygenase-dependent pathway. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Tsutomu Inoue,et al.  Connective tissue growth factor expressed in tubular epithelium plays a pivotal role in renal fibrogenesis. , 2004, Journal of the American Society of Nephrology : JASN.

[48]  Raluca Niesner,et al.  Noniterative biexponential fluorescence lifetime imaging in the investigation of cellular metabolism by means of NAD(P)H autofluorescence. , 2004, Chemphyschem : a European journal of chemical physics and physical chemistry.

[49]  Y. Ohno,et al.  Ultrastructural changes during in situ early postmortem autolysis in kidney, pancreas, liver, heart and skeletal muscle of rats. , 2004, Legal medicine.

[50]  B. Molitoris,et al.  Mechanism of Actin Polymerization in Cellular ATP Depletion* , 2004, Journal of Biological Chemistry.

[51]  T. P. Cid,et al.  ANTIOXIDANT NUTRIENTS PROTECT AGAINST CYCLOSPORINE A NEPHROTOXICITY , 2003 .

[52]  R. Mayer,et al.  Nitric Oxide Inhibitor Nω-Nitro-l-arginine Methyl Ester Potentiates Induction of Heme Oxygenase-1 in Kidney Ischemia/Reperfusion Model: A Novel Mechanism for Regulation of the Oxygenase , 2003, Journal of Pharmacology and Experimental Therapeutics.

[53]  W. Webb,et al.  Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Chi‐Hang Lee,et al.  Acetylcysteine for prevention of acute deterioration of renal function following elective coronary angiography and intervention: a randomized controlled trial. , 2003, JAMA.

[55]  L. Truong,et al.  A role for uric acid in the progression of renal disease. , 2002, Journal of the American Society of Nephrology : JASN.

[56]  Watt W Webb,et al.  Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. , 2002, Biophysical journal.

[57]  Paul M Johnson,et al.  Antioxidant-induced changes in oxidized DNA , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[58]  L. Truong,et al.  Role of the microvascular endothelium in progressive renal disease. , 2002, Journal of the American Society of Nephrology : JASN.

[59]  D. Richter,et al.  Oscillations and hypoxic changes of mitochondrial variables in neurons of the brainstem respiratory centre of mice , 2001, The Journal of physiology.

[60]  R S Balaban,et al.  Direct imaging of dehydrogenase activity within living cells using enzyme-dependent fluorescence recovery after photobleaching (ED-FRAP). , 2001, Biophysical journal.

[61]  G. Becker,et al.  Ischemic acute renal failure: long-term histology of cell and matrix changes in the rat. , 2000, Kidney international.

[62]  Masahiro Higuchi,et al.  Regulation of reactive oxygen species-induced apoptosis and necrosis by caspase 3-like proteases , 1998, Oncogene.

[63]  C. Des Rosiers,et al.  Effects of N-acetylcysteine in the rat heart reperfused after low-flow ischemia: evidence for a direct scavenging of hydroxyl radicals and a nitric oxide-dependent increase in coronary flow. , 1995, Free radical biology & medicine.

[64]  M. Brezis,et al.  Physiology of Renal Hypoxia a , 1994, Annals of the New York Academy of Sciences.

[65]  J. Lakowicz,et al.  Fluorescence lifetime imaging of free and protein-bound NADH. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[66]  T. Yoshida,et al.  Degradation of heme by a soluble peptide of heme oxygenase obtained from rat liver microsomes by mild trypsinization. , 1991, European journal of biochemistry.

[67]  Ruben M Sandoval,et al.  In vivo multiphoton imaging of mitochondrial structure and function during acute kidney injury. , 2013, Kidney international.

[68]  Mu‐Shun Huang,et al.  N-acetylcysteine for the prevention of contrast-induced nephropathy in the emergency department. , 2012, Internal medicine.

[69]  M. Ahmad,et al.  Molecular mechanisms of N-acetylcysteine actions , 2003, Cellular and Molecular Life Sciences CMLS.

[70]  F. Carballo Álvarez,et al.  Antioxidant nutrients protect against cyclosporine A nephrotoxicity. , 2003, Toxicology.