The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy

Eduardo Molina-Jijón, Omar Emiliano Aparicio-Trejo, Rafael Rodríguez-Muñoz, Juan Carlos León-Contreras, María del Carmen Cárdenas-Aguayo, Omar Noel Medina-Campos, Edilia Tapia, Laura Gabriela Sánchez-Lozada, Rogelio Hernández-Pando, José L. Reyes, Laura Arreola-Mendoza, José Pedraza-Chaverri

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Abstract

© 2016 International Union of Biochemistry and Molecular Biology We have previously reported that the antioxidant curcumin exerts nephroprotection in maleate-induced renal damage, a model associated with oxidative stress. However, the mechanisms involved in curcumin protective effect were not explored, to assess this issue, curcumin was administered daily by gavage (150 mg/kg) five days before a single maleate (400 mg/kg)-injection. Curcumin prevented maleate-induced proteinuria, increased heat shock protein of 72 KDa (Hsp72) expression, and decreased plasma glutathione peroxidase activity. Maleate-induced oxidative stress by increasing the nicotinamide–adenine dinucleotide phosphate oxidase 4 (NOX4) and mitochondrial complex I-dependent superoxide anion (O2•—) production, formation of malondialdehyde (MDA)- and 3-nitrotyrosine (3-NT)-protein adducts and protein carbonylation and decreased GSH/GSSG ratio. Curcumin treatment ameliorated all the above-described changes. The maleate-induced epithelial damage, evaluated by claudin-2 and occludin expressions, was ameliorated by curcumin. It was found that maleate-induced oxidative stress promoted mitochondrial fission, evaluated by dynamin-related protein (Drp) 1 and fission (Fis) 1 expressions and by electron-microscopy, and autophagy, evaluated by phospho-threonine 389 from p70 ribosomal protein S6 kinase (p-Thr 389 p70S6K), beclin 1, microtubule-associated protein 1A/1B-light chain 3 phosphatidylethanolamine conjugate (LC3-II), autophagy-related gene 5 and 12 (Atg5-Atg12) complex, p62, and lysosomal-associated membrane protein (LAMP)-2 expressions in isolated proximal tubules and by electron-microscopy and LC-3 immunolabelling. Curcumin treatment ameliorated these changes. Moreover, curcumin alone induced autophagy in proximal tubules. These data suggest that the nephroprotective effect exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. © 2016 BioFactors, 42(6):686–702, 2016.
Original languageAmerican English
Pages (from-to)686-702
Number of pages615
JournalBioFactors
DOIs
StatePublished - 1 Nov 2016

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Mitochondrial Dynamics
Curcumin
Autophagy
Kidney
Oxidative stress
Oxidative Stress
Lysosomal-Associated Membrane Protein 2
Electron microscopy
Electron Microscopy
Claudin-2
HSP72 Heat-Shock Proteins
Protein Carbonylation
Ribosomal Protein S6 Kinases
70-kDa Ribosomal Protein S6 Kinases
Occludin
Dynamins
maleic acid
Carbonylation
Proteins
Microtubule-Associated Proteins

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Molina-Jijón, E., Aparicio-Trejo, O. E., Rodríguez-Muñoz, R., León-Contreras, J. C., del Carmen Cárdenas-Aguayo, M., Medina-Campos, O. N., ... Pedraza-Chaverri, J. (2016). The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. BioFactors, 686-702. https://doi.org/10.1002/biof.1313
Molina-Jijón, Eduardo ; Aparicio-Trejo, Omar Emiliano ; Rodríguez-Muñoz, Rafael ; León-Contreras, Juan Carlos ; del Carmen Cárdenas-Aguayo, María ; Medina-Campos, Omar Noel ; Tapia, Edilia ; Sánchez-Lozada, Laura Gabriela ; Hernández-Pando, Rogelio ; Reyes, José L. ; Arreola-Mendoza, Laura ; Pedraza-Chaverri, José. / The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. In: BioFactors. 2016 ; pp. 686-702.
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abstract = "{\circledC} 2016 International Union of Biochemistry and Molecular Biology We have previously reported that the antioxidant curcumin exerts nephroprotection in maleate-induced renal damage, a model associated with oxidative stress. However, the mechanisms involved in curcumin protective effect were not explored, to assess this issue, curcumin was administered daily by gavage (150 mg/kg) five days before a single maleate (400 mg/kg)-injection. Curcumin prevented maleate-induced proteinuria, increased heat shock protein of 72 KDa (Hsp72) expression, and decreased plasma glutathione peroxidase activity. Maleate-induced oxidative stress by increasing the nicotinamide–adenine dinucleotide phosphate oxidase 4 (NOX4) and mitochondrial complex I-dependent superoxide anion (O2•—) production, formation of malondialdehyde (MDA)- and 3-nitrotyrosine (3-NT)-protein adducts and protein carbonylation and decreased GSH/GSSG ratio. Curcumin treatment ameliorated all the above-described changes. The maleate-induced epithelial damage, evaluated by claudin-2 and occludin expressions, was ameliorated by curcumin. It was found that maleate-induced oxidative stress promoted mitochondrial fission, evaluated by dynamin-related protein (Drp) 1 and fission (Fis) 1 expressions and by electron-microscopy, and autophagy, evaluated by phospho-threonine 389 from p70 ribosomal protein S6 kinase (p-Thr 389 p70S6K), beclin 1, microtubule-associated protein 1A/1B-light chain 3 phosphatidylethanolamine conjugate (LC3-II), autophagy-related gene 5 and 12 (Atg5-Atg12) complex, p62, and lysosomal-associated membrane protein (LAMP)-2 expressions in isolated proximal tubules and by electron-microscopy and LC-3 immunolabelling. Curcumin treatment ameliorated these changes. Moreover, curcumin alone induced autophagy in proximal tubules. These data suggest that the nephroprotective effect exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. {\circledC} 2016 BioFactors, 42(6):686–702, 2016.",
author = "Eduardo Molina-Jij{\'o}n and Aparicio-Trejo, {Omar Emiliano} and Rafael Rodr{\'i}guez-Mu{\~n}oz and Le{\'o}n-Contreras, {Juan Carlos} and {del Carmen C{\'a}rdenas-Aguayo}, Mar{\'i}a and Medina-Campos, {Omar Noel} and Edilia Tapia and S{\'a}nchez-Lozada, {Laura Gabriela} and Rogelio Hern{\'a}ndez-Pando and Reyes, {Jos{\'e} L.} and Laura Arreola-Mendoza and Jos{\'e} Pedraza-Chaverri",
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Molina-Jijón, E, Aparicio-Trejo, OE, Rodríguez-Muñoz, R, León-Contreras, JC, del Carmen Cárdenas-Aguayo, M, Medina-Campos, ON, Tapia, E, Sánchez-Lozada, LG, Hernández-Pando, R, Reyes, JL, Arreola-Mendoza, L & Pedraza-Chaverri, J 2016, 'The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy', BioFactors, pp. 686-702. https://doi.org/10.1002/biof.1313

The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. / Molina-Jijón, Eduardo; Aparicio-Trejo, Omar Emiliano; Rodríguez-Muñoz, Rafael; León-Contreras, Juan Carlos; del Carmen Cárdenas-Aguayo, María; Medina-Campos, Omar Noel; Tapia, Edilia; Sánchez-Lozada, Laura Gabriela; Hernández-Pando, Rogelio; Reyes, José L.; Arreola-Mendoza, Laura; Pedraza-Chaverri, José.

In: BioFactors, 01.11.2016, p. 686-702.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy

AU - Molina-Jijón, Eduardo

AU - Aparicio-Trejo, Omar Emiliano

AU - Rodríguez-Muñoz, Rafael

AU - León-Contreras, Juan Carlos

AU - del Carmen Cárdenas-Aguayo, María

AU - Medina-Campos, Omar Noel

AU - Tapia, Edilia

AU - Sánchez-Lozada, Laura Gabriela

AU - Hernández-Pando, Rogelio

AU - Reyes, José L.

AU - Arreola-Mendoza, Laura

AU - Pedraza-Chaverri, José

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Y1 - 2016/11/1

N2 - © 2016 International Union of Biochemistry and Molecular Biology We have previously reported that the antioxidant curcumin exerts nephroprotection in maleate-induced renal damage, a model associated with oxidative stress. However, the mechanisms involved in curcumin protective effect were not explored, to assess this issue, curcumin was administered daily by gavage (150 mg/kg) five days before a single maleate (400 mg/kg)-injection. Curcumin prevented maleate-induced proteinuria, increased heat shock protein of 72 KDa (Hsp72) expression, and decreased plasma glutathione peroxidase activity. Maleate-induced oxidative stress by increasing the nicotinamide–adenine dinucleotide phosphate oxidase 4 (NOX4) and mitochondrial complex I-dependent superoxide anion (O2•—) production, formation of malondialdehyde (MDA)- and 3-nitrotyrosine (3-NT)-protein adducts and protein carbonylation and decreased GSH/GSSG ratio. Curcumin treatment ameliorated all the above-described changes. The maleate-induced epithelial damage, evaluated by claudin-2 and occludin expressions, was ameliorated by curcumin. It was found that maleate-induced oxidative stress promoted mitochondrial fission, evaluated by dynamin-related protein (Drp) 1 and fission (Fis) 1 expressions and by electron-microscopy, and autophagy, evaluated by phospho-threonine 389 from p70 ribosomal protein S6 kinase (p-Thr 389 p70S6K), beclin 1, microtubule-associated protein 1A/1B-light chain 3 phosphatidylethanolamine conjugate (LC3-II), autophagy-related gene 5 and 12 (Atg5-Atg12) complex, p62, and lysosomal-associated membrane protein (LAMP)-2 expressions in isolated proximal tubules and by electron-microscopy and LC-3 immunolabelling. Curcumin treatment ameliorated these changes. Moreover, curcumin alone induced autophagy in proximal tubules. These data suggest that the nephroprotective effect exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. © 2016 BioFactors, 42(6):686–702, 2016.

AB - © 2016 International Union of Biochemistry and Molecular Biology We have previously reported that the antioxidant curcumin exerts nephroprotection in maleate-induced renal damage, a model associated with oxidative stress. However, the mechanisms involved in curcumin protective effect were not explored, to assess this issue, curcumin was administered daily by gavage (150 mg/kg) five days before a single maleate (400 mg/kg)-injection. Curcumin prevented maleate-induced proteinuria, increased heat shock protein of 72 KDa (Hsp72) expression, and decreased plasma glutathione peroxidase activity. Maleate-induced oxidative stress by increasing the nicotinamide–adenine dinucleotide phosphate oxidase 4 (NOX4) and mitochondrial complex I-dependent superoxide anion (O2•—) production, formation of malondialdehyde (MDA)- and 3-nitrotyrosine (3-NT)-protein adducts and protein carbonylation and decreased GSH/GSSG ratio. Curcumin treatment ameliorated all the above-described changes. The maleate-induced epithelial damage, evaluated by claudin-2 and occludin expressions, was ameliorated by curcumin. It was found that maleate-induced oxidative stress promoted mitochondrial fission, evaluated by dynamin-related protein (Drp) 1 and fission (Fis) 1 expressions and by electron-microscopy, and autophagy, evaluated by phospho-threonine 389 from p70 ribosomal protein S6 kinase (p-Thr 389 p70S6K), beclin 1, microtubule-associated protein 1A/1B-light chain 3 phosphatidylethanolamine conjugate (LC3-II), autophagy-related gene 5 and 12 (Atg5-Atg12) complex, p62, and lysosomal-associated membrane protein (LAMP)-2 expressions in isolated proximal tubules and by electron-microscopy and LC-3 immunolabelling. Curcumin treatment ameliorated these changes. Moreover, curcumin alone induced autophagy in proximal tubules. These data suggest that the nephroprotective effect exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. © 2016 BioFactors, 42(6):686–702, 2016.

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Molina-Jijón E, Aparicio-Trejo OE, Rodríguez-Muñoz R, León-Contreras JC, del Carmen Cárdenas-Aguayo M, Medina-Campos ON et al. The nephroprotection exerted by curcumin in maleate-induced renal damage is associated with decreased mitochondrial fission and autophagy. BioFactors. 2016 Nov 1;686-702. https://doi.org/10.1002/biof.1313