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Thioredoxin-Interacting Protein: The Redoxissome Complex in Glomerular Lesion

Year 2022, Volume: 81 Issue: 2, 274 - 280, 29.12.2022
https://doi.org/10.26650/EurJBiol.2022.1163544

Abstract

Chronic Kidney Disease (CKD) affects millions of people worldwide and is a global health problem with few treatment options. The mechanisms underlying the pathogenesis of CKD include oxidative damage and inflammation. Damage to the glomeruli may be observed during the course of co-associated diseases such diabetes, but also in specific conditions such as focal segmental glomerulosclerosis. During its early manifestation, podocyte’s damage and death are key factors to glomerulopathies and its protection may represent an important therapeutic approach. Importantly, podocytes pathology involves inflammation and cellular damage, principally due to excessive oxidative stress. Underlying mechanisms associated to both inflammation and oxidative stress during the course of a renal lesion must be elucidated for the development of better clinical and research approaches to kidney physiology. Thus, here we discuss the role of the Thioredoxin system, an antioxidant mechanism, and TXNIP, a thioredoxin inhibitor linked to NRLP3 inflammasome activation, as a pivotal axis in the pathophysiology of glomerular lesions.

Supporting Institution

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

References

  • 1. Hill NR, Fatoba ST, Oke JL, Hirst JA, O’Callaghan CA, Lasserson DS, et al. Global prevalence of chronic kidney disease - A systematic review and meta-Analysis. PLoS One 2016; 11: e0158765. https:// doi.org/10.1371/journal.pone.0158765. google scholar
  • 2. KDIGO. Kidney Disease: improving global outcomes (kdigo) glomerular diseases work group. KDIGO 2021 Clinical practice guideline for the management of glomerular diseases. Kidney Int 2021; 100: S1-276. google scholar
  • 3. Campbell KN, Tumlin JA. Protecting podocytes: A key target for therapy of focal segmental glomerulosclerosis. Am J Nephrol 2018; 47: 14-29. google scholar
  • 4. Otalora L, Chavez E, Watford D, Tueros L, Correa M, Nair V, et al. Identification of glomerular and podocyte-specific genes and pathways activated by sera of patients with focal segmental glomerulosclerosis. PLoS One 2019; 14: e0222948. https://doi. org/10.1371/journal.pone.0222948. google scholar
  • 5. Daehn I, Casalena G, Zhang T, Shi S, Fenninger F, Barasch N, et al. Endothelial mitochondrial oxidative stress determines podocyte depletion in segmental glomerulosclerosis. J Clin Invest 2014; 124: 1608-21. google scholar
  • 6. Collet J-F, Messens J. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 2010; 13: 1205-16. google scholar
  • 7. Yoshihara E, Masaki S, Matsuo Y, Chen Z, Tian H, Yodoi J. Thioredox-in/Txnip: Redoxisome, as a redox switch for the pathogenesis of diseases. Front Immunol 2014; 4. google scholar
  • 8. Cao X, He W, Pang Y, Cao Y, Qin A. Redox-dependent and independent effects of thioredoxin interacting protein. Biol Chem 2020; 401: 1215-31. google scholar
  • 9. Jaganjac M, Milkovic L, Sunjic SB, Zarkovic N. The NRF2, Thioredoxin, and glutathione system in tumorigenesis and anticancer therapies. Antioxidants (Basel) 2020; 9: 1151. google scholar
  • 10. Hwang J, Suh H-W, Jeon YH, Hwang E, Nguyen LT, Yeom J, et al. The structural basis for the negative regulation of thioredoxin by thioredoxin-interacting protein. Nat Commun 2014;5:2958. google scholar
  • 11. Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, et al. Identification of thioredoxin-binding protein-2/vitamin D3 up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem 1999;274:21645-50. google scholar
  • 12. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010; 11: 136-40. google scholar
  • 13. Kim S-K, Choe J-Y, Park K-Y. TXNIP-mediated nuclear factor-KB signaling pathway and intracellular shifting of TXNIP in uric acid-induced NLRP3 inflammasome. Biochem Biophys Res Commun 2019; 511: 725-31. google scholar
  • 14. Wu M, Li R, Hou Y, Song S, Han W, Chen N, et al. Thioredoxin-interacting protein deficiency ameliorates kidney inflammation and fibrosis in mice with unilateral ureteral obstruction. Lab Invest 2018; 98: 1211-24. google scholar
  • 15. Song S, Qiu D, Wang Y, Wei J, Wu H, Wu M, et al. TXNIP deficiency mitigates podocyte apoptosis via restraining the activation of mTOR or p38 MAPK signaling in diabetic nephropathy. Exp Cell Res 2020; 388: 111862. google scholar
  • 16. Shah A, Xia L, Masson EAY, Gui C, Momen A, Shikatani EA, et al. Thioredoxin-Interacting Protein Deficiency Protects against Diabetic Nephropathy. JASN 2015; 26: 2963-77. google scholar
  • 17. Huang C, Zhang Y, Kelly DJ, Tan CYR, Gill A, Cheng D, et al. Thioredoxin interacting protein (TXNIP) regulates tubular autophagy and mitophagy in diabetic nephropathy through the mTOR signaling pathway. Sci Rep 2016; 6: 29196. google scholar
  • 18. Gao P, Meng X-F, Su H, He F-F, Chen S, Tang H, et al. Thioredoxin-interacting protein mediates NALP3 inflammasome activation in podocytes during diabetic nephropathy. Biochim Biophys Acta-Mol Cell Res 2014; 1843: 2448-60. google scholar
  • 19. Thieme K, Pereira BMV, da Silva KS, Fabre NT, Catanozi S, Passarelli M, et al. Chronic advanced-glycation end products treatment induces TXNIP expression and epigenetic changes in glomerular podocytes in vivo and in vitro. Life Sci 2021; 270: 118997. google scholar
  • 20. Monteiro MB, Santos-Bezerra DP, Thieme K, Admoni SN, Perez RV, Machado CG, et al. Thioredoxin interacting protein expression in the urinary sediment associates with renal function decline in type 1 diabetes. Free Radic Res 2016; 50: 101-10. google scholar
  • 21. Chong C-R, Chan WPA, Nguyen TH, Liu S, Procter NEK, Ngo DT, et al. Thioredoxin-Interacting Protein: Pathophysiology and Emerging Pharmacotherapeutics in Cardiovascular Disease and Diabetes. Cardiovasc Drugs Ther 2014; 28: 347-60. google scholar
  • 22. Mohamed IN, Li L, Ismael S, Ishrat T, El-Remessy AB. Thioredoxin interacting protein, a key molecular switch between oxidative stress and sterile inflammation in cellular response. World J Diabetes 2021; 12: 1979-99. google scholar
  • 23. Rogers N, Stephenson M, Kitching A, Horowitz J, Coates P. Amelioration ofrenal ischaemia-reperfusion injury by liposomal delivery of curcumin to renal tubular epithelial and antigen-presenting cells. Br J Pharmacol 2012; 166: 194-209. google scholar
  • 24. Li Y, Li J, Li S, Li Y, Wang X, Liu B, et al. Curcumin attenuates glutamate neurotoxicity in the hippocampus by suppression of ER stress-associated TXNIP/NLRP3 inflammasome activation in a manner dependent on AMPK. Toxicol Appl Pharmacol 2015; 286: 53-63. google scholar
  • 25. Rodriguez-Garcia A, Hevia D, Mayo JC, Gonzalez-Menendez P, Coppo L, Lu J, et al. Thioredoxin 1 modulates apoptosis induced by bioactive compounds in prostate cancer cells. Redox Biol 2017; 12: 634-47. google scholar
  • 26. Dai X, Liao R, Liu C, Liu S, Huang H, Liu J, et al. Epigenetic regulation of TXNIP-mediated oxidative stress and NLRP3 inflammasome activation contributes to SAHH inhibition- aggravated diabetic nephropathy. Redox Biol 2021; 45: 102033. google scholar
  • 27. Siddiqi FS, Majumder S, Thai K, Abdalla M, Hu P, Advani SL, et al. The histone methyltransferase enzyme enhancer of zeste homolog 2 protects against podocyte oxidative stress and renal injury in diabetes. JASN 2016; 27: 2021-34. google scholar
  • 28. Gao K, Chi Y, Sun W, Takeda M, Yao J. 5'-AMP-Activated Protein Kinase Attenuates Adriamycin-Induced Oxidative Podocyte Injury through Thioredoxin-Mediated Suppression of the Apoptosis Signal-Regulating Kinase 1-P38 Signaling Pathway. Mol Pharmacol 2014; 85: 460-71. google scholar
  • 29. Gao P, He F-F, Tang H, Lei C-T, Chen S, Meng X-F, et al. NADPH oxidase-induced NALP3 inflammasome activation is driven by thioredoxin-interacting protein which contributes to podocyte injury in hyperglycemia. J Diabetes Res 2015; 2015: 504761. google scholar
  • 30. Song S, Qiu D, Shi Y, Wang S, Zhou X, Chen N, et al. Thioredoxin-interacting protein deficiency alleviates phenotypic alterations of podocytes via inhibition of mTOR activation in diabetic nephropathy. J Cell Physiol 2019; 234: 16485-502. google scholar
  • 31. Mao Z, Huang Y, Zhang Z, Yang X, Zhang X, Huang Y, et al. Pharmacological levels of hydrogen sulfide inhibit oxidative cell injury through regulating the redox state of thioredoxin. Free Radic Biol Med 2019; 134: 190-9. google scholar
  • 32. Feng H, Gu J, Gou F, Huang W, Gao C, Chen G, et al. High Glucose and Lipopolysaccharide Prime NLRP3 Inflammasome via ROS/ TXNIP Pathway in Mesangial Cells. J Diabetes Res 2016; 2016: 6973175. google scholar
  • 33. Wang S, Zhao X, Yang S, Chen B, Shi J. Salidroside alleviates high glucose-induced oxidative stress and extracellular matrix accumulation in rat glomerular mesangial cells by the TXNIP-NLRP3 inflammasome pathway. Chem Biol Interac 2017; 278: 48-53. google scholar
  • 34. Shi Y, Ren Y, Zhao L, Du C, Wang Y, Zhang Y, et al. Knockdown of thioredoxin interacting protein attenuates high glucose-induced apoptosis and activation of ASK1 in mouse mesangial cells. FEBS Letters 2011; 585: 1789-95. google scholar
  • 35. Shah A, Xia L, Goldberg H, Lee KW, Quaggin SE, Fantus IG. Thioredoxin-interacting protein mediates high glucose-induced reactive oxygen species generation by mitochondria and the NADPH oxidase, Nox4, in Mesangial Cells. J Biol Chem 2013; 288: 6835-48. google scholar
  • 36. Xu W, Wang L, Li J, Cai Y, Xue Y. TXNIP mediated the oxidative stress response in glomerular mesangial cells partially through AMPK pathway. Biomed Pharmacother 2018; 107: 785- 92. google scholar
  • 37. Wu M, Han W, Song S, Du Y, Liu C, Chen N, et al. NLRP3 deficiency ameliorates renal inflammation and fibrosis in diabetic mice. Mol Cell Endocrinol 2018; 478: 115-25. google scholar
  • 38. Zhang X, Mao Z, Huang Y, Zhang Z, Yao J. Gap junctions amplify TRPV4 activation-initiated cell injury via modification of intracellular Ca 2+ and Ca 2+ -dependent regulation of TXNIP. Channels 2020; 14: 246-56. google scholar
Year 2022, Volume: 81 Issue: 2, 274 - 280, 29.12.2022
https://doi.org/10.26650/EurJBiol.2022.1163544

Abstract

References

  • 1. Hill NR, Fatoba ST, Oke JL, Hirst JA, O’Callaghan CA, Lasserson DS, et al. Global prevalence of chronic kidney disease - A systematic review and meta-Analysis. PLoS One 2016; 11: e0158765. https:// doi.org/10.1371/journal.pone.0158765. google scholar
  • 2. KDIGO. Kidney Disease: improving global outcomes (kdigo) glomerular diseases work group. KDIGO 2021 Clinical practice guideline for the management of glomerular diseases. Kidney Int 2021; 100: S1-276. google scholar
  • 3. Campbell KN, Tumlin JA. Protecting podocytes: A key target for therapy of focal segmental glomerulosclerosis. Am J Nephrol 2018; 47: 14-29. google scholar
  • 4. Otalora L, Chavez E, Watford D, Tueros L, Correa M, Nair V, et al. Identification of glomerular and podocyte-specific genes and pathways activated by sera of patients with focal segmental glomerulosclerosis. PLoS One 2019; 14: e0222948. https://doi. org/10.1371/journal.pone.0222948. google scholar
  • 5. Daehn I, Casalena G, Zhang T, Shi S, Fenninger F, Barasch N, et al. Endothelial mitochondrial oxidative stress determines podocyte depletion in segmental glomerulosclerosis. J Clin Invest 2014; 124: 1608-21. google scholar
  • 6. Collet J-F, Messens J. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 2010; 13: 1205-16. google scholar
  • 7. Yoshihara E, Masaki S, Matsuo Y, Chen Z, Tian H, Yodoi J. Thioredox-in/Txnip: Redoxisome, as a redox switch for the pathogenesis of diseases. Front Immunol 2014; 4. google scholar
  • 8. Cao X, He W, Pang Y, Cao Y, Qin A. Redox-dependent and independent effects of thioredoxin interacting protein. Biol Chem 2020; 401: 1215-31. google scholar
  • 9. Jaganjac M, Milkovic L, Sunjic SB, Zarkovic N. The NRF2, Thioredoxin, and glutathione system in tumorigenesis and anticancer therapies. Antioxidants (Basel) 2020; 9: 1151. google scholar
  • 10. Hwang J, Suh H-W, Jeon YH, Hwang E, Nguyen LT, Yeom J, et al. The structural basis for the negative regulation of thioredoxin by thioredoxin-interacting protein. Nat Commun 2014;5:2958. google scholar
  • 11. Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, et al. Identification of thioredoxin-binding protein-2/vitamin D3 up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem 1999;274:21645-50. google scholar
  • 12. Zhou R, Tardivel A, Thorens B, Choi I, Tschopp J. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol 2010; 11: 136-40. google scholar
  • 13. Kim S-K, Choe J-Y, Park K-Y. TXNIP-mediated nuclear factor-KB signaling pathway and intracellular shifting of TXNIP in uric acid-induced NLRP3 inflammasome. Biochem Biophys Res Commun 2019; 511: 725-31. google scholar
  • 14. Wu M, Li R, Hou Y, Song S, Han W, Chen N, et al. Thioredoxin-interacting protein deficiency ameliorates kidney inflammation and fibrosis in mice with unilateral ureteral obstruction. Lab Invest 2018; 98: 1211-24. google scholar
  • 15. Song S, Qiu D, Wang Y, Wei J, Wu H, Wu M, et al. TXNIP deficiency mitigates podocyte apoptosis via restraining the activation of mTOR or p38 MAPK signaling in diabetic nephropathy. Exp Cell Res 2020; 388: 111862. google scholar
  • 16. Shah A, Xia L, Masson EAY, Gui C, Momen A, Shikatani EA, et al. Thioredoxin-Interacting Protein Deficiency Protects against Diabetic Nephropathy. JASN 2015; 26: 2963-77. google scholar
  • 17. Huang C, Zhang Y, Kelly DJ, Tan CYR, Gill A, Cheng D, et al. Thioredoxin interacting protein (TXNIP) regulates tubular autophagy and mitophagy in diabetic nephropathy through the mTOR signaling pathway. Sci Rep 2016; 6: 29196. google scholar
  • 18. Gao P, Meng X-F, Su H, He F-F, Chen S, Tang H, et al. Thioredoxin-interacting protein mediates NALP3 inflammasome activation in podocytes during diabetic nephropathy. Biochim Biophys Acta-Mol Cell Res 2014; 1843: 2448-60. google scholar
  • 19. Thieme K, Pereira BMV, da Silva KS, Fabre NT, Catanozi S, Passarelli M, et al. Chronic advanced-glycation end products treatment induces TXNIP expression and epigenetic changes in glomerular podocytes in vivo and in vitro. Life Sci 2021; 270: 118997. google scholar
  • 20. Monteiro MB, Santos-Bezerra DP, Thieme K, Admoni SN, Perez RV, Machado CG, et al. Thioredoxin interacting protein expression in the urinary sediment associates with renal function decline in type 1 diabetes. Free Radic Res 2016; 50: 101-10. google scholar
  • 21. Chong C-R, Chan WPA, Nguyen TH, Liu S, Procter NEK, Ngo DT, et al. Thioredoxin-Interacting Protein: Pathophysiology and Emerging Pharmacotherapeutics in Cardiovascular Disease and Diabetes. Cardiovasc Drugs Ther 2014; 28: 347-60. google scholar
  • 22. Mohamed IN, Li L, Ismael S, Ishrat T, El-Remessy AB. Thioredoxin interacting protein, a key molecular switch between oxidative stress and sterile inflammation in cellular response. World J Diabetes 2021; 12: 1979-99. google scholar
  • 23. Rogers N, Stephenson M, Kitching A, Horowitz J, Coates P. Amelioration ofrenal ischaemia-reperfusion injury by liposomal delivery of curcumin to renal tubular epithelial and antigen-presenting cells. Br J Pharmacol 2012; 166: 194-209. google scholar
  • 24. Li Y, Li J, Li S, Li Y, Wang X, Liu B, et al. Curcumin attenuates glutamate neurotoxicity in the hippocampus by suppression of ER stress-associated TXNIP/NLRP3 inflammasome activation in a manner dependent on AMPK. Toxicol Appl Pharmacol 2015; 286: 53-63. google scholar
  • 25. Rodriguez-Garcia A, Hevia D, Mayo JC, Gonzalez-Menendez P, Coppo L, Lu J, et al. Thioredoxin 1 modulates apoptosis induced by bioactive compounds in prostate cancer cells. Redox Biol 2017; 12: 634-47. google scholar
  • 26. Dai X, Liao R, Liu C, Liu S, Huang H, Liu J, et al. Epigenetic regulation of TXNIP-mediated oxidative stress and NLRP3 inflammasome activation contributes to SAHH inhibition- aggravated diabetic nephropathy. Redox Biol 2021; 45: 102033. google scholar
  • 27. Siddiqi FS, Majumder S, Thai K, Abdalla M, Hu P, Advani SL, et al. The histone methyltransferase enzyme enhancer of zeste homolog 2 protects against podocyte oxidative stress and renal injury in diabetes. JASN 2016; 27: 2021-34. google scholar
  • 28. Gao K, Chi Y, Sun W, Takeda M, Yao J. 5'-AMP-Activated Protein Kinase Attenuates Adriamycin-Induced Oxidative Podocyte Injury through Thioredoxin-Mediated Suppression of the Apoptosis Signal-Regulating Kinase 1-P38 Signaling Pathway. Mol Pharmacol 2014; 85: 460-71. google scholar
  • 29. Gao P, He F-F, Tang H, Lei C-T, Chen S, Meng X-F, et al. NADPH oxidase-induced NALP3 inflammasome activation is driven by thioredoxin-interacting protein which contributes to podocyte injury in hyperglycemia. J Diabetes Res 2015; 2015: 504761. google scholar
  • 30. Song S, Qiu D, Shi Y, Wang S, Zhou X, Chen N, et al. Thioredoxin-interacting protein deficiency alleviates phenotypic alterations of podocytes via inhibition of mTOR activation in diabetic nephropathy. J Cell Physiol 2019; 234: 16485-502. google scholar
  • 31. Mao Z, Huang Y, Zhang Z, Yang X, Zhang X, Huang Y, et al. Pharmacological levels of hydrogen sulfide inhibit oxidative cell injury through regulating the redox state of thioredoxin. Free Radic Biol Med 2019; 134: 190-9. google scholar
  • 32. Feng H, Gu J, Gou F, Huang W, Gao C, Chen G, et al. High Glucose and Lipopolysaccharide Prime NLRP3 Inflammasome via ROS/ TXNIP Pathway in Mesangial Cells. J Diabetes Res 2016; 2016: 6973175. google scholar
  • 33. Wang S, Zhao X, Yang S, Chen B, Shi J. Salidroside alleviates high glucose-induced oxidative stress and extracellular matrix accumulation in rat glomerular mesangial cells by the TXNIP-NLRP3 inflammasome pathway. Chem Biol Interac 2017; 278: 48-53. google scholar
  • 34. Shi Y, Ren Y, Zhao L, Du C, Wang Y, Zhang Y, et al. Knockdown of thioredoxin interacting protein attenuates high glucose-induced apoptosis and activation of ASK1 in mouse mesangial cells. FEBS Letters 2011; 585: 1789-95. google scholar
  • 35. Shah A, Xia L, Goldberg H, Lee KW, Quaggin SE, Fantus IG. Thioredoxin-interacting protein mediates high glucose-induced reactive oxygen species generation by mitochondria and the NADPH oxidase, Nox4, in Mesangial Cells. J Biol Chem 2013; 288: 6835-48. google scholar
  • 36. Xu W, Wang L, Li J, Cai Y, Xue Y. TXNIP mediated the oxidative stress response in glomerular mesangial cells partially through AMPK pathway. Biomed Pharmacother 2018; 107: 785- 92. google scholar
  • 37. Wu M, Han W, Song S, Du Y, Liu C, Chen N, et al. NLRP3 deficiency ameliorates renal inflammation and fibrosis in diabetic mice. Mol Cell Endocrinol 2018; 478: 115-25. google scholar
  • 38. Zhang X, Mao Z, Huang Y, Zhang Z, Yao J. Gap junctions amplify TRPV4 activation-initiated cell injury via modification of intracellular Ca 2+ and Ca 2+ -dependent regulation of TXNIP. Channels 2020; 14: 246-56. google scholar
There are 38 citations in total.

Details

Primary Language English
Journal Section Themed Articles - Reviews
Authors

Gabriel Pereira 0000-0002-7836-4280

Emily Pereira Dos Santos This is me 0000-0002-2026-7250

Maria Augusta Ruy-barbosa This is me 0000-0002-4195-6186

Sofía Tomaselli Arioni This is me 0000-0001-8079-3191

Thabata Caroline De Oliveira Santos This is me 0000-0002-7770-8758

Débora Tavares De Resende E Silva This is me 0000-0002-3813-7139

Juan Sebastian Henao Agudelo This is me 0000-0003-4123-6741

Maria Do Carmo Pinho Franco This is me 0000-0003-0604-7689

Ricardo Fernandez This is me 0000-0002-6760-3952

Rafael Luiz Pereira This is me 0000-0002-6056-724X

Danilo Cândido De Almeida This is me 0000-0003-3661-2124

Publication Date December 29, 2022
Submission Date August 30, 2022
Published in Issue Year 2022 Volume: 81 Issue: 2

Cite

AMA Pereira G, Dos Santos EP, Ruy-barbosa MA, Arioni ST, Santos TCDO, De Resende E Silva DT, Agudelo JSH, Franco MDCP, Fernandez R, Pereira RL, De Almeida DC. Thioredoxin-Interacting Protein: The Redoxissome Complex in Glomerular Lesion. Eur J Biol. December 2022;81(2):274-280. doi:10.26650/EurJBiol.2022.1163544