Epigenetics and acute kidney injury_West China Medical Journal

Authors：

LIU Feng , TANG Jinhua ,  ZHUANG Shougang

Department of Nephrology, Shanghai East Hospital, Tongji University School of Medicine, Shanghai 200120, P. R. China;

Corresponding?author：

ZHUANG Shougang, Email: szhuang@lifespan.org

Keywords：

Epigenetics; Acetylation; Methylation; MicroRNA; Acute kidney injury

DOI：

10.7507/1002-0179.201806093

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Recent advances in epigenetics indicate that several epigenetic modifications, including acetylation, methylatio, and microRNA (miRNA), play an important role in the pathogenesis of acute kidney injury (AKI). Our study reveales that enhancement of protein acetylation by pharmacological inhibition of class I histone deacetylases leads to more severe tubular injury, and delays the restoration of renal structure and function. The changes in promoter DNA methylation occurs in the kidney with ischemia/reperfusion. MiRNA expression is associated with the regulation of both renal injury and regeneration after AKI. Targeting the epigenetic process may provide a therapeutic treatment for patients with AKI. The purpose of this review is to summarize recent advances in epigenetic regulation of AKI and provide mechanistic insight into the role of acetylation, methylation, and miRNA expression in the pathological processes of AKI.

Citation： LIU Feng, TANG Jinhua, ZHUANG Shougang. Epigenetics and acute kidney injury. West China Medical Journal, 2018, 33(7): 824-830. doi: 10.7507/1002-0179.201806093 Copy

1.	Lafrance JP, Miller DR. Acute kidney injury associates with increased long-term mortality. J Am Soc Nephrol, 2010, 21(2): 345-352.
2.	Lameire N, Van Biesen W, Vanholder R. The changing epidemiology of acute renal failure. Nat Clin Pract Nephrol, 2006, 2(7): 364-377.
3.	Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest, 2011, 121(11): 4210-4221.
4.	Chawla LS. Acute kidney injury leading to chronic kidney disease and long-term outcomes of acute kidney injury: the best opportunity to mitigate acute kidney injury?. Contrib Nephrol, 2011, 174: 182-190.
5.	Humphreys BD, Valerius MT, Kobayashi A, et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell, 2008, 2(3): 284-291.
6.	Humphreys BD, Czerniak S, DiRocco DP, et al. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA, 2011, 108(22): 9226-9231.
7.	Wen X, Murugan R, Peng Z, et al. Pathophysiology of acute kidney injury: a new perspective. Contrib Nephrol, 2010, 165: 39-45.
8.	Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol, 2003(Suppl 1): S55-S61.
9.	He S, Liu N, Bayliss G, et al. EGFR activity is required for renal tubular cell dedifferentiation and proliferation in a murine model of folic acid-induced acute kidney injury. Am J Physiol Renal Physiol, 2013, 304(4): F356-F366.
10.	Wallin A, Zhang G, Jones TW, et al. Mechanism of the nephrogenic repair response. Studies on proliferation and vimentin expression after 35S-1, 2-dichlorovinyl-L-cysteine nephrotoxicity in vivo and in cultured proximal tubule epithelial cells. Lab Invest, 1992, 66(4): 474-484.
11.	Tang JH, Yan YL, Zhao TC, et al. Class I HDAC activity is required for renal protection and regeneration after acute kidney injury. Am J Physiol Renal Physiol, 2014, 307(3): F303-F316.
12.	Tang J, Shi Y, Liu N, et al. Blockade of histone deacetylase 6 protects against cisplatin-induced acute kidney injury. Clin Sci (Lond), 2018, 132(3): 339-359.
13.	Shi Y, Xu L, Tang J, et al. Inhibition of HDAC6 protects against rhabdomyolysis-induced acute kidney injury. Am J Physiol Renal Physiol, 2017, 312(3): F502-F515.
14.	Fontecha-Barriuso M, Martin-Sanchez D, Ruiz-Andres O, et al. Targeting epigenetic DNA and histone modifications to treat kidney disease. Nephrol Dial Transplant, 2018. doi: 10.1093/ndt/gfy009.
15.	Zhang H, Zhang W, Jiao F, et al. The nephroprotective effect of MS-275 on lipopolysaccharide (LPS)-induced acute kidney injury by inhibiting reactive oxygen species (ROS)-oxidative stress and endoplasmic reticulum stress. Med Sci Monit, 2018, 24: 2620-2630.
16.	Tang J, Zhuang S. Upregulation of AMWAP: a novel mechanism for HDAC inhibitors to protect against cisplatin nephrotoxicity. Kidney Int, 2016, 89(2): 267-269.
17.	Ranganathan P, Hamad R, Mohamed R, et al. Histone deacetylase-mediated silencing of AMWAP expression contributes to cisplatin nephrotoxicity. Kidney Int, 2016, 89(2): 317-326.
18.	Novitskaya T, McDermott L, Zhang KX, et al. A PTBA small molecule enhances recovery and reduces postinjury fibrosis after aristolochic acid-induced kidney injury. Am J Physiol Renal Physiol, 2014, 306(5): 496-504.
19.	Feng Y, Huang R, Guo F, et al. Selective histone deacetylase 6 inhibitor 23BB alleviated rhabdomyolysis-induced acute kidney injury by regulating endoplasmic reticulum stress and apoptosis. Front Pharmacol, 2018, 9: 274.
20.	Marumo T, Hishikawa K, Yoshikawa M, et al. Epigenetic regulation of BMP7 in the regenerative response to ischemia. J Am Soc Nephrol, 2008, 19(7): 1311-1320.
21.	Villanueva S, Céspedes C, Vio CP. Ischemic acute renal failure induces the expression of a wide range of nephrogenic proteins. Am J Physiol Regul Integr Comp Physiol, 2006, 290(4): R861-R870.
22.	Xu S, Gao Y, Zhang Q, et al. SIRT1/3 activation by resveratrol attenuates acute kidney injury in a septic rat model. Oxid Med Cell, 2016: 7296092.
23.	Erkasap S, Erkasap N, Bradford B, et al. The effect of leptin and resveratrol on JAK/STAT pathways and Sirt-1 gene expression in the renal tissue of ischemia/reperfusion induced rats. Bratisl Lek Listy, 2017, 118(8): 443-448.
24.	Pratt JR, Parker MD, Affleck LJ, et al. Ischemic epigenetics and the transplanted kidney. Transplant Proc, 2006, 38(10): 3344-3346.
25.	Mehta TK, Hoque MO, Ugarte R, et al. Quantitative detection of promoter hypermethylation as a biomarker of acute kidney injury during transplantation. Transplant Proc, 2006, 38(10): 3420-3426.
26.	Endo K, Kito N, Fukushima Y, et al. A novel biomarker for acute kidney injury using TaqMan-based unmethylated DNA-specific polymerase chain reaction. Biomed Res, 2014, 35(3): 207-213.
27.	Kang SW, Shih PA, Mathew RO, et al. Renal kallikrein excretion and epigenetics in human acute kidney injury: expression, mechanisms and Consequences. BMC, Nephrol, 2011, 12: 27.
28.	Huang N, Tan L, Xue Z, et al. Reduction of DNA hydroxymethylation in the mouse kidney insulted by ischemia reperfusion. Biochem Biophys Res Commun, 2012, 422(4): 697-702.
29.	Guo C, Pei L, Xiao X, et al. DNA methylation protects against cisplatin-induced kidney injury by regulating specific genes, including interferon regulatory factor 8. Kidney Int, 2017, 92(5): 1194-1205.
30.	Nguyen AT, Zhang Y. The diverse functions of Dot1 and H3K79 methylation. Genes Dev, 2011, 25(13): 1345-1358.
31.	Nelson JD, Denisenko O, Sova P, et al. Fast chromatin immunoprecipitation assay. Nucleic Acids Res, 2006, 34(1): e2.
32.	Johnson AC, Ware LB, Himmelfarb J, et al. HMG-CoA reductase activation and urinary pellet cholesterol elevations in acute kidney injury. Clin J Am Soc Nephrol, 2011, 6(9): 2108-2113.
33.	Naito M, Bomsztyk K, Zager RA. Endotoxin mediates recruitment of RNA polymeraseⅡto target genes in acute renal failure. J Am Soc Nephrol, 2008, 19(7): 1321-1330.
34.	Parker MD, Chambers PA, Lodge JP, et al. Ischemia- reperfusion injury and its influence on the epigenetic modification of the donor kidney genome. Transplantation, 2008, 86(12): 1818-1823.
35.	Zhou X, Zang X, Ponnusamy M, et al. Enhancer of zeste homolog 2 inhibition attenuates renal fibrosis by maintaining Smad7 and phosphatase and tensin homolog expression. J Am Soc Nephrol, 2016, 27(7): 2092-2108.
36.	Whyte WA, Bilodeau S, Orlando DA, et al. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature, 2012, 482(7384): 221-225.
37.	Shen Q, Jin H, Wang X. Epidermal stem cells and their epigenetic regulation. Int J Mol Sci, 2013, 14(9): 17861-17880.
38.	He Y, Yu H, Sun S, et al. Trans-2-phenylcyclopropylamine regulates zebrafish lateral line neuromast development mediated by depression of LSD1 activity. Int J Dev Biol, 2013, 57(5): 365-373.
39.	Irifuku T, DoiS, Sasaki K, et al. Inhibition of H3K9 histone methyltransferase G9a attenuates renal fibrosis and retains klotho expression. Kidney Int, 2016, 89(1): 147-157.
40.	Li LX, Fan LX, Zhou JX, et al. Lysine methyltransferase SMYD2 promotes cyst growth in autosomal dominant polycystic kidney disease. J Clin Invest, 2017, 127(7): 2751-2764.
41.	Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet, 2011, 12(2): 99-110.
42.	Wei Q, Bhatt K, He HZ, et al. Targeted deletion of Dicer from proximal tubules protects against renal ischemia-reperfusion injury. J Am Soc Nephrol, 2010, 21(5): 756-761.
43.	Cantaluppi V, Gatti S, Medica D, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int, 2012, 82(4): 412-427.
44.	Lorenzen JM, Kaucsar T, Schauerte C, et al. MicroRNA-24 antagonism prevents renal ischemia reperfusion injury. J Am Soc Nephrol, 2014, 25(12): 2717-2729.
45.	Lan YF, Chen HH, Lai PF, et al. MicroRNA-494 reduces ATF3 expression and promotes AKI. J Am Soc Nephrol, 2012, 23(12): 2012-2023.
46.	Godwin JG, Ge XP, Stephan K, et al. Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci USA, 2010, 107(32): 14339-14344.
47.	Aguado-Fraile E, Ramos E, Sáenz-Morales D, et al. miR-127 protects proximal tubule cells against ischemia/reperfusion: identification of kinesin family member 3B as miR-127 target. PLoS One, 2012, 7(9): e44305.
48.	Bhatt K, Wei Q, Pabla N, et al. MicroRNA-687 induced by hypoxia-inducible factor-1 targets phosphatase and tensin homolog in renal ischemia-reperfusion injury. J Am Soc Nephrol, 2015, 26(7): 1588-1596.
49.	Rossetto D, Avvakumov N, C?té J. Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics, 2012, 7(10): 1098-1108.
50.	Metzger E, Imhof A, Patel D, et al. Phosphorylation of histone H3T6 by PKCbeta(Ⅰ) controls demethylation at histone H3K4. Nature, 2010, 464(7289): 792-796.
51.	Guo C, Wei Q, Su Y, et al. SUMOylation occurs in acute kidney injury and plays a cytoprotective role. Biochim Biophys Acta, 2015, 1852(3): 482-489.
52.	Ruiz-Andres O, Sanchez-Ni?o MD, Cannata-Ortiz P, et al. Histone lysine crotonylation during acute kidney injury in mice. Dis Model Mech, 2016, 9(6): 633-645.
53.	Sabari BR, Tang Z, Huang H, et al. Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol Cell, 2015, 58(2): 203-215.
54.	Sanz AB, Izquierdo MC, Sanchez-Ni?o MD, et al. TWEAK and the progression of renal disease: clinical translation. Nephrol Dial Transplant, 2014, 29(Suppl 1): i54-i62.
55.	Martins-Marques T, Ribeiro-Rodrigues T, Pereira P, et al. Autophagy and ubiquitination in cardiovascular diseases. DNA Cell Biol, 2015, 34(4): 243-251.
56.	Varol B, Co?kun ?, Karabulut S, et al. Clinical significance of serum ADP-ribosylation and NAD glycohydrolase activity in patients with colorectal cancer. Tumour Biol, 2014, 35(6): 5575-5582.
57.	Ravidà A, Musante L, Kreivi M, et al. Glycosylation patterns of kidney proteins differ in rat diabetic nephropathy. Kidney Int, 2015, 87(5): 963-974.

1. Lafrance JP, Miller DR. Acute kidney injury associates with increased long-term mortality. J Am Soc Nephrol, 2010, 21(2): 345-352.
2. Lameire N, Van Biesen W, Vanholder R. The changing epidemiology of acute renal failure. Nat Clin Pract Nephrol, 2006, 2(7): 364-377.
3. Bonventre JV, Yang L. Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest, 2011, 121(11): 4210-4221.
4. Chawla LS. Acute kidney injury leading to chronic kidney disease and long-term outcomes of acute kidney injury: the best opportunity to mitigate acute kidney injury?. Contrib Nephrol, 2011, 174: 182-190.
5. Humphreys BD, Valerius MT, Kobayashi A, et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell, 2008, 2(3): 284-291.
6. Humphreys BD, Czerniak S, DiRocco DP, et al. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci USA, 2011, 108(22): 9226-9231.
7. Wen X, Murugan R, Peng Z, et al. Pathophysiology of acute kidney injury: a new perspective. Contrib Nephrol, 2010, 165: 39-45.
8. Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol, 2003(Suppl 1): S55-S61.
9. He S, Liu N, Bayliss G, et al. EGFR activity is required for renal tubular cell dedifferentiation and proliferation in a murine model of folic acid-induced acute kidney injury. Am J Physiol Renal Physiol, 2013, 304(4): F356-F366.
10. Wallin A, Zhang G, Jones TW, et al. Mechanism of the nephrogenic repair response. Studies on proliferation and vimentin expression after 35S-1, 2-dichlorovinyl-L-cysteine nephrotoxicity in vivo and in cultured proximal tubule epithelial cells. Lab Invest, 1992, 66(4): 474-484.
11. Tang JH, Yan YL, Zhao TC, et al. Class I HDAC activity is required for renal protection and regeneration after acute kidney injury. Am J Physiol Renal Physiol, 2014, 307(3): F303-F316.
12. Tang J, Shi Y, Liu N, et al. Blockade of histone deacetylase 6 protects against cisplatin-induced acute kidney injury. Clin Sci (Lond), 2018, 132(3): 339-359.
13. Shi Y, Xu L, Tang J, et al. Inhibition of HDAC6 protects against rhabdomyolysis-induced acute kidney injury. Am J Physiol Renal Physiol, 2017, 312(3): F502-F515.
14. Fontecha-Barriuso M, Martin-Sanchez D, Ruiz-Andres O, et al. Targeting epigenetic DNA and histone modifications to treat kidney disease. Nephrol Dial Transplant, 2018. doi: 10.1093/ndt/gfy009.
15. Zhang H, Zhang W, Jiao F, et al. The nephroprotective effect of MS-275 on lipopolysaccharide (LPS)-induced acute kidney injury by inhibiting reactive oxygen species (ROS)-oxidative stress and endoplasmic reticulum stress. Med Sci Monit, 2018, 24: 2620-2630.
16. Tang J, Zhuang S. Upregulation of AMWAP: a novel mechanism for HDAC inhibitors to protect against cisplatin nephrotoxicity. Kidney Int, 2016, 89(2): 267-269.
17. Ranganathan P, Hamad R, Mohamed R, et al. Histone deacetylase-mediated silencing of AMWAP expression contributes to cisplatin nephrotoxicity. Kidney Int, 2016, 89(2): 317-326.
18. Novitskaya T, McDermott L, Zhang KX, et al. A PTBA small molecule enhances recovery and reduces postinjury fibrosis after aristolochic acid-induced kidney injury. Am J Physiol Renal Physiol, 2014, 306(5): 496-504.
19. Feng Y, Huang R, Guo F, et al. Selective histone deacetylase 6 inhibitor 23BB alleviated rhabdomyolysis-induced acute kidney injury by regulating endoplasmic reticulum stress and apoptosis. Front Pharmacol, 2018, 9: 274.
20. Marumo T, Hishikawa K, Yoshikawa M, et al. Epigenetic regulation of BMP7 in the regenerative response to ischemia. J Am Soc Nephrol, 2008, 19(7): 1311-1320.
21. Villanueva S, Céspedes C, Vio CP. Ischemic acute renal failure induces the expression of a wide range of nephrogenic proteins. Am J Physiol Regul Integr Comp Physiol, 2006, 290(4): R861-R870.
22. Xu S, Gao Y, Zhang Q, et al. SIRT1/3 activation by resveratrol attenuates acute kidney injury in a septic rat model. Oxid Med Cell, 2016: 7296092.
23. Erkasap S, Erkasap N, Bradford B, et al. The effect of leptin and resveratrol on JAK/STAT pathways and Sirt-1 gene expression in the renal tissue of ischemia/reperfusion induced rats. Bratisl Lek Listy, 2017, 118(8): 443-448.
24. Pratt JR, Parker MD, Affleck LJ, et al. Ischemic epigenetics and the transplanted kidney. Transplant Proc, 2006, 38(10): 3344-3346.
25. Mehta TK, Hoque MO, Ugarte R, et al. Quantitative detection of promoter hypermethylation as a biomarker of acute kidney injury during transplantation. Transplant Proc, 2006, 38(10): 3420-3426.
26. Endo K, Kito N, Fukushima Y, et al. A novel biomarker for acute kidney injury using TaqMan-based unmethylated DNA-specific polymerase chain reaction. Biomed Res, 2014, 35(3): 207-213.
27. Kang SW, Shih PA, Mathew RO, et al. Renal kallikrein excretion and epigenetics in human acute kidney injury: expression, mechanisms and Consequences. BMC, Nephrol, 2011, 12: 27.
28. Huang N, Tan L, Xue Z, et al. Reduction of DNA hydroxymethylation in the mouse kidney insulted by ischemia reperfusion. Biochem Biophys Res Commun, 2012, 422(4): 697-702.
29. Guo C, Pei L, Xiao X, et al. DNA methylation protects against cisplatin-induced kidney injury by regulating specific genes, including interferon regulatory factor 8. Kidney Int, 2017, 92(5): 1194-1205.
30. Nguyen AT, Zhang Y. The diverse functions of Dot1 and H3K79 methylation. Genes Dev, 2011, 25(13): 1345-1358.
31. Nelson JD, Denisenko O, Sova P, et al. Fast chromatin immunoprecipitation assay. Nucleic Acids Res, 2006, 34(1): e2.
32. Johnson AC, Ware LB, Himmelfarb J, et al. HMG-CoA reductase activation and urinary pellet cholesterol elevations in acute kidney injury. Clin J Am Soc Nephrol, 2011, 6(9): 2108-2113.
33. Naito M, Bomsztyk K, Zager RA. Endotoxin mediates recruitment of RNA polymeraseⅡto target genes in acute renal failure. J Am Soc Nephrol, 2008, 19(7): 1321-1330.
34. Parker MD, Chambers PA, Lodge JP, et al. Ischemia- reperfusion injury and its influence on the epigenetic modification of the donor kidney genome. Transplantation, 2008, 86(12): 1818-1823.
35. Zhou X, Zang X, Ponnusamy M, et al. Enhancer of zeste homolog 2 inhibition attenuates renal fibrosis by maintaining Smad7 and phosphatase and tensin homolog expression. J Am Soc Nephrol, 2016, 27(7): 2092-2108.
36. Whyte WA, Bilodeau S, Orlando DA, et al. Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature, 2012, 482(7384): 221-225.
37. Shen Q, Jin H, Wang X. Epidermal stem cells and their epigenetic regulation. Int J Mol Sci, 2013, 14(9): 17861-17880.
38. He Y, Yu H, Sun S, et al. Trans-2-phenylcyclopropylamine regulates zebrafish lateral line neuromast development mediated by depression of LSD1 activity. Int J Dev Biol, 2013, 57(5): 365-373.
39. Irifuku T, DoiS, Sasaki K, et al. Inhibition of H3K9 histone methyltransferase G9a attenuates renal fibrosis and retains klotho expression. Kidney Int, 2016, 89(1): 147-157.
40. Li LX, Fan LX, Zhou JX, et al. Lysine methyltransferase SMYD2 promotes cyst growth in autosomal dominant polycystic kidney disease. J Clin Invest, 2017, 127(7): 2751-2764.
41. Huntzinger E, Izaurralde E. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat Rev Genet, 2011, 12(2): 99-110.
42. Wei Q, Bhatt K, He HZ, et al. Targeted deletion of Dicer from proximal tubules protects against renal ischemia-reperfusion injury. J Am Soc Nephrol, 2010, 21(5): 756-761.
43. Cantaluppi V, Gatti S, Medica D, et al. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int, 2012, 82(4): 412-427.
44. Lorenzen JM, Kaucsar T, Schauerte C, et al. MicroRNA-24 antagonism prevents renal ischemia reperfusion injury. J Am Soc Nephrol, 2014, 25(12): 2717-2729.
45. Lan YF, Chen HH, Lai PF, et al. MicroRNA-494 reduces ATF3 expression and promotes AKI. J Am Soc Nephrol, 2012, 23(12): 2012-2023.
46. Godwin JG, Ge XP, Stephan K, et al. Identification of a microRNA signature of renal ischemia reperfusion injury. Proc Natl Acad Sci USA, 2010, 107(32): 14339-14344.
47. Aguado-Fraile E, Ramos E, Sáenz-Morales D, et al. miR-127 protects proximal tubule cells against ischemia/reperfusion: identification of kinesin family member 3B as miR-127 target. PLoS One, 2012, 7(9): e44305.
48. Bhatt K, Wei Q, Pabla N, et al. MicroRNA-687 induced by hypoxia-inducible factor-1 targets phosphatase and tensin homolog in renal ischemia-reperfusion injury. J Am Soc Nephrol, 2015, 26(7): 1588-1596.
49. Rossetto D, Avvakumov N, C?té J. Histone phosphorylation: a chromatin modification involved in diverse nuclear events. Epigenetics, 2012, 7(10): 1098-1108.
50. Metzger E, Imhof A, Patel D, et al. Phosphorylation of histone H3T6 by PKCbeta(Ⅰ) controls demethylation at histone H3K4. Nature, 2010, 464(7289): 792-796.
51. Guo C, Wei Q, Su Y, et al. SUMOylation occurs in acute kidney injury and plays a cytoprotective role. Biochim Biophys Acta, 2015, 1852(3): 482-489.
52. Ruiz-Andres O, Sanchez-Ni?o MD, Cannata-Ortiz P, et al. Histone lysine crotonylation during acute kidney injury in mice. Dis Model Mech, 2016, 9(6): 633-645.
53. Sabari BR, Tang Z, Huang H, et al. Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol Cell, 2015, 58(2): 203-215.
54. Sanz AB, Izquierdo MC, Sanchez-Ni?o MD, et al. TWEAK and the progression of renal disease: clinical translation. Nephrol Dial Transplant, 2014, 29(Suppl 1): i54-i62.
55. Martins-Marques T, Ribeiro-Rodrigues T, Pereira P, et al. Autophagy and ubiquitination in cardiovascular diseases. DNA Cell Biol, 2015, 34(4): 243-251.
56. Varol B, Co?kun ?, Karabulut S, et al. Clinical significance of serum ADP-ribosylation and NAD glycohydrolase activity in patients with colorectal cancer. Tumour Biol, 2014, 35(6): 5575-5582.
57. Ravidà A, Musante L, Kreivi M, et al. Glycosylation patterns of kidney proteins differ in rat diabetic nephropathy. Kidney Int, 2015, 87(5): 963-974.

West China Medical Journal

Epigenetics and acute kidney injury

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content