Curcumin protects renal tubular epithelial cells from high glucose-induced epithelial-to-mesenchymal transition through Nrf2-mediated upregulation of heme oxygenase-1

Molecular Medicine Reports

Volumn 12, Issue 1, 2015, Pages 1347-1355

  Zhang, Xiuli ^a,b   Liang, Dan ^c   Guo, Lin ^c   Liang, Wei ^a   Jiang, Yan ^a   Li, Hongjuan ^c   Zhao, Yue ^b   Lu, Shumin ^a   Chi, Zhi Hong ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^c Troops of 95935 Unit   (China)

Author keywords

Curcumin; Epithelial to mesenchymal transition; High glucose; Nuclear factor (erythroid derived 2) like 2; Renal tubular epithelial cells

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CURCUMIN; GLUCOSE; HEME OXYGENASE 1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NRF2; UVOMORULIN; HEME OXYGENASE; HMOX1 PROTEIN, RAT; NFE2L2 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; EPITHELIAL MESENCHYMAL TRANSITION; GENE SILENCING; GLUCOSE INTAKE; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE EPITHELIUM; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; RENAL PROTECTION; UPREGULATION; ANIMAL; BIOSYNTHESIS; DIABETIC NEPHROPATHY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KIDNEY TUBULE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

RATTUS;

ANIMALS; CURCUMIN; DIABETIC NEPHROPATHIES; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GLUCOSE; HEME OXYGENASE (DECYCLIZING); HUMANS; KIDNEY TUBULES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RATS; SIGNAL TRANSDUCTION;

EID: 84926641042     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2015.3556     Document Type: Article

References (61)

1. Schena FP and Gesualdo L: Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol 16 (Suppl 1): S30-S33, 2005.
2. Lapice E, Pinelli M, Riccardi G and Vaccaro O: Pro12Ala polymorphism in the PPARG gene contributes to the development of diabetic nephropathy in Chinese type 2 diabetic patients: comment on the study by Liu et al. Diabetes Care 33: e114; author reply e115, 2010.
3. Ayodele OE, Alebiosu CO and Salako BL: Diabetic nephropathy-A review of the natural history, burden, risk factors and treatment. J Natl Med Assoc 96: 1445-1454, 2004.
4. Yeh CH, Chang CK, Cheng KC, Li YX, Zhang YW and Cheng JT: Role of bone morphogenetic proteins-7 (BMP-7) in the renal improvement effect of DangGui (Angelica sinensis) in type-1 diabetic rats. Evid Based Complement Alternat Med 2011: 796723, 2011.
5. Gilbert RE and Cooper ME: The tubulointerstitium in progressive diabetic kidney disease: more than an aftermath of glomerular injury? Kidney Int 56: 1627-1637, 1999.
6. Simonson MS: Phenotypic transitions and fibrosis in diabetic nephropathy. Kidney Int 71: 846-854, 2007.
7. Tang SC and Lai KN: The pathogenic role of the renal proximal tubular cell in diabetic nephropathy. Nephrol Dial Transplant 27: 3049-3056,2012.
8. Zeisberg M and Kalluri R: The role of epithelial-to-mesenchymal transition in renal fibrosis. J Mol Med Berl 82: 175-181, 2004.
9. Iwano M, Plieth D, Danoff TM, Xue C, Okada H and Neilson EG: Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350, 2002.
10. Liu Y: New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol 21: 212-222, 2010.
11. Burns WC, Twigg SM, Forbes JM, et al: Connective tissue growth factor plays an important role in adVanced glycation end product-induced tubular epithelial-to-mesenchymal transition: implications for diabetic renal disease. J Am Soc Nephrol 17: 2484-2494, 2006.
12. Lv ZM, Wang Q, Wan Q, et al: The role of the p38 MAPK signaling pathway in high glucose-induced epithelial-mesenchymal transition of cultured human renal tubular epithelial cells. PLoS One 6: e22806, 2011.
13. Lee YJ and Han HJ: Troglitazone ameliorates high glucose-induced EMT and dysfunction of SGLTs through PI3K/Akt, GSK-3β, Snail1, and β-catenin in renal proximal tubule cells. Am J Physiol Renal Physiol 298: F1263-F1275, 2010.
14. Dogukan A, Sahin N, Tuzcu M, Juturu V, Orhan C, Onderci M, et al: The effects of chromium histidinate on mineral status of serum and tissue in fat-fed and streptozotocin-treated type II diabetic rats. Biol Trace Elem Res 131: 124-132,2009.
15. Simonian MH and Smith JA: Spectrophotometric and colorimetric determination of protein concentration. Curr Protoc Mol Biol 10: Unit 10.1A, 2006.
16. Kalluri R and Neilson EG: Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784, 2003.
17. Chen H, Zhang B, Yuan X, et al: Isoliquiritigenin-induced effects on Nrf2 mediated antioxidant defence in the HL-60 cell monocytic differentiation. Cell Biol Int 37: 1215-1224, 2013.
18. Jiang T, Huang Z, Lin Y, Zhang Z, Fang D and Zhang DD: The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy. Diabetes 59: 850-860,2010.
19. Yoh K, Hirayama A, Ishizaki K, Yamada A, Takeuchi M, Yamagishi S, et al: Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells 13: 1159-1170,2008.
20. Abraham NG and Kappas A: Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 60: 79-127, 2008.
21. Sikorski EM, Hock T, Hill-Kapturczak N and Agarwal A: The story so far: Molecular regulation of the heme oxygenase-1 gene in renal injury. Am J Physiol Renal Physiol 286: F425-F441, 2004.
22. Chan K, Han XD and Kan YW: An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 98: 4611-4616, 2001.
23. Abraham NG, Cao J, Sacerdoti D, Li X and Drummond G: Heme oxygenase: the key to renal function regulation. Am J Physiol Renal Physiol 297: F1137-F1152, 2009.
24. Bolisetty S, Traylor A, Zarjou A, et al: Mitochondria-targeted heme oxygenase-1 decreases oxidative stress in renal epithelial cells. Am J Physiol Renal Physiol 305: F255-F264, 2013.
25. Quan S, Kaminski PM, Yang L, Morita T, Inaba M, Ikehara S, et al: Heme oxygenase-1 prevents superoxide anion-associated endothelial cell sloughing in diabetic rats. Biochem Biophys Res Commun 315: 509-516, 2004.
26. Kie JH, Kapturczak MH, Traylor A, Agarwal A and Hill-Kapturczak N: Heme oxygenase-1 deficiency promotes epithelial-mesenchymal transition and renal fibrosis. J Am Soc Nephrol 19: 1681-1691, 2008.
27. Soetikno V, Sari FR, Lakshmanan AP, et al: Curcumin alleviates oxidative stress, inflammation, and renal fibrosis in remnant kidney through the Nrf2-keap1 pathway. Mol Nutr Food Res 57: 1649-1659, 2013.
28. Farhangkhoee H, Khan ZA, Chen S and Chakrabarti S: Differential effects of curcumin on vasoactive factors in the diabetic rat heart. Nutr Metab (Lond) 3: 27, 2006.
29. Kowluru RA and Kanwar M: Effects of curcumin on retinal oxidative stress and inflammation in diabetes. Nutr Metab (Lond) 4: 8, 2007.
30. Maheshwari RK, Singh AK, Gaddipati J and Srimal RC: Multiple biological activities of curcumin: a short review. Life Sci 78: 2081-2087, 2006.
31. Sharma OP: Antioxidant activity of curcumin and related compounds. Biochem Pharmacol 25: 1811-1812, 1976.
32. Yao QY, Xu BL, Wang JY, et al: Inhibition by curcumin of multiple sites of the transforming growth factor-beta1 signalling pathway ameliorates the progression of liver fibrosis induced by carbon tetrachloride in rats. BMC Complement Altern Med 12: 156, 2012.
33. Suzuki M, Betsuyaku T, Ito Y, et al: Curcumin attenuates elastase-and cigarette smoke-induced pulmonary emphysema in mice. Am J Physiol Lung Cell Mol Physiol 296: L614-L623, 2009.
34. Gaedeke J, Noble NA and Border WA: Curcumin blocks multiple sites of the TGF-beta signaling cascade in renal cells. Kidney Int 66: 112-120, 2004.
35. Kuwabara N, Tamada S, Iwai T, et al: Attenuation of renal fibrosis by curcumin in rat obstructive nephropathy. Urology 67: 440-446, 2006.
36. Murugan P and Pari L: Influence of tetrahydrocurcumin on hepatic and renal functional markers and protein levels in experimental type 2 diabetic rats. Basic Clin Pharmacol Toxicol 101: 241-245, 2007.
37. Sharma S, Kulkarni SK and Chopra K: Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin Exp Pharmacol Physiol 33: 940-945, 2006.
38. Bayrak O, Uz E, Bayrak R, Turgut F, Atmaca AF, Sahin S, et al: Curcumin protects against ischemia/reperfusion injury in rat kidneys. World J Urol 26: 285-291,2008.
39. Hill-Kapturczak N, ThamilselVan V, Liu F, Nick HS and Agarwal A: Mechanism of heme oxygenase-1 gene induction by curcumin in human renal proximal tubule cells. Am J Physiol Renal Physiol 281: F851-F859, 2001.
40. Gaedeke J, Noble NA and Border WA: Curcumin blocks fibrosis in anti-Thy 1 glomerulonephritis through up-regulation of heme oxygenase 1. Kidney Int 68: 2042-2049, 2005.
41. Zhang X, Zhao Y, Chu Q, Wang ZY, Li H and Chi ZH: Zinc modulates high glucose-induced apoptosis by suppressing oxidative stress in renal tubular epithelial cells. Biol Trace Elem Res 158: 259-267, 2014.
42. Holmström TH and Eriksson JE: Phosphorylation-based signaling in Fas receptor-mediated apoptosis. Crit Rev Immunol 20: 121-152,2000.
43. Nishiura T and Abe K: Alpha1-adrenergic receptor stimulation induces the expression of receptor activator of nuclear factor kappaB ligand gene via protein kinase C and extracellular signal-regulated kinase pathways in MC3T3-E1 osteoblast-like cells. Arch Oral Biol 52: 778-785, 2007.
44. Zhang LY, Zhou YY, Chen F, et al: Taurine inhibits serum deprivation-induced osteoblast apoptosis via the taurine transporter/ERK signaling pathway. Braz J Med Biol Res 44: 618-623, 2011.
45. Chen YC, Chow JM , Lin CW, Wu CY and Shen SC: Baicalein inhibition of oxidative-stress-induced apoptosis via modulation of ERKs activation and induction of HO-1 gene expression in rat glioma cells C6. Toxicol Appl Pharmacol 216: 263-273, 2006.
46. Parfenova H, Basuroy S, Bhattacharya S, Tcheranova D, Qu Y, Regan RF and Leffler CW: Glutamate induces oxidative stress and apoptosis in cerebral vascular endothelial cells: Contributions of HO-1 and HO-2 to cytoprotection. Am J Physiol Cell Physiol 290: C1399-C1410, 2006.
47. Yang C, ZhangX, Fan H and Liu Y: Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res 1282: 133-141, 2009.
48. Sahin K, Orhan C, Tuzcu Z, Tuzcu M and Sahin N: Curcumin ameliorates heat stress via inhibtion of oxidative stress and modulation of Nrf2/HO-1 pathway in quail. Food Chem Toxicol 50: 4035-4041, 2012.
49. Uc A, Reszka KJ, Buettner GR and Stokes JB: Tin protoporphyrin induces intestinal chloride secretion by inducing light oxidation processes. Am J Physiol Cell Physiol 292: C1906-C1914, 2007.
50. Hills CE, Al-Rasheed N, Al-Rasheed N, Willars GB and Brunskill NJ: C-peptide reverses TGF-beta1-induced changes in renal proximal tubular cells: implications for treatment of diabetic nephropathy. Am J Physiol Renal Physiol 296: F614-F621, 2009.
51. Lan HY: Tubular epithelial-myofibroblast transdifferentiation mechanisms in proximal tubule cells. Curr Opin Nephrol Hypertens 12: 25-29, 2003.
52. Oldfield MD, Bach LA, Forbes JM, Nikolic-Paterson D, McRobert A, Thallas V, et al: AdVanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for adVanced glycation end products (RAGE). J Clin Invest 108: 1853-1863, 2001.
53. Li R, Wang Y, Liu Y, et al: Curcumin inhibits transforming growth factor-β1-induced EMT via PPARγ pathway, not Smad pathway in renal tubular epithelial cells. PLoS One 8: e58848, 2013.
54. Kosugi T and Sato W: Midkine and the kidney: health and diseases. Nephrol Dial Transplant 27: 16-21, 2012.
55. Shih AY, Li P and Murphy TH: A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J Neurosci 25: 10321-10335, 2005.
56. Cho HY, Reddy SP, Yamamoto M and Kleeberger SR: The transcription factor NRF2 protects against pulmonary fibrosis. FASEB J 18: 1258-1260, 2004.
57. Leonard MO, Kieran NE, Howell K, Burne MJ, Varadarajan R, Dhakshinamoorthy S, et al: Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J 20: 2624-2626, 2006.
58. Liu M, Grigoryev DN, Crow MT, Haas M, Yamamoto M, Reddy SP and Rabb H: Transcription factor Nrf2 is protective during ischemic and nephrotoxic acute kidney injury in mice. Kidney Int 76: 277-285, 2009.
59. Kanki K, Umemura T, Kitamura Y, et al: A possible role of nrf2 in prevention of renal oxidative damage by ferric nitrilotriacetate. Toxicol Pathol 36: 353-361, 2008.
60. Biswas SK, McClure D, Jimenez LA, Megson IL and Rahman I: Curcumin induces glutathione biosynthesis and inhibits NF-kappaB activation and interleukin-8 release in alveolar epithelial cells: mechanism of free radical scavenging activity. Antioxid Redox Signal 7: 32-41, 2005.
61. Balogun E, Foresti R, Green CJ and Motterlini R: Changes in temperature modulate heme oxygenase-1 induction by curcumin in renal epithelial cells. Biochem Biophys Res Commun 308: 950-955, 2003.