Curcumin ameliorates streptozotocin-induced liver damage through modulation of endoplasmic reticulum stress-mediated apoptosis in diabetic rats

Free Radical Research

Volumn 49, Issue 3, 2015, Pages 279-289

  Afrin, R ^a   Arumugam, S ^a   Soetikno, V ^a   Thandavarayan, R A ^a,b   Pitchaimani, V ^a   Karuppagounder, V ^a   Sreedhar, R ^a   Harima, M ^a   Suzuki, H ^a,c   Miyashita, S ^a   Nomoto, M ^a   Suzuki, K ^d   Watanabe, K ^a  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^c NIIGATA UNIVERSITY   (Japan)

^d NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Apoptosis; Curcumin; Diabetes mellitus; Endoplasmic reticulum stress; Liver

Indexed keywords

CASPASE 3; CCAAT ENHANCER BINDING PROTEIN; CURCUMIN; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE R; STREPTOZOCIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; ANTIDIABETIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; EXPERIMENTAL DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KUPFFER CELL; LIVER INJURY; MALE; NONHUMAN; RAT; TREATMENT DURATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; CHEMICALLY INDUCED; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; LIVER;

RATTUS;

ANIMALS; APOPTOSIS; CURCUMIN; DIABETES MELLITUS, EXPERIMENTAL; ENDOPLASMIC RETICULUM STRESS; HYPOGLYCEMIC AGENTS; LIVER; MALE; RATS; UNFOLDED PROTEIN RESPONSE;

EID: 84925804765     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2014.999674     Document Type: Article

References (70)

1. Das AV, Padayatti PS, Paulose CS. Effect of leaf extract of Aegle marmelose (L.) Correa ex Roxb. on histological and ultrastructural changes in tissues of streptozotocin induced diabetic rats. Indian J Exp Biol 1996; 34: 341-345.
2. Latry P, Bioulac-Sage P, Echinard E, Gin H, Boussarie L, Grimaud JA, Balabaud C. Perisinusoidal fibrosis and basement membrane-like material in the livers of diabetic patients. Hum Pathol 1987; 18: 775-780.
3. Harrison SA. Liver disease in patients with diabetes mellitus. J Clin Gastroenterol 2006; 40: 68-76.
4. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006; 440: 944-948.
5. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004; 306: 457-461.
6. Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and beta-cell dysfunction. Endocr Rev 2008; 29: 351-366.
7. West IC. Radicals and oxidative stress in diabetes. Diabet Med 2000; 17: 171-180.
8. Shams ME, Al-Gayyar MM, Barakat EA. Type 2 diabetes mellitus induced hyperglycemia in patients with NAFLD and normal LFTs: relationship to lipid profile, oxidative stress and pro-inflammatory cytokines. Sci Pharm 2011; 79: 623-634.
9. de Cavanagh EM, Inserra F, Toblli J, Stella I, Fraga CG, Ferder L. Enalapril attenuates oxidative stress in diabetic rats. Hypertension 2001; 38: 1130-1136.
10. Scheuner D, Vander MD, Song B, Flamez D, Creemers JW, Tsukamoto K, et al. Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 2005; 11: 757-764.
11. Yusta B, Baggio LL, Estall JL, Koehler JA, Holland DP, Li H, et al. GLP-1 receptor activation improves beta cell function and survival following induction of endoplasmic reticulum stress. Cell Metab 2006: 4: 391-406.
12. Huang CJ, Lin CY, Haataja L, Gurlo T, Butler AE, Rizza RA, Butler PC. High expression rates of human islet amyloid polypeptide induce endoplasmic reticulum stress mediated beta-cell apoptosis, a characteristic of humans with type 2 but not type 1 diabetes. Diabetes 2007; 56: 2016-2027.
13. Laybutt DR, Preston AM, Akerfeldt MC, Kench JG, Busch AK, Biankin AV, Biden TJ. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007; 50: 752-763.
14. Song B, Scheuner D, Ron D, Pennathur S, Kaufman RJ. Chop deletion reduces oxidative stress, improves β cell function and promotes cell survival in multiple mouse models of diabetes. J Clin Invest 2008; 118: 3378-3389.
15. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein 5response. Nat Rev Mol Cell Biol 2007; 8: 519-529.
16. Lakshmanan AP, Harima M, Suzuki K, Soetikno V, Nagata M, Nakamura T, et al. The hyperglycemia stimulated myocardial endoplasmic reticulum (ER) stress contributes to diabetic cardiomyopathy in the transgenic non-obese type 2 diabetic rats: a differential role of unfolded protein response (UPR) signaling proteins. Int J Biochem Cell Biol 2013; 45: 438-447.
17. Rutkowski DT, Wu J, Back SH, Callaghan MU, Ferris SP, Iqbal J, et al. UPR pathways combine to prevent hepatic steatosis caused by ER stress-mediated suppression of transcriptional master regulators. Dev Cell 2008; 15: 829-840.
18. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi LJ, et al. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 2006; 16: 4273-4280.
19. Hotamisligil GS. Role of endoplasmic reticulum stress and c-Jun NH2-terminal kinase pathways in inflammation and origin of obesity and diabetes. Diabetes 2005; 54: S73-S78.
20. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403: 98-103.
21. Hatcher H, Planalp R, Cho J, Torti SV. Curcumin from ancient medicine to current clinical trials. Cell Mol Life Sci 2008; 65: 1631-1652.
22. Liu JY, Lin SJ, Lin JK. Inhibitory effects of curcumin on protein kinase C activity induced by 12-O-tetradecanoylphorbol-13-acetate in NIH 3T3 cells. Carcinogenesis 1993; 14: 857-861.
23. Mahmmoud YA. Curcumin modulation of Na,K-ATPase: phosphoenzyme accumulation, decreased K + occlusion, and inhibition of hydrolytic activity. Br J Pharmacol 2005; 145: 236-245.
24. Choi H, Chun YS, Kim SW, Kim MS, Park JW. Curcumin inhibits hypoxia-inducible factor-1 by degrading aryl hydrocarbon receptor nuclear translocator: a mechanism of tumor growth inhibition. Mol Pharmacol 2006; 70: 1664-1671.
25. Singh S, Aggarwal BB. Activation of transcription factor NFkappa B is suppressed by curcumin (diferuloylmethane). J Biol Chem 1995; 270: 24995-5000.
26. Mito S, Thandavarayan R, Ma M, Lakshman A, Suzuki K, Kodama M, Watanabe K. Inhibition of cardiac oxidative and endoplasmic reticulum stress-mediated apoptosis by curcumin treatment contributes to protection against acute myocarditis. Free Radic Res 2011; 45: 1223-1231.
27. Reyes-Gordillo K, Segovia J, Shibayama M, Vergara P, Moreno MG, Muriel P. Curcumin protects against acute liver damage in the rat by inhibiting NF-kappa B, proinflammatory cytokines production and oxidative stress. Biochim Biophys. Acta 2007; 1770: 989-996.
28. Watanabe K, Ohta Y, Nakazawa M, Higuchi H, Hasegawa G, Naito M, et al. Low dose carvedilol inhibits progression of heart failure in rats with dilated cardiomyopathy. Br J Pharmacol 2000; 130: 1489-1495.
29. Jain SK, Rains J, Croad J, Larson B, Jones K. Curcumin supplementation lowers TNF-alpha, IL-6, IL-8, and MCP-1 secretion in high glucose-treated cultured monocytes and blood levels of TNF-alpha, IL-6, MCP-1, glucose, and glycosylated hemoglobin in diabetic rats. Antioxid Redox Signal 2009; 11: 241-249.
30. Thallas-Bonke V, Thorpe SR, Coughlan MT, Fukami K, Yap FY, Sourris KC, et al. Inhibition of NADPH oxidase prevents advanced glycation end product-mediated damage in diabetic nephropathy through a protein kinase C-alpha dependent pathway. Diabetes 2008; 57: 460-469.
31. Guven A, Yavuz O, Cam M, Ercan F, Bukan N, Comunoglu C, Gokce F. Effects of melatonin on streptozocin - induced diabetic liver injury in rats. Acta Histochem 2006; 108: 85-93.
32. Soetikno V, Harima M, Suzuki K, Watanabe K. Amelioration of Liver Injury by Curcumin in Streptozotocin - Induced Diabetic Rats. International Conference on Medical and Pharmaceutical Sciences;2012 June 16-17; Bangkok.
33. Soetikno V, Sari FR, Veeraveedu PT, Thandavarayan RA, Harima M, Sukumaran V, et al. Curcumin ameliorates macrophage infiltration by inhibiting NF-κB activation and proinflammatory cytokines in streptozotocin induced-diabetic nephropathy. Nutr Metab 2011; 8: 35
34. Chanpoo M, Petchpiboonthai H, Panyarachun B, Anupunpisit V. Effect of curcumin in the amelioration of pancreatic islets in streptozotocin-induced diabetic mice. J Med Assoc Thai 2010; 93: S152-S159.
35. Meghana K, Sanjeev G, Ramesh B. Curcumin prevents streptozotocin-induced islet damage by scavenging free radicals: a prophylactic and protective role. Eu J Pharmacol 2007; 577: 183-191.
36. Chung HY, Sung B, Jung KJ, Zon Y, Yu BP. The molecular inflammatory process in aging. Antioxid Redox Signal 2006; 8: 572-581.
37. Navarro-Gonzalez JF, Mora-Fernadez C, De Fuentes MM, Garcia-Perz J. Inflammatory molecules and pathways in pathogenesis of diabetic nephropathy. Nat Rev Nephrol 2011; 7: 327-340.
38. Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and βcell loss in type 1 diabetes. Nat Rev Endocrinol 2009; 5: 219-226.
39. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005; 5: 953-964.
40. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol 2005; 23: 901-944.
41. Boden G, Duan X, Homko C, Molina EJ, Song W, Perez O, et al. Increase in endoplasmic reticulum stress related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 2008; 57: 2438-2444.
42. Gregor MF, Yang L, Fabbrini E, Mohammed BS, Eagon JC, Hotamisligil GS, Klein S. Endoplasmic reticulum stress is reduced in tissues of obese subjects after weight loss. Diabetes 2009; 58: 693-700.
43. Puri P, Mirshahi F, Cheung O, Natarajan R, Maher JW, Kellum JM, Sanyal AJ. Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 2008; 134: 568-576.
44. Sharma NK, Das SK, Mondal AK, Hackney OG, Chu WS, et al. Endoplasmic reticulum stress markers are associated with obesity in nondiabetic subjects. J Clin Endocrinol Metab 2008; 93: 4532-4541.
45. Gu F, Ngusen DT, Stible M, Dube N, Tremblay ML, Chevet E. Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic stress. J Biol Chem 2004; 279: 49689-49693.
46. Ji C, Kaplowitz N. ER stress: Can the liver cope? J Hepatol 2006; 45: 321-333.
47. Schr der M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74: 739-789.
48. Lee AH, Scapa EF, Cohen DE, Glimcher LH. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 2008; 320: 1492-1496.
49. Yamamoto K, Takahara K, Oyadomari S, Okada T, Sato T, Harada A, More k. Induction of liver steatosis and lipid droplet formation in ATF6alpha-knockout mice burdened with pharmacological endoplasmic reticulum stress. Mol Biol Cell 2010; 21: 2975-2986.
50. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 2004; 14: 20-28.
51. Zhang K, Kaufman RJ. From endoplasmic reticulum stress to the inflammatory response. Nature 2008; 454: 455-462.
52. Gotoh T, Mori M. Nitric oxide and endoplasmic reticulum stress. Arterioscler Thromb Vasc Biol 2006; 26: 1439-1446.
53. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004; 11: 381-389.
54. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families: activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000; 150: 887-894.
55. Morishima N, Nakanishi K, Takenouchi H, Shibata T, Yasuhiko Y. An endoplasmic reticulum stress-speci ficcaspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002; 277: 34287-34294.
56. Homma K, Katagiri K, Nishitoh H, Ichijo H. Targeting ASK1 in ER stress-related neurodegenerative diseases. Expert Opin Ther Targets 2009; 13: 653-664.
57. Hattori K, Naguro I, Runchel C, and Ichijo H. The roles of ASK family proteins in stress responses and diseases. Cell Commun Signal 2009; 7: 1-10.
58. Schroder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res 2005; 569: 29-63.
59. Harding HP, Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 2002; 51: S455-S461.
60. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 2000; 6: 1099-1108.
61. Hollien J, Weissman JS. Decay of endoplasmic reticulumlocalized mRNAs during the unfolded protein response. Science 2006; 313: 104-107.
62. Hollien J, Lin JH, Li H, Stevens N, Walter P, Weissman JS. Regulated Ire1 dependent decay of messenger RNAs in mammalian cells. J Cell Biol 2009; 186: 323-331.
63. Hetz C, Glimcher LH. Fine-tuning of the unfolded protein response: assembling the IRE1 α interactome. Mol Cell 2009; 35: 551-561.
64. Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kB activation and downregulation of TRAF2 expression. Mol Cell Biol 2006; 26: 3071-3084.
65. Nguyen DT, Kebache S, Fazel A, Wong HN, Jenna S, et al. Nck-dependent activation of extracellular signal-regulated kinase-1 and regulation of cell survival during endoplasmic reticulum stress. Mol Biol Cell 2004; 15: 4248-4260.
66. Li Y, Schwabe RF, DeVries-Seimon T, Yao PM, Gerbod-Giannone MC, Tall AR, et al. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-α and interleukin-6: model of NF-κ B-and map kinase-dependent in flammation in advanced atherosclerosis. J Biol Chem 2005; 280: 21763-21772.
67. Gargalovic PS, Gharavi NM, Clark MJ, Pagnon J, Yang WP, He A. The unfolded protein response is an important regulator of in flammatory genes in endothelial cells. Arterioscler Thromb Vasc Biol 2006; 26: 2490-2496.
68. Nanji AA, Jokelainen K, Tipoe GL, Rahemtulla A, Thomas P, Dannenberg AJ. Curcumin prevents alcohol-induced liver disease in rats by inhibiting the expression of NF-kappa Bdependent genes. Am J Physiol Gastrointest Liver Physiol 2003; 284: G321-G327.
69. Stienstra R, Saudale F, Duval C, Keshtkar S, Groener JE, van Rooijen N, et al. Kupffer Cells Promote Hepatic Steatosis Via Interleukin-1β -Dependent Suppression of Peroxisome Proliferator-Activated Receptor α Activity. Hepatology 2010; 51: 511-522.
70. Rouse M, Younes A, Egan JM. Resveratrol and curcumin enhance pancreatic β-cell function by inhibiting phosphordiesterase activity. J Endocrinol 2014; 223: 107-117.