Protective effects of tocotrienols against lipid-induced nephropathy in experimental type-2 diabetic rats by modulation in TGF-β expression

Toxicology and Applied Pharmacology

Volumn 273, Issue 2, 2013, Pages 314-324

  Siddiqui, Shabeena ^a   Ahsan, Haseeb ^b   Khan, Mohammad Rashid ^a,c   Siddiqui, Waseem A ^a  

^a HAMDARD UNIVERSITY   (India)

^b JAMIA MILLIA ISLAMIA CENTRAL UNIVERSITY   (India)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Diabetic nephropathy; Fibronectin; TGF ; Tocotrienol rich fraction; Tocotrienols

Indexed keywords

ALPHA TOCOTRIENOL; COLLAGEN TYPE 4; FIBRINOGEN; LIPID; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; HYPOLIPEMIA; KIDNEY DISEASE; LIPID BLOOD LEVEL; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; RAT; RENAL PROTECTION;

DIABETIC NEPHROPATHY; FIBRONECTIN; TGF-Β; TOCOTRIENOL RICH FRACTION; TOCOTRIENOLS;

ANIMALS; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; GENE EXPRESSION REGULATION; LIPIDS; MALE; PLANT EXTRACTS; PROTECTIVE AGENTS; RANDOM ALLOCATION; RATS; RATS, WISTAR; TOCOTRIENOLS; TRANSFORMING GROWTH FACTOR BETA;

RATTUS; RATTUS NORVEGICUS;

EID: 84888200905     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.09.004     Document Type: Article

References (84)

1. Ajuluchukwu J.N., Okubadejo N.U., Mabayoje M., Ojini F.I., Okwudiafor R.N., Mbakwem A.C., Fasanmade O.A., Oke D.A. Comparative study of the effect of tocotrienols and tocopherol on fasting serum lipid profiles in patients with mild hypercholesterolaemia: a preliminary report. Niger. Postgrad. Med. J. 2007, 14:30-33.
2. Arreola-Mendoza L., Reyes J.L., Melendez E., Martin D., Namorado M.C., Sanchez E., Del Razo L.M. Alpha-tocopherol protects against the renal damage caused by potassium dichromate. Toxicology 2006, 218:237-246.
3. Baliarsingh S., Beg Z.H., Ahmad J. The therapeutic impacts of tocotrienols in type 2 diabetic patients with hyperlipidemia. Atherosclerosis 2005, 182:367-374.
4. Border W.A., Noble N.A. Evidence that TGF-beta should be a therapeutic target in diabetic nephropathy. Kidney Int. 1998, 54:1390-1391.
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
6. Budin J.T., Breene W.M., Putnam D.H. Some compositional properties of camelina (Camelina sativa L. Crantz) seeds and oils. J. Am. Oil Chem. Soc. 1995, 72:309-315.
7. Budin S.B., Othman F., Louis S.R., Bakar M.A., Das S., Mohamed J. The effects of palm oil tocotrienol-rich fraction supplementation on biochemical parameters, oxidative stress and the vascular wall of streptozotocin-induced diabetic rats. Clinics (Sao Paulo) 2009, 64:235-244.
8. Cai H., Harrison D.G. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ. Res. 2000, 87:840-844.
9. Carlberg I., Mannerviek B. Glutathione reductase levels in rat brain. J. Biol. Chem. 1975, 250:5475-5480.
10. Chou T.W., Ma C.Y., Cheng H.H., Chen Y.Y., Lai M.H. A rice bran oil diet improves lipid abnormalities and suppress hyperinsulinemic responses in rats with streptozotocin/nicotinamide-induced type-2 diabetes. J. Clin. Biochem. Nutr. 2009, 45:29-36.
11. Claiborne A. Catalase activity. CRC Handbook of Methods for Oxygen Radical Research 1985, 283-284. CRC Press, Boca Raton, FL. R.A. Green Wald (Ed.).
12. Corsini A., Mazzotti M., Raiteri M., Soma M.R., Gabbiani G., Fumagalli R., Paoletti R. Relationship between mevalonate pathway and arterial myocyte proliferation: in vitro studies with inhibitors of HMG-CoA reductase. Atherosclerosis 1993, 101:117-125.
13. Creely J.J., DiMari S.J., Howe A.M., Haralson M.A. Effects of transforming growth factor-beta on collagen synthesis by normal rat kidney epithelial cells. Am. J. Pathol. 1992, 140:45-55.
14. Danda R.S., Habiba N.M., Rincon-Choles H., Bhandari B.K., Barnes J.L., Abboud H.E., Pergola P.E. Kidney involvement in a nongenetic rat model of type-2 diabetes. Kidney Int. 2005, 68:2562-2571.
15. Dominguez J.H., Tang N., Xu W., Evan A.P., Siakotos A.N., Agarwal R., Walsh J., Deeg M., Pratt J.H., March K.L., Monnier V.M., Weiss M.F., Baynes J.W., Peterson R. Studies of renal injury III: lipid-induced nephropathy in type II diabetes. Kidney Int. 2000, 57:92-104.
16. Falk R.J., Scheinman J.I., Mauer S.M., Michael A.F. Polyantigenic expansion of basement membrane constituents in diabetic nephropathy. Diabetes 1983, 32:34-39.
17. Fang F., Kang Z., Wong C. Vitamin E tocotrienols improve insulin sensitivity through activating peroxisome proliferator-activated receptors. Mol. Nutr. Food Res. 2010, 54:345-352.
18. Friedewald W.T., Levy R.I., Fred Rickson D.S. Estimation of the concentration of low-density Lipoprotein in cholesterol in plasma without use of the preparative ultracentrifuge. Clin. Chem. 1972, 18:499-500.
19. Gall M.A., Hougaard P., Borch-Johnsen P., Parving H.H. Risk factors for development of incipient and overt diabetic nephropathy in patients with noninsulin dependent diabetes mellitus: prospective, observational study. BMJ 1997, 314:783-788.
20. Gilbert R.E., Wilkinson-Berka J.L., Johnson D.W., Cox A., Soulis T., Wu L.L., Kelly D.J., Jerums G., Pollock C.A., Cooper M.E. Renal expression of transforming growth factor-beta inducible gene-h3 (beta ig-h3) in normal and diabetic rats. Kidney Int. 1998, 54:1052-1062.
21. Goldfarb S., Ziyadeh F.N. TGF-β: a crucial component of the pathogenesis of diabetic nephropathy. Trans. Am. Clin. Climatol. Assoc. 2001, 112:27-33.
22. Goldstein J.L., Brown M.S. Regulation of the mevalonate pathway. Nature 1990, 343(6257):425-430.
23. Grone H.J., Walli A., Grone E., Niedmann P., Thiery J., Seidel D., Helmchen U. Induction of glomerulosclerosis by dietary lipids. A functional and morphologic study in the rat. Lab. Invest. 1989, 60:433-446.
24. Ha H., Kim K.H. Role of protein kinase C-mediated oxidative stress in increased TGF-β1 and fibronectin mRNAs in mesangial cells: implications for diabetic nephropathy. Nephrology 1997, 3(Suppl. 1):A736.
25. Ha H., Lee H.B. Reactive oxygen species as glucose signaling molecules in mesangial cells cultured under high glucose. Kidney Int. Suppl. 2000, 77:S19-S25.
26. Hattori M., Ito K., Kawaguchi H., Yamaguchi Y. Probucol reduces renal injury in the ExHC rat. Nephron 1994, 67:459-468.
27. Hill C., Flyvbjerg A., Gronbaek H., Petrik J., Hill D.J., Thomas C.R., Sheppard M.C., Logan A. The renal expression of transforming growth factor-beta isoforms and their receptors in acute and chronic experimental diabetes in rats. Endocrinology 2000, 141:1196-1208.
28. Ishii N., Ogawa Z., Suzuki K., Numakami K., Saruta T., Itoh H. Glucose loading induces DNA fragmentation in rat proximal tubular cells. Metabolism 1996, 45:1348-1353.
29. Jenkins A.J., Lyons T.J., Zheng D., Otvos J.D., Lackland D.T., McGee D., Garvey W.T., Klein R.L., the DCCT/EDIC Research Group Lipoproteins in the DCCT/EDIC cohort: association with diabetic nephropathy. Kidney Int. 2003, 64:817-828.
30. Jiang Z., Seo J.Y., Ha H., Yu M.R., Kwon M.K., Lee H.B. Reactive oxygen species mediated TGF-β1-induced plasminogen activator inhibitor-1 upregulation in mesangial cells. Biochem. Biophys. Res. Commun. 2003, 309:961-966.
31. Kamal-Eldin A., Appelqvist L.A. The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 1996, 31:671-701.
32. Kanaya Y., Doi T., Sasaki H., Fujita A., Matsuno S., Okamoto K., Nakano Y., Tsujiwaki S., Furuta H., Nishi M., Tsuno T., Taniguchi H., Nanjo K. Rice bran extract prevents the elevation of plasma peroxylipid in KKAy diabetic mice. Diabetes Res. Clin. Pract. 2004, 66(Suppl. 1):S157-S160.
33. Kaplan R., Aynedjian H.S., Schlondorff D., Bank N. Renal vasoconstriction caused by short-term cholesterol feeding is corrected by thromboxane antagonist or probucol. J. Clin. Invest. 1990, 86:1707-1714.
34. Keane W.F., Kasiske L.B., O'Donnell M.P., Kim Y. The role of altered lipid metabolism in the progression of renal disease: experimental evidence. Am. J. Kidney Dis. 1991, 17(5 Suppl. 1):38-42.
35. Kim Y., Kleppel M.M., Butkowski R., Mauer S.M., Wieslander J., Michael A.F. Differential expression of basement membrane collagen chains in diabetic nephropathy. Am. J. Pathol. 1991, 138:413-420.
36. Kiyomoto H., Abboud S.L., Abboud H.E. Expression of transforming growth factor-beta and type IV collagen in early streptozotocin-induced diabetes. Diabetes 1997, 46:473-480.
37. Kraegen E.W., Cooney G.J., Ye J., Thompson A.L. Triglycerides, fatty acids and insulin resistance - hyperinsulinemia. Exp. Clin. Endocrinol. Diabetes 2001, 109:S516-S526.
38. Kuhad A., Chopra K. Attenuation of diabetic nephropathy by tocotrienol: involvement of NFkB signaling pathway. Life Sci. 2009, 84:296-301.
39. Lam K.S., Cheng I.K., Janus E.D., Pang R.W. Cholesterol-lowering therapy may retard the progression of diabetic nephropathy. Diabetologia 1995, 38:604-609.
40. Le Marchand-Brustel Y., Gual P., Gremeaux T., Gonzalez T., Barres R., Tanti J.F. Fatty acid-induced insulin resistance: role of insulin receptor substrate 1 serine phosphorylation in the retroregulation of insulin signaling. Biochem. Soc. Trans. 2003, 31:1152-1156.
41. Maack T.M. Renal handling of low molecular weight proteins. Am. J. Med. 1975, 58:57-64.
42. Margherita R., Cristina A., Simona R. Tocopherols and tocotrienols as free radical scavengers in refined vegetable oils and their stability during deep-fat frying. Food Chem. 2007, 102:812-817.
43. Marklund S., Marklund G. Involvement of the superoxide anion radical in the auto oxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47:469-474.
44. Mason R.M., Wahab N.A. Extracellular matrix metabolism in diabetic nephropathy. J. Am. Soc. Nephrol. 2003, 14:1358-1373.
45. Mohandas J., Marshall J.J., Duggin G.G., Horvath J.S., Tiller D.J. Low activities of glutathione-related enzymes as factors in the genesis of urinary bladder cancer. Cancer Res. 1984, 44:5086-5091.
46. Mulec H., Blohme G., Grande B., Bjorck S. Progression of overt diabetic nephropathy (DN) - role metabolic control. J. Am. Soc. Nephrol. 1995, 6(3):453-453.
47. Mulec H., Blohmé G., Grände B., Bjorck S. The effect of metabolic control on rate of decline in renal function in insulin-dependent diabetes mellitus with overt diabetic nephropathy. Nephrol. Dial. Transplant. 1998, 13:651-655.
48. Nakamura T., Fukui M., Ebihara I., Osada S., Nagaoka I., Tomino Y., Koide H. mRNA expression of growth factors in glomeruli of diabetic rats. Diabetes 1993, 42:450-456.
49. Ng M.H., Choo Y.M., Ma A.N., Chuah C.H., Hashim M.A. Separation of vitamin E (tocopherol, tocotrienol, and tocomonoenol) in palm oil. Lipids 2004, 39:1031-1035.
50. Nishida Y., Yorioka N., Oda H., Yamakido M. Effect of lipoproteins on cultured human mesangial cells. Am. J. Kidney Dis. 1997, 29:919-930.
51. O'Donnell M.P., Kasiske B.L., Kim Y., Atluru D., Keane W.F. Lovastatin inhibits proliferation of rat mesangial cells. J. Clin. Invest. 1993, 91(1):83-87.
52. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
53. Onody A., Csonka C., Giricz Z., Ferdinandy P. Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts. Cardiovasc. Res. 2003, 58:663-670.
54. Ortiz A., Ziyadeh F.N., Neilson E.G. Expression of apoptosis-regulatory genes in renal proximal tubular epithelial cells exposed to high ambient glucose and in diabetic kidneys. J. Investig. Med. 1997, 45:50-56.
55. Pacher P., Schulz R., Liaudet L., Szabo C. Nitrosative stress and pharmacological modulation of heart failure. Trends Pharmacol. Sci. 2005, 26:302-310.
56. Park I., Kiyomoto H., Abboud S., Abboud H. Expression of transforming growth factor-beta and type IV collagen in early streptozotocin-induced diabetes. Diabetes 1997, 46:473-480.
57. Parker R., Pearce B., Clark R., Gordon D., Wright J. Tocotrienols regulates cholesterol production in mammalian cells by post-transcriptional suppression of 3-hydroxy-3-methylglutaryl-coenzyme A reductase. J. Biol. Chem. 1993, 268:11230-11238.
58. Pennell J.P., Meinking T.L. Pattern of urinary proteins in experimental diabetes. Kidney Int. 1982, 21:709-713.
59. Qureshi A.A., Bradlow B.A., Salser W.A., Brace L.D. Novel tocotrienols of rice bran modulate cardiovascular disease risk parameters of hypercholesterolemic humans. J. Nutr. Biochem. 1997, 8:290-298.
60. Qureshi A.A., Sami S.A., Khan F.A. Effects of stabilized rice bran, its soluble and fiber fractions on blood glucose levels and serum lipid parameters in humans with diabetes mellitus Types I and II. J. Nutr. Biochem. 2002, 13:175-187.
61. Ravid M., Brosh D., Ravid-Safran D., Levy Z., Rachmani R. Main risk factors for nephropathy in type-2 diabetes mellitus are plasma cholesterol levels, mean blood pressure, and hyperglycemia. Arch. Intern. Med. 1998, 158:998-1004.
62. Ritz E., Rychlik I., Locatelli F., Halimi S. End-stage renal failure in type-2 diabetes: a medical catastrophe of worldwide dimensions. Am. J. Kidney Dis. 1999, 34:795-808.
63. Schlondorff D. Cellular mechanism of lipid injury in the glomerulus. Am. J. Kidney Dis. 1993, 22:72-82.
64. Serbinonva E.A., Packer L. Antioxidant properties of tocopherol and tocotrienol. Methods Enzymol. 1994, 234:354-367.
65. Serbinova E., Kagan V., Han D., Packer L. Free radical recycling and intramembrane mobility in the antioxidant properties of alpha-tocopherol and alpha tocotrienol. Free Radic. Biol. Med. 1991, 10:263-275.
66. Sharma S., Anjaneyulu M., Kulkarni S.K., Chopra K. Resveratrol, a polyphenolic phytoalexin, attenuates diabetic nephropathy in rats. Pharmacology 2006, 76:69-75.
67. Sharma S., Kulkarni S.K., Chopra K. Curcumin, the active principle of turmeric (Curcuma longa), ameliorates diabetic nephropathy in rats. Clin. Exp. Pharmacol. Physiol. 2006, 33:940-945.
68. Shoji T., Emoto M., Kawagishi T., Kimoto E., Yamada A., Tabata T., Ishimura E., Inaba M., Okuno M., Nishizawa Y. Atherogenic lipoprotein changes in diabetic nephropathy. Atherosclerosis 2001, 156:425-433.
69. Shulman G.I. Cellular mechanisms of insulin resistance. J. Clin. Invest. 2000, 106(2):171-176.
70. Siddiqui S., Khan M.R., Siddiqui W.A. Comparative hypoglycemic and nephroprotective effects of tocotrienol rich fraction (TRF) from palm oil and rice bran oil against hyperglycemia induced nephropathy in type 1 diabetic rats. Chem. Biol. Interact. 2010, 188:651-658.
71. Spencer M.W., Muhlfeld A.S., Segerer S., Hudkins K.L., Kirk E., LeBoeuf R.C., Alpers C.E. Hyperglycemia and hyperlipidemia act synergistically to induce renal disease in LDL receptor-deficient BALB mice. Am. J. Nephrol. 2004, 24:20-31.
72. Steffes M.W., Bilous R.W., Sutherland D.E., Mauer S.M. Cell and matrix components of the glomerular mesangium in type I diabetes. Diabetes 1992, 41:679-684.
73. Steinbrecher U.P. Role of superoxide in endothelial-cell modification of low-density lipoproteins. Biochim. Biophys. Acta 1988, 959:20-30.
74. Suzuki Y.J., Tsuchiya M., Wassall S.R., Choo Y.M., Govil G., Kagan V.E., Packer L. Structural and dynamic membrane properties of alpha-tocopherol and alphatocotrienol: implication to the molecular mechanism of their antioxidant potency. Biochemistry 1993, 32:10692-10699.
75. Theriault A., Chao J.T., Wang Q., Gapor A., Adeli K. Tocotrienol: a review of its therapeutic potential. Clin. Biochem. 1999, 32:309-319.
76. Traber M.G. Vitamin E regulatory mechanisms. Annu. Rev. Nutr. 2007, 27:347-362.
77. Trachtman H. Vitamin E prevents glucose-induced lipid peroxidation and increased collagen production in cultured rat mesangial cells. Microvasc. Res. 1994, 47(2):232-239.
78. Wan Nazaimoon W.M., Khalid B.A. Tocotrienols-rich diet decreases advanced glycosylation end-products in non-diabetic rats and improves glycemic control in streptozotocin-induced diabetic rats. Malays. J. Pathol. 2002, 24:77-82.
79. Weiss S.J., King G.W., LoBuglio A.F. Superoxide generation by human monocytes and macrophages. Am. J. Hematol. 1978, 4:1-8.
80. Wolf G., Ritz E. Diabetic nephropathy in type-2 diabetes prevention and patient management. J. Am. Soc. Nephrol. 2003, 14:1396-1405.
81. Yamamoto T., Noble N.A., Cohen A.H., Nast C.C., Hishida A., Gold L.I., Border W.A. Expression of transforming growth factor-beta isoforms in human glomerular diseases. Kidney Int. 1996, 49:461-469.
82. Zhang X.L., Selbi W., de la Motte C., Hascall V., Phillips A. Renal proximal tubular epithelial cell transforming growth factor-β1 generation and monocyte binding. Am. J. Pathol. 2004, 165(3):763-773.
83. Ziyadeh F.N. Mediators of diabetic renal disease: the case for TGF-β as the major mediator. J. Am. Soc. Nephrol. 2004, 15:S55-S57.
84. Ziyadeh F., Han D.C. Involvement of transforming growth factor-b and its receptors in the pathogenesis of diabetic nephropathy. Kidney Int. 1997, 52(Suppl. 60):S7-S11.