A light microscopic investigation of the renoprotective effects of α-lipoic acid and α-tocopherol in an experimental diabetic rat model

References

• Agardh CD, Stenram U, Torffvit O, Agardh E. 2002. Effects of inhibition of glycation and oxidative stress on the development of diabetic nephropathy in rats. J Diabetes Compl. 16:395–400.
   PubMed Web of Science ®Google Scholar
• Ahmed N. 2005. Advanced glycation end products role in pathology of diabetic complications. Diabetes Res Clin Pract. 67:3–21.
   PubMed Web of Science ®Google Scholar
• Allen DA, Harwood SM, Varagunam M, Raftery MJ, Yaqoob MM. 2003. High glucose-induced oxidative stress causes apoptosis in proximal tubular epithelial cells and is mediated by multiple caspases. FASEB J. 17:908–910.
   PubMed Web of Science ®Google Scholar
• Altan N, Dinçel AS, Koca C. 2006. Diabetes mellitus and oxidative stress. Turk J Biochem. 31:51–56.
   Google Scholar
• Bamri-Ezzine S, Ao ZJ, Londono I, Gingras D, Bendayan M. 2003. Apoptosis of tubular epithelial cells in glycogen nephrosis during diabetes. Lab Invest. 83:1069–1080.
   PubMed Web of Science ®Google Scholar
• Biewenga GP, Haenen GR, Bast A. 1997. The pharmacology of the antioxidant lipoic acid. Gen Pharmacol. 29:315–331.
   PubMedGoogle Scholar
• Brezniceanu ML, Liu F, Wei CC, Chénier I, Godin N, Zhang SL, Filep JG, Ingelfinger JR, Craven PA, DeRubertis FR, Kagan VE, Melhem M, Studer RK. 1997. Effects of supplementation with vitamin C or E on albuminuria, glomerular TGF-beta, and glomerular size in diabetes. J Am Soc Nephrol. 8:1405–1414.
   PubMed Web of Science ®Google Scholar
• Bruno S, Bussolati B, Grange C, Collino F, di Cantogno LV, Herrera MB, Biancone L, Tetta C, Segoloni G, Camussi G. 2009. Isolation and characterization of resident mesenchymal stem cells in human glomeruli. Stem Cells Dev. 18:867–880.
   PubMed Web of Science ®Google Scholar
• Büyükdevrim AS. 1989. Diabetes mellitus I. İstanbul Üniversitesi Basımevi ve Film Merkezi. 187–209.
   Google Scholar
• Cam M, Yavuz O, Guven A, Ercan F, Bukan N, Ustundag N. 2003. Protective effects of chronic melatonin treatment against renal injury in streptozotocin-induced diabetic rats. J Pineal Res. 35:212–220.
   PubMed Web of Science ®Google Scholar
• Cardiff RD, Miller CH, Munn RJ. 2014. Manual hematoxylin and eosin staining of mouse tissue sections. Cold Spring Harb Protoc. 6:655–658.
   Google Scholar
• Carney SL, Wong NLM, Dirks JH. 1979. Acute effects of streptozotocin diabetes on rat renal fonction. J Lab Clin Med. 93:950–960.
   PubMed Web of Science ®Google Scholar
• Chapple ILC. 2006. Oxidative stress, nutrition and neutrogenomics in periodontal health and disease. Int J Dent Hyg. 4:15–21.
   PubMedGoogle Scholar
• Chen HC, Guh JH, Shin SJ, Tsai JH. 2000. Reactive oxygen species enhances endothelin-1 production of diabetic rat glomeruli in vitro and in vivo. J Lab Clin Med. 309–315.
   PubMed Web of Science ®Google Scholar
• Cortes P, Dumler F, Goldman J, Levin NW. 1987. Relationship between renal function and metabolic alterations in early streptozotocin-ınduced diabetes in rats. Diabetes. 36:80–87.
   PubMed Web of Science ®Google Scholar
• Crawford JM, Cotran RS. 1999. The pancreas. In: Cotran RS, Kumar V, Collins T, Eds. Pathologic Basis of Disease. Philadelphia (PA): WB Saunders Co.; pp. 913-920.
   Google Scholar
• Das J, Vasan V, Sil PC. 2012. Taurine exerts hypoglycemic effect in alloxan-induced diabetic rats, improves insulin-mediated glucose transport signaling pathway in heart and ameliorates cardiac oxidative stress and apoptosis. Toxicol Appl Pharmacol. 258:296–308.
   PubMed Web of Science ®Google Scholar
• Devaraj S, Jialal I. 2000a. Low-density lipoprotein postsecretory modification, monocyte function, and circulating adhesion molecules in type 2 diabetic patients with and without macrovascular complications. The effect of α-tocopherol supplementation. Circulation. 102:191–196.
   Google Scholar
• Devaraj S, Jialal I. 2000b. Alpha tocopherol supplementatıon decreases serum c-reactive proteın and monocyte interleukin-6 levels in normal volunteers and type 2 diabetic patients. Free Rad Biol Med. 29:790–792.
   PubMed Web of Science ®Google Scholar
• Donath M. 2014. Targeting inflammation in the treatment of type 2 diabetes time to start. Nat Rev Drug Discov. 13:465–476.
   PubMed Web of Science ®Google Scholar
• Eguíluz Lumbreras P, Hernández AP, Gómez Zancajo VR, Zorzo OH, Garcia G, Arriba FC, Avisrror U. 2010. Nephrectomy in polycystic kidney disease before transplantation. Arch Esp Urol. 63:403–409.
   PubMedGoogle Scholar
• Forbes JM, Thallas V, Thomas MC, Founds HW, Burns WC, Jerums G, Cooper ME. 2003. The breakdown of preexisting advanced glycation end products is associated with reduced renal fibrosis in experimental diabetes. FASEB J. 17:1762–1764.
   PubMed Web of Science ®Google Scholar
• Fuchs J, Schofer H, Milbradt R, Freisleben HJ, Buhl R, Siems W, Grune T. 1993. Studies on lipoate effects on blood redox state in human immunodeficiency virus infected patients. Arz Forsch. 43:1359–1362.
   Google Scholar
• Fujihara CK, Padilha RM, Zatz R. 1992. Glomerular abnormalities in long-term experimental diabetes. Diabetes. 41:286–293.
   PubMed Web of Science ®Google Scholar
• Gaber L, Walton C, Brown S, Bakris G. 1994. Effects of different antihypertensive treatments on morphological progression of diabetic nephropathy in uninephrectomized dogs. Kidney Int. 46:161–169.
   PubMed Web of Science ®Google Scholar
• Gotoda T, Arita M, Arai H, Inoue K, Yokota T, Fukuo Y, Yazaki Y, Yamada N. 1995. Adult-onset spinocerebellar dysfunction caused by a mutation in the gene for the alpha tocopherol-transfer protein. N Engl J Med. 333:1313–1318.
   PubMed Web of Science ®Google Scholar
• Graham LT, Bin Yang BE, Wagner JS, Meguid El Nahas A. 1998. Cellular apoptosis and proliferation in experimental renal fibrosis. Nephrol Dial Transplant. 13:2216–2226.
   PubMed Web of Science ®Google Scholar
• Gu X, Song X, Dong Y, Cai H, Walters E, Zhang R, Pang X, Xie T, Guo Y, Sridhar R, Califano JA. 2008. Vitamin E succinate induces ceramide-mediated apoptosis in head and neck squamous cell carcinoma ın vitro and ın vivo. Clin Cancer Res. 14:1840–1848.
   PubMed Web of Science ®Google Scholar
• Ha H, Lee HB. 2000. Reactive oxygen species as glucose signaling molecules in mesangial cells cultured under high glucose. Kidney Int. 58:19–25.
   Web of Science ®Google Scholar
• Haliga RE, Butcovan D, Oboroceanu T, Pınzariu AC, Costan VV, Craucıuc DV, Sındılar A, Lupusoru RV, Mocanu V. 2017. Flaxseed and vitamin E exert synergic antioxidant action on diabetic nephropathy in experimental diabetes. Rev Chim. 68:1451.
   Web of Science ®Google Scholar
• Halliwell B. 2002. Vitamin E and the treatment and prevention of diabetes: a case for a controlled clinical trial. Singapore Med J. 43:479–484.
   PubMedGoogle Scholar
• Haluzik M, Nedvidkova J, Skrha J. 1998. The influence of NO synthase inhibitor and free oxygen radicals scavenger, methylene blue on streptozotocin-induced diabetes in rats. Physiol Res. 47:337–341.
   PubMed Web of Science ®Google Scholar
• Henriksen EJ, Jacob S, Streeper RS, Fogt DL, Hokama JY, Tritschler HJ. 1997. Stimulation by -lipoic acid of glucose transport activity in skeletal muscle of lean and obese Zucker rats. Life Sci. 61:805–812.
   PubMed Web of Science ®Google Scholar
• Herr RR, Eble TE, Bergy ME, Jahnke HK. 1960. Isolation and characterization of streptozotocin. Antibiot Ann. 7:236–240.
   Google Scholar
• Hirose K, Qsterby R, Nozawa M, Jorgen H, Gundersen G. 1982. Development of glomerular lesions in experimental long-term diabetes in the rat. Kidney Int. 21:689–695.
   PubMed Web of Science ®Google Scholar
• Hishikawa K, Takase O, Yoshikawa M, Tsujimura T, Nangaku M, Takato T. 2015. Adult stem-like cells in kidney. World J Stem Cells. 7:490–494.
   PubMedGoogle Scholar
• Hsu R.M, Devaraj S, Jialal I. 2002. Autoantibodies to oxidized low-density lipoprotein in patients with type 2 diabetes mellitus. Clin Chim Acta. 317:145–150
   PubMed Web of Science ®Google Scholar
• Imaeda A, Kaneko T, Aoki T, Kondo Y, Nagase H. 2002. DNA damage and the effect of antioxidants in streptozotocin-treated mice. Food Chem Toxicol. 7:979–987.
   Google Scholar
• Ishii N, Patel KP, Lane PH, Taylor T, Bian K, Murad F, Pollock JS, Carmines PK. 2001. Nitric oxide synthesis and oxidative stress in the renal cortex of rats with diabetes mellitus. J Am Soc Nephrol. 12:1630–1639.
   PubMed Web of Science ®Google Scholar
• Kang DH, Joly AH, Oh SE, Hugo C, Kerjaschki D, Gordon KL, Mazzali M, Jefferson JA, Hughes J, Madsen KM, Schreiner GF, Johnson RJ. 2001. Impaired angiogenesis in the remnant kidney model: I. potential role of vascular endothelial growth factor and thrombospondin-1. J Am Soc Nephrol. 12:1434–1447.
   Google Scholar
• Kim BM, Han YM, Shin YJ, Min BH, Park IS. 2001. Clusterin expression during regeneration of pancreatic islet cells in streptozotocin-induced diabetic rats. Diabetology. 44:2192–2202.
   PubMed Web of Science ®Google Scholar
• Kim K, Park BH, Ihm H, Kim KM, Jeong J, Chang JW, Cho YM. 2011. Expression of stem cell marker CD133 in fetal and adult human kidneys and pauci-immune crescentic glomerulonephritis. Histol Histopathol. 26:223–232.
   PubMed Web of Science ®Google Scholar
• Kitamura S, Yamasaki Y, Kinomura M, Sugaya T, Sugiyama H, Maeshima Y, Makino H. 2005. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J. 19:1789–1796.
   PubMed Web of Science ®Google Scholar
• Koo JR, Ni Z, Oviesi F, Vaziri ND. 2002. Antioxidant therapy potentiates antihypertensive action of insulin in diabetic rats. Clin Exp Hypertens. 24:333–344.
   PubMed Web of Science ®Google Scholar
• Kutlubay R, Oğuz EO, Güven C, Can B, Sinik Z, Tuncay ÖL. 2007. Histological and ultrastructural evidence for protective effects on aluminium-ınduced kidney damage by ıntraperitoneal administration of α-tocopherol. Int J Toxicol. 26:95–101.
   PubMed Web of Science ®Google Scholar
• Lenzen S. 2008. The mechanisms of alloxan- and streptozotocin-induced diabetes. Diabetology. 51:216–226.
   PubMed Web of Science ®Google Scholar
• Liptakova A, Carsky J, Ulicna O, Vancova O, Bazek P, Durackova Z. 2002. Influence of β-resorcylidene aminogua- nidine on selected metabolic parameters and antioxidant status of rats with diabetes mellitus. Physiol Res. 51:277–284.
   PubMed Web of Science ®Google Scholar
• Maritim AC, Sanders RA, Watkins JB. 2003. Effects of alpha-lipoic acid on biomarkers of oxidative stress in streptozotocin-induced diabetic rats. J Nutr Biochem. 14:288–294.
   PubMed Web of Science ®Google Scholar
• Melhem MF, Craven PA, Liachenko J, Derubertis FR. 2002. α-Lipoic acid attenuates hyperglycemia and prevents glomerular mesangial matrix expansion in diabetes. J Am Soc Nephrol. 13:108–116.
   PubMed Web of Science ®Google Scholar
• Melin J, Hellberg O, Akyürek LM, Kallskog Ö, Larsson E, Fellström BC. 1997. Ischemia causes rapidly progressive nephropathy in the diabetic rat. Kidney Int. 52:985–991.
   PubMed Web of Science ®Google Scholar
• Memişoğulları R. 2005. The role of free radicals and the effect of antioxidants in diabetes. Duzce Med J. 3:30–39.
   Google Scholar
• Meruva AD, Sahukari R, Ganjikunta VS, Bhasha S, Kesireddy SR. 2016. Therapeutic insights of hydromethanolic leaf extract of xanthium indicum and α-tocopherol in streptozotocin induced diabetic renal oxidative stress. S Asian J Exp Biol. 6:158–166.
   Google Scholar
• Montonen J, Knekt P, Jarvinen R, Reunanen A. 2004. Antioxidant intake and risk of type 2 diabetes. Diabetes Care. 27:1836–1852.
   Web of Science ®Google Scholar
• Neumann A, Schinzel R, Palm D, Riederer P, Munch G. 1999. High molecular weight hyaluronic acid acid inhibits advanced glycation end product induced NF-kB activation and cytokine expression. FEBS Lett. 453:283–287.
   PubMed Web of Science ®Google Scholar
• Ohkuwa T, Sato Y, Naoi M. 1995. Hydroxyl radical formation in diabetic rats induced by streptozotocin. Life Sci. 56:1789–1798.
   PubMed Web of Science ®Google Scholar
• Ortiz A. 2000. Apoptotic regulatory proteins in renal injury. Kidney Int. 58:467–485.
   PubMed Web of Science ®Google Scholar
• Özkan Y, Yılmaz Ö, Öztürk A, Ercan Y. 2005. Effects of triple antioxidant combination (vitamin E, vitamin C and a-lipoic acid) with insulin on lipid and cholesterol levels and fatty acid composition of brain tissue in experimental diabetic and non-diabetic rats. Cell Biol Internat. 29:754–760.
   PubMed Web of Science ®Google Scholar
• Packer L. 1998. Alpha-lipoic acid: a metabolic antioxidant which regulates NF-kappa B signal transduction and protects against oxidative injury. Drug Metab Rev. 30:245–275.
   PubMed Web of Science ®Google Scholar
• Packer L, Tritschler HJ, Wessel K. 1997. Neuroprotection by the metabolic antioxidant lipoic acid. Free Rad Biol Med. 22:359–378.
   PubMed Web of Science ®Google Scholar
• Packer L, Witt EH, Tritschler HJ. 1995. Lipoic acid as a biological antioxidant. Free Rad Biol Med. 19:227–250.
   PubMed Web of Science ®Google Scholar
• Pazdro R, Burgess J.R. 2010. The role of vitamin E and oxidative stress in diabetes complications. Mech Ageing Dev. 4:276–286.
   Google Scholar
• Podda M, Grundmann-kollmann M. 2001. Low molecular weight antioxidants and their role in skin ageing. Clin Exp Dermatol. 26:578–582.
   PubMed Web of Science ®Google Scholar
• Pourova J, Kottova M, Voprsalova M, Pour M. 2010. Reactive oxygen and nitrogen species in normal physiological processes. Acta Physiol. 198:15–35.
   PubMed Web of Science ®Google Scholar
• Privratsky JR, Wold LE, Sowers JR, Quinn MT, Ren J. 2003. AT1 blockade prevents glucose-induced cardiac dysfunction in ventricular myocytes: role of the AT1 receptor and NADPH oxidase. Hypertension. 42:206–212.
   PubMed Web of Science ®Google Scholar
• Rajbala A, Sane AS, Zope J, Mishra VV, Trivedi HL. 1997. Oxidative stress status in children with nephrotic syndrome. Panminerva Med. 39:165–168.
   PubMed Web of Science ®Google Scholar
• Reed LJ, Gunsalus IC, Schnakenberg GHF, Soper QF, Boaz HE, Kern SF, Parke TV. 1953. Isolation, characterization and structure of α-lipoic acid. J Am Chem Soc. 75:1267–1277.
   Web of Science ®Google Scholar
• Richard MJ, Arnaud J, Jurkovitz C, Hachache R, Meftahi H, Laporte F, Foret M, Favier A, Cordonnier D. 1991. Trace elements and lipid peroxidation abnormalities in patients with chronic renal failure. Nephron. 57:10–15.
   PubMed Web of Science ®Google Scholar
• Rodrigo R, Guichard C, Charles R. 2007. Clinical pharmacology and therapeutic use of antioxidant vitamins. Fund Clin Pharmacol. 21:111–127.
   PubMed Web of Science ®Google Scholar
• Romero FJ, Ordonez I, Arduini A, Cadenas E. 1992. The reactivity of thiols and disulfides with different redox states of myoglobin. Redox and addition reactions and formation of thiyl radical intermediates. J Biol Chem. 267:1680–1688.
   Google Scholar
• Saborio P, Krieg RJ, Kuemmerle NB, Norkus EP, Schwartz CC, Chan JCM. 2000. α-Tocopherol modulates lipoprotein cytotoxicity in obstructive nephropathy. Pediatr Nephrol. 14: 740–746.
   PubMed Web of Science ®Google Scholar
• Saldeen K, Saldeen T. 2005. Importance of tocopherols beyond a-tocopherol: evidence from animal and human studies. Nutr Res. 25:877–889.
   Web of Science ®Google Scholar
• Sanai T, Sobka T, Johnson T, Essawy M, Muchaneta-Kubara EC, Ben Gharbia O, Oldroyd S, Nahas AM. 2000. Expression of cytoskeletal proteins during the course of experimental diabetic nephropathy. Diabetologia. 43:91–100.
   PubMed Web of Science ®Google Scholar
• Sargın AK. 2009. The assessment of structural features of renal mesangial cells under natural and experimental conditions. Department of Histology-Embryology Ankara University Faculty of Medicine. Ankara. (Thesis)
   Google Scholar
• Satman I. 2011. TURDEP-II sonuçları. Türk Endokronol Metab Derneği http://www.turkendokrin.org/fi les/fi le/TURDEP_II_.
   Google Scholar
• Shin H, Eo H, Lim Y. 2016. Similarities and differences between alpha-tocopherol and gamma-tocopherol in amelioration of inflammation, oxidative stress and pre-fibrosis in hyperglycemia induced acute kidney inflammation. Nutr Res Pract. 10:33–41.
   PubMed Web of Science ®Google Scholar
• Suzuki YJ, Tsuchiya M, Packer L. 1992. Lipoate prevents glucose-induced protein modifications. Free Rad Res Com. 17:211–217.
   PubMed Web of Science ®Google Scholar
• Tan AL, Forbes JM, Cooper ME. 2007. AGE, RAGE, and ROS in diabetic nephropathy. Sem Nephrol. 27:130–143.
   PubMed Web of Science ®Google Scholar
• Tanaka Y, Shimizu H, Sato N, Mori M, Shimomura Y. 1995. Involvement of spontaneous nitric oxide production in the diabetogenic action of streptozotocin. Pharmacology. 50:69–73.
   PubMed Web of Science ®Google Scholar
• Tozzo E, Gnudi L, Kahn BB. 1997. Amelioration of insulin resistance in streptozotocin diabetic mice by transgenic overexpression of GLUT4 driven by an adipose-spesific promoter. Endocrinology. 138:1604–1611.
   PubMed Web of Science ®Google Scholar
• Tunçdemir M. 1998. The effects of calcium channel blocker and somatostatin analogue on kidney tissue in newborn streptozotocin diabetic rats. Medical Biology Department, İstanbul University, Institute of Health Science, İstanbul (Thesis)
   Google Scholar
• Tunçdemir M. 2006. The effects of ACE inhibitor and angiotensin receptor blocker on clusterin and apoptosis in the kidney tissue of streptozotocin-diabetic rats. Medical Biology Department, İstanbul University, Institute of Health Science, İstanbul (Thesis)
   Google Scholar
• Vardı N, Iraz M, Gül M, Öztürk F, Uçar M, Otlu A. 2006. Improving effects of aminoguanidine on the histologic alterations in rat kidneys in diabetes. Turk Klin J Med Sci. 26:603–604.
   Google Scholar
• Vardı N, Iraz M, Öztürk F, Uçar M, Gül M, Eşrefoğlu M, Otlu A. 2005. Improving effects of melatonin on the histologic alterations of rat kidneys ınduced by experimental diabetes. J Turk Ozal Med Cent. 12:145–152.
   Google Scholar
• Ward HH, Romero E, Welford A, Pickett G, Bacallao R, Gattone VH, Ness SA, Wandinger-Ness A, Roitbak T. 2011. Adult human CD133/1(+) kidney cells isolated from papilla integrate into developing kidney tubules. Biochim Biophys Acta. 1812:1344–1357.
   PubMed Web of Science ®Google Scholar
• Winiarska K, Szymanski K, Gorniak P, Dudziak M, Bryla J. 2009. Hypoglycaemic, antioxidative and nephroprotective effects of taurine in alloxan diabetic rabbits. Biochimie. 91:261–270.
   PubMed Web of Science ®Google Scholar
• Wolf G, Ziyadeh FN. 1999. Molecular mechanisms of diabetic renal hypertrophy. Kidney Int. 56:393–405.
   PubMed Web of Science ®Google Scholar
• Wu JHY, Ward NC, Indrawan AP, Almeida C-A, Hodgson JM, Proudfoot JM, PuddeyIB, Croft KD. 2007. Effects of α-tocopherol and mixed tocopherol supplementation on markers of oxidative stres and inflammation in type 2 diabetes. Clin Chem. 53:511–519.
   PubMed Web of Science ®Google Scholar
• Yaworsky K, Somwar R, Ramlal T, Tritschler HJ, Klip A. 2000. Engagement of the insülin-sensitive pathway in the stimulation of glucose transport by alpha-lipoic acid in 3T3-L1 adipocytes. Diabetologia. 43:294–303.
   PubMed Web of Science ®Google Scholar
• Yoo KH, Thornhill BA, Chevalier RL. 2000. Angiotensin stimulates TGF-beta1 and clusterin in the hydronephrotic neonatal rat kidney. Am J Physiol Reg Integr Comp Physiol. 278:640–645.
   Web of Science ®Google Scholar
• Ziegler D, Reljanovic M, Mehnert H, Gries FA. 1999. Lipoic acid in the treatment of diabetic polyneuropathy in Germany: current evidence from clinical trials. Exp Clin Endocr Diabetes. 107:421–430.
   PubMed Web of Science ®Google Scholar
• Ziyadeh FN, Goldfarb S. 1991. The renal tubulointerstitium in diabetes mellitus. Kidney Int. 39:464–475.
   PubMed Web of Science ®Google Scholar