Gamma-tocopherol supplementation ameliorated hyper-inflammatory response during the early cutaneous wound healing in alloxan-induced diabetic mice

Experimental Biology and Medicine

Volumn 242, Issue 5, 2017, Pages 505-515

  Shin, Jihyun ^a   Yang, Soo Jin ^b   Lim, Yunsook ^a  

^a Kyung Hee University   (South Korea)

^b Seoul Women University   (South Korea)

Author keywords

cutaneous wound healing; diabetes; Gamma tocopherol; inflammation; oxidative stress

Indexed keywords

4 HYDROXYNONENAL; ALANINE AMINOTRANSFERASE; ALLOXAN; ASPARTATE AMINOTRANSFERASE; C REACTIVE PROTEIN; CATALASE; GAMMA TOCOPHEROL; GLUTATHIONE PEROXIDASE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; MANGANESE SUPEROXIDE DISMUTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SIRTUIN 1; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR; ANTIOXIDANT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIABETES MELLITUS; FOOD INTAKE; GLUCOSE BLOOD LEVEL; INFLAMMATION; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SKIN INJURY; VITAMIN SUPPLEMENTATION; WESTERN BLOTTING; WOUND CLOSURE; WOUND HEALING IMPAIRMENT; ANIMAL; COMPLICATION; DIETARY SUPPLEMENT; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; INJURIES; INSTITUTE FOR CANCER RESEARCH MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; SKIN; WOUND HEALING;

ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DIETARY SUPPLEMENTS; GAMMA-TOCOPHEROL; INFLAMMATION; MALE; MICE; MICE, INBRED ICR; SKIN; WOUND HEALING;

EID: 85012870909     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370216683836     Document Type: Article

References (67)

1. Quondamatteo F. Skin and diabetes mellitus: what do we know? Cell Tissue Res 2014; 355: 1–21.
2. Al-Watban FA, Zhang XY, Andres BL. Low-level laser therapy enhances wound healing in diabetic rats: a comparison of different lasers. Photomed Laser Surg 2007; 25: 72–7.
3. Afanas’ev I. Signaling of reactive oxygen and nitrogen species in Diabetes mellitus. Oxid Med Cell Longev 2010; 3: 361–73.
4. Low PA, Nickander KK, Tritschler HJ. The roles of oxidative stress and antioxidant treatment in experimental diabetic neuropathy. Diabetes 1997; 46: S38–42.
5. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003; 83: 835–70.
6. Midwood KS, Williams LV, Schwarzbauer JE. Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 2004; 36: 1031–7.
7. Greenhalgh DG. The role of apoptosis in wound healing. Int J Biochem Cell Biol 1998; 30: 1019–30.
8. Hubner G, Brauchle M, Smola H, Madlener M, Fassler R, Werner S. Differential regulation of pro-inflammatory cytokines during wound healing in normal and glucocorticoid-treated mice. Cytokine 1996; 8: 548–56.
9. Li Q, Verma IM. NF-kappaB regulation in the immune system. Nat Rev Immunol 2002; 2: 725–34.
10. Salil G, Nithya R, Nevin KG, Rajamohan T. Dietary coconut kernel protein beneficially modulates NFkappaB and RAGE expression in streptozotocin induced diabetes in rats. J Food Sci Technol 2014; 51: 2141–7.
11. Eo H, Lim Y. Combined mulberry leaf and fruit extract improved early stage of cutaneous wound healing in high-fat diet-induced obese mice. J Med Food 2016; 19: 161–9.
12. Haigis MC, Sinclair DA. Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 2010; 5: 253–95.
13. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005; 434: 113–8.
14. Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, Wagner RA, Greaves DR, Murray PJ, Chawla A. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab 2006; 4: 13–24.
15. Yang H, Zhang W, Pan H, Feldser HG, Lainez E, Miller C, Leung S, Zhong Z, Zhao H, Sweitzer S, Considine T, Riera T, Suri V, White B, Ellis JL, Vlasuk GP, Loh C. SIRT1 activators suppress inflammatory responses through promotion of p65 deacetylation and inhibition of NF-kappaB activity. PLoS One 2012; 7: e46364–e46364.
16. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995; 80: 293–9.
17. Kwon HK, Shin HJ, Lee JH, Park SH, Kwon MC, Panneerselvam S, Lee CG, Kim SG, Kim JH, Choi S. Etoposide induces necrosis through p53-mediated antiapoptosis in human kidney proximal tubule cells. Toxicol Sci 2015; 148: 204–19.
18. Zhang J, Cheng Y, Gu J, Wang S, Zhou S, Wang Y, Tan Y, Feng W, Fu Y, Mellen N, Cheng R, Ma J, Zhang C, Li Z, Cai L. Fenofibrate increases cardiac autophagy via FGF21/SIRT1 and prevents fibrosis and inflammation in the hearts of type 1 diabetic mice. Clin Sci 2016; 130: 625–41.
19. Schmid H, Boucherot A, Yasuda Y, Henger A, Brunner B, Eichinger F, Nitsche A, Kiss E, Bleich M, Grone HJ, Nelson PJ, Schlondorff D, Cohen CD, Kretzler M, European Renal c DNABC. Modular activation of nuclear factor-kappaB transcriptional programs in human diabetic nephropathy. Diabetes 2006; 55: 2993–3003.
20. Chang SY, Chen YW, Zhao XP, Chenier I, Tran S, Sauve A, Ingelfinger JR, Zhang SL. Catalase prevents maternal diabetes-induced perinatal programming via the Nrf2-HO-1 defense system. Diabetes 2012; 61: 2565–74.
21. Jiang T, Huang Z, Lin Y, Zhang Z, Fang D, Zhang DD. The protective role of Nrf2 in streptozotocin-induced diabetic nephropathy. Diabetes 2010; 59: 850–60.
22. Long M, Rojo de la Vega M, Wen Q, Bharara M, Jiang T, Zhang R, Zhou S, Wong PK, Wondrak GT, Zheng H, Zhang DD. An essential role of NRF2 in diabetic wound healing. Diabetes 2015; 65: 780–93.
23. Sesso HD, Buring JE, Christen WG, Kurth T, Belanger C, MacFadyen J, Bubes V, Manson JE, Glynn RJ, Gaziano JM. Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians’ Health Study II randomized controlled trial. JAMA 2008; 300: 2123–33.
24. Shen XH, Tang QY, Huang J, Cai W. Vitamin E regulates adipocytokine expression in a rat model of dietary-induced obesity. Exp Biol Med (Maywood) 2010; 235: 47–51.
25. Ju J, Picinich SC, Yang Z, Zhao Y, Suh N, Kong AN, Yang CS. Cancer-preventive activities of tocopherols and tocotrienols. Carcinogenesis 2010; 31: 533–42.
26. Wu JH, Ward NC, Indrawan AP, Almeida CA, Hodgson JM, Proudfoot JM, Puddey IB, Croft KD. Effects of alpha-tocopherol and mixed tocopherol supplementation on markers of oxidative stress and inflammation in type 2 diabetes. Clin Chem 2007; 53: 511–9.
27. Devaraj S, Jialal I. Alpha-tocopherol decreases tumor necrosis factor-alpha mRNA and protein from activated human monocytes by inhibition of 5-lipoxygenase. Free Radic Biol Med 2005; 38: 1212–20.
28. Devaraj S, Jialal I. Alpha-tocopherol decreases interleukin-1 beta release from activated human monocytes by inhibition of 5-lipoxygenase. Arterioscler Thromb Vasc Biol 1999; 19: 1125–33.
29. Bieri JG, Evarts RP. Gamma tocopherol: metabolism, biological activity and significance in human vitamin E nutrition. Am J Clin Nutr 1974; 27: 980–6.
30. Jiang Q, Christen S, Shigenaga MK, Ames BN. Gamma-tocopherol, the major form of vitamin E in the US diet, deserves more attention. Am J Clin Nutr 2001; 74: 714–22.
31. Jiang Q, Elson-Schwab I, Courtemanche C, Ames BN. Gamma-tocopherol and its major metabolite, in contrast to alpha-tocopherol, inhibit cyclooxygenase activity in macrophages and epithelial cells. Proc Natl Acad Sci USA 2000; 97: 11494–9.
32. Noh HH, Kim Y, Cho YO. Intakes and major food sources of vitamin A and vitamin E of Koean adults living in Seoul and Gyeonggi areas. Kor J Nutr 2010; 43: 628–37.
33. Vomhof-Dekrey EE, Picklo MJ, Sr. The Nrf2-antioxidant response element pathway: a target for regulating energy metabolism. J Nutr Biochem 2012; 23: 1201–6.
34. Park NY, Lim Y. Short term supplementation of dietary antioxidants selectively regulates the inflammatory responses during early cutaneous wound healing in diabetic mice. Nutr Metab 2011; 8: 80–80.
35. Reiter E, Jiang Q, Christen S. Anti-inflammatory properties of alpha- and gamma-tocopherol. Mol Aspects Med 2007; 28: 668–91.
36. Shin H, Eo H, Lim Y. 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 2016; 10: 33–41.
37. Salahudeen AK, Kanji V, Reckelhoff JF, Schmidt AM. Pathogenesis of diabetic nephropathy: a radical approach. Nephrol Dial Transplant 1997; 12: 664–8.
38. Faid I, Al-Hussaini H, Kilarkaje N. Resveratrol alleviates diabetes-induced testicular dysfunction by inhibiting oxidative stress and c-Jun N-terminal kinase signaling in rats. Toxicol Appl Pharmacol 2015; 289: 482–94.
39. Higashi S, Katagi K, Shintani N, Ikeda K, Sugimoto Y, Tsuchiya S, Inoue N, Tanaka S, Koumoto M, Kasai A, Nakazawa T, Hayata-Takano A, Hamagami K, Tomimoto S, Yoshida T, Ohkubo T, Nagayasu K, Ago Y, Onaka Y, Hashimoto R, Ichikawa A, Baba A, Hashimoto H. p13 overexpression in pancreatic beta-cells ameliorates type 2 diabetes in high-fat-fed mice. Biochem Biophys Res Commun 2015; 461: 612–7.
40. Schafer M, Werner S. Oxidative stress in normal and impaired wound repair. Pharmacol Res 2008; 58: 165–71.
41. Yu L. Free radical scavenging properties of conjugated linoleic acids. J Agric Food Chem 2001; 49: 3452–6.
42. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA 2002; 99: 11908–13.
43. Musalmah M, Nizrana MY, Fairuz AH, NoorAini AH, Azian AL, Gapor MT, Wan Ngah WZ. Comparative effects of palm vitamin E and alpha-tocopherol on healing and wound tissue antioxidant enzyme levels in diabetic rats. Lipids 2005; 40: 575–80.
44. Musalmah M, Fairuz AH, Gapor MT, Ngah WZ, Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 2009; 1: a001651–a001651.
45. Boshtam M, Rafiei M, Golshadi ID, Ani M, Shirani Z, Rostamshirazi M. Long term effects of oral vitamin E supplement in type II diabetic patients. Int J Vitam Nutr Res 2005; 75: 341–6.
46. Gray B, Swick J, Ronnenberg AG. Vitamin E and adiponectin: proposed mechanism for vitamin E-induced improvement in insulin sensitivity. Nutr Rev 2011; 69: 155–61.
47. Jialal I, Devaraj S, Venugopal SK. Oxidative stress, inflammation, and diabetic vasculopathies: the role of alpha tocopherol therapy. Free Radic Res 2002; 36: 1331–6.
48. Yamamoto Y, Gaynor RB. Therapeutic potential of inhibition of the NF-kappaB pathway in the treatment of inflammation and cancer. J Clin Invest 2001; 107: 135–42.
49. Baeuerle PA, Henkel T. Function and activation of NF-kappa B in the immune system. Annu Rev Immunol 1994; 12: 141–79.
50. Allen RG, Tresini M. Oxidative stress and gene regulation. Free Radic Biol Med 2000; 28: 463–99.
51. Kohler HB, Knop J, Martin M, de Bruin A, Huchzermeyer B, Lehmann H, Kietzmann M, Meier B, Nolte I. Involvement of reactive oxygen species in TNF-alpha mediated activation of the transcription factor NF-kappaB in canine dermal fibroblasts. Vet Immunol Immunopathol 1999; 71: 125–42.
52. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, Huang TT, Bos JL, Medema RH, Burgering BM. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002; 419: 316–21.
53. Filgueiras LR, Jr Martins JO, Serezani CH, Capelozzi VL, Montes MB, Jancar S. Sepsis-induced acute lung injury (ALI) is milder in diabetic rats and correlates with impaired NFkB activation. PLoS One 2012; 7: e44987–e44987.
54. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 2009; 1: a001651–a001651.
55. Eklund CM. Proinflammatory cytokines in CRP baseline regulation. Adv Clin Chem 2009; 48: 111–36.
56. Barzilay JI, Abraham L, Heckbert SR, Cushman M, Kuller LH, Resnick HE, Tracy RP. The relation of markers of inflammation to the development of glucose disorders in the elderly: the Cardiovascular Health Study. Diabetes 2001; 50: 2384–9.
57. Sun C, Zhang F, Ge X, Yan T, Chen X, Shi X, Zhai Q. SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metab 2007; 6: 307–19.
58. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004; 23: 2369–80.
59. Bagul PK, Deepthi N, Sultana R, Banerjee SK. Resveratrol ameliorates cardiac oxidative stress in diabetes through deacetylation of NFkB-p65 and histone 3. J Nutr Biochem 2015; 26: 1298–307.
60. Wang F, Tong Q. SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1’s repressive interaction with PPARgamma. Mol Biol Cell 2009; 20: 801–8.
61. Wang F, Nguyen M, Qin FX, Tong Q. SIRT2 deacetylates FOXO3a in response to oxidative stress and caloric restriction. Aging Cell 2007; 6: 505–14.
62. Tanno M, Kuno A, Yano T, Miura T, Hisahara S, Ishikawa S, Shimamoto K, Horio Y. Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem 2010; 285: 8375–82.
63. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, Pandita TK, Guarente L, Weinberg RA. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 2001; 107: 149–59.
64. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 2007; 26: 1913–23.
65. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, Lehman JJ, Kelly DP, Spiegelman BM. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Natl Acad Sci USA 2001; 98: 3820–5.
66. Eo H, Lee HJ, Lim Y. Ameliorative effect of dietary genistein on diabetes induced hyper-inflammation and oxidative stress during early stage of wound healing in alloxan induced diabetic mice. Biochem Biophys Res Commun 2016; 478: 1021–7.
67. Shin H, Eo H, Lim Y. 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 2016; 10: 33–41.