Genistein accelerates refractory wound healing by suppressing superoxide and FoxO1/iNOS pathway in type 1 diabetes

Journal of Nutritional Biochemistry

Volumn 24, Issue 1, 2013, Pages 88-96

  Tie, Lu ^a   An, Yu ^a   Han, Jing ^a   Xiao, Yuan ^a   Xiaokaiti, Yilixiati ^a   Fan, Shengjun ^a   Liu, Shaoqiang ^a,b   Chen, Alex F ^c   Li, Xuejun ^a  

^a PEKING UNIVERSITY   (China)

^b PEKING UNIVERSITY THIRD HOSPITAL   (China)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Diabetes; FoxO1; Genistein; INOS; Nitrotyrosine; Oxidative stress

Indexed keywords

3 NITROTYROSINE; GENISTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRITE; OXYGEN; SUPEROXIDE; TRANSCRIPTION FACTOR FKHR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY TUBE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; WOUND HEALING; WOUND HEALING IMPAIRMENT;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FORKHEAD TRANSCRIPTION FACTORS; GENISTEIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; SIRTUIN 1; STREPTOZOCIN; SUPEROXIDES; TYROSINE; WOUND HEALING;

MUS;

EID: 84870432218     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.02.011     Document Type: Article

References (44)

1. Singer A.J., Clark R.A. Cutaneous wound healing. N Engl J Med 1999, 341:738-746.
2. Boulton A.J., Vileikyte L., Ragnarson-Tennvall G., Apelqvist J. The global burden of diabetic foot disease. Lancet 2005, 366:1719-1724.
3. Brem H., Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest 2007, 117:1219-1222.
4. Falanga V. Wound healing and its impairment in the diabetic foot. Lancet 2005, 366:1736-1743.
5. Giacco F., Brownlee M. Oxidative stress and diabetic complications. Circ Res 2010, 107:1058-1070.
6. Fadini G.P., Albiero M., Menegazzo L., Boscaro E., Pagnin E., Iori E., et al. The redox enzyme p66Shc contributes to diabetes and ischemia-induced delay in cutaneous wound healing. Diabetes 2010, 59:2306-2314.
7. Gallagher K.A., Liu Z.J., Xiao M., Chen H., Goldstein L.J., Buerk D.G., et al. Diabetic impairments in NO-mediated endothelial progenitor cell mobilization and homing are reversed by hyperoxia and SDF-1 alpha. J Clin Invest 2007, 117:1249-1259.
8. Luo J.D., Wang Y.Y., Fu W.L., Wu J., Chen A.F. Gene therapy of endothelial nitric oxide synthase and manganese superoxide dismutase restores delayed wound healing in type 1 diabetic mice. Circulation 2004, 110:2484-2493.
9. Tie L., Li X.J., Wang X., Channon K.M., Chen A.F. Endothelium-specific GTP cyclohydrolase I overexpression accelerates refractory wound healing by suppressing oxidative stress in diabetes. Am J Physiol 2009, 296:E1423-E1429.
10. Mudge B.P., Harris C., Gilmont R.R., Adamson B.S., Rees R.S. Role of glutathione redox dysfunction in diabetic wounds. Wound Repair Regen 2002, 10:52-58.
11. Musalmah M., Nizrana M.Y., Fairuz A.H., NoorAini A.H., Azian A.L., Gapor M.T., et al. Comparative effects of palm vitamin E and alpha-tocopherol on healing and wound tissue antioxidant enzyme levels in diabetic rats. Lipids 2005, 40:575-580.
12. Anderson J.J., Anthony M., Messina M., Garne S.C. Effects of phyto-oestrogens on tissues. Nutr Res Rev 1999, 12:75-116.
13. Baluchnejadmojarad T., Roghani M. Chronic administration of genistein improves aortic reactivity of streptozotocin-diabetic rats: mode of action. Vascul Pharmacol 2008, 49:1-5.
14. Valsecchi A.E., Franchi S., Panerai A.E., Rossi A., Sacerdote P., Colleoni M. The soy isoflavone genistein reverses oxidative and inflammatory state, neuropathic pain, neurotrophic and vasculature deficits in diabetes mouse model. Eur J Pharmacol 2011, 650:694-702.
15. Xu S.Z., Zhong W., Ghavideldarestani M., Saurabh R., Lindow S.W., Atkin S.L. Multiple mechanisms of soy isoflavones against oxidative stress-induced endothelium injury. Free Radic Biol Med 2009, 47:167-175.
16. Hallinan E.A., Tsymbalov S., Dorn C.R., Pitzele B.S., Hansen D.W., Moore W.M., et al. Synthesis and biological characterization of L-N(6)-(1-iminoethyl)lysine 5-tetrazole-amide, a prodrug of a selective iNOS inhibitor. J Med Chem 2002, 45:1686-1689.
17. Nagareddy P.R., Soliman H., Lin G., Rajput P.S., Kumar U., McNeill J.H., et al. Selective inhibition of protein kinase C beta(2) attenuates inducible nitric oxide synthase-mediated cardiovascular abnormalities in streptozotocin-induced diabetic rats. Diabetes 2009, 58:2355-2364.
18. Wu L., Mayeux P.R. Effects of the inducible nitric-oxide synthase inhibitor L-N(6)-(1-iminoethyl)-lysine on microcirculation and reactive nitrogen species generation in the kidney following lipopolysaccharide administration in mice. J Pharmacol Exp Ther 2007, 320:1061-1067.
19. Marrotte E.J., Chen D.D., Hakim J.S., Chen A.F. Manganese superoxide dismutase expression in endothelial progenitor cells accelerates wound healing in diabetic mice. J Clin Invest 2010, 120(12):4207-4219.
20. Xie H.H., Zhou S., Chen D.D., Channon K.M., Su D.F., Chen A.F. GTP cyclohydrolase I/BH4 pathway protects EPCs via suppressing oxidative stress and thrombospondin-1 in salt-sensitive hypertension. Hypertension 2010, 56(6):1137-1144.
21. Asahara T., Murohara T., Sullivan A., Silver M., Vanderzee R., Li T., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science (New York, NY) 1997, 275:964-967.
22. Ii M., Takenaka H., Asai J., Ibusuki K., Mizukami Y., Maruyama K., et al. Endothelial progenitor thrombospondin-1 mediates diabetes-induced delay in reendothelialization following arterial injury. Circ Res 2006, 98:697-704.
23. Bauerova K., Bezek A. Role of reactive oxygen and nitrogen species in etiopathogenesis of rheumatoid arthritis. Gen Physiol Biophys 1999, 18 Spec No:15-20.
24. Tanaka J., Qiang L., Banks A.S., Welch C.L., Matsumoto M., Kitamura T., et al. Foxo1 links hyperglycemia to LDL oxidation and endothelial nitric oxide synthase dysfunction in vascular endothelial cells. Diabetes 2009, 58:2344-2354.
25. Choi M.S., Jung U.J., Yeo J., Kim M.J., Lee M.K. Genistein and daidzein prevent diabetes onset by elevating insulin level and altering hepatic gluconeogenic and lipogenic enzyme activities in non-obese diabetic (NOD) mice. Diabetes Metab Res Rev 2008, 24:74-81.
26. Liu D., Zhen W., Yang Z., Carter J.D., Si H., Reynolds K.A. Genistein acutely stimulates insulin secretion in pancreatic beta-cells through a cAMP-dependent protein kinase pathway. Diabetes 2006, 55:1043-1050.
27. Valsecchi A.E., Franchi S., Panerai A.E., Rossi A., Sacerdote P., Colleoni M. The soy isoflavone genistein reverses oxidative and inflammatory state, neuropathic pain, neurotrophic and vasculature deficits in diabetes mouse model. Eur J Pharmacol 2011, 650:694-702.
28. Blakytny R., Jude E. The molecular biology of chronic wounds and delayed healing in diabetes. Diabet Med 2006, 23:594-608.
29. Costa C., Incio J., Soares R. Angiogenesis and chronic inflammation: cause or consequence?. Angiogenesis 2007, 10:149-166.
30. Farina H.G., Pomies M., Alonso D.F., Gomez D.E. Antitumor and antiangiogenic activity of soy isoflavone genistein in mouse models of melanoma and breast cancer. Oncol Rep 2006, 16:885-891.
31. Guo Y., Wang S., Hoot D.R., Clinton S.K. Suppression of VEGF-mediated autocrine and paracrine interactions between prostate cancer cells and vascular endothelial cells by soy isoflavones. J Nutr Biochem 2007, 18:408-417.
32. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139:4252-4263.
33. Froyen E.B., Steinberg F.M. Soy isoflavones increase quinone reductase in hepa-1c1c7 cells via estrogen receptor beta and nuclear factor erythroid 2-related factor 2 binding to the antioxidant response element. J Nutr Biochem 2011, 22:843-848.
34. Emmerson E., Campbell L., Ashcroft G.S., Hardman M.J. The phytoestrogen genistein promotes wound healing by multiple independent mechanisms. Mol Cell Endocrinol 2010, 321(2):184-193.
35. Leopold J.A., Loscalzo J. Oxidative enzymopathies and vascular disease. Arterioscler Thromb Vasc Biol 2005, 25:1332-1340.
36. Nagareddy P.R., Xia Z., McNeill J.H., MacLeod K.M. Increased expression of iNOS is associated with endothelial dysfunction and impaired pressor responsiveness in streptozotocin-induced diabetes. Am J Physiol 2005, 289:H2144-H2152.
37. Nagareddy P.R., McNeill J.H., MacLeod K.M. Chronic inhibition of inducible nitric oxide synthase ameliorates cardiovascular abnormalities in streptozotocin diabetic rats. Eur J Pharmacol 2009, 611:53-59.
38. Huisman A., Vos I., van Faassen E.E., Joles J.A., Grone H.J., Martasek P., et al. Anti-inflammatory effects of tetrahydrobiopterin on early rejection in renal allografts: modulation of inducible nitric oxide synthase. FASEB J 2002, 16:1135-1137.
39. Xiong S., Salazar G., Patrushev N., Alexander R.W. FoxO1 mediates an autofeedback loop regulating SIRT1 expression. J Biol Chem 2011, 286(7):5289-5299.
40. Chae H.D., Broxmeyer H.E. SIRT1 deficiency downregulates PTEN/JNK/FOXO1 pathway to block ROS-induced apoptosis in mouse embryonic stem cells. Stem Cells Dev 2011, 20(7):1277-1285.
41. Bastien-Dionne P.O., Valenti L., Kon N., Gu W., Buteau J. Glucagon-like peptide 1 inhibits the sirtuin deacetylase SirT1 to stimulate pancreatic beta-cell mass expansion. Diabetes 2011, 60:3217-3222.
42. Orimo M., Minamino T., Miyauchi H., Tateno K., Okada S., Moriya J., et al. Protective role of SIRT1 in diabetic vascular dysfunction. Arterioscler Thromb Vasc Biol 2009, 29:889-894.
43. Kikuno N., Shiina H., Urakami S., Kawamoto K., Hirata H., Tanaka Y., et al. Genistein mediated histone acetylation and demethylation activates tumor suppressor genes in prostate cancer cells. Int J Cancer 2008, 123:552-560.
44. Rasbach K.A., Schnellmann R.G. Isoflavones promote mitochondrial biogenesis. J Pharmacol Exp Ther 2008, 325:536-543.