The Nrf2-antioxidant response element pathway: A target for regulating energy metabolism

Journal of Nutritional Biochemistry

Volumn 23, Issue 10, 2012, Pages 1201-1206

  Vomhof DeKrey, Emilie E ^a   Picklo, Matthew J ^a,b  

^a GRAND FORKS HUMAN NUTRITION RESEARCH CENTER   (United States)

^b UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Adipogenesis; Lipid metabolism; Liver energy metabolism; Mitochondrial biogenesis; Sulforaphane

Indexed keywords

ANTIOXIDANT; BARDOXOLONE; GLYCOGEN SYNTHASE KINASE 3BETA; IMIDAZOLE; LEVACECARNINE; PROTEIN KINASE B; TRANSCRIPTION FACTOR NRF2;

ADIPOCYTE; ANTIOXIDANT RESPONSIVE ELEMENT; BIOGENESIS; CELL DIFFERENTIATION; COMORBIDITY; DATA ANALYSIS; DIABETES MELLITUS; DIET; ENERGY METABOLISM; EXAMINATION; HUMAN; LIPID DIET; LIVER METABOLISM; MACRONUTRIENT; NONHUMAN; OBESITY; PHYSIOLOGY; PROTEIN FUNCTION; REVIEW;

ADIPOCYTES; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; CELL DIFFERENTIATION; CELL LINE; DIET, HIGH-FAT; ENERGY METABOLISM; GENE EXPRESSION REGULATION; HUMANS; LIVER; MITOCHONDRIAL TURNOVER; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

ANIMALIA; GLYCINE MAX;

EID: 84866333520     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.03.005     Document Type: Review

References (55)

1. Nioi P., McMahon M., Itoh K., Yamamoto M., Hayes J.D. Identification of a novel Nrf2-regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem J 2003, 374(Pt 2):337-348.
2. Kaspar J.W., Niture S.K., Jaiswal A.K. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009, 47(9):1304-1309.
3. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007, 47:89-116.
4. Kwak M.K., Itoh K., Yamamoto M., Kensler T.W. Enhanced expression of the transcription factor Nrf2 by cancer chemopreventive agents: role of antioxidant response element-like sequences in the nrf2 promoter. Mol Cell Biol 2002, 22(9):2883-2892.
5. Kay H.Y., Kim W.D., Hwang S.J., Choi H.S., Gilroy R.K., Wan Y.J., et al. Nrf2 inhibits LXRalpha-dependent hepatic lipogenesis by competing with FXR for acetylase binding. Antioxid Redox Signal 2011, 15(8):2135-2146.
6. Katoh Y., Iida K., Kang M.I., Kobayashi A., Mizukami M., Tong K.I., et al. Evolutionary conserved N-terminal domain of Nrf2 is essential for the Keap1-mediated degradation of the protein by proteasome. Arch Biochem Biophys 2005, 433(2):342-350.
7. Zhang D.D. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 2006, 38(4):769-789.
8. Lo S.C., Hannink M. PGAM5, a Bcl-XL-interacting protein, is a novel substrate for the redox-regulated Keap1-dependent ubiquitin ligase complex. J Biol Chem 2006, 281(49):37893-37903.
9. Lo S.C., Hannink M. PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp Cell Res 2008, 314(8):1789-1803.
10. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., et al. 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 U S A 2002, 99(18):11908-11913.
11. Eggler A.L., Liu G., Pezzuto J.M., van Breemen R.B., Mesecar A.D. Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc Natl Acad Sci U S A 2005, 102(29):10070-10075.
12. Huang H.C., Nguyen T., Pickett C.B. Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 2002, 277(45):42769-42774.
13. Jaiswal A.K. Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 2004, 36(10):1199-1207.
14. Kobayashi M., Yamamoto M. Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species. Adv Enzyme Regul 2006, 46:113-140.
15. Salazar M., Rojo A.I., Velasco D., de Sagarra R.M., Cuadrado A. Glycogen synthase kinase-3beta inhibits the xenobiotic and antioxidant cell response by direct phosphorylation and nuclear exclusion of the transcription factor Nrf2. J Biol Chem 2006, 281(21):14841-14851.
16. Kitteringham N.R., Abdullah A., Walsh J., Randle L., Jenkins R.E., Sison R., et al. Proteomic analysis of Nrf2 deficient transgenic mice reveals cellular defence and lipid metabolism as primary Nrf2-dependent pathways in the liver. J Proteomics 2010, 73(8):1612-1631.
17. Pearl L.H., Barford D. Regulation of protein kinases in insulin, growth factor and Wnt signalling. Curr Opin Struct Biol 2002, 12(6):761-767.
18. Rada P., Rojo A.I., Chowdhry S., McMahon M., Hayes J.D., Cuadrado A. SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 2011, 31(6):1121-1133.
19. Jain A.K., Jaiswal A.K. GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 2007, 282(22):16502-16510.
20. Niture S.K., Jain A.K., Shelton P.M., Jaiswal A.K. Src subfamily kinases regulate nuclear export and degradation of transcription factor Nrf2 to switch off Nrf2-mediated antioxidant activation of cytoprotective gene expression. J Biol Chem 2011, 286(33):28821-28832.
21. Pi J., Leung L., Xue P., Wang W., Hou Y., Liu D., et al. Deficiency in the nuclear factor E2-related factor-2 transcription factor results in impaired adipogenesis and protects against diet-induced obesity. J Biol Chem 2010, 285(12):9292-9300.
22. 2 during adipogenesis. Free Radic Biol Med 2011.
23. Shin S., Wakabayashi N., Misra V., Biswal S., Lee G.H., Agoston E.S., et al. NRF2 modulates aryl hydrocarbon receptor signaling: influence on adipogenesis. Mol Cell Biol 2007, 27(20):7188-7197.
24. Chan K., Lu R., Chang J.C., Kan Y.W. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci U S A 1996, 93(24):13943-13948.
25. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 1997, 236(2):313-322.
26. Xu J. Preparation, culture, and immortalization of mouse embryonic fibroblasts. Curr Protoc Mol Biol 2005, [Chapter 28:Unit 28 1].
27. Shin S., Wakabayashi J., Yates M.S., Wakabayashi N., Dolan P.M., Aja S., et al. Role of Nrf2 in prevention of high-fat diet-induced obesity by synthetic triterpenoid CDDO-imidazolide. Eur J Pharmacol 2009, 620(1-3):138-144.
28. Tanaka Y., Aleksunes L.M., Yeager R.L., Gyamfi M.A., Esterly N., Guo G.L., et al. NF-E2-related factor 2 inhibits lipid accumulation and oxidative stress in mice fed a high-fat diet. J Pharmacol Exp Ther 2008, 325(2):655-664.
29. Gaikwad A., Long D.J., Stringer J.L., Jaiswal A.K. In vivo role of NAD(P)H:quinone oxidoreductase 1 (NQO1) in the regulation of intracellular redox state and accumulation of abdominal adipose tissue. J Biol Chem 2001, 276(25):22559-22564.
30. Wu K.C., Cui J.Y., Klaassen C.D. Beneficial role of Nrf2 in regulating NADPH generation and consumption. Toxicol Sci 2011, 123(2):590-600.
31. Yates M.S., Tran Q.T., Dolan P.M., Osburn W.O., Shin S., McCulloch C.C., et al. Genetic versus chemoprotective activation of Nrf2 signaling: overlapping yet distinct gene expression profiles between Keap1 knockout and triterpenoid-treated mice. Carcinogenesis 2009, 30(6):1024-1031.
32. Huang J., Tabbi-Anneni I., Gunda V., Wang L. Transcription factor Nrf2 regulates SHP and lipogenic gene expression in hepatic lipid metabolism. Am J Physiol Gastrointest Liver Physiol 2010, 299(6):G1211-G1221.
33. Tan Y., Ichikawa T., Li J., Si Q., Yang H., Chen X., et al. Diabetic downregulation of Nrf2 activity via ERK contributes to oxidative stress-induced insulin resistance in cardiac cells in vitro and in vivo. Diabetes 2011, 60(2):625-633.
34. Yu Z.W., Li D., Ling W.H., Jin T.R. Role of nuclear factor (erythroid-derived 2)-like 2 in metabolic homeostasis and insulin action: a novel opportunity for diabetes treatment?. World J Diabetes 2012, 3(1):19-28.
35. Moule S.K., Denton R.M. Multiple signaling pathways involved in the metabolic effects of insulin. Am J Cardiol 1997, 80(3A):41A-49A.
36. Fernandez-Marcos P.J., Auwerx J. Regulation of PGC-1alpha, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr 2011, 93(4):884S-890S.
37. Hood D.A. Invited review: contractile activity-induced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 2001, 90(3):1137-1157.
38. Joseph A.M., Pilegaard H., Litvintsev A., Leick L., Hood D.A. Control of gene expression and mitochondrial biogenesis in the muscular adaptation to endurance exercise. Essays Biochem 2006, 42:13-29.
39. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 2008, 88(2):611-638.
40. Vina J., Gomez-Cabrera M.C., Borras C., Froio T., Sanchis-Gomar F., Martinez-Bello V.E., et al. Mitochondrial biogenesis in exercise and in ageing. Adv Drug Deliv Rev 2009, 61(14):1369-1374.
41. Piantadosi C.A., Carraway M.S., Babiker A., Suliman H.B. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 2008, 103(11):1232-1240.
42. Hota K.B., Hota S.K., Chaurasia O.P., Singh S.B. Acetyl-l-carnitine-mediated neuroprotection during hypoxia is attributed to ERK1/2-Nrf2-regulated mitochondrial biosynthesis. Hippocampus 2011.
43. Zhang Y., Tang L. Discovery and development of sulforaphane as a cancer chemopreventive phytochemical. Acta Pharmacol Sin 2007, 28(9):1343-1354.
44. Yu Z., Shao W., Chiang Y., Foltz W., Zhang Z., Ling W., et al. Oltipraz upregulates the nuclear factor (erythroid-derived 2)-like 2 [corrected](NRF2) antioxidant system and prevents insulin resistance and obesity induced by a high-fat diet in C57BL/6J mice. Diabetologia 2011, 54(4):922-934.
45. Aleksunes L.M., Reisman S.A., Yeager R.L., Goedken M.J., Klaassen C.D. Nuclear factor erythroid 2-related factor 2 deletion impairs glucose tolerance and exacerbates hyperglycemia in type 1 diabetic mice. J Pharmacol Exp Ther 2010, 333(1):140-151.
46. Hayes J.D., McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 2009, 34(4):176-188.
47. Kim Y.R., Oh J.E., Kim M.S., Kang M.R., Park S.W., Han J.Y., et al. Oncogenic NRF2 mutations in squamous cell carcinomas of oesophagus and skin. J Pathol 2010, 220(4):446-451.
48. Toye A.A., Dumas M.E., Blancher C., Rothwell A.R., Fearnside J.F., Wilder S.P., et al. Subtle metabolic and liver gene transcriptional changes underlie diet-induced fatty liver susceptibility in insulin-resistant mice. Diabetologia 2007, 50(9):1867-1879.
49. Kim S., Sohn I., Ahn J.I., Lee K.H., Lee Y.S., Lee Y.S. Hepatic gene expression profiles in a long-term high-fat diet-induced obesity mouse model. Gene 2004, 340(1):99-109.
50. Levonen A.L., Landar A., Ramachandran A., Ceaser E.K., Dickinson D.A., Zanoni G., et al. Cellular mechanisms of redox cell signalling: role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. Biochem J 2004, 378(Pt 2):373-382.
51. Ceaser E.K., Ramachandran A., Levonen A.L., Darley-Usmar V.M. Oxidized low-density lipoprotein and 15-deoxy-delta 12,14-PGJ2 increase mitochondrial complex I activity in endothelial cells. Am J Physiol Heart Circ Physiol 2003, 285(6):H2298-H2308.
52. Gao L., Wang J., Sekhar K.R., Yin H., Yared N.F., Schneider S.N., et al. Novel n-3 fatty acid oxidation products activate Nrf2 by destabilizing the association between Keap1 and Cullin3. J Biol Chem 2007, 282(4):2529-2537.
53. Long E.K., Picklo M.J. Trans-4-hydroxy-2-hexenal, a product of n-3 fatty acid peroxidation: make some room HNE. Free Radic Biol Med 2010, 49(1):1-8.
54. Majkova Z., Layne J., Sunkara M., Morris A.J., Toborek M., Hennig B. Omega-3 fatty acid oxidation products prevent vascular endothelial cell activation by coplanar polychlorinated biphenyls. Toxicol Appl Pharmacol 2011, 251(1):41-49.
55. Niture S.K., Kaspar J.W., Shen J., Jaiswal A.K. Nrf2 signaling and cell survival. Toxicol Appl Pharmacol 2010, 244(1):37-42.