Progress on the role of nuclear factor-erythroid 2-related factor 2 in regulating cell proliferation_West China Medical Journal

Authors：

CHEN Chen , LIU Jieyu , WU Jing ,  AN Yan

Department of Toxicology, Medical College of Soochow University, Suzhou, Jiangsu 215123, P. R. China;

Corresponding author：

AN Yan, Email: dranyan@126.com

Keywords：

Nuclear factor-erythroid 2-related factor 2; Reactive oxygen species; Cell proliferation; Mitochondrial function; Inflammatory response

DOI：

10.7507/1002-0179.201905203

Video：

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Abstract Full text Figures/Tables Video References Cited by

Nuclear factor-erythroid 2-related factor 2 (Nrf2) is an important factor for cells to resist oxidative stress and electrophilic attack. It is involved in the formation and control of oxidative stress defense pathways. It is associated with oxidative stress-related diseases, including cancer, neurodegenerative diseases, cardiovascular diseases and aging, and is a potential pharmacological target for the treatment of chronic diseases. This article will review the important role of Nrf2 in the regulation of cell proliferation, including direct regulation of cell proliferation, regulation of reactive oxygen species, intracellular metabolism, regulation of mitochondrial function, cell lifespan and inflammatory response. The aim is to provide a theoretical basis for further research on how to use Nrf2 to regulate cell proliferation.

Citation： CHEN Chen, LIU Jieyu, WU Jing, AN Yan. Progress on the role of nuclear factor-erythroid 2-related factor 2 in regulating cell proliferation. West China Medical Journal, 2019, 34(12): 1440-1445. doi: 10.7507/1002-0179.201905203 Copy

1.	Schmoll D, Engel CK, Glombik H. The Keap1-Nrf2 protein-protein interaction: a suitable target for small molecules. Drug Discov Today Technol, 2017(24): 11-17.
2.	Zheng JQ, Zhang GR, Li J, et al. Neutrophil elastase inhibitor suppresses oxidative stress in obese asthmatic rats by activating Keap1/Nrf2 signaling pathway. Eur Rev Med Pharmacol Sci, 2019, 23(1): 361-369.
3.	Jeong Y, Hoang NT, Lovejoy A, et al. Role of KEAP1/NRF2 and TP53 mutations in lung squamous cell carcinoma development and radiation resistance. Cancer Discov, 2017, 7(1): 86-101.
4.	Yuan L, Duan X, Zhang R, et al. Aloe polysaccharide protects skin cells from UVB irradiation through Keap1/Nrf2/ARE signal pathway. J Dermatolog Treat, 2019: 1-9.
5.	Zhang H, Davies KJA, Forman HJ. Oxidative stress response and Nrf2 signaling in aging. Free Radic Biol Med, 2015, 88(Pt B): 314-336.
6.	Ye ZW, Zhang J, Townsend DM, et al. Oxidative stress, redox regulation and diseases of cellular differentiation. Biochim Biophys Acta, 2015, 1850(8): 1607-1621.
7.	Wang Z, Liang M, Li H, et al. l-Methionine activates Nrf2-ARE pathway to induce endogenous antioxidant activity for depressing ROS-derived oxidative stress in growing rats. J Sci Food Agric, 2019, 99(10): 4849-4862.
8.	Zhang J, Wang X, Vikash V, et al. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev, 2016, 2016: 4350965.
9.	Xu J, Zhou L, Weng Q, et al. Curcumin analogues attenuate Aβ_25-35-induced oxidative stress in PC12 cells via Keap1/Nrf2/HO-1 signaling pathways. Chem Biol Interact, 2019, 305: 171-179.
10.	Huang K, Gao X, Wei W. The crosstalk between Sirt1 and Keap1/Nrf2/ARE anti-oxidative pathway forms a positive feedback loop to inhibit FN and TGF-β1 expressions in rat glomerular mesangial cells. Exp Cell Res, 2017, 361(1): 63-72.
11.	Xiang Y, Fan X, Zhao M, et al. CKIP-1 alleviates oxygen-glucose deprivation/reoxygenation-induced apoptosis and oxidative stress in cultured hippocampal neurons by downregulating Keap1 and activating Nrf2/ARE signaling. Eur J Pharmacol, 2019, 848: 140-149.
12.	Wang Z, Han N, Zhao K, et al. Protective effects of pyrroloquinoline quinine against oxidative stress-induced cellular senescence and inflammation in human renal tubular epithelial cells via Keap1/Nrf2 signaling pathway. Int Immunopharmacol, 2019, 72: 445-453.
13.	Zhao XJ, Yu HW, Yang YZ, et al. Polydatin prevents fructose-induced liver inflammation and lipid deposition through increasing miR-200a to regulate Keap1/Nrf2 pathway. Redox Biol, 2018, 18: 124-137.
14.	Qi G, Mi Y, Wang Y, et al. Neuroprotective action of tea polyphenols on oxidative stress-induced apoptosis through the activation of the TrkB/CREB/BDNF pathway and Keap1/Nrf2 signaling pathway in SH-SY5Y cells and mice brain. Food Funct, 2017, 8(12): 4421-4432.
15.	Sharath Babu GR, Anand T, Ilaiyaraja N, et al. Pelargonidin modulates Keap1/Nrf2 pathway gene expression and ameliorates citrinin-induced oxidative stress in HepG2 cells. Front Pharmacol, 2017, 8: 868.
16.	Murakami S, Motohashi H. Roles of Nrf2 in cell proliferation and differentiation. Free Radic Biol Med, 2015, 88(Pt B): 168-178.
17.	Tsai JJ, Dudakov JA, Takahashi K, et al. Nrf2 regulates haematopoietic stem cell function. Nat Cell Biol, 2013, 15(3): 309-316.
18.	Kim JH, Thimmulappa RK, Kumar V, et al. NRF2-mediated Notch pathway activation enhances hematopoietic reconstitution following myelosuppressive radiation. J Clin Invest, 2014, 124(2): 730-741.
19.	Sun J, Hoshino H, Takaku K, et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J, 2002, 21(19): 5216-5224.
20.	Malhotra D, Portales-Casamar E, Singh A, et al. Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChIP-Seq profiling and network analysis. Nucleic Acids Res, 2010, 38(17): 5718-5734.
21.	Hirotsu Y, Katsuoka F, Funayama R, et al. Nrf2-MafG heterodimers contribute globally to antioxidant and metabolic networks. Nucleic Acids Res, 2012, 40(20): 10228-10239.
22.	Hu M, Zou Y, Nambiar SM, et al. Keap1 modulates the redox cycle and hepatocyte cell cycle in regenerating liver. Cell Cycle, 2014, 13(15): 2349-2358.
23.	Zou Y, Hu M, Lee J, et al. Nrf2 is essential for timely M phase entry of replicating hepatocytes during liver regeneration. Am J Physiol Gastrointest Liver Physiol, 2015, 308(4): G262-G268.
24.	Reddy NM, Kleeberger SR, Bream JH, et al. Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling. Oncogene, 2008, 27(44): 5821-5832.
25.	Morales-González JA, Madrigal-Santillán E, Morales-González Á, et al. What is known regarding the participation of factor Nrf-2 in liver regeneration?. Cells, 2015, 4(2): 169-177.
26.	Raghunath A, Sundarraj K, Arfuso F, et al. Dysregulation of Nrf2 in hepatocellular carcinoma: role in cancer progression and chemoresistance. Cancers (Basel), 2018, 10(12): 481.
27.	Sun X, Ou Z, Chen R, et al. Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology, 2016, 63(1): 173-184.
28.	Sadeghi MR, Jeddi F, Soozangar N, et al. Nrf2/P-glycoprotein axis is associated with clinicopathological characteristics in colorectal cancer. Biomed Pharmacother, 2018, 104: 458-464.
29.	Zhu J, Wang H, Chen F, et al. Triptolide enhances chemotherapeutic efficacy of antitumor drugs in non-small-cell lung cancer cells by inhibiting Nrf2-ARE activity. Toxicol Appl Pharmacol, 2018, 358: 1-9.
30.	Onodera Y, Motohashi H, Takagi K, et al. NRF2 immunolocalization in human breast cancer patients asa prognostic factor. Endocr Relat Cancer, 2014, 21(2): 241-252.
31.	Huang H, Wu Y, Fu W, et al. Downregulation of Keap1 contributes to poor prognosis and Axitinib resistance of renal cell carcinoma via upregulation of Nrf2 expression. Int J Mol Med, 2019, 43(5): 2044-2054.
32.	Gonzalez-Donquiles C, Alonso-Molero J, Fernandez-Villa T, et al. The NRF2 transcription factor plays a dual role in colorectal cancer: a systematic review. PLoS One, 2017, 12(5): e0177549.
33.	Lee S, Hallis SP, Jung KA, et al. Impairment of HIF-1α-mediated metabolic adaption by NRF2-silencing in breast cancer cells. Redox Biol, 2019, 24: 101210.
34.	Mitsuishi Y, Taguchi K, Kawatani Y, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell, 2012, 22(1): 66-79.
35.	Chartoumpekis DV, Wakabayashi N, Kensler TW. Keap1/Nrf2 pathway in the frontiers of cancer and non-cancer cell metabolism. Biochem Soc Trans, 2015, 43(4): 639-644.
36.	Ahmad F, Dixit D, Sharma V, et al. Nrf2-driven TERT regulates pentose phosphate pathway in glioblastoma. Cell Death Dis, 2016, 7: e2213.
37.	Chowdhry S, Nazmy MH, Meakin PJ, et al. Loss of Nrf2 markedly exacerbates nonalcoholic steatohepatitis. Free Radic Biol Med, 2010, 48(2): 357-371.
38.	Saha PK, Reddy VT, Konopleva M, et al. The triterpenoid 2-cyano-3, 12-dioxooleana-1, 9-dien-28-oic-acid methyl ester has potent anti-diabetic effects in diet-induced diabetic mice and Lepr(db/db) mice. J Biol Chem, 2010, 285(52): 40581-40592.
39.	DeNicola GM, Chen PH, Mullarky E, et al. Erratum: NRF2 regulates serine biosynthesis in non-small cell lung cancer. Nat Genet, 2016, 48(4): 473.
40.	Sant KE, Hansen JM, Williams LM, et al. The role of Nrf1 and Nrf2 in the regulation of glutathione and redox dynamics in the developing zebrafish embryo. Redox Biol, 2017, 13: 207-218.
41.	Chorley BN, Campbell MR, Wang X, et al. Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoidX receptor alpha. Nucleic Acids Res, 2012, 40(15): 7416-7429.
42.	Ray U, Roy SS. Aberrant lipid metabolism in cancer cells - the role of oncolipid-activated signaling. FEBS J, 2017, 285(3): 432-443.
43.	Kaur S, Nag A, Singh AK, et al. PPARγ-targeting potential for radioprotection. Curr Drug Targets, 2018, 19(15): 1818-1830.
44.	Holmström KM, Baird L, Zhang Y, et al. Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration. Biol Open, 2013, 2(8): 761-770.
45.	Itoh K, Ye P, Matsumiya T, et al. Emerging functional cross-talk between the Keap1-Nrf2 system and mitochondria. J Clin Biochem Nutr, 2015, 56(2): 91-97.
46.	Dinkova-Kostova AT, Abramov AY. The emerging role of Nrf2 in mitochondrial function. Free Radic Biol Med, 2015, 88(Pt B): 179-188.
47.	Im JY, Lee KW, Woo JM, et al. DJ-1 induces thioredoxin1 expression through the Nrf2 pathway. Hum Mol Genet, 2012, 21(13): 3013-3024.
48.	Gan L, Johnson DA, Johnson JA. Keap1-Nrf2 activation in the presence and absence of DJ-1. Eur J Neurosci, 2010, 31(6): 967-977.
49.	Paek J, Lo JY, Narasimhan SD, et al. Mitochondrial SKN-1/Nrf mediates a conserved starvation response. Cell Metab, 2012, 16(4): 526-537.
50.	Bishop NA, Guarente L. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature, 2007, 447(7144): 545-549.
51.	Lewis KN, Wason E, Edrey YH, et al. Regulation of Nrf2 signaling and longevity in naturally long-lived rodents. Proc Natl Acad SciU S A, 2015, 112(12): 3722-3727.
52.	Spiers JG, Breda C, Robinson S, et al. Drosophila Nrf2/Keap1 mediated redox signaling supports synaptic function and longevity and impacts on circadian activity. Front Mol Neurosci, 2019, 12: 86.
53.	Tsakiri EN, Gumeni S, Iliaki KK, et al. Hyperactivation of Nrf2 increases stress tolerance at the cost of aging acceleration due to metabolic deregulation. Aging Cell, 2019, 18(1): e12845.
54.	Ahmed SM, Luo L, Namani A, et al. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta Mol Basis Dis, 2017, 1863(2): 585-597.
55.	Perico L, Wyatt CM, Benigni A. A new BEACON of hope for the treatment of inflammation? The endogenous metabolite itaconate as an alternative activator of the KEAP1-Nrf2 system. Kidney Int, 2018, 94(4): 646-649.
56.	Nagashima R, Kosai H, Masuo M, et al. Nrf2 suppresses allergic lung inflammation by attenuating the type 2 innate lymphoid cell response. J Immunol, 2019, 202(5): 1331-1339.
57.	Lampiasi N, Montana G. An in vitro inflammation model to study the Nrf2 and NF-κB crosstalk in presence of ferulic acid as modulator. Immunobiology, 2018, 223(4/5): 349-355.
58.	Chia AJ, Goldring CE, Kitteringham NR, et al. Differential effect of covalent protein modification and glutathione depletion on the transcriptional response of Nrf2 and NF-kappaB. Biochem Pharmacol, 2010, 80(3): 410-421.
59.	Banning A, Brigelius-Flohé R. NF-kappaB, Nrf2, and HO-1 interplay in redox-regulated VCAM-1 expression. Antioxid Redox Signal, 2005, 7(7/8): 889-899.

1. Schmoll D, Engel CK, Glombik H. The Keap1-Nrf2 protein-protein interaction: a suitable target for small molecules. Drug Discov Today Technol, 2017(24): 11-17.
2. Zheng JQ, Zhang GR, Li J, et al. Neutrophil elastase inhibitor suppresses oxidative stress in obese asthmatic rats by activating Keap1/Nrf2 signaling pathway. Eur Rev Med Pharmacol Sci, 2019, 23(1): 361-369.
3. Jeong Y, Hoang NT, Lovejoy A, et al. Role of KEAP1/NRF2 and TP53 mutations in lung squamous cell carcinoma development and radiation resistance. Cancer Discov, 2017, 7(1): 86-101.
4. Yuan L, Duan X, Zhang R, et al. Aloe polysaccharide protects skin cells from UVB irradiation through Keap1/Nrf2/ARE signal pathway. J Dermatolog Treat, 2019: 1-9.
5. Zhang H, Davies KJA, Forman HJ. Oxidative stress response and Nrf2 signaling in aging. Free Radic Biol Med, 2015, 88(Pt B): 314-336.
6. Ye ZW, Zhang J, Townsend DM, et al. Oxidative stress, redox regulation and diseases of cellular differentiation. Biochim Biophys Acta, 2015, 1850(8): 1607-1621.
7. Wang Z, Liang M, Li H, et al. l-Methionine activates Nrf2-ARE pathway to induce endogenous antioxidant activity for depressing ROS-derived oxidative stress in growing rats. J Sci Food Agric, 2019, 99(10): 4849-4862.
8. Zhang J, Wang X, Vikash V, et al. ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev, 2016, 2016: 4350965.
9. Xu J, Zhou L, Weng Q, et al. Curcumin analogues attenuate Aβ_25-35-induced oxidative stress in PC12 cells via Keap1/Nrf2/HO-1 signaling pathways. Chem Biol Interact, 2019, 305: 171-179.
10. Huang K, Gao X, Wei W. The crosstalk between Sirt1 and Keap1/Nrf2/ARE anti-oxidative pathway forms a positive feedback loop to inhibit FN and TGF-β1 expressions in rat glomerular mesangial cells. Exp Cell Res, 2017, 361(1): 63-72.
11. Xiang Y, Fan X, Zhao M, et al. CKIP-1 alleviates oxygen-glucose deprivation/reoxygenation-induced apoptosis and oxidative stress in cultured hippocampal neurons by downregulating Keap1 and activating Nrf2/ARE signaling. Eur J Pharmacol, 2019, 848: 140-149.
12. Wang Z, Han N, Zhao K, et al. Protective effects of pyrroloquinoline quinine against oxidative stress-induced cellular senescence and inflammation in human renal tubular epithelial cells via Keap1/Nrf2 signaling pathway. Int Immunopharmacol, 2019, 72: 445-453.
13. Zhao XJ, Yu HW, Yang YZ, et al. Polydatin prevents fructose-induced liver inflammation and lipid deposition through increasing miR-200a to regulate Keap1/Nrf2 pathway. Redox Biol, 2018, 18: 124-137.
14. Qi G, Mi Y, Wang Y, et al. Neuroprotective action of tea polyphenols on oxidative stress-induced apoptosis through the activation of the TrkB/CREB/BDNF pathway and Keap1/Nrf2 signaling pathway in SH-SY5Y cells and mice brain. Food Funct, 2017, 8(12): 4421-4432.
15. Sharath Babu GR, Anand T, Ilaiyaraja N, et al. Pelargonidin modulates Keap1/Nrf2 pathway gene expression and ameliorates citrinin-induced oxidative stress in HepG2 cells. Front Pharmacol, 2017, 8: 868.
16. Murakami S, Motohashi H. Roles of Nrf2 in cell proliferation and differentiation. Free Radic Biol Med, 2015, 88(Pt B): 168-178.
17. Tsai JJ, Dudakov JA, Takahashi K, et al. Nrf2 regulates haematopoietic stem cell function. Nat Cell Biol, 2013, 15(3): 309-316.
18. Kim JH, Thimmulappa RK, Kumar V, et al. NRF2-mediated Notch pathway activation enhances hematopoietic reconstitution following myelosuppressive radiation. J Clin Invest, 2014, 124(2): 730-741.
19. Sun J, Hoshino H, Takaku K, et al. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J, 2002, 21(19): 5216-5224.
20. Malhotra D, Portales-Casamar E, Singh A, et al. Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChIP-Seq profiling and network analysis. Nucleic Acids Res, 2010, 38(17): 5718-5734.
21. Hirotsu Y, Katsuoka F, Funayama R, et al. Nrf2-MafG heterodimers contribute globally to antioxidant and metabolic networks. Nucleic Acids Res, 2012, 40(20): 10228-10239.
22. Hu M, Zou Y, Nambiar SM, et al. Keap1 modulates the redox cycle and hepatocyte cell cycle in regenerating liver. Cell Cycle, 2014, 13(15): 2349-2358.
23. Zou Y, Hu M, Lee J, et al. Nrf2 is essential for timely M phase entry of replicating hepatocytes during liver regeneration. Am J Physiol Gastrointest Liver Physiol, 2015, 308(4): G262-G268.
24. Reddy NM, Kleeberger SR, Bream JH, et al. Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling. Oncogene, 2008, 27(44): 5821-5832.
25. Morales-González JA, Madrigal-Santillán E, Morales-González Á, et al. What is known regarding the participation of factor Nrf-2 in liver regeneration?. Cells, 2015, 4(2): 169-177.
26. Raghunath A, Sundarraj K, Arfuso F, et al. Dysregulation of Nrf2 in hepatocellular carcinoma: role in cancer progression and chemoresistance. Cancers (Basel), 2018, 10(12): 481.
27. Sun X, Ou Z, Chen R, et al. Activation of the p62-Keap1-NRF2 pathway protects against ferroptosis in hepatocellular carcinoma cells. Hepatology, 2016, 63(1): 173-184.
28. Sadeghi MR, Jeddi F, Soozangar N, et al. Nrf2/P-glycoprotein axis is associated with clinicopathological characteristics in colorectal cancer. Biomed Pharmacother, 2018, 104: 458-464.
29. Zhu J, Wang H, Chen F, et al. Triptolide enhances chemotherapeutic efficacy of antitumor drugs in non-small-cell lung cancer cells by inhibiting Nrf2-ARE activity. Toxicol Appl Pharmacol, 2018, 358: 1-9.
30. Onodera Y, Motohashi H, Takagi K, et al. NRF2 immunolocalization in human breast cancer patients asa prognostic factor. Endocr Relat Cancer, 2014, 21(2): 241-252.
31. Huang H, Wu Y, Fu W, et al. Downregulation of Keap1 contributes to poor prognosis and Axitinib resistance of renal cell carcinoma via upregulation of Nrf2 expression. Int J Mol Med, 2019, 43(5): 2044-2054.
32. Gonzalez-Donquiles C, Alonso-Molero J, Fernandez-Villa T, et al. The NRF2 transcription factor plays a dual role in colorectal cancer: a systematic review. PLoS One, 2017, 12(5): e0177549.
33. Lee S, Hallis SP, Jung KA, et al. Impairment of HIF-1α-mediated metabolic adaption by NRF2-silencing in breast cancer cells. Redox Biol, 2019, 24: 101210.
34. Mitsuishi Y, Taguchi K, Kawatani Y, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell, 2012, 22(1): 66-79.
35. Chartoumpekis DV, Wakabayashi N, Kensler TW. Keap1/Nrf2 pathway in the frontiers of cancer and non-cancer cell metabolism. Biochem Soc Trans, 2015, 43(4): 639-644.
36. Ahmad F, Dixit D, Sharma V, et al. Nrf2-driven TERT regulates pentose phosphate pathway in glioblastoma. Cell Death Dis, 2016, 7: e2213.
37. Chowdhry S, Nazmy MH, Meakin PJ, et al. Loss of Nrf2 markedly exacerbates nonalcoholic steatohepatitis. Free Radic Biol Med, 2010, 48(2): 357-371.
38. Saha PK, Reddy VT, Konopleva M, et al. The triterpenoid 2-cyano-3, 12-dioxooleana-1, 9-dien-28-oic-acid methyl ester has potent anti-diabetic effects in diet-induced diabetic mice and Lepr(db/db) mice. J Biol Chem, 2010, 285(52): 40581-40592.
39. DeNicola GM, Chen PH, Mullarky E, et al. Erratum: NRF2 regulates serine biosynthesis in non-small cell lung cancer. Nat Genet, 2016, 48(4): 473.
40. Sant KE, Hansen JM, Williams LM, et al. The role of Nrf1 and Nrf2 in the regulation of glutathione and redox dynamics in the developing zebrafish embryo. Redox Biol, 2017, 13: 207-218.
41. Chorley BN, Campbell MR, Wang X, et al. Identification of novel NRF2-regulated genes by ChIP-Seq: influence on retinoidX receptor alpha. Nucleic Acids Res, 2012, 40(15): 7416-7429.
42. Ray U, Roy SS. Aberrant lipid metabolism in cancer cells - the role of oncolipid-activated signaling. FEBS J, 2017, 285(3): 432-443.
43. Kaur S, Nag A, Singh AK, et al. PPARγ-targeting potential for radioprotection. Curr Drug Targets, 2018, 19(15): 1818-1830.
44. Holmström KM, Baird L, Zhang Y, et al. Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration. Biol Open, 2013, 2(8): 761-770.
45. Itoh K, Ye P, Matsumiya T, et al. Emerging functional cross-talk between the Keap1-Nrf2 system and mitochondria. J Clin Biochem Nutr, 2015, 56(2): 91-97.
46. Dinkova-Kostova AT, Abramov AY. The emerging role of Nrf2 in mitochondrial function. Free Radic Biol Med, 2015, 88(Pt B): 179-188.
47. Im JY, Lee KW, Woo JM, et al. DJ-1 induces thioredoxin1 expression through the Nrf2 pathway. Hum Mol Genet, 2012, 21(13): 3013-3024.
48. Gan L, Johnson DA, Johnson JA. Keap1-Nrf2 activation in the presence and absence of DJ-1. Eur J Neurosci, 2010, 31(6): 967-977.
49. Paek J, Lo JY, Narasimhan SD, et al. Mitochondrial SKN-1/Nrf mediates a conserved starvation response. Cell Metab, 2012, 16(4): 526-537.
50. Bishop NA, Guarente L. Two neurons mediate diet-restriction-induced longevity in C. elegans. Nature, 2007, 447(7144): 545-549.
51. Lewis KN, Wason E, Edrey YH, et al. Regulation of Nrf2 signaling and longevity in naturally long-lived rodents. Proc Natl Acad SciU S A, 2015, 112(12): 3722-3727.
52. Spiers JG, Breda C, Robinson S, et al. Drosophila Nrf2/Keap1 mediated redox signaling supports synaptic function and longevity and impacts on circadian activity. Front Mol Neurosci, 2019, 12: 86.
53. Tsakiri EN, Gumeni S, Iliaki KK, et al. Hyperactivation of Nrf2 increases stress tolerance at the cost of aging acceleration due to metabolic deregulation. Aging Cell, 2019, 18(1): e12845.
54. Ahmed SM, Luo L, Namani A, et al. Nrf2 signaling pathway: pivotal roles in inflammation. Biochim Biophys Acta Mol Basis Dis, 2017, 1863(2): 585-597.
55. Perico L, Wyatt CM, Benigni A. A new BEACON of hope for the treatment of inflammation? The endogenous metabolite itaconate as an alternative activator of the KEAP1-Nrf2 system. Kidney Int, 2018, 94(4): 646-649.
56. Nagashima R, Kosai H, Masuo M, et al. Nrf2 suppresses allergic lung inflammation by attenuating the type 2 innate lymphoid cell response. J Immunol, 2019, 202(5): 1331-1339.
57. Lampiasi N, Montana G. An in vitro inflammation model to study the Nrf2 and NF-κB crosstalk in presence of ferulic acid as modulator. Immunobiology, 2018, 223(4/5): 349-355.
58. Chia AJ, Goldring CE, Kitteringham NR, et al. Differential effect of covalent protein modification and glutathione depletion on the transcriptional response of Nrf2 and NF-kappaB. Biochem Pharmacol, 2010, 80(3): 410-421.
59. Banning A, Brigelius-Flohé R. NF-kappaB, Nrf2, and HO-1 interplay in redox-regulated VCAM-1 expression. Antioxid Redox Signal, 2005, 7(7/8): 889-899.

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Progress on the role of nuclear factor-erythroid 2-related factor 2 in regulating cell proliferation

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