Nrf2 is essential for timely M phase entry of replicating hepatocytes during liver regeneration

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 308, Issue 4, 2015, Pages G262-G268

  Zou, Yuhong ^a   Hu, Min ^a,b   Lee, Joonyong ^a   Nambiar, Shashank Manohar ^a   Garcia, Veronica ^a   Bao, Qi ^a   Chan, Jefferson Y ^c   Dai, Guoli ^a  

^a Biology SL332   (United States)

^b ANHUI UNIVERSITY OF CHINESE MEDICINE   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Hepa tocyte proliferation; Hepatocyte mitosis; Nuclear factor erythroid 2 related factor 2

Indexed keywords

CYCLIN A2; CYCLIN B1; CYCLIN DEPENDENT KINASE 1; MESSENGER RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); TRANSCRIPTION FACTOR NRF2; CCNA2 PROTEIN, MOUSE; CCNB1 PROTEIN, MOUSE; CELL CYCLE PROTEIN; NFE2L2 PROTEIN, MOUSE; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE; WEE1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL DIVISION; CELL METABOLISM; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; DETOXIFICATION; DNA SYNTHESIS; G2 PHASE CELL CYCLE CHECKPOINT; GENE TARGETING; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIVER CELL; LIVER REGENERATION; MALE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; TRANSIENT TRANSFECTION; WESTERN BLOTTING; WILD TYPE; 129 MOUSE; ANIMAL; C57BL MOUSE; DEFICIENCY; GENE EXPRESSION REGULATION; GENETICS; KINETICS; KNOCKOUT MOUSE; LIVER; LIVER RESECTION; METABOLISM; MITOSIS; PATHOLOGY; SURGERY;

ANIMALS; CDC2 PROTEIN KINASE; CELL CYCLE PROTEINS; CELL DIVISION; CYCLIN A2; CYCLIN B1; GENE EXPRESSION REGULATION; HEPATECTOMY; HEPATOCYTES; KINETICS; LIVER; LIVER REGENERATION; MALE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOSIS; NF-E2-RELATED FACTOR 2; NUCLEAR PROTEINS; PROTEIN-TYROSINE KINASES; RNA, MESSENGER;

EID: 84922935931     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00332.2014     Document Type: Article

References (38)

1. Aleksunes LM, Slitt AL, Maher JM, Dieter MZ, Knight TR, Goedken M, Cherrington NJ, Chan JY, Klaassen CD, Manautou JE. Nuclear factor-E2-related factor 2 expression in liver is critical for induction of NAD(P)H:quinone oxidoreductase 1 during cholestasis. Cell Stress Chap-erones 11: 356–363, 2006.
2. Beyer TA, Xu W, Teupser D, auf dem Keller U, Bugnon P, Hildt E, Thiery J, Kan YW, Werner S. Impaired liver regeneration in Nrf2 knockout mice: role of ROS-mediated insulin/IGF-1 resistance. EMBO J 27: 212–223, 2008.
3. Bryan HK, Olayanju A, Goldring CE, Park BK. The Nrf2 cell defence pathway: Keap1-dependent and -independent mechanisms of regulation. Biochem Pharmacol 85: 705–717, 2013.
4. Buitrago-Molina LE, Marhenke S, Longerich T, Sharma AD, Bouk-ouris AE, Geffers R, Guigas B, Manns MP, Vogel A. The degree of liver injury determines the role of p21 in liver regeneration and hepato-carcinogenesis in mice. Hepatology 58: 1143–1152, 2013.
5. Chan K, Han XD, Kan YW. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc Natl Acad Sci USA 98: 4611–4616, 2001.
6. Chan K, Lu R, Chang JC, Kan YW. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci USA 93: 13943–13948, 1996.
7. Dai G, He L, Bu P, Wan YJ. Pregnane X receptor is essential for normal progression of liver regeneration. Hepatology 47: 1277–1287, 2008.
8. Dayoub R, Vogel A, Schuett J, Lupke M, Spieker SM, Kettern N, Hildt E, Melter M, Weiss TS. Nrf2 activates augmenter of liver regeneration (ALR) via antioxidant response element and links oxidative stress to liver regeneration. Mol Med 19: 237–244, 2013.
9. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K, Mangal D, Yu KH, Yeo CJ, Calhoun ES, Scrimieri F, Winter JM, Hruban RH, Iacobuzio-Donahue C, Kern SE, Blair IA, Tuveson DA. Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475: 106–109, 2011.
10. Fausto N, Campbell JS, Riehle KJ. Liver regeneration. Hepatology 43: S45–S53, 2006.
11. Fisher D, Krasinska L, Coudreuse D, Novak B. Phosphorylation network dynamics in the control of cell cycle transitions. J Cell Sci 125: 4703–4711, 2012.
12. Greene AK, Puder M. Partial hepatectomy in the mouse: technique and perioperative management. J Invest Surg 16: 99–102, 2003.
13. Hayes JD, Dinkova-Kostova AT. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism. Trends Biochem Sci 39: 199–218, 2014.
14. Hu R, Saw CL, Yu R, Kong AN. Regulation of NF-E2-related factor 2 signaling for cancer chemoprevention: antioxidant coupled with antiin-flammatory. Antioxid Redox Signal 13: 1679–1698, 2010.
15. 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 299: G1211–G1221, 2010.
16. Iida K, Itoh K, Kumagai Y, Oyasu R, Hattori K, Kawai K, Shimazui T, Akaza H, Yamamoto M. Nrf2 is essential for the chemopreventive efficacy of oltipraz against urinary bladder carcinogenesis. Cancer Res 64: 6424–6431, 2004.
17. Jaramillo MC, Zhang DD. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 27: 2179–2191, 2013.
18. Karaca G, Swiderska-Syn M, Xie G, Syn WK, Kruger L, Machado MV, Garman K, Choi SS, Michelotti GA, Burkly LC, Ochoa B, Diehl AM. TWEAK/Fn14 signaling is required for liver regeneration after partial hepatectomy in mice. PLoS ONE 9: e83987, 2014.
19. Khor TO, Huang MT, Prawan A, Liu Y, Hao X, Yu S, Cheung WK, Chan JY, Reddy BS, Yang CS, Kong AN. Increased susceptibility of Nrf2 knockout mice to colitis-associated colorectal cancer. Cancer Prev Res 1: 187–191, 2008.
20. Kohler UA, Kurinna S, Schwitter D, Marti A, Schafer M, Hellerbrand C, Speicher T, Werner S. Activated Nrf2 impairs liver regeneration in mice by activation of genes involved in cell cycle control and apoptosis. Hepatology 60: 670–678, 2014.
21. Liao Y, Shikapwashya ON, Shteyer E, Dieckgraefe BK, Hruz PW, Rudnick DA. Delayed hepatocellular mitotic progression and impaired liver regeneration in early growth response-1-deficient mice. J Biol Chem 279: 43107–43116, 2004.
22. Matsuo T, Yamaguchi S, Mitsui S, Emi A, Shimoda F, Okamura H. Control mechanism of the circadian clock for timing of cell division in vivo. Science 302: 255–259, 2003.
23. Michalopoulos GK. Liver regeneration after partial hepatectomy: critical analysis of mechanistic dilemmas. Am J Pathol 176: 2–13, 2010.
24. Michalopoulos GK. NRF2, not always friendly but perhaps misunderstood. Hepatology 60: 461–463, 2014.
25. Michalopoulos GK, DeFrances M. Liver regeneration. Adv Biochem Eng Biotechnol 93: 101–134, 2005.
26. Mitsuishi Y, Motohashi H, Yamamoto M. The Keap1-Nrf2 system in cancers: stress response and anabolic metabolism (Abstract). Frontier Oncol 2: 200, 2012.
27. Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, Yamamoto M, Motohashi H. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell 22: 66–79, 2012.
28. Miyaoka Y, Ebato K, Kato H, Arakawa S, Shimizu S, Miyajima A. Hypertrophy and unconventional cell division of hepatocytes underlie liver regeneration. Curr Biol 22: 1166–1175, 2012.
29. Parry DH, O’Farrell PH. The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Curr Biol 11: 671–683, 2001.
30. Ramos-Gomez M, Kwak MK, Dolan PM, Itoh K, Yamamoto M, Talalay P, Kensler TW. Sensitivity to carcinogenesis is increased and chemoprotective efficacy of enzyme inducers is lost in nrf2 transcription factor-deficient mice. Proc Natl Acad Sci USA 98: 3410–3415, 2001.
31. Sporn MB, Liby KT. NRF2 and cancer: the good, the bad and the importance of context. Nat Rev 12: 564–571, 2012.
32. Sullivan M, Morgan DO. Finishing mitosis, one step at a time. Nat Rev Mol Cell Biol 8: 894–903, 2007.
33. Wakabayashi N, Shin S, Slocum SL, Agoston ES, Wakabayashi J, Kwak MK, Misra V, Biswal S, Yamamoto M, Kensler TW. Regulation of notch1 signaling by nrf2: implications for tissue regeneration (Abstract). Sci Signal 3: 52, 2010.
34. Xu C, Huang MT, Shen G, Yuan X, Lin W, Khor TO, Conney AH, Kong AN. Inhibition of 7,12-dimethylbenz(a)anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2-related factor 2. Cancer Res 66: 8293–8296, 2006.
35. Yasutis KM, Kozminski KG. Cell cycle checkpoint regulators reach a zillion. Cell Cycle 12: 1501–1509, 2013.
36. Zou Y, Bao Q, Kumar S, Hu M, Wang GY, Dai G. Four waves of hepatocyte proliferation linked with three waves of hepatic fat accumulation during partial hepatectomy-induced liver regeneration. PLoS ONE 7: e30675, 2012.
37. Zou Y, Hu M, Bao Q, Chan JY, Dai G. Nrf2 participates in regulating maternal hepatic adaptations to pregnancy. J Cell Sci 126: 1618–1625, 2013.
38. Zou Y, Lee J, Nambiar SM, Hu M, Rui W, Bao Q, Chan JY, Dai G. Nrf2 Is Involved in Maintaining Hepatocyte Identity during Liver Regeneration. PLoS ONE 9: e107423, 2014.