Notch-Nrf2 axis: Regulation of Nrf2 gene expression and cytoprotection by notch signaling

Molecular and Cellular Biology

Volumn 34, Issue 4, 2014, Pages 653-663

  Wakabayashi, Nobunao ^a   Skoko, John J ^a,c   Chartoumpekis, Dionysios V ^a   Kimura, Shoko ^a   Slocum, Stephen L ^a,d   Noda, Kentaro ^b   Palliyaguru, Dushani L ^a   Fujimuro, Masahiro ^f   Boley, Patricia A ^a   Tanaka, Yugo ^b   Shigemura, Norihisa ^b   Biswal, Shyam ^e   Yamamoto, Masayuki ^g   Kensler, Thomas W ^a,c,d,e  

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

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^g TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; NOTCH RECEPTOR; PARACETAMOL; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENOTYPE; HEPATOMEGALY; INTRAHEPATIC BILE DUCT; LIVER DEVELOPMENT; LIVER PROTECTION; LIVER TOXICITY; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION INITIATION;

ANIMALS; CELL DIFFERENTIATION; CYTOPROTECTION; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; LIVER; MICE; MICE, TRANSGENIC; NF-E2-RELATED FACTOR 2; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 84892956594     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01408-13     Document Type: Article

References (48)

1. Kensler TW, Wakabayashi N, Biswal S. 2007. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47:89-116. http://dx.doi.org/10.1146/annurev.pharmtox.46 .120604.141046.
2. Itoh K, Mimura J, Yamamoto M. 2010. Discovery of the negative regulator of Nrf2, Keap1: a historical overview. Antioxid. Redox Signal. 13: 1665-1678. http://dx.doi.org/10.1089/ars.2010.3222.
3. Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, O'Connor T, Harada T, Yamamoto M. 2001. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol. Sci. 59:169-177. http://dx.doi.org/10.1093/toxsci/59.1.169.
4. Okawa H, Motohashi H, Kobayashi A, Aburatani H, Kensler TW, Yamamoto M. 2006. Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity. Biochem. Biophys. Res. Commun. 339:79-88. http://dx.doi.org/10.1016 /j.bbrc.2005.10.185.
5. Taguchi K, Maher JM, Suzuki T, Kawatani Y, Motohashi H, Yamamoto M. 2010. Genetic analysis of cytoprotective functions supported by graded expression of Keap1. Mol. Cell. Biol. 30:3016-3026. http://dx.doi.org/10 .1128/MCB.01591-09.
6. Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW. 2010. When NRF2 talks, who's listening? Antioxid. Redox Signal. 13:1649-1663. http: //dx.doi.org/10.1089/ars.2010.3216.
7. Beyer TA, Werner S. 2008. The cytoprotective Nrf2 transcription factor controls insulin receptor signaling in the regenerating liver. Cell Cycle 7:874-878. http://dx.doi.org/10.4161/cc.7.7.5617.
8. Artavanis-Tsakonas S, Rand MD, Lake RJ. 1999. Notch signaling: cell fate control and signal integration in development. Science 284:770-776. http://dx.doi.org/10.1126/science.284.5415.770.
9. Croquelois A, Blindenbacher A, Terracciano L, Wang X, Langer I, Radtke F, Heim MH. 2005. Inducible inactivation of Notch1 causes nodular regenerative hyperplasia in mice. Hepatology 41:487-496. http: //dx.doi.org/10.1002/hep.20571.
10. Geisler F, Nagl F, Mazur PK, Lee M, Zimber-Strobl U, Strobl LJ, Radtke F, Schmid RM, Siveke JT. 2008. Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology 48:607-616. http://dx.doi.org/10.1002/hep.22381.
11. Alam J. 2006. The mammalian Cap and Collar family of transcription factors. Antioxid. Redox Signal. 8:39-42. http://dx.doi.org/10.1089/ars .2006.8.39.
12. Wakabayashi N, Shin S, Slocum SL, Agoston ES, Wakabayashi J, Kwak MK, Misra V, Biswal S, Yamamoto M, Kensler TW. 2010. Regulation of notch1 signaling by nrf2: implications for tissue regeneration. Sci. Signal. 3:ra52. http://dx.doi.org/10.1126/scisignal.2000762.
13. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA. 2003. Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. U. S. A. 100:14920-14925. http://dx.doi.org/10.1073/pnas.2436557100.
14. Postic C, Magnuson MA. 2000. DNA excision in liver by an albumin-Cre transgene occurs progressively with age. Genesis 26:149-150. http://dx .doi.org/10.1002/(SICI)1526-968X(200002)26:2149::AID-GENE16 3 .0.CO;2-V.
15. Reddy NM, Potteti HR, Mariani TJ, Biswal S, Reddy SP. 2011. Conditional deletion of Nrf2 in airway epithelium exacerbates acute lung injury and impairs the resolution of inflammation. Am. J. Respir. Cell Mol. Biol. 45:1161-1168. http://dx.doi.org/10.1165/rcmb.2011-0144OC.
16. Song YK, Liu F, Zhang G, Liu D. 2002. Hydrodynamics-based transfection: simple and efficient method for introducing and expressing transgenes in animals by intravenous injection of DNA. Methods Enzymol. 346:92-105. http://dx.doi.org/10.1016/S0076-6879(02)46050-8.
17. Wakabayashi N, Dinkova-Kostova AT, Holtzclaw WD, Kang MI, Kobayashi A, Yamamoto M, Kensler TW, Talalay P. 2004. Protection against electrophile and oxidant stress by induction of the phase 2 response: fate of cysteines of the Keap1 sensor modified by inducers. Proc. Natl. Acad. Sci. U. S. A. 101:2040-2045. http://dx.doi.org/10.1073/pnas .0307301101.
18. Kwak MK, Itoh K, Yamamoto M, Kensler TW. 2002. 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. 22:2883-2892. http://dx.doi.org/10.1128/MCB.22.9.2883 -2892.2002.
19. Chen C, Okayama H. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
20. Dignam JD, Lebovitz RM, Roeder RG. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489. http://dx.doi.org/10 .1093/nar/11.5.1475.
21. Wells J, Farnham PJ. 2002. Characterizing transcription factor binding sites using formaldehyde crosslinking and immunoprecipitation. Methods 26:48-56. http://dx.doi.org/10.1016/S1046-2023(02)00007-5.
22. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. http://dx.doi.org/10.1093 /nar/29.9.e45.
23. Tun T, Hamaguchi Y, Matsunami N, Furukawa T, Honjo T, Kawaichi M. 1994. Recognition sequence of a highly conserved DNA binding protein RBP-J kappa. Nucleic Acids Res. 22:965-971. http://dx.doi.org/10 .1093/nar/22.6.965.
24. Hayward SD, Liu J, Fujimuro M. 2006. Notch and Wnt signaling: mimicry and manipulation by gamma herpesviruses. Sci. STKE 2006:re4. http: //dx.doi.org/10.1126/stke.3352006re4.
25. Zimber-Strobl U, Strobl LJ, Meitinger C, Hinrichs R, Sakai T, Furukawa T, Honjo T, Bornkamm GW. 1994. Epstein-Barr virus nuclear antigen 2 exerts its transactivating function through interaction with recombination signal binding protein RBP-J kappa, the homologue of Drosophila Suppressor of Hairless. EMBO J. 13:4973-4982.
26. Hsieh JJ, Henkel T, Salmon P, Robey E, Peterson MG, Hayward SD. 1996. Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol. Cell. Biol. 16:952-959.
27. Sakai T, Taniguchi Y, Tamura K, Minoguchi S, Fukuhara T, Strobl LJ, Zimber-Strobl U, Bornkamm GW, Honjo T. 1998. Functional replacement of the intracellular region of the Notch1 receptor by Epstein-Barr virus nuclear antigen 2. J. Virol. 72:6034-6039.
28. Kwak MK, Wakabayashi N, Itoh K, Motohashi H, Yamamoto M, Kensler TW. 2003. Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J. Biol. Chem. 278:8135-8145. http: //dx.doi.org/10.1074/jbc.M211898200.
29. Katoh M, Katoh M. 2007. Notch signaling in gastrointestinal tract (review). Int. J. Oncol. 30:247-251. http://www.spandidos-publications.com /ijo/30/1/247.
30. Komatsu M. 2012. Liver autophagy: physiology and pathology. J. Biochem. 152:5-15. http://dx.doi.org/10.1093/jb/mvs059.
31. Taguchi K, Fujikawa N, Komatsu M, Ishii T, Unno M, Akaike T, Motohashi H, Yamamoto M. 2012. Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc. Natl. Acad. Sci. U. S. A. 109:13561-13566. http://dx.doi.org/10.1073/pnas.1121572109.
32. Sparks EE, Huppert KA, Brown MA, Washington MK, Huppert SS. 2010. Notch signaling regulates formation of the three-dimensional architecture of intrahepatic bile ducts in mice. Hepatology 51:1391-1400. http: //dx.doi.org/10.1002/hep.23431.
33. Chan K, Han XD, Kan YW. 2001. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc. Natl. Acad. Sci. U. S. A. 98:4611- 4616. http://dx.doi.org/10.1073/pnas .081082098.
34. Aleksunes LM, Slitt AL, Maher JM, Augustine LM, Goedken MJ, Chan JY, Cherrington NJ, Klaassen CD, Manautou JE. 2008. Induction of Mrp3 and Mrp4 transporters during acetaminophen hepatotoxicity is dependent on Nrf2. Toxicol. Appl. Pharmacol. 226:74-83. http://dx.doi.org /10.1016/j.taap.2007.08.022.
35. Reisman SA, Buckley DB, Tanaka Y, Klaassen CD. 2009. CDDO-Im protects from acetaminophen hepatotoxicity through induction of Nrf2- dependent genes. Toxicol. Appl. Pharmacol. 236:109-114. http://dx.doi .org/10.1016/j.taap.2008.12.024.
36. Komatsu M, Kurokawa H, Waguri S, Taguchi K, Kobayashi A, Ichimura Y, Sou YS, Ueno I, Sakamoto A, Tong KI, Kim M, Nishito Y, Iemura S, Natsume T, Ueno T, Kominami E, Motohashi H, Tanaka K, Yamamoto M. 2010. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12:213-223. http://dx.doi.org/10.1038/ncb2021.
37. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169:425-434. http://dx.doi.org/10.1083 /jcb.200412022.
38. Gupta-Rossi N, Le Bail O, Gonen H, Brou C, Logeat F, Six E, Ciechanover A, Israel A. 2001. Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J. Biol. Chem. 276:34371-34378. http://dx.doi.org/10.1074/jbc.M101343200.
39. Sparks EE, Perrien DS, Huppert KA, Peterson TE, Huppert SS. 2011. Defects in hepatic Notch signaling result in disruption of the communicating intrahepatic bile duct network in mice. Dis. Model. Mech. 4:359- 367. http://dx.doi.org/10.1242/dmm.005793.
40. Kraman M, McCright B. 2005. Functional conservation of Notch1 and Notch2 intracellular domains. FASEB J. 19:1311-1313. http://dx.doi.org /10.1096/fj.04-3407fje.
41. Louis AA, Van Eyken P, Haber BA, Hicks C, Weinmaster G, Taub R, Rand EB. 1999. Hepatic jagged1 expression studies. Hepatology 30:1269- 1275. http://dx.doi.org/10.1002/hep.510300512.
42. Okada K, Shoda J, Taguchi K, Maher JM, Ishizaki K, Inoue Y, Ohtsuki M, Goto N, Sugimoto H, Utsunomiya H, Oda K, Warabi E, Ishii T, Yamamoto M. 2009. Nrf2 counteracts cholestatic liver injury via stimulation of hepatic defense systems. Biochem. Biophys. Res. Commun. 389: 431-436. http://dx.doi.org/10.1016/j.bbrc.2009.08.156.
43. Tan KP, Wood GA, Yang M, Ito S. 2010. Participation of nuclear factor (erythroid 2-related), factor 2 in ameliorating lithocholic acid-induced cholestatic liver injury in mice. Br. J. Pharmacol. 161:1111-1121. http://dx .doi.org/10.1111/j.1476-5381.2010.00953.x.
44. Weerachayaphorn J, Mennone A, Soroka CJ, Harry K, Hagey LR, Kensler TW, Boyer JL. 2012. Nuclear factor-E2-related factor 2 is a major determinant of bile acid homeostasis in the liver and intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 302:G925-G936. http://dx.doi.org/10 .1152/ajpgi.00263.2011.
45. Gridley T. 2004. Kick it up a Notch: NOTCH1 activation in T-ALL. Cancer Cell 6:431-432. http://dx.doi.org/10.1016/j.ccr.2004.10.019.
46. Radtke F, Raj K. 2003. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat. Rev. Cancer 3:756-767. http://dx.doi.org/10 .1038/nrc1186.
47. Kensler TW, Wakabayashi N. 2010. Nrf2: friend or foe for chemoprevention? Carcinogenesis 31:90-99. http://dx.doi.org/10.1093/carcin/bgp231.
48. Taguchi K, Motohashi H, Yamamoto M. 2011. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 16:123-140. http://dx.doi.org/10.1111/j.1365-2443.2010.01473.x.