Distinct Regulations of HO-1 Gene Expression for Stress Response and Substrate Induction

REFERENCES

• Kikuchi G, Yoshida T, Noguchi M. 2005. Heme oxygenase and heme degradation. Biochem Biophys Res Commun 338:558–567. https://doi.org/10.1016/j.bbrc.2005.08.020.
   PubMed Web of Science ®Google Scholar
• Cruse I, Maines MD. 1988. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J Biol Chem 263:3348–3353. https://doi.org/10.1016/S0021-9258(18)69078-7.
   PubMed Web of Science ®Google Scholar
• Shibahara S. 2003. The heme oxygenase dilemma in cellular homeostasis: new insights for the feedback regulation of heme catabolism. Tohoku J Exp Med 200:167–186. https://doi.org/10.1620/tjem.200.167.
   PubMed Web of Science ®Google Scholar
• Ryter SW, Alam J, Choi AM. 2006. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86:583–650. https://doi.org/10.1152/physrev.00011.2005.
   PubMed Web of Science ®Google Scholar
• Itoh K, Igarashi K, Hayashi N, Nishizawa M, Yamamoto M. 1995. Cloning and characterization of a novel erythroid cell-derived CNC family transcription factor heterodimerizing with the small Maf family proteins. Mol Cell Biol 15:4184–4193. https://doi.org/10.1128/MCB.15.8.4184.
   PubMed Web of Science ®Google Scholar
• Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, Oyake T, Hayashi N, Satoh K, Hatayama I, Yamamoto M, Nabeshima Y. 1997. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 236:313–322. https://doi.org/10.1006/bbrc.1997.6943.
   PubMed Web of Science ®Google Scholar
• Ishii T, Itoh K, Takahashi S, Sato H, Yanagawa T, Katoh Y, Bannai S, Yamamoto M. 2000. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 275:16023–16029. https://doi.org/10.1074/jbc.275.21.16023.
   PubMed Web of Science ®Google Scholar
• Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. 1999. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13:76–86. https://doi.org/10.1101/gad.13.1.76.
   PubMed Web of Science ®Google Scholar
• Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, Yamamoto M. 2003. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 35:238–245. https://doi.org/10.1038/ng1248.
   PubMed Web of Science ®Google Scholar
• Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, Yamamoto M. 2004. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 24:7130–7139. https://doi.org/10.1128/MCB.24.16.7130-7139.2004.
   PubMed Web of Science ®Google Scholar
• Baird L, Yamamoto M. 2020. The molecular mechanisms regulating the KEAP1-NRF2 pathway. Mol Cell Biol 40:e00099-20. https://doi.org/10.1128/MCB.00099-20.
   PubMed Web of Science ®Google Scholar
• Otsuki A, Yamamoto M. 2020. Cis-element architecture of Nrf2-sMaf heterodimer binding sites and its relation to diseases. Arch Pharm Res 43:275–285. https://doi.org/10.1007/s12272-019-01193-2.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Motohashi H, Yamamoto M. 2013. Toward clinical application of the Keap1-Nrf2 pathway. Trends Pharmacol Sci 34:340–346. https://doi.org/10.1016/j.tips.2013.04.005.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Kensler TW, Motohashi H. 2018. The KEAP1-NRF2 system: a thiol-based sensor-effector apparatus for maintaining redox homeostasis. Physiol Rev 98:1169–1203. https://doi.org/10.1152/physrev.00023.2017.
   PubMed Web of Science ®Google Scholar
• Liby K, Hock T, Yore MM, Suh N, Place AE, Risingsong R, Williams CR, Royce DB, Honda T, Honda Y, Gribble GW, Hill-Kapturczak N, Agarwal A, Sporn MB. 2005. The synthetic triterpenoids, CDDO and CDDO-imidazolide, are potent inducers of heme oxygenase-1 and Nrf2/ARE signaling. Cancer Res 65:4789–4798. https://doi.org/10.1158/0008-5472.CAN-04-4539.
   PubMed Web of Science ®Google Scholar
• Yates MS, Tauchi M, Katsuoka F, Flanders KC, Liby KT, Honda T, Gribble GW, Johnson DA, Johnson JA, Burton NC, Guilarte TR, Yamamoto M, Sporn MB, Kensler TW. 2007. Pharmacodynamic characterization of chemopreventive triterpenoids as exceptionally potent inducers of Nrf2-regulated genes. Mol Cancer Ther 6:154–162. https://doi.org/10.1158/1535-7163.MCT-06-0516.
   PubMed Web of Science ®Google Scholar
• Bomprezzi R. 2015. Dimethyl fumarate in the treatment of relapsing-remitting multiple sclerosis: an overview. Ther Adv Neurol Disord 8:20–30. https://doi.org/10.1177/1756285614564152.
   PubMed Web of Science ®Google Scholar
• Cao M, Onyango EO, Williams CR, Royce DB, Gribble GW, Sporn MB, Liby KT. 2015. Novel synthetic pyridyl analogues of CDDO-imidazolide are useful new tools in cancer prevention. Pharmacol Res 100:135–147. https://doi.org/10.1016/j.phrs.2015.07.024.
   PubMed Web of Science ®Google Scholar
• Kikuchi G, Yoshida T. 1983. Function and induction of the microsomal heme oxygenase. Mol Cell Biochem 53–54:163–183. https://doi.org/10.1007/BF00225252.
   PubMed Web of Science ®Google Scholar
• Christodoulides N, Durante W, Kroll MH, Schafer AI. 1995. Vascular smooth muscle cell heme oxygenases generate guanylyl cyclase-stimulatory carbon monoxide. Circulation 91:2306–2309. https://doi.org/10.1161/01.cir.91.9.2306.
   PubMed Web of Science ®Google Scholar
• Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C, Sassa S, Hayashi N, Yamamoto M, Shibahara S, Fujita H, Igarashi K. 2001. Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J 20:2835–2843. https://doi.org/10.1093/emboj/20.11.2835.
   PubMed Web of Science ®Google Scholar
• Sun J, Brand M, Zenke Y, Tashiro S, Groudine M, Igarashi K. 2004. Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network. Proc Natl Acad Sci USA 101:1461–1466. https://doi.org/10.1073/pnas.0308083100.
   PubMed Web of Science ®Google Scholar
• Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, Taketo MM, Yamamoto M, Igarashi K. 2002. Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J 21:5216–5224. https://doi.org/10.1093/emboj/cdf516.
   PubMed Web of Science ®Google Scholar
• Suzuki H, Tashiro S, Hira S, Sun J, Yamazaki C, Zenke Y, Ikeda-Saito M, Yoshida M, Igarashi K. 2004. Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1. EMBO J 23:2544–2553. https://doi.org/10.1038/sj.emboj.7600248.
   PubMed Web of Science ®Google Scholar
• Zenke-Kawasaki Y, Dohi Y, Katoh Y, Ikura T, Ikura M, Asahara T, Tokunaga F, Iwai K, Igarashi K. 2007. Heme induces ubiquitination and degradation of the transcription factor Bach1. Mol Cell Biol 27:6962–6971. https://doi.org/10.1128/MCB.02415-06.
   PubMed Web of Science ®Google Scholar
• Lignitto L, LeBoeuf SE, Homer H, Jiang S, Askenazi M, Karakousi TR, Pass HI, Bhutkar AJ, Tsirigos A, Ueberheide B, Sayin VI, Papagiannakopoulos T, Pagano M. 2019. Nrf2 activation promotes lung cancer metastasis by inhibiting the degradation of Bach1. Cell 178:316–329.e318. https://doi.org/10.1016/j.cell.2019.06.003.
   PubMed Web of Science ®Google Scholar
• Kohyama M, Ise W, Edelson BT, Wilker PR, Hildner K, Mejia C, Frazier WA, Murphy TL, Murphy KM. 2009. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457:318–321. https://doi.org/10.1038/nature07472.
   PubMed Web of Science ®Google Scholar
• Gozzelino R, Soares MP. 2014. Coupling heme and iron metabolism via ferritin H chain. Antioxid Redox Signal 20:1754–1769. https://doi.org/10.1089/ars.2013.5666.
   PubMed Web of Science ®Google Scholar
• Casares L, García V, Garrido-Rodríguez M, Millán E, Collado JA, García-Martín A, Peñarando J, Calzado MA, de la Vega L, Muñoz E. 2020. Cannabidiol induces antioxidant pathways in keratinocytes by targeting BACH1. Redox Biol 28:101321. https://doi.org/10.1016/j.redox.2019.101321.
   PubMed Web of Science ®Google Scholar
• Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, Choi AM. 1997. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272:5375–5381. https://doi.org/10.1074/jbc.272.9.5375.
   PubMed Web of Science ®Google Scholar
• Taketani S, Kohno H, Yoshinaga T, Tokunaga R. 1988. Induction of heme oxygenase in rat hepatoma cells by exposure to heavy metals and hyperthermia. Biochem Int 17:665–672.
   PubMedGoogle Scholar
• Christova TY, Gorneva GA, Taxirov SI, Duridanova DB, Setchenska MS. 2003. Effect of cisplatin and cobalt chloride on antioxidant enzymes in the livers of Lewis lung carcinoma-bearing mice: protective role of heme oxygenase. Toxicol Lett 138:235–242. https://doi.org/10.1016/s0378-4274(02)00416-2.
   PubMed Web of Science ®Google Scholar
• Kaliman PA, Nikitchenko IV, Sokol OA, Strel'chenko EV. 2001. Regulation of heme oxygenase activity in rat liver during oxidative stress induced by cobalt chloride and mercury chloride. Biochemistry (Mosc) 66:77–82. https://doi.org/10.1023/a:1002889814723.
   PubMed Web of Science ®Google Scholar
• Loboda A, Jazwa A, Wegiel B, Jozkowicz A, Dulak J. 2005. Heme oxygenase-1-dependent and -independent regulation of angiogenic genes expression: effect of cobalt protoporphyrin and cobalt chloride on VEGF and IL-8 synthesis in human microvascular endothelial cells. Cell Mol Biol (Noisy-le-grand) 51:347–355.
   PubMed Web of Science ®Google Scholar
• Muñoz-Sánchez J, Chánez-Cárdenas ME. 2019. The use of cobalt chloride as a chemical hypoxia model. J Appl Toxicol 39:556–570. https://doi.org/10.1002/jat.3749.
   PubMed Web of Science ®Google Scholar
• Tomaro ML, Frydman J, Frydman RB. 1991. Heme oxygenase induction by CoCl2, Co-protoporphyrin IX, phenylhydrazine, and diamide: evidence for oxidative stress involvement. Arch Biochem Biophys 286:610–617. https://doi.org/10.1016/0003-9861(91)90088-z.
   PubMed Web of Science ®Google Scholar
• Gong P, Hu B, Stewart D, Ellerbe M, Figueroa YG, Blank V, Beckman BS, Alam J. 2001. Cobalt induces heme oxygenase-1 expression by a hypoxia-inducible factor-independent mechanism in Chinese hamster ovary cells: regulation by Nrf2 and MafG transcription factors. J Biol Chem 276:27018–27025. https://doi.org/10.1074/jbc.M103658200.
   PubMed Web of Science ®Google Scholar
• Zhang W, Feng JQ, Harris SE, Contag PR, Stevenson DK, Contag CH. 2001. Rapid in vivo functional analysis of transgenes in mice using whole body imaging of luciferase expression. Transgenic Res 10:423–434. https://doi.org/10.1023/a:1012042506002.
   PubMed Web of Science ®Google Scholar
• Mamiya T, Katsuoka F, Hirayama A, Nakajima O, Kobayashi A, Maher JM, Matsui H, Hyodo I, Yamamoto M, Hosoya T. 2008. Hepatocyte-specific deletion of heme oxygenase-1 disrupts redox homeostasis in basal and oxidative environments. Tohoku J Exp Med 216:331–339. https://doi.org/10.1620/tjem.216.331.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Kelly VP, Motohashi H, Nakajima O, Takahashi S, Nishimura S, Yamamoto M. 2008. Deletion of the selenocysteine tRNA gene in macrophages and liver results in compensatory gene induction of cytoprotective enzymes by Nrf2. J Biol Chem 283:2021–2030. https://doi.org/10.1074/jbc.M708352200.
   PubMed Web of Science ®Google Scholar
• Niwa H, Araki K, Kimura S, Taniguchi S, Wakasugi S, Yamamura K. 1993. An efficient gene-trap method using poly A trap vectors and characterization of gene-trap events. J Biochem 113:343–349. https://doi.org/10.1093/oxfordjournals.jbchem.a124049.
   PubMed Web of Science ®Google Scholar
• Poss KD, Tonegawa S. 1997. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci USA 94:10925–10930. https://doi.org/10.1073/pnas.94.20.10925.
   PubMed Web of Science ®Google Scholar
• Numata I, Okuyama R, Memezawa A, Ito Y, Takeda K, Furuyama K, Shibahara S, Aiba S. 2009. Functional expression of heme oxygenase-1 in human differentiated epidermis and its regulation by cytokines. J Invest Dermatol 129:2594–2603. https://doi.org/10.1038/jid.2009.119.
   PubMed Web of Science ®Google Scholar
• Igarashi K, Sun J. 2006. The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation. Antioxid Redox Signal 8:107–118. https://doi.org/10.1089/ars.2006.8.107.
   PubMed Web of Science ®Google Scholar
• Haldar M, Kohyama M, So AY, Kc W, Wu X, Briseño CG, Satpathy AT, Kretzer NM, Arase H, Rajasekaran NS, Wang L, Egawa T, Igarashi K, Baltimore D, Murphy TL, Murphy KM. 2014. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156:1223–1234. https://doi.org/10.1016/j.cell.2014.01.069.
   PubMed Web of Science ®Google Scholar
• Suzuki N, Matsuo-Tezuka Y, Sasaki Y, Sato K, Miyauchi K, Kato K, Saito S, Shimonaka Y, Hirata M, Yamamoto M. 2018. Iron attenuates erythropoietin production by decreasing hypoxia-inducible transcription factor 2α concentrations in renal interstitial fibroblasts. Kidney Int 94:900–911. https://doi.org/10.1016/j.kint.2018.06.028.
   PubMed Web of Science ®Google Scholar
• Waza AA, Hamid Z, Ali S, Bhat SA, Bhat MA. 2018. A review on heme oxygenase-1 induction: is it a necessary evil. Inflamm Res 67:579–588. https://doi.org/10.1007/s00011-018-1151-x.
   PubMed Web of Science ®Google Scholar
• Zhang J, Ohta T, Maruyama A, Hosoya T, Nishikawa K, Maher JM, Shibahara S, Itoh K, Yamamoto M. 2006. BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress. Mol Cell Biol 26:7942–7952. https://doi.org/10.1128/MCB.00700-06.
   PubMed Web of Science ®Google Scholar
• Zhang J, Hosoya T, Maruyama A, Nishikawa K, Maher JM, Ohta T, Motohashi H, Fukamizu A, Shibahara S, Itoh K, Yamamoto M. 2007. Nrf2 Neh5 domain is differentially utilized in the transactivation of cytoprotective genes. Biochem J 404:459–466. https://doi.org/10.1042/BJ20061611.
   PubMed Web of Science ®Google Scholar
• Maruyama A, Mimura J, Harada N, Itoh K. 2013. Nrf2 activation is associated with Z-DNA formation in the human HO-1 promoter. Nucleic Acids Res 41:5223–5234. https://doi.org/10.1093/nar/gkt243.
   PubMed Web of Science ®Google Scholar
• Maruyama A, Mimura J, Itoh K. 2014. Non-coding RNA derived from the region adjacent to the human HO-1 E2 enhancer selectively regulates HO-1 gene induction by modulating Pol II binding. Nucleic Acids Res 42:13599–13614. https://doi.org/10.1093/nar/gku1169.
   PubMed Web of Science ®Google Scholar
• Lathrop JT, Timko MP. 1993. Regulation by heme of mitochondrial protein transport through a conserved amino acid motif. Science 259:522–525. https://doi.org/10.1126/science.8424176.
   PubMed Web of Science ®Google Scholar
• Paine A, Eiz-Vesper B, Blasczyk R, Immenschuh S. 2010. Signaling to heme oxygenase-1 and its anti-inflammatory therapeutic potential. Biochem Pharmacol 80:1895–1903. https://doi.org/10.1016/j.bcp.2010.07.014.
   PubMed Web of Science ®Google Scholar
• Alam J, Cook JL. 2007. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 36:166–174. https://doi.org/10.1165/rcmb.2006-0340TR.
   PubMed Web of Science ®Google Scholar
• Koizumi S, Gong P, Suzuki K, Murata M. 2007. Cadmium-responsive element of the human heme oxygenase-1 gene mediates heat shock factor 1-dependent transcriptional activation. J Biol Chem 282:8715–8723. https://doi.org/10.1074/jbc.M609427200.
   PubMed Web of Science ®Google Scholar
• Alam J, Den Z. 1992. Distal AP-1 binding sites mediate basal level enhancement and TPA induction of the mouse heme oxygenase-1 gene. J Biol Chem 267:21894–21900. https://doi.org/10.1016/S0021-9258(19)36696-7.
   PubMed Web of Science ®Google Scholar
• Lavrovsky Y, Schwartzman ML, Levere RD, Kappas A, Abraham NG. 1994. Identification of binding sites for transcription factors NF-kappa B and AP-2 in the promoter region of the human heme oxygenase 1 gene. Proc Natl Acad Sci USA 91:5987–5991. https://doi.org/10.1073/pnas.91.13.5987.
   PubMed Web of Science ®Google Scholar
• Peterson SJ, Rubinstein R, Faroqui M, Raza A, Boumaza I, Zhang Y, Stec D, Abraham NG. 2019. Positive effects of heme oxygenase upregulation on adiposity and vascular dysfunction: gene targeting vs. pharmacologic therapy. Int J Mol Sci 20:2514. https://doi.org/10.3390/ijms20102514.
   PubMed Web of Science ®Google Scholar
• McMahon M, Ding S, Acosta-Jimenez LP, Frangova TG, Henderson CJ, Wolf CR. 2018. Measuring in vivo responses to endogenous and exogenous oxidative stress using a novel haem oxygenase 1 reporter mouse. J Physiol 596:105–127. https://doi.org/10.1113/JP274915.
   PubMed Web of Science ®Google Scholar
• Kanda H, Yamawaki K. 2020. Bardoxolone methyl: drug development for diabetic kidney disease. Clin Exp Nephrol 24:857–864. https://doi.org/10.1007/s10157-020-01917-5.
   PubMed Web of Science ®Google Scholar
• Saito R, Suzuki T, Hiramoto K, Asami S, Naganuma E, Suda H, Iso T, Yamamoto H, Morita M, Baird L, Furusawa Y, Negishi T, Ichinose M, Yamamoto M. 2016. Characterizations of three major cysteine sensors of Keap1 in stress response. Mol Cell Biol 36:271–284. https://doi.org/10.1128/MCB.00868-15.
   PubMed Web of Science ®Google Scholar
• Clausen BE, Burkhardt C, Reith W, Renkawitz R, Förster I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8:265–277. https://doi.org/10.1023/a:1008942828960.
   PubMed Web of Science ®Google Scholar