Hepatocyte-specific deletion of heme oxygenase-1 disrupts redox homeostasis in Basal and oxidative environments

Tohoku Journal of Experimental Medicine

Volumn 216, Issue 4, 2008, Pages 331-339

  Mamiya, Takashi ^a   Katsuoka, Fumiki ^b   Hirayama, Aki ^c   Nakajima, Osamu ^a   Kobayashi, Akira ^a   Maher, Jonathan M ^b   Matsui, Hirofumi ^a   Hyodo, Ichinosuke ^a   Yamamoto, Masayuki ^a,b   Hosoya, Tomonori ^a  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Carbon tetrachloride; Heme oxygenase 1; In vivo EPR; Oxidative stress; Reactive oxygen species

Indexed keywords

CARBON TETRACHLORIDE; GLUTATHIONE TRANSFERASE P1; HEME OXYGENASE 1; RADICAL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE QUINONE 1; SCAVENGER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; FEMALE; GENETIC SUSCEPTIBILITY; HISTOPATHOLOGY; HOMEOSTASIS; IN VIVO STUDY; LIVER CELL; LIVER TOXICITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; SEROLOGY; ANIMAL; ANTIBODY SPECIFICITY; C57BL MOUSE; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; LIVER; LIVER DISEASE; METABOLISM; MOLECULAR CLONING; MOUSE MUTANT; OXIDATION REDUCTION REACTION; PATHOLOGY;

ANIMALS; CARBON TETRACHLORIDE; CLONING, MOLECULAR; FREE RADICAL SCAVENGERS; GENE DELETION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HEPATOCYTES; HOMEOSTASIS; LIVER; LIVER DISEASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGAN SPECIFICITY; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 59149086031     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1620/tjem.216.331     Document Type: Article

References (28)

1. Alam, J., Stewart, D., Touchard, C., Boinapally, S., Choi, A.M. & Cook, J.L. (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem., 274, 26071-26078.
2. Bauer, I., Wanner, G.A., Rensing, H., Alte, C., Miescher, E.A., Wolf, B., Pannen, B.H., Clemens, M.G. & Bauer, C. (2003) Expression pattern of heme oxygenase isoenzymes 1 and 2 in normal and stress-exposed rat liver. Hepatology, 27, 829-838.
3. 4 in the perfused rat liver and in vivo. J. Biol. Chem., 261, 4542-4548.
4. Eipel, C., Eisold, M., Schuett, H. & Vollmar, B. (2007) Inhibition of heme oxygenase-1 protects against tissue injury in carbon tetrachloride exposed livers. J. Surg. Res., 139, 113-120.
5. 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.
6. Furuyama, K., Kaneko, K. & Vargas, P.D. (2007) Heme as a magnificent molecule with multiple missions: heme determines its own fate and governs cellular homeostasis. Tohoku J. Exp. Med., 213, 1-16.
7. Gemsa, D., Woo, C.H., Fudenberg, H.H. & Schmid, R. (1974) Stimulation of heme oxygenase in macrophages and liver by endotoxin. J. Clin. Invest., 53, 647-651.
8. Hirayama, A., Yoh, K., Nagase, S., Ueda, A., Itoh, K., Morito, N., Hirayama, K., Takahashi, S., Yamamoto, M. & Koyama, A. (2003) EPR imaging of reducing activity in Nrf2 transcriptional factor-deficient mice. Free Radic. Biol. Med., 34, 1236-1242.
9. Hosoya, T., Oda, Y., Takahashi, S., Morita, M., Kawauchi, S., Ema, M., Yamamoto, M. & Fujii-Kuriyama, Y. (2001) Defective development of secretory neurones in the hypothalamus of Arnt2-knockout mice. Genes Cells, 6, 361-374.
10. 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.
11. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., Igarashi, K., Engel, J.D. & Yamamoto, M. (1999) Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the N-terminal Neh2 domain. Genes Dev., 13, 76-86.
12. Itoh, K., Tong, K.I. & Yamamoto, M. (2004) Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med., 36, 1208-1213.
13. Kato, H., Amersi, F., Buelow, R., Melinek, J., Coito, A.J., Ke, B., Busuttil, R.W. & Kupiec-Weglinski, J.W. (2001) Heme oxygenase-1 overexpression protects rat livers from ischemia/reperfusion injury with extended cold preservation. Am. J. Transplant., 1, 121-128.
14. Katsuoka, F., Motohashi, H., Ishii, T., Aburatani, H., Engel, J.D. & Yamamoto, M. (2005) Genetic evidence that small maf proteins are essential for the activation of antioxidant response element-dependent genes. Mol. Cell. Biol., 25, 8044-8051.
15. Kobayashi, M. & Yamamoto, M. (2005) Molecular mechanisms activating Nrf2-Keap1 pathway in regulation of antioxidant genes. Antioxidants Redox Signaling, 7, 384-395.
16. Keyse, S.M. & Tyrrell, R.M. (1989) Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl. Acad. Sci. USA, 86, 99-103.
17. Marquis, J.C. & Demple, B. (1998) Complex genetic response of human cells to sublethal levels of pure nitric oxide. Cancer Res., 58, 3435-3440.
18. Motohashi, H. & Yamamoto. M. (2004) Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol. Med., 10, 549-557.
19. Nakahira, K., Takahashi, T., Shimizu, H., Maeshima, K., Uehara, K., Fujii, H., Nakatsuka, H., Yokoyama, M., Akagi, R. & Morita, K. (2003) Protective role of heme oxygenase-1 induction in carbon tetrachloride-induced hepatotoxicity. Biochem. Pharmacol., 66, 1091-1105.
20. Otterbein, L.E., Mantell, L.L. & Choi, A.M. (1999) Carbon monoxide provides protection against hyperoxic lung injury. Am. J. Physiol., 276, L688-694.
21. Poss, K.D. & Tonegawa, S. (1997a) Heme oxygenase 1 is required for mammalian iron reutilization. Proc. Natl. Acad. Sci. USA, 94, 10919-10924.
22. Poss, K.D. & Tonegawa, S. (1997b) Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. USA, 94, 10925-10930.
23. Postic, C., Shiota, M., Niswender, K.D., Jetton, T.L., Chen, Y., Moates, J.M., Shelton. K.D., Lindner, J., Cherrington, A.D., & Magnuson, M.A. (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem., 274, 305-315.
24. 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.
25. Sun, J., Hoshino, H., Takaku, K., Nakajima, O., Muto, A., Suzuki, H., Tashiro, S., Takahashi, S., Shibahara, S., Alam, J., Taketo, M.M., Yamamoto, M. & Igarashi, K. (2002) Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J., 21, 5216-5224.
26. Stocker, R., Yamamoto, Y., McDonagh, A.F., Glazer, A.N. & Ames, B.N. (1987) Bilirubin is an antioxidant of possible physiological importance. Science, 235, 1043-1046.
27. Tong, K.I., Padmanabhan, B., Kobayashi, A., Shang, C., Hirotsu, Y., Yokoyama, S. & Yamamoto, M. (2007) Different electrostatic potentials define ETGE and DLG motifs as hinge and latch in oxidative stress response. Mol. Cell. Biol., 27, 7511-7521.
28. Vidal, F., Sage, J., Cuzin, F. & Rassoulzadegan, M. (1998) Cre expression in primary spermatocytes: a tool for genetic engineering of the germ line. Mol. Reprod. Dev., 51, 274-280.