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Originally published In Press as doi:10.1074/jbc.M209939200 on January 2, 2003

J. Biol. Chem., Vol. 278, Issue 11, 9125-9133, March 14, 2003
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Bach1 Functions as a Hypoxia-inducible Repressor for the Heme Oxygenase-1 Gene in Human Cells*

Tomomi KitamuroDagger , Kazuhiro TakahashiDagger , Kazuhiro OgawaDagger §, Reiko Udono-FujimoriDagger , Kazuhisa TakedaDagger , Kazumichi FuruyamaDagger , Masaharu NakayamaDagger , Jiying SunDagger ||, Hiroyoshi Fujita§, Wataru Hida**, Toshio HattoriDagger Dagger , Kunio Shirato§§, Kazuhiko Igarashi||, and Shigeki ShibaharaDagger ¶¶

From the Dagger  Department of Molecular Biology and Applied Physiology, Tohoku University School of Medicine, Sendai 980-8575, Japan, the § Laboratory of Environmental Biology, Hokkaido University School of Medicine, Sapporo 060-8638, Japan, the || Department of Medical Chemistry, Hiroshima University School of Medicine, Hiroshima 734-8551, Japan, the ** Health Administration Center, Tohoku University, Sendai 980-8576, Japan, and the Departments of Dagger Dagger  Respiratory and Infectious Diseases and §§ Cardiovascular Medicine, Tohoku University School of Medicine, Sendai 980-8574, Japan

Heme oxygenase 1 (HO-1) catalyzes heme breakdown, eventually releasing iron, carbon monoxide, and bilirubin IXalpha . HO-1 is induced by its substrate heme and various environmental factors, which represents a protective response against oxidative stresses. Here we show that hypoxia represses HO-1 expression in three human cell types but induces it in rat, bovine, and monkey cells, indicating the inter-species difference in the hypoxic regulation of HO-1 expression. The hypoxia-mediated repression of HO-1 expression is consistently associated with the induction of Bach1, a heme-regulated transcriptional repressor, in human cells. Bach1 is a basic leucine zipper protein, forming a heterodimer with a small Maf protein. Expression of HO-1 was also reduced in human cells when exposed to interferon-gamma or an iron chelator desferrioxamine, each of which induced Bach1 expression. In contrast, induction of HO-1 expression by CoCl2 is associated with reduced expression of Bach1 mRNA. Thus, expression of HO-1 and Bach1 is inversely regulated. We have identified a Maf recognition element in the human HO-1 gene that is required for repression of a reporter gene by hypoxia and targeted by Bach1. Therefore, Bach1 functions as a hypoxia-inducible repressor for the HO-1 gene, thereby contributing to fine-tuning of oxygen homeostasis in human cells.

* This study was supported by grants-in-aid for Scientific Research (B), for Exploratory Research, and for Scientific Research on Priority Areas from the Ministry of Education, Science, Sports and Culture of Japan, and by a grant provided by the Uehara Memorial Foundation.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

This paper is dedicated to the late emeritus Prof. Tamotsu Takishima who was instrumental in initiating the collaborative work on hypoxic response.

Present address: Laboratory of Molecular Pharmacology, Tohoku University School of Medicine, Sendai 980-8575, Japan.

¶¶ To whom correspondence should be addressed: Dept. of Molecular Biology and Applied Physiology, Tohoku University School of Medicine, 2-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi 980-8575, Japan. Tel.: 81-22-717-8117; Fax: 81-22-717-8118; E-mail: shibahar@mail.cc.tohoku.ac.jp.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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