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Science 289 (5482): 1159-1164

Copyright © 2000 by the American Association for the Advancement of Science

Cytochrome c Release and Apoptosis Induced by Mitochondrial Targeting of Nuclear Orphan Receptor TR3

Hui Li,1 Siva Kumar Kolluri,1 Jian Gu,1 Marcia I. Dawson,2 Xihua Cao,1 Peter D. Hobbs,3 Bingzhen Lin,1 Guo-quen Chen,1 Jiang-song Lu,4 Feng Lin,1 Zhihua Xie,1 Joseph A. Fontana,4 John C. Reed,1 Xiao-kun Zhang1*

TR3, an immediate-early response gene and an orphan member of the steroid-thyroid hormone-retinoid receptor superfamily of transcription factors, regulates apoptosis through an unknown mechanism. In response to apoptotic stimuli, TR3 translocates from the nucleus to mitochondria to induce cytochrome c release and apoptosis. Mitochondrial targeting of TR3, but not its DNA binding and transactivation, is essential for its proapoptotic effect. Our results reveal a mechanism by which a nuclear transcription factor translocates to mitochondria to initiate apoptosis.

1 The Burnham Institute, 10901 North Torrey Pines Road, La Jolla, CA 92037, USA.
2 Molecular Medicine Research Institute, 325 East Middlefield Road, Mountain View, CA 94043, USA.
3 Retinoid Program, SRI, Menlo Park, CA 94025, USA.
4 Karmanos Cancer Institute, Wayne State University, and the John D. Dingel VA Medical Center, 4646 John R Street, Detroit, MI 48201, USA.
*   To whom correspondence should be addressed: E-mail: xzhang{at}burnham-inst.org

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C. I. Seye, M. W.M. Knaapen, D. Daret, C. Desgranges, A. G. Herman, M. M. Kockx, and H. Bult (2004)
Cardiovasc Res 64, 144-153
   Abstract »    Full Text »    PDF »
The 1.4-MDa apoptosome is a critical intermediate in apoptosome maturation.
E. Beem, L. S. Holliday, and M. S. Segal (2004)
Am J Physiol Cell Physiol 287, C664-C672
   Abstract »    Full Text »    PDF »
Induction of orphan nuclear receptor Nur77 gene expression and its role in cadmium-induced apoptosis in lung.
H.-J. Shin, B.-H. Lee, M. G. Yeo, S.-H. Oh, J.-D. Park, K.-K. Park, J.-H. Chung, C.-K. Moon, and M.-O. Lee (2004)
Carcinogenesis 25, 1467-1475
   Abstract »    Full Text »    PDF »
Casein Kinase 1{alpha} Interacts with Retinoid X Receptor and Interferes with Agonist-induced Apoptosis.
Y. Zhao, S. Qin, L. I. Atangan, Y. Molina, Y. Okawa, H. T. Arpawong, C. Ghosn, J.-H. Xiao, V. Vuligonda, G. Brown, et al. (2004)
J. Biol. Chem. 279, 30844-30849
   Abstract »    Full Text »    PDF »
Alternative, Nonapoptotic Programmed Cell Death: MEDIATION BY ARRESTIN 2, ERK2, AND Nur77.
S. Castro-Obregon, R. V. Rao, G. del Rio, S. F. Chen, K. S. Poksay, S. Rabizadeh, S. Vesce, X.-k. Zhang, R. A. Swanson, and D. E. Bredesen (2004)
J. Biol. Chem. 279, 17543-17553
   Abstract »    Full Text »    PDF »
Inhibitory Effect of 12-O-Tetradecanoylphorbol-13-acetate Alone or in Combination with All-trans-Retinoic Acid on the Growth of LNCaP Prostate Tumors in Immunodeficient Mice.
X. Zheng, R. L. Chang, X.-X. Cui, G. E. Avila, S. Lee, Y. P. Lu, Y. R. Lou, W. J. Shih, Y. Lin, K. Reuhl, et al. (2004)
Cancer Res. 64, 1811-1820
   Abstract »    Full Text »    PDF »
Gene Expression in HL60 Granulocytoids and Human Polymorphonuclear Leukocytes Exposed to Candida albicans{dagger}.
A. Mullick, M. Elias, P. Harakidas, A. Marcil, M. Whiteway, B. Ge, T. J. Hudson, A. W. Caron, L. Bourget, S. Picard, et al. (2004)
Infect. Immun. 72, 414-429
   Abstract »    Full Text »    PDF »
Mitogenic Effect of Orphan Receptor TR3 and Its Regulation by MEKK1 in Lung Cancer Cells.
S. K. Kolluri, N. Bruey-Sedano, X. Cao, B. Lin, F. Lin, Y.-H. Han, M. I. Dawson, and X.-k. Zhang (2003)
Mol. Cell. Biol. 23, 8651-8667
   Abstract »    Full Text »    PDF »
TR3 Orphan Nuclear Receptor Mediates Apoptosis through Up-regulating E2F1 in Human Prostate Cancer LNCaP Cells.
X. Mu and C. Chang (2003)
J. Biol. Chem. 278, 42840-42845
   Abstract »    Full Text »    PDF »
Gene expression analysis of thymocyte selection in vivo.
I. Schmitz, L. K. Clayton, and E. L. Reinherz (2003)
Int. Immunol. 15, 1237-1248
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Phospholipid Scramblase 3 Controls Mitochondrial Structure, Function, and Apoptotic Response.
J. Liu, Q. Dai, J. Chen, D. Durrant, A. Freeman, T. Liu, D. Grossman, and R. M. Lee (2003)
Mol. Cancer Res. 1, 892-902
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TR3/Nur77 in Colon Cancer Cell Apoptosis.
A. J. Wilson, D. Arango, J. M. Mariadason, B. G. Heerdt, and L. H. Augenlicht (2003)
Cancer Res. 63, 5401-5407
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TR3 Orphan Receptor Is Expressed in Vascular Endothelial Cells and Mediates Cell Cycle Arrest.
E. K. Arkenbout, M. van Bragt, E. Eldering, C. van Bree, J. M. Grimbergen, P. H.A. Quax, H. Pannekoek, and C. J.M. de Vries (2003)
Arterioscler Thromb Vasc Biol 23, 1535-1540
   Abstract »    Full Text »    PDF »
Characterization of Transcriptional Regulation During Negative Selection In Vivo.
D. DeRyckere, D. L. Mann, and J. DeGregori (2003)
J. Immunol. 171, 802-811
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