Identification of TFII-I as the Endoplasmic Reticulum Stress Response Element Binding Factor ERSF: Its Autoregulation by Stress and Interaction with ATF6

doi:10.1128/MCB.21.9.3220-3233.2001

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Molecular and Cellular Biology, May 2001, p. 3220-3233, Vol. 21, No. 9
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.9.3220-3233.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Identification of TFII-I as the Endoplasmic Reticulum Stress Response Element Binding Factor ERSF: Its Autoregulation by Stress and Interaction with ATF6

Ronald Parker,¹ Trevor Phan,¹ Peter Baumeister,¹ Binayak Roy,¹ Venugopalan Cheriyath,² Ananda L. Roy,² and Amy S. Lee¹^,^*

Department of Biochemistry and Molecular Biology and the USC/Norris Comprehensive Cancer Center, Keck School of Medicine of the University of Southern California, Los Angeles, California 90089-9176,¹ and Department of Pathology and Programs in Immunology and Genetics, Tufts University School of Medicine, Boston, Massachusetts 02111²

Received 4 October 2000/Returned for modification 1 December 2000/Accepted 29 January 2001

When mammalian cells are subjected to stress targeted to the endoplasmic reticulum (ER), such as depletion of the ER Ca²⁺ store, the transcription of a family of glucose-regulated protein(GRP) genes encoding ER chaperones is induced. The GRP promoterscontain multiple copies of the ER stress response element (ERSE),consisting of a unique tripartite structure, CCAAT(N₉)CCACG. Withina subset of mammalian ERSEs, N₉ represents a GC-rich sequenceof 9 bp that is conserved across species. A novel complex (termedERSF) exhibits enhanced binding to the ERSE of the grp78 and ERp72promoters using HeLa nuclear extracts prepared from ER-stressedcells. Optimal binding of ERSF to ERSE and maximal ERSE-mediatedstress inducibility require the conserved GGC motif within the9-bp region. Through chromatographic purification and subsequentmicrosequencing, we have identified ERSF as TFII-I. Whereas TFII-Iremains predominantly nuclear in both nontreated NIH 3T3 cellsand cells treated with thapsigargin (Tg), a potent inducer ofthe GRP stress response through depletion of the ER Ca²⁺ store, the level of TFII-I transcript was elevated in Tg-stressedcells, correlating with an increase in TFII-I protein level inthe nuclei of Tg-stressed cells. Purified recombinant TFII-I isoformsbind directly to the ERSEs of grp78 and ERp72 promoters. The stimulationof ERSE-mediated transcription by TFII-I requires the consensustyrosine phosphorylation site of TFII-I and the GGC sequence motifof the ERSE. We further discovered that TFII-I is an interactiveprotein partner of ATF6 and that optimal stimulation of ERSE byATF6 requires TFII-I.

^* Corresponding author. Mailing address: USC/Norris Comprehensive Cancer Center, 1441 Eastlake Ave., Room 5308, MC-9176, LosAngeles, CA 90089-9176. Phone: (323) 865-0507. Fax: (323) 865-0094.E-mail: amylee{at}hsc.usc.edu.

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