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Molecular and Cellular Biology, November 2003, p. 7448-7459, Vol. 23, No. 21
0270-7306/03/$08.00+0     DOI: 10.1128/MCB.23.21.7448-7459.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

XBP-1 Regulates a Subset of Endoplasmic Reticulum Resident Chaperone Genes in the Unfolded Protein Response

Ann-Hwee Lee,1 Neal N. Iwakoshi,1 and Laurie H. Glimcher1,2*

Department of Immunology and Infectious Diseases, Harvard School of Public Health,1 Department of Medicine, Harvard Medical School, Boston, Massachusetts 021152

Received 9 June 2003/ Returned for modification 7 July 2003/ Accepted 22 July 2003

The mammalian unfolded protein response (UPR) protects the cell against the stress of misfolded proteins in the endoplasmic reticulum (ER). We have investigated here the contribution of the UPR transcription factors XBP-1, ATF6{alpha}, and ATF6ß to UPR target gene expression. Gene profiling of cell lines lacking these factors yielded several XBP-1-dependent UPR target genes, all of which appear to act in the ER. These included the DnaJ/Hsp40-like genes, p58IPK, ERdj4, and HEDJ, as well as EDEM, protein disulfide isomerase-P5, and ribosome-associated membrane protein 4 (RAMP4), whereas expression of BiP was only modestly dependent on XBP-1. Surprisingly, given previous reports that enforced expression of ATF6{alpha} induced a subset of UPR target genes, cells deficient in ATF6{alpha}, ATF6ß, or both had minimal defects in upregulating UPR target genes by gene profiling analysis, suggesting the presence of compensatory mechanism(s) for ATF6 in the UPR. Since cells lacking both XBP-1 and ATF6{alpha} had significantly impaired induction of select UPR target genes and ERSE reporter activation, XBP-1 and ATF6{alpha} may serve partially redundant functions. No UPR target genes that required ATF6ß were identified, nor, in contrast to XBP-1 and ATF6{alpha}, did the activity of the UPRE or ERSE promoters require ATF6ß, suggesting a minor role for it during the UPR. Collectively, these results suggest that the IRE1/XBP-1 pathway is required for efficient protein folding, maturation, and degradation in the ER and imply the existence of subsets of UPR target genes as defined by their dependence on XBP-1. Further, our observations suggest the existence of additional, as-yet-unknown, key regulators of the UPR.

* Corresponding author. Mailing address: Department of Immunology and Infectious Diseases, Harvard School of Public Health, 651 Huntington Ave., FXB-2, Boston, MA 02115-6017. Phone: (617) 432-0622. Fax: (617) 432-0084. E-mail: lglimche{at}hsph.harvard.edu.

Molecular and Cellular Biology, November 2003, p. 7448-7459, Vol. 23, No. 21
0022-538X/03/$08.00+0     DOI: 10.1128/MCB.23.21.7448-7459.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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