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J. Biol. Chem., Vol. 279, Issue 43, 44497-44503, October 22, 2004

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Developmentally Dictated Expression of Heat Shock Factors: Exclusive Expression of HSF4 in the Postnatal Lens and Its Specific Interaction with B-crystallin Heat Shock Promoter^*

T. Somasundaram and Suraj P. Bhat¶||

From the Jules Stein Eye Institute, Brain Research Institute, and ^¶Molecular Biology Institute, University of California, Los Angeles, California 90095-7000

The molecular cascade of stress response in higher eukaryotes commences in the cytoplasm with the trimerization of the heat shock factor 1 (HSF1), followed by its transport to the nucleus, where it binds to the heat shock element leading to the activation of transcription from the down-stream gene(s). This well-established paradigm has been mostly studied in cultured cells. The developmental and tissue-specific control of the heat shock transcription factors (HSFs) and their interactions with heat shock promoters remain unexplored. We report here that in the rat lens, among the three mammalian HSFs, expression of HSF1 and HSF2 is largely fetal, whereas the expression of HSF4 is predominantly postnatal. Similar pattern of expression of HSF1 and HSF4 is seen in fetal and adult human lenses. This stage-specific inverse relationship between the expression of HSF1/2 and HSF4 suggests tissue-specific management of stress depending on the presence or absence of specific HSF(s). In addition to real-time PCR and immunoblotting, gel mobility shift assays, coupled with specific antibodies and HSE probes, derived from three different heat shock promoters, establish that there is no HSF1 or HSF2 binding activity in the postnatal lens nuclear extracts. Using this unique, developmentally modulated in vivo system, we demonstrate 1) specific patterns of HSF4 binding to heat shock elements derived from B-crystallin, Hsp70, and Hsp82 promoters and 2) that it is HSF4 and not HSF1 or HSF2 that interacts with the canonical heat shock element of the B-crystallin gene.

Received for publication, May 25, 2004 , and in revised form, July 26, 2004.

^* This work was supported by NEI, National Institutes of Health grants (to S. P. B.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^|| Research To Prevent Blindness Inc., Wasserman Merit Scholar. To whom correspondence should be addressed:100 Stein Plaza, Rm. BH-623, UCLA School of Medicine, Los Angeles, CA 90095-7000. Tel.: 310-825-9543; Fax: 310-794-2144; E-mail: bhat{at}jsei.ucla.edu.

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