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Abstract
Heat shock transcription factor 1 (HSF1) is the main regulator of the stress response that triggers the transcription of several genes encoding heat shock proteins (Hsps). Hsps act as molecular chaperones involved in protein folding, stability, and trafficking. HSF1 is highly expressed in oocytes and Hsf1 knock-out in mice revealed that in the absence of stress this factor plays an important role in female reproduction. We previously reported that Hsf1(-/-) females produce oocytes but no viable embryos. Consequently, we asked whether oocytes require HSF1 to regulate a particular set of Hsps necessary for them to develop. We find that Hsp90alpha (Hspaa1) is the major HSF1-dependent chaperone inasmuch as Hsf1 knock-out resulted in Hsp90-depleted oocytes. These oocytes exhibited delayed germinal vesicle breakdown (or G(2)/M transition), partial meiosis I block, and defective asymmetrical division. To probe the role of Hsp90alpha in this meiotic syndrome, we analyzed meiotic maturation in wild-type oocytes treated with a specific inhibitor of Hsp90, 17-allylamino-17-demethoxy-geldanamycin, and observed similar defects. At the molecular level we showed that, together with these developmental anomalies, CDK1 and MAPK, key meiotic kinases, were significantly disturbed. Thus, our data demonstrate that HSF1 is a maternal transcription factor essential for normal progression of meiosis.
Highlights
In mammals there are several heat shock factors (HSF1, -2, and -4)3 that share a similar DNA binding domain, but Heat shock transcription factor 1 (HSF1) appears to be the major transcriptional regulator responsible
HSF1 Differentially Regulates heat shock proteins (Hsps) Expression in Oocytes— Using reverse transcription followed by real-time PCR, we examined mRNA levels of the major members of several Hsp families: Hsp25, Hsp60, Hsp70.1, Hsp70.3, Hsp90␣, Hsp90, Hsp105
Compared with Hsf1ϩ/ϩ, Hsf1Ϫ/Ϫ oocytes were markedly depleted in Hsp90␣ and exhibited visible down-regulation for Hsp70.1 and Hsp25 transcripts, but there was no difference for Hsp60 or Hsp90 transcripts (Fig. 1B)
Summary
In mammals there are several heat shock factors (HSF1, -2, and -4)3 that share a similar DNA binding domain, but HSF1 appears to be the major transcriptional regulator responsible. HSF1 Differentially Regulates Hsp Expression in Oocytes— Using reverse transcription followed by real-time PCR (qPCR), we examined mRNA levels of the major members of several Hsp families: Hsp25, Hsp60, Hsp70.1, Hsp70.3, Hsp90␣, Hsp90, Hsp105 (see gene descriptions in supplemental Table S1).
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