Hsp90 selectively modulates phenotype in vertebrate development.

Compromised heat shock protein 90 (Hsp90) function reveals cryptic phenotypes in flies and plants. These observations were interpreted to suggest that this molecular stress-response chaperone has a capacity to buffer underlying genetic variation. Conversely, the protective role of Hsp90 could accoun...

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Main Authors: Patricia L Yeyati, Ruth M Bancewicz, John Maule, Veronica van Heyningen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-03-01
Series:PLoS Genetics
Online Access:https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.0030043&type=printable
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author Patricia L Yeyati
Ruth M Bancewicz
John Maule
Veronica van Heyningen
author_facet Patricia L Yeyati
Ruth M Bancewicz
John Maule
Veronica van Heyningen
author_sort Patricia L Yeyati
collection DOAJ
description Compromised heat shock protein 90 (Hsp90) function reveals cryptic phenotypes in flies and plants. These observations were interpreted to suggest that this molecular stress-response chaperone has a capacity to buffer underlying genetic variation. Conversely, the protective role of Hsp90 could account for the variable penetrance or severity of some heritable developmental malformations in vertebrates. Using zebrafish as a model, we defined Hsp90 inhibitor levels that did not induce a heat shock response or perturb phenotype in wild-type strains. Under these conditions the severity of the recessive eye phenotype in sunrise, caused by a pax6b mutation, was increased, while in dreumes, caused by a sufu mutation, it was decreased. In another strain, a previously unobserved spectrum of severe structural eye malformations, reminiscent of anophthalmia, microphthalmia, and nanophthalmia complex in humans, was uncovered by this limited inhibition of Hsp90 function. Inbreeding of offspring from selected unaffected carrier parents led to significantly elevated malformation frequencies and revealed the oligogenic nature of this phenotype. Unlike in Drosophila, Hsp90 inhibition can decrease developmental stability in zebrafish, as indicated by increased asymmetric presentation of anophthalmia, microphthalmia, and nanophthalmia and sunrise phenotypes. Analysis of the sunrise pax6b mutation suggests a molecular mechanism for the buffering of mutations by Hsp90. The zebrafish studies imply that mild perturbation of Hsp90 function at critical developmental stages may underpin the variable penetrance and expressivity of many developmental anomalies where the interaction between genotype and environment plays a major role.
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spelling doaj-art-5575e61cd1fd4c22ac449da109433fec2025-08-20T02:38:29ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042007-03-0133e4310.1371/journal.pgen.0030043Hsp90 selectively modulates phenotype in vertebrate development.Patricia L YeyatiRuth M BancewiczJohn MauleVeronica van HeyningenCompromised heat shock protein 90 (Hsp90) function reveals cryptic phenotypes in flies and plants. These observations were interpreted to suggest that this molecular stress-response chaperone has a capacity to buffer underlying genetic variation. Conversely, the protective role of Hsp90 could account for the variable penetrance or severity of some heritable developmental malformations in vertebrates. Using zebrafish as a model, we defined Hsp90 inhibitor levels that did not induce a heat shock response or perturb phenotype in wild-type strains. Under these conditions the severity of the recessive eye phenotype in sunrise, caused by a pax6b mutation, was increased, while in dreumes, caused by a sufu mutation, it was decreased. In another strain, a previously unobserved spectrum of severe structural eye malformations, reminiscent of anophthalmia, microphthalmia, and nanophthalmia complex in humans, was uncovered by this limited inhibition of Hsp90 function. Inbreeding of offspring from selected unaffected carrier parents led to significantly elevated malformation frequencies and revealed the oligogenic nature of this phenotype. Unlike in Drosophila, Hsp90 inhibition can decrease developmental stability in zebrafish, as indicated by increased asymmetric presentation of anophthalmia, microphthalmia, and nanophthalmia and sunrise phenotypes. Analysis of the sunrise pax6b mutation suggests a molecular mechanism for the buffering of mutations by Hsp90. The zebrafish studies imply that mild perturbation of Hsp90 function at critical developmental stages may underpin the variable penetrance and expressivity of many developmental anomalies where the interaction between genotype and environment plays a major role.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.0030043&type=printable
spellingShingle Patricia L Yeyati
Ruth M Bancewicz
John Maule
Veronica van Heyningen
Hsp90 selectively modulates phenotype in vertebrate development.
PLoS Genetics
title Hsp90 selectively modulates phenotype in vertebrate development.
title_full Hsp90 selectively modulates phenotype in vertebrate development.
title_fullStr Hsp90 selectively modulates phenotype in vertebrate development.
title_full_unstemmed Hsp90 selectively modulates phenotype in vertebrate development.
title_short Hsp90 selectively modulates phenotype in vertebrate development.
title_sort hsp90 selectively modulates phenotype in vertebrate development
url https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.0030043&type=printable
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AT ruthmbancewicz hsp90selectivelymodulatesphenotypeinvertebratedevelopment
AT johnmaule hsp90selectivelymodulatesphenotypeinvertebratedevelopment
AT veronicavanheyningen hsp90selectivelymodulatesphenotypeinvertebratedevelopment