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Genetic inactivation of essential HSF1 reveals an isolated transcriptional stress response selectively induced by protein misfolding
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.ORCID iD: 0000-0001-6065-8216
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.ORCID iD: 0000-0002-8920-4370
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2023 (English)In: Molecular Biology of the Cell, ISSN 1059-1524, E-ISSN 1939-4586, Vol. 34, no 11, article id ar101Article in journal (Refereed) Published
Abstract [en]

Heat Shock Factor 1 (Hsf1) in yeast drives the basal transcription of key proteostasis factors and its activity is induced as part of the core heat shock response. Exploring Hsf1 specific functions has been challenging due to the essential nature of the HSF1 gene and the extensive overlap of target promoters with environmental stress response (ESR) transcription factors Msn2 and Msn4 (Msn2/4). In this study, we constructed a viable hsf1 increment strain by replacing the HSF1 open reading frame with genes that constitutively express Hsp40, Hsp70, and Hsp90 from Hsf1-independent promoters. Phenotypic analysis showed that the hsf1 increment strain grows slowly, is sensitive to heat as well as protein misfolding and accumulates protein aggregates. Transcriptome analysis revealed that the transcriptional response to protein misfolding induced by azetidine-2-carboxylic acid is fully dependent on Hsf1. In contrast, the hsf1 increment strain responded to heat shock through the ESR. Following HS, Hsf1 and Msn2/4 showed functional compensatory induction with stronger activation of the remaining stress pathway when the other branch was inactivated. Thus, we provide a long-overdue genetic test of the function of Hsf1 in yeast using the novel hsf1 increment construct. Our data highlight that the accumulation of misfolded proteins is uniquely sensed by Hsf1-Hsp70 chaperone titration inducing a highly selective transcriptional stress response.

Place, publisher, year, edition, pages
2023. Vol. 34, no 11, article id ar101
National Category
Biochemistry Molecular Biology
Identifiers
URN: urn:nbn:se:su:diva-223766DOI: 10.1091/mbc.E23-05-0153ISI: 001085485400001PubMedID: 37467033Scopus ID: 2-s2.0-85168240028OAI: oai:DiVA.org:su-223766DiVA, id: diva2:1812296
Available from: 2023-11-15 Created: 2023-11-15 Last updated: 2025-02-20Bibliographically approved
In thesis
1. Regulation of Proteostasis and Stress Response: Insights into Hsf1 and Chaperone Dynamics
Open this publication in new window or tab >>Regulation of Proteostasis and Stress Response: Insights into Hsf1 and Chaperone Dynamics
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Protein homeostasis (proteostasis) refers to the balance between protein production, folding, and degradation, and is coordinated by components of the proteostasis network. Preserving cellular proteins in their native, folded, and active state is vital to proteostasis and, therefore, essential for cell viability.

Stress induces perturbations in the proteome, leading to the accumulation of misfolded proteins and toxic aggregates. The heat shock response (HSR) is a central eukaryotic stress-responsive pathway mediated by Heat Shock Factor 1 (Hsf1), which is activated in response to various stressors. Hsf1 leads the expression of the crucial proteostasis factors, particularly heat shock proteins (HSPs), in order to build an effective response against stress and restore the equilibrium. The overall aim of the work presented in this thesis is to elucidate the role of Hsf1 and the impact of Hsp70 and misfolded proteins on its regulation, using Saccharomyces cerevisiae and human cells as models.

   In Study I, we describe a transcriptional stress response pathway triggered by protein misfolding, which is uniquely sensed by Hsf1 in yeast. Using a hsf1Δ strain, we show that while Hsf1 plays an important role in maintaining protein homeostasis under basal conditions, it is not essential for driving an effective response to heat stress. However, it is the sole transcription factor responsible for initiating a stress response against the accumulation of misfolded proteins, relieving Hsf1 from negative regulation by Hsp70. In Study II, we demonstrate that HSF1-HSP70 chaperone titration is conserved in human. Specifically, high levels of HSP70 reduce HSF1 DNA-binding capacity in vitro. Moreover, the addition of misfolded proteins in vitro or the induction of misfolding of newly synthesized proteins by feeding HEK293T cells a proteotoxic proline analog titrates HSP70, thereby activating HSF1. 

   In Study III, we discover a new dedicated chaperone, Chp1, which interacts with the ribosome to assist in the synthesis of the first domain of eEF1A. Additionally, we show that deletion of Chp1 leads to the production of nonfunctional eEF1A, immediately degraded, and to induction of the heat shock response. 

Finally, in Study IV, we develop a new strategy for delivering HSP70 into cells using a cell-penetrating peptide, PepFect14. We show that PepFect14 forms a complex with HSP70 to facilitate its delivery into cells. This interaction does not impair HSP70 activity, which is biologically available in the cytoplasm. Protein delivery using PepFect14 could represent a valid method for increasing chaperone levels in diseases associated with the formation of aggregates.

   Overall, the findings presented in this thesis enhance our understanding of how cells manage their response to stress through the regulation of Hsf1 and protein folding. Moreover, they provide new tools for future proteostasis studies and potential therapeutic applications.

Place, publisher, year, edition, pages
Stockholm: Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, 2024. p. 68
Keywords
proteostasis, heat shock proteins, stress, protein misfolding, heat shock response, Hsf1, Hsp70, Chp1, eEF1A, PepFect14, HEK293T, Saccharomyces cerevisiae
National Category
Biochemistry Molecular Biology
Research subject
Molecular Bioscience
Identifiers
urn:nbn:se:su:diva-232814 (URN)978-91-8014-909-9 (ISBN)978-91-8014-910-5 (ISBN)
Public defence
2024-10-11, Hörsal 6, Södra huset, hus C, Frescativägen 10C, Stockholm, 09:30 (English)
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Available from: 2024-09-18 Created: 2024-08-26 Last updated: 2025-02-20Bibliographically approved

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Ciccarelli, MichelaMasser, Anna E.Kaimal, Jayasankar MohanakrishnanPlanells, JordiAndréasson, Claes

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