Sse1, Hsp110 Chaperone of Yeast, Controls the Cellular Fate During Endoplasmic Reticulum Stress

Overview

Journal G3 (Bethesda)

Publisher Oxford University Press

Specialties Genetics
Molecular Biology

Date 2024 Apr 5

PMID 38577891

Authors

Mainak Pratim Jha

Vignesh Kumar

Asmita Ghosh

Koyeli Mapa

Affiliations

Soon will be listed here.

Abstract

Sse1 is a cytosolic Hsp110 molecular chaperone of yeast, Saccharomyces cerevisiae. Its multifaceted roles in cellular protein homeostasis as a nucleotide exchange factor (NEF), as a protein-disaggregase and as a chaperone linked to protein synthesis (CLIPS) are well documented. In the current study, we show that SSE1 genetically interacts with IRE1 and HAC1, the endoplasmic reticulum-unfolded protein response (ER-UPR) sensors implicating its role in ER protein homeostasis. Interestingly, the absence of this chaperone imparts unusual resistance to tunicamycin-induced ER stress which depends on the intact Ire1-Hac1 mediated ER-UPR signaling. Furthermore, cells lacking SSE1 show inefficient ER-stress-responsive reorganization of translating ribosomes from polysomes to monosomes that drive uninterrupted protein translation during tunicamycin stress. In consequence, the sse1Δ strain shows prominently faster reversal from ER-UPR activated state indicating quicker restoration of homeostasis, in comparison to the wild-type (WT) cells. Importantly, Sse1 plays a critical role in controlling the ER-stress-mediated cell division arrest, which is escaped in sse1Δ strain during chronic tunicamycin stress. Accordingly, sse1Δ strain shows significantly higher cell viability in comparison to WT yeast imparting the stark fitness following short-term as well as long-term tunicamycin stress. These data, all together, suggest that cytosolic chaperone Sse1 is an important modulator of ER stress response in yeast and it controls stress-induced cell division arrest and cell death during overwhelming ER stress induced by tunicamycin.

References

Polier S, Dragovic Z, Hartl F, Bracher A . Structural basis for the cooperation of Hsp70 and Hsp110 chaperones in protein folding. Cell. 2008; 133(6):1068-79. DOI: 10.1016/j.cell.2008.05.022. View

Maity S, Rajkumar A, Matai L, Bhat A, Ghosh A, Agam G . Oxidative Homeostasis Regulates the Response to Reductive Endoplasmic Reticulum Stress through Translation Control. Cell Rep. 2016; 16(3):851-65. DOI: 10.1016/j.celrep.2016.06.025. View

Dragovic Z, Broadley S, Shomura Y, Bracher A, Hartl F . Molecular chaperones of the Hsp110 family act as nucleotide exchange factors of Hsp70s. EMBO J. 2006; 25(11):2519-28. PMC: 1478182. DOI: 10.1038/sj.emboj.7601138. View

Rosebrock A . Analysis of the Budding Yeast Cell Cycle by Flow Cytometry. Cold Spring Harb Protoc. 2017; 2017(1). DOI: 10.1101/pdb.prot088740. View

Igbaria A, Merksamer P, Trusina A, Tilahun F, Johnson J, Brandman O . Chaperone-mediated reflux of secretory proteins to the cytosol during endoplasmic reticulum stress. Proc Natl Acad Sci U S A. 2019; 116(23):11291-11298. PMC: 6561268. DOI: 10.1073/pnas.1904516116. View

Liu Q, Hendrickson W . Insights into Hsp70 chaperone activity from a crystal structure of the yeast Hsp110 Sse1. Cell. 2007; 131(1):106-20. PMC: 2041797. DOI: 10.1016/j.cell.2007.08.039. View

Niwa M . A cell cycle checkpoint for the endoplasmic reticulum. Biochim Biophys Acta Mol Cell Res. 2020; 1867(12):118825. PMC: 7558805. DOI: 10.1016/j.bbamcr.2020.118825. View

Mukai H, Kuno T, Tanaka H, Hirata D, Miyakawa T, Tanaka C . Isolation and characterization of SSE1 and SSE2, new members of the yeast HSP70 multigene family. Gene. 1993; 132(1):57-66. DOI: 10.1016/0378-1119(93)90514-4. View

Wu H, Ng B, Thibault G . Endoplasmic reticulum stress response in yeast and humans. Biosci Rep. 2014; 34(4). PMC: 4076835. DOI: 10.1042/BSR20140058. View

10.

Millan-Zambrano G, Chavez S . Nuclear functions of prefoldin. Open Biol. 2014; 4(7). PMC: 4118604. DOI: 10.1098/rsob.140085. View

11.

Sanchez-Adria I, Sanmartin G, Prieto J, Estruch F, Randez-Gil F . Slt2 Is Required to Activate ER-Stress-Protective Mechanisms through TORC1 Inhibition and Hexosamine Pathway Activation. J Fungi (Basel). 2022; 8(2). PMC: 8877190. DOI: 10.3390/jof8020092. View

12.

Jonikas M, Collins S, Denic V, Oh E, Quan E, Schmid V . Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science. 2009; 323(5922):1693-7. PMC: 2877488. DOI: 10.1126/science.1167983. View

13.

Kumar V, Peter J, Sagar A, Ray A, Jha M, Rebeaud M . Interdomain communication suppressing high intrinsic ATPase activity of Sse1 is essential for its co-disaggregase activity with Ssa1. FEBS J. 2019; 287(4):671-694. DOI: 10.1111/febs.15045. View

14.

Liu Y, Chang A . Heat shock response relieves ER stress. EMBO J. 2008; 27(7):1049-59. PMC: 2323268. DOI: 10.1038/emboj.2008.42. View

15.

Andreasson C, Fiaux J, Rampelt H, Druffel-Augustin S, Bukau B . Insights into the structural dynamics of the Hsp110-Hsp70 interaction reveal the mechanism for nucleotide exchange activity. Proc Natl Acad Sci U S A. 2008; 105(43):16519-24. PMC: 2575452. DOI: 10.1073/pnas.0804187105. View

16.

Hrizo S, Gusarova V, Habiel D, Goeckeler J, Fisher E, Brodsky J . The Hsp110 molecular chaperone stabilizes apolipoprotein B from endoplasmic reticulum-associated degradation (ERAD). J Biol Chem. 2007; 282(45):32665-75. PMC: 2666968. DOI: 10.1074/jbc.M705216200. View

17.

Andreasson C, Fiaux J, Rampelt H, Mayer M, Bukau B . Hsp110 is a nucleotide-activated exchange factor for Hsp70. J Biol Chem. 2008; 283(14):8877-84. DOI: 10.1074/jbc.M710063200. View

18.

Geissler S, Siegers K, Schiebel E . A novel protein complex promoting formation of functional alpha- and gamma-tubulin. EMBO J. 1998; 17(4):952-66. PMC: 1170445. DOI: 10.1093/emboj/17.4.952. View

19.

Higuchi-Sanabria R, Frankino P, Paul 3rd J, Tronnes S, Dillin A . A Futile Battle? Protein Quality Control and the Stress of Aging. Dev Cell. 2018; 44(2):139-163. PMC: 5896312. DOI: 10.1016/j.devcel.2017.12.020. View

20.

Rospert S, Dubaquie Y, Gautschi M . Nascent-polypeptide-associated complex. Cell Mol Life Sci. 2002; 59(10):1632-9. PMC: 11337418. DOI: 10.1007/pl00012490. View