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Hormetic heat stress and HSF-1 induce autophagy to improve survival and proteostasis in C. elegans
Abstract
Stress-response pathways have evolved to maintain cellular homeostasis and to ensure the survival of organisms under changing environmental conditions. Whereas severe stress is detrimental, mild stress can be beneficial for health and survival, known as hormesis. Although the universally conserved heat-shock response regulated by transcription factor HSF-1 has been implicated as an effector mechanism, the role and possible interplay with other cellular processes, such as autophagy, remains poorly understood. Here we show that autophagy is induced in multiple tissues of Caenorhabditis elegans following hormetic heat stress or HSF-1 overexpression. Autophagy-related genes are required for the thermoresistance and longevity of animals exposed to hormetic heat shock or HSF-1 overexpression. Hormetic heat shock also reduces the progressive accumulation of PolyQ aggregates in an autophagy-dependent manner. These findings demonstrate that autophagy contributes to stress resistance and hormesis, and reveal a requirement for autophagy in HSF-1-regulated functions in the heat-shock response, proteostasis and ageing.
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SQSTM1 upregulation, and at least transient increases in the amount of SQSTM1, is seen in some situations where there is an increase in autophagic flux.
“For example, SQSTM1 upregulation, and at least transient increases in the amount of SQSTM1, is seen in some situations where there is an increase in autophagic flux [571-573].”
From Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition) 1 (2021) · cites this paper as [572]
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Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894
Self-citationAutophagy and the Integrated Stress Response
Kroemer, G., Mariño, G., & Levine, B. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.023 · Cited by 3,506
Regulation of aging and age-related disease by DAF-16 and heat-shock factor
Hsu, A.-L., Murphy, C. T., & Kenyon, C. (2003) · Science · doi:10.1126/science.1083701 · Cited by 1,513
Autophagy and aging: The importance of maintaining "clean" cells
Cuervo, A. M., Bergamini, E., Brunk, U. T., Dröge, W., Ffrench, M., & Terman, A. (2005) · Autophagy · doi:10.4161/auto.1.3.2017 · Cited by 792
Progressive disruption of cellular protein folding in models of polyglutamine diseases
Gidalevitz, T., Ben-Zvi, A., Ho, K. H., Brignull, H. R., & Morimoto, R. I. (2006) · Science · doi:10.1126/science.1124514 · Cited by 643
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Research works printed but not linked: 65
- GuhaThakurta, D. et al. Identification of a novel cis-regulatory element involved in the heat shock response in Caenorhabditis elegans using microarray gene expression and computational methods. Genome Res. 12, 701–712 (2002). · DOI
- Richter, K., Haslbeck, M. & Buchner, J. The heat shock response: life on the verge of death. Mol. Cell 40, 253–266 (2010). · DOI
- Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W. & Dillin, A. Opposing activities protect against age-onset proteotoxicity. Science 313, 1604–1610 (2006). · DOI · Paper page
- Ben-Zvi, A., Miller, E. A. & Morimoto, R. I. Collapse of proteostasis represents an early molecular event in Caenorhabditis elegans aging. Proc. Natl Acad. Sci. USA 106, 14914–14919 (2009). · DOI · Paper page
- Morley, J. F. & Morimoto, R. I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell 15, 657–664 (2004). · DOI
- Polling, S., Hill, A. F. & Hatters, D. M. Polyglutamine aggregation in Huntington and related diseases. Adv. Exp. Med. Biol. 769, 125–140 (2012). · DOI
- Sakahira, H., Breuer, P., Hayer-Hartl, M. K. & Hartl, F. U. Molecular chaperones as modulators of polyglutamine protein aggregation and toxicity. Proc. Natl Acad. Sci. USA 99, 16412–16418 (2002). · DOI
- Morley, J. F., Brignull, H. R., Weyers, J. J. & Morimoto, R. I. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 99, 10417–10422 (2002). · DOI
- Shemesh, N., Shai, N. & Ben-Zvi, A. Germline stem cell arrest inhibits the collapse of somatic proteostasis early in Caenorhabditis elegans adulthood. Aging Cell 12, 814–822 (2013). · DOI
- Labbadia, J. & Morimoto, R. I. Repression of the heat shock response is a programmed event at the onset of reproduction. Mol. Cell 59, 639–650 (2015). · DOI
- Shai, N., Shemesh, N. & Ben-Zvi, A. Remodeling of proteostasis upon transition to adulthood is linked to reproduction onset. Curr. Genomics 15, 122–129 (2014). · DOI
- Brehme, M. et al. A chaperome subnetwork safeguards proteostasis in aging and neurodegenerative disease. Cell Rep. 9, 1135–1150 (2014). · DOI · Paper page
- Rattan, S. I. Hormetic modulation of aging and longevity by mild heat stress. Dose Response 3, 533–546 (2005). · DOI
- Gems, D. & Partridge, L. Stress-response hormesis and aging: “that which does not kill us makes us stronger”. Cell Metab. 7, 200–203 (2008). · DOI
- Lithgow, G. J., White, T. M., Melov, S. & Johnson, T. E. Thermotolerance and extended life-span conferred by single-gene mutations and induced by thermal stress. Proc. Natl Acad. Sci. USA 92, 7540–7544 (1995). · DOI · Paper page
- Butov, A. et al. Hormesis and debilitation effects in stress experiments using the nematode worm Caenorhabditis elegans: the model of balance between cell damage and HSP levels. Exp. Gerontol. 37, 57–66 (2001). · DOI
- Cypser, J. R. & Johnson, T. E. Multiple stressors in Caenorhabditis elegans induce stress hormesis and extended longevity. J. Gerontol. A Biol. Sci. Med. Sci. 57, B109–B114 (2002). · DOI
- Khazaeli, A. A., Tatar, M., Pletcher, S. D. & Curtsinger, J. W. Heat-induced longevity extension in Drosophila. I. Heat treatment, mortality, and thermotolerance. J. Gerontol. A Biol. Sci. Med. Sci. 52, B48–B52 (1997). · DOI
- Hercus, M. J., Loeschcke, V. & Rattan, S. I. Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress. Biogerontology 4, 149–156 (2003). · DOI
- Le Bourg, E., Minois, N., Bullens, P. & Baret, P. A mild stress due to hypergravity exposure at young age increases longevity in Drosophila melanogaster males. Biogerontology 1, 145–155 (2000). · DOI
- Scannapieco, A. C., Sorensen, J. G., Loeschcke, V. & Norry, F. M. Heat-induced hormesis in longevity of two sibling Drosophila species. Biogerontology 8, 315–325 (2007). · DOI
- Rattan, S. I. & Ali, R. E. Hormetic prevention of molecular damage during cellular aging of human skin fibroblasts and keratinocytes. Ann. N. Y. Acad. Sci. 1100, 424–430 (2007). · DOI · Paper page
- Kristensen, T. N., Sorensen, J. G. & Loeschcke, V. Mild heat stress at a young age in Drosophila melanogaster leads to increased Hsp70 synthesis after stress exposure later in life. J. Genet. 82, 89–94 (2003). · DOI
- Fonager, J., Beedholm, R., Clark, B. F. & Rattan, S. I. Mild stress-induced stimulation of heat-shock protein synthesis and improved functional ability of human fibroblasts undergoing aging in vitro. Exp. Gerontol. 37, 1223–1228 (2002). · DOI
- Mendenhall, A. R. et al. Expression of a single-copy hsp-16.2 reporter predicts life span. J. Gerontol. A Biol. Sci. Med. Sci. 67, 726–733 (2012). · DOI
- Cypser, J. R. & Johnson, T. E. Hormesis in Caenorhabditis elegans dauer-defective mutants. Biogerontology 4, 203–214 (2003). · DOI
- Lapierre, L. R., Kumsta, C., Sandri, M., Ballabio, A. & Hansen, M. Transcriptional and epigenetic regulation of autophagy in aging. Autophagy 11, 867–880 (2015). · DOI
- Shemesh N., Ben-Zvi A. in: Heat Shock Factor (ed. Nakai, A.) 93–113 (Springer, 2016). · DOI
- Dokladny, K., Myers, O. B. & Moseley, P. L. Heat shock response and autophagy--cooperation and control. Autophagy 11, 200–213 (2015). · DOI
- Melendez, A. et al. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science 301, 1387–1391 (2003). · DOI · Paper page
- Gelino, S. et al. Correction: intestinal autophagy improves healthspan and longevity in C. elegans during dietary restriction. PLoS Genet. 12, e1006271 (2016). · DOI
- Manil-Segalen, M. et al. The C. elegans LC3 acts downstream of GABARAP to degrade autophagosomes by interacting with the HOPS subunit VPS39. Dev. Cell 28, 43–55 (2014). · DOI · Paper page
- Zhang, H. et al. Guidelines for monitoring autophagy in Caenorhabditis elegans. Autophagy 11, 9–27 (2015).
- Wilkinson, D. S. et al. Phosphorylation of LC3 by the Hippo kinases STK3/STK4 is essential for autophagy. Mol. Cell. 57, 55–68 (2015). · DOI
- Xie, Y. et al. Posttranslational modification of autophagy-related proteins in macroautophagy. Autophagy 11, 28–45 (2015). · DOI · Paper page
- Wiegant, F. A., de Poot, S. A., Boers-Trilles, V. E. & Schreij, A. M. Hormesis and cellular quality control: a possible explanation for the molecular mechanisms that underlie the benefits of mild stress. Dose Response 11, 413–430 (2012).
- Chiang, W. C., Ching, T. T., Lee, H. C., Mousigian, C. & Hsu, A. L. HSF-1 regulators DDL-1/2 link insulin-like signaling to heat-shock responses and modulation of longevity. Cell 148, 322–334 (2012). · DOI · Paper page
- Lapierre, L. R. et al. The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans. Nat. Commun. 4, 2267 (2013). · DOI · Paper page
- O'Rourke, E. J. & Ruvkun, G. MXL-3 and HLH-30 transcriptionally link lipolysis and autophagy to nutrient availability. Nat. Cell Biol. 15, 668–676 (2013). · DOI
- Visvikis, O. et al. Innate host defense requires TFEB-mediated transcription of cytoprotective and antimicrobial genes. Immunity 40, 896–909 (2014). · DOI
- Shore, D. E., Carr, C. E. & Ruvkun, G. Induction of cytoprotective pathways is central to the extension of lifespan conferred by multiple longevity pathways. PLoS Genet. 8, e1002792 (2012). · DOI
- Furuhashi, T. & Sakamoto, K. FoxO/Daf-16 restored thrashing movement reduced by heat stress in Caenorhabditis elegans. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 170, 26–32 (2014). · DOI
- Olsen, A., Vantipalli, M. C. & Lithgow, G. J. Lifespan extension of Caenorhabditis elegans following repeated mild hormetic heat treatments. Biogerontology 7, 221–230 (2006). · DOI
- Cumming, R. C., Simonsen, A. & Finley, K. D. Quantitative analysis of autophagic activity in Drosophila neural tissues by measuring the turnover rates of pathway substrates. Methods Enzymol. 451, 639–651 (2008). · DOI
- Prahlad, V. & Morimoto, R. I. Integrating the stress response: lessons for neurodegenerative diseases from C. elegans. Trends Cell Biol. 19, 52–61 (2009). · DOI
- Mohri-Shiomi, A. & Garsin, D. A. Insulin signaling and the heat shock response modulate protein homeostasis in the Caenorhabditis elegans intestine during infection. J. Biol. Chem. 283, 194–201 (2008). · DOI
- Flower, T. R., Chesnokova, L. S., Froelich, C. A., Dixon, C. & Witt, S. N. Heat shock prevents alpha-synuclein-induced apoptosis in a yeast model of Parkinson's disease. J. Mol. Biol. 351, 1081–1100 (2005). · DOI
- Jia, K., Hart, A. C. & Levine, B. Autophagy genes protect against disease caused by polyglutamine expansion proteins in Caenorhabditis elegans. Autophagy 3, 21–25 (2007). · DOI
- Pietrocola, F. et al. Regulation of autophagy by stress-responsive transcription factors. Semin. Cancer Biol. 23, 310–322 (2013). · DOI
- Baird, N. A. et al. HSF-1-mediated cytoskeletal integrity determines thermotolerance and life span. Science 346, 360–363 (2014). · DOI
- Tong, Z. et al. HSF-1 is involved in attenuating the release of inflammatory cytokines induced by LPS through regulating autophagy. Shock 41, 449–453 (2014). · DOI
- Dokladny, K. et al. Regulatory coordination between two major intracellular homeostatic systems: heat shock response and autophagy. J. Biol. Chem. 288, 14959–14972 (2013). · DOI
- Desai, S. et al. Heat shock factor 1 (HSF1) controls chemoresistance and autophagy through transcriptional regulation of autophagy-related protein 7 (ATG7). J. Biol. Chem. 288, 9165–9176 (2013). · DOI
- Cypser, J. & Johnson, T. E. Hormesis extends the correlation between stress resistance and life span in long-lived mutants of Caenorhabditis elegans. Hum. Exp. Toxicol. 20, 295–296 discussion 319-20 (2001). · DOI
- Wong, E. & Cuervo, A. M. Autophagy gone awry in neurodegenerative diseases. Nat. Neurosci. 13, 805–811 (2010). · DOI · Paper page
- Alavez, S., Vantipalli, M. C., Zucker, D. J., Klang, I. M. & Lithgow, G. J. Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472, 226–229 (2011). · DOI · Paper page
- Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974). · DOI
- Kamath, R. S. & Ahringer, J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313–321 (2003). · DOI
- Rual, J. F. et al. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res. 14, 2162–2168 (2004). · DOI
- Dillin, A., Crawford, D. K. & Kenyon, C. Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 298, 830–834 (2002). · DOI · Paper page
- Rea, S. L., Ventura, N. & Johnson, T. E. Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 5, e259 (2007). · DOI · Paper page
- Kumsta, C. et al. Integrin-linked kinase modulates longevity and thermotolerance in C. elegans through neuronal control of HSF-1. Aging Cell 13, 419–430 (2014). · DOI
- Taubert, S., Van Gilst, M. R., Hansen, M. & Yamamoto, K. R. A Mediator subunit, MDT-15, integrates regulation of fatty acid metabolism by NHR-49-dependent and -independent pathways in C. elegans. Genes Dev. 20, 1137–1149 (2006). · DOI
- Hoogewijs, D., Houthoofd, K., Matthijssens, F., Vandesompele, J. & Vanfleteren, J. R. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol. 9, 9 (2008). · DOI
- Hansen, M., Hsu, A. L., Dillin, A. & Kenyon, C. New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen. PLoS Genet. 1, 119–128 (2005). · DOI
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Metadata
- Authors
- Kumsta, C., Chang, J. T., Schmalz, J., & Hansen, M.
- Venue
- Nature Communications
- Published
- 2017-02-15
- Volume
- 8
- Issue
- 1
- ISSN
- 2041-1723
- PMC
- PMC5316864
- Cited by
- 293
- References
- 5
- Language
- en
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