Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress
10.1038/ncb2838
Crossref journal-article
Springer Science and Business Media LLC
Nature Cell Biology (297)
Bibliography

Escusa-Toret, S., Vonk, W. I. M., & Frydman, J. (2013). Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nature Cell Biology, 15(10), 1231–1243.

Authors 3
  1. Stéphanie Escusa-Toret (first)
  2. Willianne I. M. Vonk (additional)
  3. Judith Frydman (additional)
References 65 Referenced 309
  1. Balch, W. E., Morimoto, R. I., Dillin, A. & Kelly, J. W. Adapting proteostasis for disease intervention. Science 319, 916–919 (2008). (10.1126/science.1141448) / Science by WE Balch (2008)
  2. Lindquist, S. L. & Kelly, J. W. Chemical and biological approaches for adapting proteostasis to ameliorate protein misfolding and aggregation diseases: progress and prognosis. Cold Spring Harb. Perspect. Biol. 3, 1–34 (2011). (10.1101/cshperspect.a004507) / Cold Spring Harb. Perspect. Biol. by SL Lindquist (2011)
  3. Chiti, F. & Dobson, C. M. Protein misfolding, functional amyloid, and human disease. Ann. Rev. Biochem. 75, 333–366 (2006). (10.1146/annurev.biochem.75.101304.123901) / Ann. Rev. Biochem. by F Chiti (2006)
  4. Houck, S.A., Singh, S. & Cyr, D. M. Cellular responses to misfolded proteins and protein aggregates. Methods Mol. Biol. 832, 455–461 (2012). (10.1007/978-1-61779-474-2_32) / Methods Mol. Biol. by SA Houck (2012)
  5. Chen, B., Retzlaff, M., Roos, T. & Frydman, J. Cellular strategies of protein quality control. Cold Spring Harb. Perspect. Biol. 3, a004374 (2011). (10.1101/cshperspect.a004374) / Cold Spring Harb. Perspect. Biol. by B Chen (2011)
  6. Kaganovich, D., Kopito, R. & Frydman, J. Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088–1095 (2008). (10.1038/nature07195) / Nature by D Kaganovich (2008)
  7. Specht, S., Miller, S. B., Mogk, A. & Bukau, B. Hsp42 is required for sequestration of protein aggregates into deposition sites in Saccharomyces cerevisiae. J. Cell Biol. 195, 617–629 (2011). (10.1083/jcb.201106037) / J. Cell Biol. by S Specht (2011)
  8. Malinovska, L., Kroschwald, S., Munder, M. C., Richter, D. & Alberti, S. Molecular chaperones and stress-inducible protein-sorting factors coordinate the spatiotemporal distribution of protein aggregates. Mol. Biol. Cell 23, 3041–3056 (2012). (10.1091/mbc.e12-03-0194) / Mol. Biol. Cell by L Malinovska (2012)
  9. Johnston, J. A., Ward, C. L. & Kopito, R. R. Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143, 1883–1898 (1998). (10.1083/jcb.143.7.1883) / J. Cell Biol. by JA Johnston (1998)
  10. Zhang, X. & Qian, S. B. Chaperone-mediated hierarchical control in targeting misfolded proteins to aggresomes. Mol. Biol. Cell 22, 3277–3288 (2011). (10.1091/mbc.e11-05-0388) / Mol. Biol. Cell by X Zhang (2011)
  11. Douglas, P. M., Summers, D. W. & Cyr, D. M. Molecular chaperones antagonize proteotoxicity by differentially modulating protein aggregation pathways. Prion 3, 51–58 (2009). (10.4161/pri.3.2.8587) / Prion by PM Douglas (2009)
  12. Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W. & Dillin, A. Opposing activities protect against age-onset proteotoxicity. Science 313, 1604–1610 (2006). (10.1126/science.1124646) / Science by E Cohen (2006)
  13. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R. & Finkbeiner, S. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805–810 (2004). (10.1038/nature02998) / Nature by M Arrasate (2004)
  14. Liu, B. et al. The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140, 257–267 (2010). (10.1016/j.cell.2009.12.031) / Cell by B Liu (2010)
  15. Nakatogawa, H., Ichimura, Y. & Ohsumi, Y. Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130, 165–178 (2007). (10.1016/j.cell.2007.05.021) / Cell by H Nakatogawa (2007)
  16. Sheth, U. & Parker, R. Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125, 1095–1109 (2006). (10.1016/j.cell.2006.04.037) / Cell by U Sheth (2006)
  17. Toshima, J. Y. et al. Spatial dynamics of receptor-mediated endocytic trafficking in budding yeast revealed by using fluorescent alpha-factor derivatives. Proc. Natl Acad. Sci. USA 103, 5793–5798 (2006). (10.1073/pnas.0601042103) / Proc. Natl Acad. Sci. USA by JY Toshima (2006)
  18. Wright, R., Basson, M., D’Ari, L. & Rine, J. Increased amounts of HMG-CoA reductase induce ”karmellae”: a proliferation of stacked membrane pairs surrounding the yeast nucleus. J. Cell Biol. 107, 101–114 (1988). (10.1083/jcb.107.1.101) / J. Cell Biol. by R Wright (1988)
  19. Shibata, Y., Voeltz, G. K. & Rapoport, T. A. Rough sheets and smooth tubules. Cell 126, 435–439 (2006). (10.1016/j.cell.2006.07.019) / Cell by Y Shibata (2006)
  20. Voeltz, G. K., Prinz, W. A., Shibata, Y., Rist, J. M. & Rapoport, T. A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573–586 (2006). (10.1016/j.cell.2005.11.047) / Cell by GK Voeltz (2006)
  21. Shibata, Y. et al. The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 283, 18892–18904 (2008). (10.1074/jbc.M800986200) / J. Biol. Chem. by Y Shibata (2008)
  22. West, M., Zurek, N., Hoenger, A. & Voeltz, G. K. A 3D analysis of yeast ER structure reveals how ER domains are organized by membrane curvature. J. Cell Biol. 193, 333–346 (2011). (10.1083/jcb.201011039) / J. Cell Biol. by M West (2011)
  23. McDonough, H. & Patterson, C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 8, 303–308 (2003). (10.1379/1466-1268(2003)008<0303:CALBTC>2.0.CO;2) / Cell Stress Chaperones by H McDonough (2003)
  24. Mayer, M. P. & Bukau, B. Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol. Life Sci. 62, 670–684 (2005). (10.1007/s00018-004-4464-6) / Cell Mol. Life Sci. by MP Mayer (2005)
  25. McClellan, A. J., Scott, M. D. & Frydman, J. Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121, 739–748 (2005). (10.1016/j.cell.2005.03.024) / Cell by AJ McClellan (2005)
  26. Coppinger, J. A. et al. A chaperone trap contributes to the onset of cystic fibrosis. PLoS One 7, e37682 (2012). (10.1371/journal.pone.0037682) / PLoS One by JA Coppinger (2012)
  27. Schneider, C. et al. Pharmacologic shifting of a balance between protein refolding and degradation mediated by Hsp90. Proc. Natl Acad. Sci. USA 93, 14536–14541 (1996). (10.1073/pnas.93.25.14536) / Proc. Natl Acad. Sci. USA by C Schneider (1996)
  28. Becker, J., Walter, W., Yan, W. & Craig, E. A. Functional interaction of cytosolic hsp70 and a DnaJ-related protein, Ydj1p, in protein translocation in vivo. Mol. Cell Biol. 16, 4378–4386 (1996). (10.1128/MCB.16.8.4378) / Mol. Cell Biol. by J Becker (1996)
  29. Caplan, A. J., Tsai, J., Casey, P. J. & Douglas, M. G. Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. J. Biol. Chem. 267, 18890–18895 (1992). (10.1016/S0021-9258(19)37044-9) / J. Biol. Chem. by AJ Caplan (1992)
  30. Flom, G. A., Lemieszek, M., Fortunato, E. A. & Johnson, J. L. Farnesylation of Ydj1 is required for in vivo interaction with Hsp90 client proteins. Mol. Biol. Cell 19, 5249–5258 (2008). (10.1091/mbc.e08-04-0435) / Mol. Biol. Cell by GA Flom (2008)
  31. Kampinga, H. H. & Craig, E. A. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. Mol. Cell Biol. 11, 579–592 (2010). (10.1038/nrm2941) / Nat. Rev. Mol. Cell Biol. by HH Kampinga (2010)
  32. Youker, R. T., Walsh, P., Beilharz, T., Lithgow, T. & Brodsky, J. L. Distinct rolesfor the Hsp40 and Hsp90 molecular chaperones during cystic fibrosis transmembrane conductance regulator degradation in yeast. Mol. Biol. Cell 15, 4787–4797 (2004). (10.1091/mbc.e04-07-0584) / Mol. Biol. Cell by RT Youker (2004)
  33. Shorter, J. & Lindquist, S. Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J. 27, 2712–2724 (2008). (10.1038/emboj.2008.194) / EMBO J. by J Shorter (2008)
  34. Tipton, K. A., Verges, K. J. & Weissman, J. S. In vivo monitoring of the prion replication cycle reveals a critical role for Sis1 in delivering substrates to Hsp104. Mol. Cell 32, 584–591 (2008). (10.1016/j.molcel.2008.11.003) / Mol. Cell by KA Tipton (2008)
  35. Gupta, R. et al. Firefly luciferase mutants as sensors of proteome stress. Nat. Methods 8, 879–884 (2011). (10.1038/nmeth.1697) / Nat. Methods by R Gupta (2011)
  36. Chernoff, Y. O., Lindquist, S. L., Ono, B., Inge-Vechtomov, S. G. & Liebman, S. W. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi +]. Science 268, 880–884 (1995). (10.1126/science.7754373) / Science by YO Chernoff (1995)
  37. Sondheimer, N. & Lindquist, S. Rnq1: an epigenetic modifier of protein function in yeast. Mol. Cell 5, 163–172 (2000). (10.1016/S1097-2765(00)80412-8) / Mol. Cell by N Sondheimer (2000)
  38. Meriin, A. B. et al. Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J. Cell Biol. 157, 997–1004 (2002). (10.1083/jcb.200112104) / J. Cell Biol. by AB Meriin (2002)
  39. Piper, P. W. The heat shock and ethanol stress responses of yeast exhibit extensive similarity and functional overlap. FEMS Microbiol. Lett. 134, 121–127 (1995). (10.1111/j.1574-6968.1995.tb07925.x) / FEMS Microbiol. Lett. by PW Piper (1995)
  40. Trotter, E. W. et al. Misfolded proteins are competent to mediate a subset of the responses to heat shock in Saccharomyces cerevisiae. J. Biol. Chem. 277, 44817–44825 (2002). (10.1074/jbc.M204686200) / J. Biol. Chem. by EW Trotter (2002)
  41. Morimoto, R. I. Proteotoxic stress and inducible chaperone networks in neurodegenerative disease and aging. Genes Dev. 22, 1427–1438 (2008). (10.1101/gad.1657108) / Genes Dev. by RI Morimoto (2008)
  42. Conn, C. S. & Qian, S. B. mTOR signaling in protein homeostasis: less is more? Cell Cycle 10, 1940–1947 (2011). (10.4161/cc.10.12.15858) / Cell Cycle by CS Conn (2011)
  43. Taylor, R. C. & Dillin, A. Aging as an event of proteostasis collapse. Cold Spring Harb. Perspect. Biol. 3, 1–17 (2011). (10.1101/cshperspect.a004440) / Cold Spring Harb. Perspect. Biol. by RC Taylor (2011)
  44. Fabrizio, P. & Longo, V. D. The chronological life span of Saccharomyces cerevisiae. Aging Cell 2, 73–81 (2003). (10.1046/j.1474-9728.2003.00033.x) / Aging Cell by P Fabrizio (2003)
  45. Narayanaswamy, R. et al. Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proc. Natl Acad. Sci. USA 106, 10147–10152 (2009). (10.1073/pnas.0812771106) / Proc. Natl Acad. Sci. USA by R Narayanaswamy (2009)
  46. Peters, T. W. et al. Tor1 regulates protein solubility in Saccharomyces cerevisiae. Mol. Biol. Cell 23, 4679–4688 (2012). (10.1091/mbc.e12-08-0620) / Mol. Biol. Cell by TW Peters (2012)
  47. Kapahi, P. et al. With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab. 11, 453–465 (2010). (10.1016/j.cmet.2010.05.001) / Cell Metab. by P Kapahi (2010)
  48. Glover, J. R. & Lindquist, S. Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73–82 (1998). (10.1016/S0092-8674(00)81223-4) / Cell by JR Glover (1998)
  49. Mandal, A. K. et al. Hsp110 chaperones control client fate determination in the hsp70-Hsp90 chaperone system. Mol. Biol. Cell 21, 1439–1448 (2010). (10.1091/mbc.e09-09-0779) / Mol. Biol. Cell by AK Mandal (2010)
  50. Huyer, G. et al. Distinct machinery is required in Saccharomyces cerevisiae for the endoplasmic reticulum-associated degradation of a multispanning membrane protein and a soluble luminal protein. J. Biol. Chem. 279, 38369–38378 (2004). (10.1074/jbc.M402468200) / J. Biol. Chem. by G Huyer (2004)
  51. Ouellet, J. & Barral, Y. Organelle segregation during mitosis: lessons from asymmetrically dividing cells. J. Cell Biol. 196, 305–313 (2012). (10.1083/jcb.201102078) / J. Cell Biol. by J Ouellet (2012)
  52. Zhou, C. et al. Motility and segregation of Hsp104-associated protein aggregates in budding yeast. Cell 147, 1186–1196 (2011). (10.1016/j.cell.2011.11.002) / Cell by C Zhou (2011)
  53. Gidalevitz, T., Krupinski, T., Garcia, S. & Morimoto, R. I. Destabilizing protein polymorphisms in the genetic background direct phenotypic expression of mutant SOD1 toxicity. PLoS Genet. 5, e1000399 (2009). (10.1371/journal.pgen.1000399) / PLoS Genet. by T Gidalevitz (2009)
  54. Olzscha, H. et al. Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144, 67–78 (2011). (10.1016/j.cell.2010.11.050) / Cell by H Olzscha (2011)
  55. Kikis, E. A., Gidalevitz, T. & Morimoto, R. I. Protein homeostasis in models of aging and age-related conformational disease. Adv. Exp. Med. Biol. 694, 138–159 (2010). (10.1007/978-1-4419-7002-2_11) / Adv. Exp. Med. Biol. by EA Kikis (2010)
  56. Shorter, J. Hsp104: a weapon to combat diverse neurodegenerative disorders. Neurosignals 16, 63–74 (2008). (10.1159/000109760) / Neurosignals by J Shorter (2008)
  57. Gidalevitz, T., Prahlad, V. & Morimoto, R. I. The stress of protein misfolding: from single cells to multicellular organisms. Cold Spring Harb. Perspect. Biol. 3, 1–18 (2011). (10.1101/cshperspect.a009704) / Cold Spring Harb. Perspect. Biol. by T Gidalevitz (2011)
  58. Durieux, J., Wolff, S. & Dillin, A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 144, 79–91 (2011). (10.1016/j.cell.2010.12.016) / Cell by J Durieux (2011)
  59. Winzeler, E. A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901–906 (1999). (10.1126/science.285.5429.901) / Science by EA Winzeler (1999)
  60. Nathan, D. F. & Lindquist, S. Mutational analysis of Hsp90 function: interactions with a steroid receptor and a protein kinase. Mol. Cell Biol. 15, 3917–3925 (1995). (10.1128/MCB.15.7.3917) / Mol. Cell Biol. by DF Nathan (1995)
  61. Kaksonen, M., Toret, C. P. & Drubin, D. G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123, 305–320 (2005). (10.1016/j.cell.2005.09.024) / Cell by M Kaksonen (2005)
  62. Longtine, M. S. et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953–961 (1998). (10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U) / Yeast by MS Longtine (1998)
  63. Janke, C. et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947–962 (2004). (10.1002/yea.1142) / Yeast by C Janke (2004)
  64. Alberti, S., Gitler, A. D. & Lindquist, S. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24, 913–919 (2007). (10.1002/yea.1502) / Yeast by S Alberti (2007)
  65. Furuta, N., Fujimura-Kamada, K., Saito, K., Yamamoto, T. & Tanaka, K. Endocytic recycling in yeast is regulated by putative phospholipid translocases and the Ypt31p/32p-Rcy1p pathway. Mol. Biol. Cell 18, 295–312 (2007). (10.1091/mbc.e06-05-0461) / Mol. Biol. Cell by N Furuta (2007)
Dates
Type When
Created 11 years, 11 months ago (Sept. 13, 2013, 1:23 a.m.)
Deposited 2 years, 3 months ago (May 18, 2023, 3:41 p.m.)
Indexed 11 hours, 37 minutes ago (Aug. 30, 2025, 1 p.m.)
Issued 11 years, 11 months ago (Sept. 15, 2013)
Published 11 years, 11 months ago (Sept. 15, 2013)
Published Online 11 years, 11 months ago (Sept. 15, 2013)
Published Print 11 years, 10 months ago (Oct. 1, 2013)
Funders 0

None

@article{Escusa_Toret_2013, title={Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress}, volume={15}, ISSN={1476-4679}, url={http://dx.doi.org/10.1038/ncb2838}, DOI={10.1038/ncb2838}, number={10}, journal={Nature Cell Biology}, publisher={Springer Science and Business Media LLC}, author={Escusa-Toret, Stéphanie and Vonk, Willianne I. M. and Frydman, Judith}, year={2013}, month=sep, pages={1231–1243} }