1,337
Views
19
CrossRef citations to date
0
Altmetric
Extra Views

Prion-based memory of heat stress in yeast

, ORCID Icon &
Pages 151-161 | Received 24 Mar 2017, Accepted 04 May 2017, Published online: 24 May 2017

REFERENCES

  • Chernova TA, Kiktev DA, Romanyuk AV, Shanks JR, Laur O, Ali M, Ghosh A, Kim D, Yang Z, Mang M, et al. Yeast short-lived actin-associated protein forms a metastable prion in response to thermal stress. Cell Rep 2017; 18(3):751-61; PMID:28099852; https://doi.org/10.1016/j.celrep.2016.12.082
  • Aguzzi A, O'Connor T. Protein aggregation diseases: pathogenicity and therapeutic perspectives. Nat Rev Drug Discov 2010; 9(3):237-48; PMID:20190788; https://doi.org/10.1038/nrd3050
  • Prusiner SB. Biology and genetics of prions causing neurodegeneration. Ann Rev Genet 2013; 47:601-23; PMID:24274755; https://doi.org/10.1146/annurev-genet-110711-155524
  • Haik S, Brandel JP. Infectious prion diseases in humans: cannibalism, iatrogenicity and zoonoses. Infect Genet Evol 2014; 26:303-12; PMID:24956437; https://doi.org/10.1016/j.meegid.2014.06.010
  • Aguzzi A, Rajendran L. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 2009; 64(6):783-90. Epub 2010/01/13; PMID:20064386
  • Jucker M, Walker LC. Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders. Ann Neurol 2011; 70(4):532-40; PMID:22028219; https://doi.org/10.1002/ana.22615
  • Prusiner SB. Cell biology. A unifying role for prions in neurodegenerative diseases. Science 2012; 336(6088):1511-3; PMID:22723400
  • Savitt JM, Dawson VL, Dawson TM. Diagnosis and treatment of Parkinson disease: molecules to medicine. J Clin Invest 2006; 116(7):1744-54; PMID:16823471; https://doi.org/10.1172/JCI29178
  • Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297(5580):353-6; PMID:12130773; https://doi.org/10.1126/science.1072994
  • Allen MT, Levy LS. Parkinson's disease and pesticide exposure–a new assessment. Critical Rev Toxicol 2013; 43(6):515-34; PMID:23844699; https://doi.org/10.3109/10408444.2013.798719
  • Duce JA, Bush AI. Biological metals and Alzheimer's disease: implications for therapeutics and diagnostics. Prog Neurobiol 2010; 92(1):1-18; PMID:20444428; https://doi.org/10.1016/j.pneurobio.2010.04.003
  • Fowler DM, Koulov AV, Balch WE, Kelly JW. Functional amyloid–from bacteria to humans. Trends Biochem Sci 2007; 32(5):217-24; PMID:17412596; https://doi.org/10.1016/j.tibs.2007.03.003
  • Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K, Rissman RA, Singru PS, Nilsson KP, Simon R, Schubert D, et al. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 2009; 325(5938):328-32. Epub 2009/06/23; PMID:19541956; https://doi.org/10.1126/science.1173155
  • Si K, Lindquist S, Kandel ER. A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 2003; 115(7):879-91; PMID:14697205; https://doi.org/10.1016/S0092-8674(03)01020-1
  • Majumdar A, Cesario WC, White-Grindley E, Jiang H, Ren F, Khan MR, Li L, Choi EM, Kannan K, Guo F, et al. Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 2012; 148(3):515-29; PMID:22284910; https://doi.org/10.1016/j.cell.2012.01.004
  • Holmes WM, Klaips CL, Serio TR. Defining the limits: Protein aggregation and toxicity in vivo. Crit Rev Biochem Mol Biol 2014; 49(4):294-303; PMID:24766537; https://doi.org/10.3109/10409238.2014.914151
  • Fowler DM, Kelly JW. Functional amyloidogenesis and cytotoxicity-insights into biology and pathology. PLoS Biol 2012; 10(12):e1001459; PMID:23300381; https://doi.org/10.1371/journal.pbio.1001459
  • Di Martino P. Bap: A New Type of Functional Amyloid. Trends Microbiol 2016; 24(9):682-4; PMID:27451288; https://doi.org/10.1016/j.tim.2016.07.004
  • Fioriti L, Myers C, Huang YY, Li X, Stephan JS, Trifilieff P, Colnaghi L, Kosmidis S, Drisaldi B, Pavlopoulos E, et al. The persistence of hippocampal-based memory requires protein synthesis mediated by the prion-like protein CPEB3. Neuron 2015; 86(6):1433-48; PMID:26074003; https://doi.org/10.1016/j.neuron.2015.05.021
  • Liebman SW, Chernoff YO. Prions in yeast. Genetics 2012; 191(4):1041-72; PMID:22879407; https://doi.org/10.1534/genetics.111.137760
  • Tuite MF. The natural history of yeast prions. Adv Appl Microbiol 2013; 84:85-137; PMID:23763759
  • Holmes DL, Lancaster AK, Lindquist S, Halfmann R. Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 2013; 153(1):153-65; PMID:23540696; https://doi.org/10.1016/j.cell.2013.02.026
  • Chernova TA, Wilkinson KD, Chernoff YO. Physiological and environmental control of yeast prions. FEMS Microbiol Rev 2014; 38(2):326-44; PMID:24236638; https://doi.org/10.1111/1574-6976.12053
  • Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK, Lindquist S. Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 2012; 482(7385):363-8; PMID:22337056; https://doi.org/10.1038/nature10875
  • Caudron F, Barral Y. A super-assembly of Whi3 encodes memory of deceptive encounters by single cells during yeast courtship. Cell 2013; 155(6):1244-57; PMID:24315096; https://doi.org/10.1016/j.cell.2013.10.046
  • McGlinchey RP, Kryndushkin D, Wickner RB. Suicidal [PSI+] is a lethal yeast prion. Proc Natl Acad Sci U S A 2011; 108(13):5337-41; PMID:21402947; https://doi.org/10.1073/pnas.1102762108
  • Wickner RB, Edskes HK, Bateman D, Kelly AC, Gorkovskiy A. The yeast prions [PSI+] and [URE3] are molecular degenerative diseases. Prion 2011; 5(4):258-62; PMID:22052353; https://doi.org/10.4161/pri.17748 10.4161/pri.5.4.17748
  • Saupe SJ. The [Het-s] prion of Podospora anserina and its role in heterokaryon incompatibility. Semin Cell Dev Biol 2011; 22(5):460-8; PMID:21334447; https://doi.org/10.1016/j.semcdb.2011.02.019
  • Serio TR, Cashikar AG, Moslehi JJ, Kowal AS, Lindquist SL. Yeast prion [psi +] and its determinant, Sup35p. Methods Enzymol 1999; 309:649-73. Epub 1999/10/03; PMID:10507053
  • Chernoff YO, Derkach IL, Inge-Vechtomov SG. Multicopy SUP35 gene induces de-novo appearance of psi-like factors in the yeast Saccharomyces cerevisiae. Curr Genet 1993; 24(3):268-70. Epub 1993/09/01; PMID:8221937; https://doi.org/10.1007/BF00351802
  • Derkatch IL, Bradley ME, Zhou P, Chernoff YO, Liebman SW. Genetic and environmental factors affecting the de novo appearance of the [PSI+] prion in Saccharomyces cerevisiae. Genetics 1997; 147(2):507-19. Epub 1997/10/23; PMID:9335589
  • Derkatch IL, Bradley ME, Hong JY, Liebman SW. Prions affect the appearance of other prions: the story of [PIN(+)]. Cell 2001; 106(2):171-82. Epub 2001/08/21; PMID:11511345; https://doi.org/10.1016/S0092-8674(01)00427-5
  • Osherovich LZ, Weissman JS. Multiple Gln/Asn-rich prion domains confer susceptibility to induction of the yeast [PSI(+)] prion. Cell 2001; 106(2):183-94. Epub 2001/08/21; PMID:11511346; https://doi.org/10.1016/S0092-8674(01)00440-8
  • Derkatch IL, Uptain SM, Outeiro TF, Krishnan R, Lindquist SL, Liebman SW. Effects of Q/N-rich, polyQ, and non-polyQ amyloids on the de novo formation of the [PSI+] prion in yeast and aggregation of Sup35 in vitro. Proc Natl Acad Sci U S A 2004; 101(35):12934-9. Epub 2004/08/25; PMID:15326312; https://doi.org/10.1073/pnas.0404968101
  • Sondheimer N, Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol Cell 2000; 5(1):163-72. Epub 2000/03/11; PMID:10678178; https://doi.org/10.1016/S1097-2765(00)80412-8
  • Meriin AB, Zhang X, He X, Newnam GP, Chernoff YO, Sherman MY. Huntington toxicity in yeast model depends on polyglutamine aggregation mediated by a prion-like protein Rnq1. J Cell Biol 2002; 157(6):997-1004; PMID:12058016; https://doi.org/10.1083/jcb.200112104
  • Derkatch IL, Liebman SW. Prion-prion interactions. Prion 2007; 1(3):161-9. Epub 2007/07/01; PMID:19164893; https://doi.org/10.4161/pri.1.3.4837
  • Alberti S, Halfmann R, King O, Kapila A, Lindquist S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 2009; 137(1):146-58. Epub 2009/04/07; PMID:19345193
  • Walker LC, LeVine H 3rd. Corruption and spread of pathogenic proteins in neurodegenerative diseases. J Biol Chem 2012; 287(40):33109-15; PMID:22879600; https://doi.org/10.1074/jbc.R112.399378
  • Yang Z, Stone DE, Liebman SW. Prion-promoted phosphorylation of heterologous amyloid is coupled with ubiquitin-proteasome system inhibition and toxicity. Mol Microbiol 2014; 93(5):1043-56; PMID:25039275; https://doi.org/10.1111/mmi.12716
  • Chernova TA, Romanyuk AV, Karpova TS, Shanks JR, Ali M, Moffatt N, Howie RL, O'Dell A, McNally JG, Liebman SW, et al. Prion induction by the short-lived, stress-induced protein Lsb2 is regulated by ubiquitination and association with the actin cytoskeleton. Mol Cell 2011; 43(2):242-52; PMID:21777813; https://doi.org/10.1016/j.molcel.2011.07.001
  • Tyler JJ, Allwood EG, Ayscough KR. WASP family proteins, more than Arp2/3 activators. Biochem Soc Trans 2016; 44(5):1339-45; PMID:27911716; https://doi.org/10.1042/BST20160176
  • Ali M, Chernova TA, Newnam GP, Yin L, Shanks J, Karpova TS, Lee A, Laur O, Subramanian S, Kim D, et al. Stress-dependent proteolytic processing of the actin assembly protein Lsb1 modulates a yeast prion. J Biol Chem 2014; 289(40):27625-39; PMID:25143386; https://doi.org/10.1074/jbc.M114.582429
  • Bagriantsev SN, Kushnirov VV, Liebman SW. Analysis of amyloid aggregates using agarose gel electrophoresis. Methods Enzymol 2006; 412:33-48. Epub 2006/10/19; PMID:17046650
  • Halfmann R, Alberti S, Krishnan R, Lyle N, O'Donnell CW, King OD, Berger B, Pappu RV, Lindquist S. Opposing effects of glutamine and asparagine govern prion formation by intrinsically disordered proteins. Mol Cell 2011; 43(1):72-84; PMID:21726811; https://doi.org/10.1016/j.molcel.2011.05.013
  • Kushnirov VV, Ter-Avanesyan MD. Structure and replication of yeast prions. Cell 1998; 94(1):13-6; PMID:9674422; https://doi.org/10.1016/S0092-8674(00)81216-7
  • Tanaka M, Collins SR, Toyama BH, Weissman JS. The physical basis of how prion conformations determine strain phenotypes. Nature 2006; 442(7102):585-9; PMID:16810177; https://doi.org/10.1038/nature04922
  • Chernoff YO, Lindquist SL, Ono B, Inge-Vechtomov SG, Liebman SW. Role of the chaperone protein Hsp104 in propagation of the yeast prion-like factor [psi+]. Science 1995; 268(5212):880-4. Epub 1995/05/12; PMID:7754373; https://doi.org/10.1126/science.7754373
  • Newnam GP, Wegrzyn RD, Lindquist SL, Chernoff YO. Antagonistic interactions between yeast chaperones Hsp104 and Hsp70 in prion curing. Mol Cell Biol 1999; 19(2):1325-33. Epub 1999/01/16; PMID:9891066; https://doi.org/10.1128/MCB.19.2.1325
  • Allen KD, Wegrzyn RD, Chernova TA, Muller S, Newnam GP, Winslett PA, Wittich KB, Wilkinson KD, Chernoff YO. Hsp70 chaperones as modulators of prion life cycle: novel effects of Ssa and Ssb on the Saccharomyces cerevisiae prion [PSI+]. Genetics 2005; 169(3):1227-42. Epub 2004/11/17; PMID:15545639; https://doi.org/10.1534/genetics.104.037168
  • Kummer E, Oguchi Y, Seyffer F, Bukau B, Mogk A. Mechanism of Hsp104/ClpB inhibition by prion curing Guanidinium hydrochloride. FEBS Lett 2013; 587(6):810-7; PMID:23416293; https://doi.org/10.1016/j.febslet.2013.02.011
  • Chernova TA, Wilkinson KD, Chernoff YO. Prions, Chaperones, and Proteostasis in Yeast. Cold Spring Harb Perspect Biol 2017; 9(2):pii: a023663; PMID:27815300; https://doi.org/10.1101/cshperspect.a023663
  • Tuite MF, Mundy CR, Cox BS. Agents that cause a high frequency of genetic change from [psi+] to [psi-] in Saccharomyces cerevisiae. Genetics 1981; 98(4):691-711; PMID:7037537
  • Cox BS, Tuite MF, McLaughlin CS. The psi factor of yeast: a problem in inheritance. Yeast 1988; 4(3):159-78; PMID:3059716; https://doi.org/10.1002/yea.320040302
  • Newnam GP, Birchmore JL, Chernoff YO. Destabilization and recovery of a yeast prion after mild heat shock. J Mol Biol 2011; 408(3):432-48; PMID:21392508; https://doi.org/10.1016/j.jmb.2011.02.034
  • Winkler J, Tyedmers J, Bukau B, Mogk A. Chaperone networks in protein disaggregation and prion propagation. J Struct Biol 2012; 179(2):152-60; PMID:22580344; https://doi.org/10.1016/j.jsb.2012.05.002
  • Winkler J, Tyedmers J, Bukau B, Mogk A. Hsp70 targets Hsp100 chaperones to substrates for protein disaggregation and prion fragmentation. J Cell Biol 2012; 198(3):387-404; PMID:22869599; https://doi.org/10.1083/jcb.201201074
  • Klaips CL, Hochstrasser ML, Langlois CR, Serio TR. Correction: Spatial quality control bypasses cell-based limitations on proteostasis to promote prion curing. eLife 2015; 4:e06494; PMID:25626954; https://doi.org/10.7554/eLife.06494
  • Liu B, Larsson L, Franssens V, Hao X, Hill SM, Andersson V, Hoglund D, Song J, Yang X, Oling D, et al. Segregation of protein aggregates involves actin and the polarity machinery. Cell 2011; 147(5):959-61; PMID:22118450; https://doi.org/10.1016/j.cell.2011.11.018
  • Ness F, Cox BS, Wongwigkarn J, Naeimi WR, Tuite MF. Over-expression of the molecular chaperone Hsp104 in Saccharomyces cerevisiae results in the malpartition of [PSI+ ] propagons. Mol Microbiol 2017; 104(1):125-43; PMID:28073182; https://doi.org/10.1111/mmi.13617
  • Fang NN, Ng AH, Measday V, Mayor T. Hul5 HECT ubiquitin ligase plays a major role in the ubiquitylation and turnover of cytosolic misfolded proteins. Nat Cell Biol 2011; 13(11):1344-52; PMID:21983566; https://doi.org/10.1038/ncb2343
  • Derkatch IL, Bradley ME, Masse SV, Zadorsky SP, Polozkov GV, Inge-Vechtomov SG, Liebman SW. Dependence and independence of [PSI(+)] and [PIN(+)]: a two-prion system in yeast? EMBO J 2000; 19(9):1942-52. Epub 2000/05/03; PMID:10790361; https://doi.org/10.1093/emboj/19.9.1942
  • Chernoff YO. Stress and prions: lessons from the yeast model. FEBS Lett 2007; 581(19):3695-701. Epub 2007/05/19; PMID:17509571
  • Tyedmers J, Madariaga ML, Lindquist S. Prion switching in response to environmental stress. PLoS Biol 2008; 6(11):e294. Epub 2008/12/11; PMID:19067491; https://doi.org/10.1371/journal.pbio.0060294
  • Li L, Kowal AS. Environmental regulation of prions in yeast. PLoS Pathog 2012; 8(11):e1002973; PMID:23166488; https://doi.org/10.1371/journal.ppat.1002973
  • Spiess M, de Craene JO, Michelot A, Rinaldi B, Huber A, Drubin DG, Winsor B, Friant S. Lsb1 is a negative regulator of las17 dependent actin polymerization involved in endocytosis. PloS One 2013; 8(4):e61147; PMID:23577202; https://doi.org/10.1371/journal.pone.0061147
  • Masison DC, Wickner RB. Prion-inducing domain of yeast Ure2p and protease resistance of Ure2p in prion-containing cells. Science 1995; 270(5233):93-5. Epub 1995/10/06; PMID:7569955; https://doi.org/10.1126/science.270.5233.93
  • Paushkin SV, Kushnirov VV, Smirnov VN, Ter-Avanesyan MD. Propagation of the yeast prion-like [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor. EMBO J 1996; 15(12):3127-34. Epub 1996/06/17; PMID:8670813
  • Colby DW, Prusiner SB. Prions. Cold Spring Harb Perspect Biol 2011; 3(1):a006833; PMID:21421910; https://doi.org/10.1101/cshperspect.a006833
  • Suzuki G, Shimazu N, Tanaka M. A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 2012; 336(6079):355-9; PMID:22517861; https://doi.org/10.1126/science.1219491
  • Pastor MT, Esteras-Chopo A, Serrano L. Hacking the code of amyloid formation: the amyloid stretch hypothesis. Prion 2007; 1(1):9-14; PMID:19164912; https://doi.org/10.4161/pri.1.1.4100
  • Paul KR, Hendrich CG, Waechter A, Harman MR, Ross ED. Generating new prions by targeted mutation or segment duplication. Proc Natl Acad Sci U S A 2015; 112(28):8584-9; PMID:26100899; https://doi.org/10.1073/pnas.1501072112
  • Sattlegger E, Chernova TA, Gogoi NM, Pillai IV, Chernoff YO, Munn AL. Yeast studies reveal moonlighting functions of the ancient actin cytoskeleton. IUBMB Life 2014; 66(8):538-45; PMID:25138357; https://doi.org/10.1002/iub.1294
  • Sampaio JP, Goncalves P. Natural populations of Saccharomyces kudriavzevii in Portugal are associated with oak bark and are sympatric with S. cerevisiae and S. paradoxus. Appl Environ Microbiol 2008; 74(7):2144-52; PMID:18281431; https://doi.org/10.1128/AEM.02396-07
  • Salvado Z, Arroyo-Lopez FN, Guillamon JM, Salazar G, Querol A, Barrio E. Temperature adaptation markedly determines evolution within the genus Saccharomyces. Appl Environ Microbiol 2011; 77(7):2292-302; PMID:21317255; https://doi.org/10.1128/AEM.01861-10

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.