1932

Abstract

Prions, a self-templating amyloidogenic state of normal cellular proteins such as PrP, have been identified as the basis of a number of disease states, particularly diseases of the nervous system. This finding has led to the notion that protein aggregation, namely prionogenic aggregates and amyloids, is primarily harmful for the organism. However, identification of proteins in a prion-like state that are not harmful and may even be beneficial has begun to change this perception. This review discusses when and how a prion-based protein conformational switch may be utilized to generate a sustained physiological change in response to a transient stimulus.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100913-013409
2015-11-13
2024-06-21
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/31/1/annurev-cellbio-100913-013409.html?itemId=/content/journals/10.1146/annurev-cellbio-100913-013409&mimeType=html&fmt=ahah

Literature Cited

  1. Adams DH. 1970. The nature of the scrapie agent. A review of recent progress. Pathol. Biol. 18:559–77 [Google Scholar]
  2. Aguzzi A, Weissmann C. 1998. Prion diseases. Haemophilia 4:619–27 [Google Scholar]
  3. Alberti S, Halfmann R, King O, Kapila A, Lindquist S. 2009. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137:146–58 [Google Scholar]
  4. Ashe KH, Zahs KR. 2010. Probing the biology of Alzheimer's disease in mice. Neuron 66:631–45 [Google Scholar]
  5. Bailey CH, Kandel ER, Si K. 2004. The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 44:49–57 [Google Scholar]
  6. Bernhardt HS. 2012. The RNA world hypothesis: the worst theory of the early evolution of life (except for all the others)a. Biol. Direct 7:23 [Google Scholar]
  7. Bossy-Wetzel E, Schwarzenbacher R, Lipton SA. 2004. Molecular pathways to neurodegeneration. Nat. Med. 10:Suppl.S2–9 [Google Scholar]
  8. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C. et al. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–32 [Google Scholar]
  9. Cai X, Chen J, Xu H, Liu S, Jiang QX. et al. 2014. Prion-like polymerization underlies signal transduction in antiviral immune defense and inflammasome activation. Cell 156:1207–22 [Google Scholar]
  10. Cai X, Chen ZJ. 2014. Prion-like polymerization as a signaling mechanism. Trends Immunol. 35:622–30 [Google Scholar]
  11. Caudron F, Barral Y. 2013. A super-assembly of Whi3 encodes memory of deceptive encounters by single cells during yeast courtship. Cell 155:1244–57 [Google Scholar]
  12. Cech TR. 2009. Evolution of biological catalysis: ribozyme to RNP enzyme. Cold Spring Harb. Symp. Quant. Biol. 74:11–16 [Google Scholar]
  13. Chernoff YO. 2004. Amyloidogenic domains, prions and structural inheritance: rudiments of early life or recent acquisition?. Curr. Opin. Chem. Biol. 8:665–71 [Google Scholar]
  14. Chien P, Weissman JS. 2001. Conformational diversity in a yeast prion dictates its seeding specificity. Nature 410:223–27 [Google Scholar]
  15. Chien P, Weissman JS, DePace AH. 2004. Emerging principles of conformation-based prion inheritance. Annu. Rev. Biochem. 73:617–56 [Google Scholar]
  16. Collinge J, Clarke AR. 2007. A general model of prion strains and their pathogenicity. Science 318:930–36 [Google Scholar]
  17. Coustou V, Deleu C, Saupe S, Begueret J. 1997. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog. PNAS 94:9773–78 [Google Scholar]
  18. Crick F. 1984. Memory and molecular turnover. Nature 312:101 [Google Scholar]
  19. Cushman M, Johnson BS, King OD, Gitler AD, Shorter J. 2010. Prion-like disorders: blurring the divide between transmissibility and infectivity. J. Cell Sci. 123:1191–201 [Google Scholar]
  20. Darwin C. 2003 (1859). The Origin of Species New York: Signet [Google Scholar]
  21. Derkatch IL, Uptain SM, Outeiro TF, Krishnan R, Lindquist SL, Liebman SW. 2004. 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. PNAS 101:12934–39 [Google Scholar]
  22. Dobson CM. 2004. Principles of protein folding, misfolding and aggregation. Semin. Cell Dev. Biol. 15:3–16 [Google Scholar]
  23. Du Z, Park KW, Yu H, Fan Q, Li L. 2008. Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae. Nat. Genet. 40:460–65 [Google Scholar]
  24. Dudai Y. 2002. Molecular bases of long-term memories: a question of persistence. Curr. Opin. Neurobiol. 12:211–16 [Google Scholar]
  25. Eaglestone SS, Cox BS, Tuite MF. 1999. Translation termination efficiency can be regulated in Saccharomyces cerevisiae by environmental stress through a prion-mediated mechanism. EMBO J. 18:1974–81 [Google Scholar]
  26. Eisenberg D, Jucker M. 2012. The amyloid state of proteins in human diseases. Cell 148:1188–203 [Google Scholar]
  27. Encalada SE, Goldstein LS. 2014. Biophysical challenges to axonal transport: motor-cargo deficiencies and neurodegeneration. Annu. Rev. Biophys. 43:141–69 [Google Scholar]
  28. Fioriti L, Myers C, Huang YY, Li X, Stephan JS. 2015. The persistence of hippocampal-based memory requires protein synthesis mediated by the prion-like protein CPEB3. Neuron 86:61433–48 [Google Scholar]
  29. Fowler DM, Koulov AV, Alory-Jost C, Marks MS, Balch WE, Kelly JW. 2006. Functional amyloid formation within mammalian tissue. PLOS Biol. 4:e6 [Google Scholar]
  30. Franklin TB, Russig H, Weiss IC, Graff J, Linder N. et al. 2010. Epigenetic transmission of the impact of early stress across generations. Biol. Psychiatry 68:408–15 [Google Scholar]
  31. Giasson BI, Forman MS, Higuchi M, Golbe LI, Graves CL. et al. 2003. Initiation and synergistic fibrillization of τ and α-synuclein. Science 300:636–40 [Google Scholar]
  32. Griffith JS. 1967. Self-replication and scrapie. Nature 215:1043–44 [Google Scholar]
  33. Halfmann R, Jarosz DF, Jones SK, Chang A, Lancaster AK, Lindquist S. 2012. Prions are a common mechanism for phenotypic inheritance in wild yeasts. Nature 482:363–68 [Google Scholar]
  34. Han TW, Kato M, Xie S, Wu LC, Mirzaei H. et al. 2012. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149:768–79 [Google Scholar]
  35. Harbi D, Harrison PM. 2014. Classifying prion and prion-like phenomena. Prion 8:161–65 [Google Scholar]
  36. Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:324–32 [Google Scholar]
  37. Heinrich SU, Lindquist S. 2011. Protein-only mechanism induces self-perpetuating changes in the activity of neuronal Aplysia cytoplasmic polyadenylation element binding protein (CPEB). PNAS 108:2999–3004 [Google Scholar]
  38. Herb BR, Wolschin F, Hansen KD, Aryee MJ, Langmead B. et al. 2012. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 15:1371–73 [Google Scholar]
  39. Holmes BB, Diamond MI. 2014. Prion-like properties of τ protein: the importance of extracellular τ as a therapeutic target. J. Biol. Chem. 289:19855–61 [Google Scholar]
  40. Holmes DL, Lancaster AK, Lindquist S, Halfmann R. 2013. Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153:153–65 [Google Scholar]
  41. Horwich AL, Weissman JS. 1997. Deadly conformations—protein misfolding in prion disease. Cell 89:499–510 [Google Scholar]
  42. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ. 2011. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146:448–61 [Google Scholar]
  43. Ishimaru D, Andrade LR, Teixeira LS, Quesado PA, Maiolino LM. et al. 2003. Fibrillar aggregates of the tumor suppressor p53 core domain. Biochemistry 42:9022–27 [Google Scholar]
  44. Iwasaki M, Paszkowski J. 2014. Epigenetic memory in plants. EMBO J. 33:1987–98 [Google Scholar]
  45. Jarosz DF, Brown JC, Walker GA, Datta MS, Ung WL. et al. 2014. Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158:1083–93 [Google Scholar]
  46. Johnson AP, Cleaves HJ, Dworkin JP, Glavin DP, Lazcano A, Bada JL. 2008. The Miller volcanic spark discharge experiment. Science 322:404 [Google Scholar]
  47. Kato M, Han TW, Xie S, Shi K, Du X. et al. 2012. Cell-free formation of RNA granules: Low complexity sequence domains form dynamic fibers within hydrogels. Cell 149:753–67 [Google Scholar]
  48. Keene JD, Tenenbaum SA. 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:1161–67 [Google Scholar]
  49. Keleman K, Kruttner S, Alenius M, Dickson BJ. 2007. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci. 10:1587–93 [Google Scholar]
  50. Kelly JW. 1998. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8:101–6 [Google Scholar]
  51. King OD, Gitler AD, Shorter J. 2012. The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res. 146261–80 [Google Scholar]
  52. Kotzbauer PT, Giasson BI, Kravitz AV, Golbe LI, Mark MH. et al. 2004. Fibrillization of α-synuclein and τ in familial Parkinson's disease caused by the A53T α-synuclein mutation. Exp. Neurol. 187:279–88 [Google Scholar]
  53. Kruttner S, Stepien B, Noordermeer JN, Mommaas MA, Mechtler K. et al. 2012. Drosophila CPEB Orb2A mediates memory independent of its RNA-binding domain. Neuron 76:383–95 [Google Scholar]
  54. Kwon I, Kato M, Xiang S, Wu L, Theodoropoulos P. et al. 2013. Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell 155:1049–60 [Google Scholar]
  55. Lansbury PT Jr. 1997. Structural neurology: Are seeds at the root of neuronal degeneration?. Neuron 19:1151–54 [Google Scholar]
  56. Lee C, Zhang H, Baker AE, Occhipinti P, Borsuk ME, Gladfelter AS. 2013. Protein aggregation behavior regulates cyclin transcript localization and cell-cycle control. Dev. Cell 25:572–84 [Google Scholar]
  57. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE. et al. 2004. Synthetic mammalian prions. Science 305:673–76 [Google Scholar]
  58. Liberski PP. 2012. Historical overview of prion diseases: a view from afar. Folia Neuropathol. 50:1–12 [Google Scholar]
  59. Liebman SW, Chernoff YO. 2012. Prions in yeast. Genetics 191:1041–72 [Google Scholar]
  60. Lim JP, Brunet A. 2013. Bridging the transgenerational gap with epigenetic memory. Trends Genet. 29:176–86 [Google Scholar]
  61. Lisman J. 1994. The CaM kinase II hypothesis for the storage of synaptic memory. Trends Neurosci. 17:406–12 [Google Scholar]
  62. Lynch G, Baudry M. 1984. The biochemistry of memory: a new and specific hypothesis. Science 224:1057–63 [Google Scholar]
  63. Maji SK, Perrin MH, Sawaya MR, Jessberger S, Vadodaria K. et al. 2009. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325:328–32 [Google Scholar]
  64. Majumdar A, Cesario WC, White-Grindley E, Jiang H, Ren F. et al. 2012. Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148:515–29 [Google Scholar]
  65. Malinovska L, Kroschwald S, Alberti S. 2013. Protein disorder, prion propensities, and self-organizing macromolecular collectives. Biochim. Biophys. Acta 1834:918–31 [Google Scholar]
  66. Martin KC, Barad M, Kandel ER. 2000. Local protein synthesis and its role in synapse-specific plasticity. Curr. Opin. Neurobiol. 10:587–92 [Google Scholar]
  67. Miller SL, Urey HC. 1959. Organic compound synthesis on the primitive earth. Science 130:245–51 [Google Scholar]
  68. Newby GA, Lindquist S. 2013. Blessings in disguise: biological benefits of prion-like mechanisms. Trends Cell Biol. 23:251–59 [Google Scholar]
  69. Patel BK, Gavin-Smyth J, Liebman SW. 2009. The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion. Nat. Cell Biol. 11:344–49 [Google Scholar]
  70. Pavlopoulos E, Trifilieff P, Chevaleyre V, Fioriti L, Zairis S. et al. 2011. Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 147:1369–83 [Google Scholar]
  71. Petrovska I, Nuske E, Munder MC, Kulasegaran G, Malinovska L. et al. 2014. Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation. eLife 3:e02409 [Google Scholar]
  72. Polymenidou M, Cleveland DW. 2012. Prion-like spread of protein aggregates in neurodegeneration. J. Exp. Med. 209:889–93 [Google Scholar]
  73. Prusiner SB. 1991. Molecular biology of prion diseases. Science 252:1515–22 [Google Scholar]
  74. Prusiner SB. 1998. Prions. PNAS 95:13363–83 [Google Scholar]
  75. Prusiner SB. 2013. Biology and genetics of prions causing neurodegeneration. Annu. Rev. Genet. 47:601–23 [Google Scholar]
  76. Prusiner SB, McKinley MP, Bowman KA, Bolton DC, Bendheim PE. et al. 1983. Scrapie prions aggregate to form amyloid-like birefringent rods. Cell 35:349–58 [Google Scholar]
  77. Ramanan VK, Saykin AJ. 2013. Pathways to neurodegeneration: mechanistic insights from GWAS in Alzheimer's disease, Parkinson's disease, and related disorders. Am. J. Neurodegenerat. Dis. 2:145–75 [Google Scholar]
  78. Ramaswami M, Taylor JP, Parker R. 2013. Altered ribostasis: RNA-protein granules in degenerative disorders. Cell 154:727–36 [Google Scholar]
  79. Raveendra BL, Siemer AB, Puthanveettil SV, Hendrickson WA, Kandel ER, McDermott AE. 2013. Characterization of prion-like conformational changes of the neuronal isoform of Aplysia CPEB. Nat. Struct. Mol. Biol. 20:495–501 [Google Scholar]
  80. Reik W. 2007. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447:425–32 [Google Scholar]
  81. Richter JD. 2007. CPEB: a life in translation. Trends Biochem. Sci. 32:279–85 [Google Scholar]
  82. Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 23:1–11 [Google Scholar]
  83. Ringrose L, Paro R. 2007. Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134:223–32 [Google Scholar]
  84. Ripaud L, Chumakova V, Antonin M, Hastie AR, Pinkert S. et al. 2014. Overexpression of Q-rich prion-like proteins suppresses polyQ cytotoxicity and alters the polyQ interactome. PNAS 111:18219–24 [Google Scholar]
  85. Roberts RB, Flexner LB. 1969. The biochemical basis of long-term memory. Q. Rev. Biophys. 2:135–73 [Google Scholar]
  86. Robertson MP, Joyce GF. 2012. The origins of the RNA world. Cold Spring Harb. Perspect. Biol. 4:006742 [Google Scholar]
  87. Rogoza T, Goginashvili A, Rodionova S, Ivanov M, Viktorovskaya O. et al. 2010. Non-Mendelian determinant [ISP+] in yeast is a nuclear-residing prion form of the global transcriptional regulator Sfp1. PNAS 107:10573–77 [Google Scholar]
  88. Roth DM, Balch WE. 2011. Modeling general proteostasis: proteome balance in health and disease. Curr. Opin. Cell Biol. 23:126–34 [Google Scholar]
  89. Sarge KD, Park-Sarge OK. 2009. Mitotic bookmarking of formerly active genes: keeping epigenetic memories from fading. Cell Cycle 8:818–23 [Google Scholar]
  90. Seong KH, Li D, Shimizu H, Nakamura R, Ishii S. 2011. Inheritance of stress-induced, ATF-2–dependent epigenetic change. Cell 145:1049–61 [Google Scholar]
  91. Shorter J, Lindquist S. 2005. Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 6:435–50 [Google Scholar]
  92. Si K, Choi YB, White-Grindley E, Majumdar A, Kandel ER. 2010. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140:421–35 [Google Scholar]
  93. Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM. et al. 2003a. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia. Cell 115:893–904 [Google Scholar]
  94. Si K, Lindquist S, Kandel ER. 2003b. A neuronal isoform of the Aplysia CPEB has prion-like properties. Cell 115:879–91 [Google Scholar]
  95. Skovronsky DM, Lee VM, Trojanowski JQ. 2006. Neurodegenerative diseases: new concepts of pathogenesis and their therapeutic implications. Annu. Rev. Pathol. 1:151–70 [Google Scholar]
  96. Soto C. 2012. Transmissible proteins: expanding the prion heresy. Cell 149:968–77 [Google Scholar]
  97. Stephan JS, Fioriti L, Lamba N, Colnaghi L, Karl K. 2015. The CPEB3 protein is a functional prion that interacts with the actin cytoskeleton. Cell Rep. 11:111772–85 [Google Scholar]
  98. Steward O, Schuman EM. 2001. Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24:299–325 [Google Scholar]
  99. Suzuki G, Shimazu N, Tanaka M. 2012. A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336:355–59 [Google Scholar]
  100. Tariq M, Wegrzyn R, Anwar S, Bukau B, Paro R. 2013. Drosophila GAGA factor polyglutamine domains exhibit prion-like behavior. BMC Genomics 14:374 [Google Scholar]
  101. Tompa P, Friedrich P. 1998. Prion proteins as memory molecules: a hypothesis. Neuroscience 86:1037–43 [Google Scholar]
  102. True HL, Berlin I, Lindquist SL. 2004. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184–87 [Google Scholar]
  103. True HL, Lindquist SL. 2000. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature 407:477–83 [Google Scholar]
  104. Walsh DM, Selkoe DJ. 2004. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44:181–93 [Google Scholar]
  105. Wang L, Maji SK, Sawaya MR, Eisenberg D, Riek R. 2008. Bacterial inclusion bodies contain amyloid-like structure. PLOS Biol. 6:e195 [Google Scholar]
  106. White-Grindley E, Li L, Mohammad Khan R, Ren F, Saraf A. et al. 2014. Contribution of Orb2A stability in regulated amyloid-like oligomerization of Drosophila Orb2. PLOS Biol. 12:e1001786 [Google Scholar]
  107. Wickner RB. 1994. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science 264:566–69 [Google Scholar]
  108. Wickner RB, Edskes HK, Shewmaker F, Nakayashiki T. 2007. Prions of fungi: inherited structures and biological roles. Nat. Rev. Microbiol. 5:611–18 [Google Scholar]
  109. Wickner RB, Masison DC, Edskes HK. 1995. [PSI] and [URE3] as yeast prions. Yeast 11:1671–85 [Google Scholar]
  110. Wickner RB, Taylor KL, Edskes HK, Maddelein ML. 2000. Prions: portable prion domains. Curr. Biol. 10:R335–37 [Google Scholar]
  111. Wiltzius JJ, Landau M, Nelson R, Sawaya MR, Apostol MI. et al. 2009. Molecular mechanisms for protein-encoded inheritance. Nat. Struct. Mol. Biol. 16:973–78 [Google Scholar]
  112. Xu H, He X, Zheng H, Huang LJ, Hou F. et al. 2014. Structural basis for the prion-like MAVS filaments in antiviral innate immunity. eLife 3:e01489 [Google Scholar]
  113. Zaidi SK, Young DW, Montecino M, Lian JB, Stein JL. et al. 2010. Architectural epigenetics: mitotic retention of mammalian transcriptional regulatory information. Mol. Cell. Biol. 30:4758–66 [Google Scholar]
  114. Zeybel M, Hardy T, Wong YK, Mathers JC, Fox CR. et al. 2012. Multigenerational epigenetic adaptation of the hepatic wound-healing response. Nat. Med. 18:1369–77 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100913-013409
Loading
/content/journals/10.1146/annurev-cellbio-100913-013409
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error