Biochemistry (Moscow)

, Volume 79, Issue 8, pp 761–775 | Cite as

Prions and chaperones: Friends or foes?

  • Y. Y. Stroylova
  • G. G. Kiselev
  • E. V. Schmalhausen
  • V. I. MuronetzEmail author


This review highlights the modern perception of anomalous folding of the prion protein and the role of chaperones therein. Special attention is paid to prion proteins from mammalian species, which are prone to amyloid-like prion diseases due to a unique aggregation pathway. Despite being a significantly popular current subject of investigations, the etiology, structure, and function of both normal and anomalous prion proteins still hold many mysteries. The most interesting of those are connected to the interaction with chaperone system, which is responsible for stabilizing protein structure and disrupting aggregates. In the case of prion proteins the following question is of the most importance — can chaperones influence different stages of the formation of pathological aggregates (these vary from intermediate oligomers to mature amyloid-like fibrils) and the whole transition from native prion protein to its amyloid-like fibril-enriched form? The existing inconsistencies and ambiguities in the observations made so far can be attributed to the fact that most of the investigations did not take into account the type and functional state of the chaperones. This review discusses in detail our previous works that have demonstrated fundamental differences between eukaryotic and prokaryotic chaperones in the action exerted on the amyloid-like transformation of the prion protein along with the dependence of the observed effects on the functional state of the chaperone.

Key words

prion chaperones GroEL TRiC (CCT) amyloid transformation of proteins aggregation neurodegenerative diseases 


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  1. 1.
    Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie, Science, 216, 136–144.PubMedCrossRefGoogle Scholar
  2. 2.
    Prusiner, S. B., Groth, D. F., Bolton, D. C., Kent, S. B., and Hood, L. E. (1984) Purification and structural studies of a major scrapie prion protein, Cell, 38, 127–134.PubMedCrossRefGoogle Scholar
  3. 3.
    Chesebro, B., Race, R., Wehrly, K., Nishio, J., Bloom, M., Lechner, D., Bergstrom, S., Robbins, K., Mayer, L., Keith, J. M., Garon, C., and Haase, A. (1985) Identification of scrapie prion protein-specific mRNA in scrapie-infected and uninfected brain, Nature, 315, 331–333.PubMedCrossRefGoogle Scholar
  4. 4.
    Oesch, B., Westaway, D., Walchli, M., McKinley, M. P., Kent, S. B., Aebersold, R., Barry, R. A., Tempst, P., Teplow, D. B., Hood, L. E., Prusiner, S. B., and Weissmann, C. (1985) A cellular gene encodes scrapie PrP 27–30 protein, Cell, 40, 735–746.PubMedCrossRefGoogle Scholar
  5. 5.
    Basler, K., Oesch, B., Scott, M., Westaway, D., Walchli, M., Groth, D. F., McKinley, M. P., Prusiner, S. B., and Weissmann, C. (1986) Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene, Cell, 46, 417–428.PubMedCrossRefGoogle Scholar
  6. 6.
    Bueler, H., Aguzzi, A., Sailer, A., Greiner, R. A., Autenried, P., Aguet, M., and Weissmann, C. (1993) Mice devoid of PrP are resistant to scrapie, Cell, 73, 1339–1347.PubMedCrossRefGoogle Scholar
  7. 7.
    Kushnirov, V. V., and Ter-Avanesyan, M. D. (1998) Structure and replication of yeast prions, Cell, 94, 13–16.PubMedCrossRefGoogle Scholar
  8. 8.
    Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N., and Ter-Avanesyan, M. D. (1997) In vitro propagation of the prionlike state of yeast Sup35 protein, Science, 277, 381–383.PubMedCrossRefGoogle Scholar
  9. 9.
    Kushnirov, V. V., Ter-Avanesyan, M. D., Telckov, M. V., Surguchov, A. P., Smirnov, V. N., and Inge-Vechtomov, S. G. (1988) Nucleotide sequence of the SUP2 (SUP35) gene of Saccharomyces cerevisiae, Gene, 66, 45–54.PubMedCrossRefGoogle Scholar
  10. 10.
    Harris, D. A. (2001) in Advances in Protein Chemistry (Byron, C., ed.) Vol. 57, Academic Press, pp. 203–228.Google Scholar
  11. 11.
    Huang, Z., Prusiner, S. B., and Cohen, F. E. (1995) Scrapie prions: a three-dimensional model of an infectious fragment, Fold. Des., 1, 13–19.PubMedCrossRefGoogle Scholar
  12. 12.
    Lysek, D. A., Schorn, C., Nivon, L. G., Esteve-Moya, V., Christen, B., Calzolai, L., von Schroetter, C., Fiorito, F., Herrmann, T., Guntert, P., and Wuthrich, K. (2005) Prion protein NMR structures of cats, dogs, pigs, and sheep, Proc. Natl. Acad. Sci. USA, 102, 640–645.PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Knaus, K. J., Morillas, M., Swietnicki, W., Malone, M., Surewicz, W. K., and Yee, V. C. (2001) Crystal structure of the human prion protein reveals a mechanism for oligomerization, Nat. Struct. Biol., 8, 770–774.PubMedCrossRefGoogle Scholar
  14. 14.
    Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. O., Riekel, C., and Eisenberg, D. (2007) Atomic structures of amyloid cross-β spines reveal varied steric zippers, Nature, 47, 453–457.CrossRefGoogle Scholar
  15. 15.
    Haire, L. F., Whyte, S. M., Vasisht, N., Gill, A. C., Verma, C., Dodson, E. J., Dodson, G. G., and Bayley, P. M. (2004) The crystal structure of the globular domain of sheep prion protein, J. Mol. Biol., 336, 1175–1183.PubMedCrossRefGoogle Scholar
  16. 16.
    Riek, R., Hornemann, S., Wider, G., Glockshuber, R., and Wuthrich, K. (1997) NMR characterization of the full-length recombinant murine prion protein, mPrP(23–231), FEBS Lett., 413, 282–288.PubMedCrossRefGoogle Scholar
  17. 17.
    Brockes, J. P. (1999) Topics in prion cell biology, Curr. Opin. Neurobiol., 9, 571–577.PubMedCrossRefGoogle Scholar
  18. 18.
    Aguzzi, A., Sigurdson, C., and Heikenwaelder, M. (2008) Molecular mechanisms of prion pathogenesis, Annu. Rev. Pathol., 3, 11–40.PubMedCrossRefGoogle Scholar
  19. 19.
    Bujdoso, R., Burke, D. F., and Thackray, A. M. (2005) Structural differences between allelic variants of the ovine prion protein revealed by molecular dynamics simulations, Proteins, 61, 840–849.PubMedCrossRefGoogle Scholar
  20. 20.
    Gossert, A. D., Bonjour, S., Lysek, D. A., Fiorito, F., and Wuthrich, K. (2005) Prion protein NMR structures of elk and of mouse/elk hybrids, Proc. Natl. Acad. Sci. USA, 102, 646–650.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Huang, Z., Gabriel, J. M., Baldwin, M. A., Fletterick, R. J., Prusiner, S. B., and Cohen, F. E. (1994) Proposed three-dimensional structure for the cellular prion protein, Proc. Natl. Acad. Sci. USA, 91, 7139–7143.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Prusiner, S. B. (1994) Neurodegeneration in humans caused by prions, West. J. Med., 161, 264–272.PubMedCentralPubMedGoogle Scholar
  23. 23.
    Prusiner, S. B., Scott, M. R., DeArmond, S. J., and Cohen, F. E. (1998) Prion protein biology, Cell, 93, 337–348.PubMedCrossRefGoogle Scholar
  24. 24.
    Kaneko, K., Ball, H. L., Wille, H., Zhang, H., Groth, D., Torchia, M., Tremblay, P., Safar, J., Prusiner, S. B., DeArmond, S. J., Baldwin, M. A., and Cohen, F. E. (2000) A synthetic peptide initiates Gerstmann-Straussler-Scheinker (GSS) disease in transgenic mice, J. Mol. Biol., 295, 997–1007.PubMedCrossRefGoogle Scholar
  25. 25.
    Kitamoto, T., Iizuka, R., and Tateishi, J. (1993) An amber mutation of prion protein in Gerstmann-Straussler syndrome with mutant PrP plaques, Biochem. Biophys. Res. Commun., 192, 525–531.PubMedCrossRefGoogle Scholar
  26. 26.
    Supattapone, S., Bosque, P., Muramoto, T., Wille, H., Aagaard, C., Peretz, D., Nguyen, H. O., Heinrich, C., Torchia, M., Safar, J., Cohen, F. E., DeArmond, S. J., Prusiner, S. B., and Scott, M. (1999) Prion protein of 106 residues creates an artificial transmission barrier for prion replication in transgenic mice, Cell, 96, 869–878.PubMedCrossRefGoogle Scholar
  27. 27.
    Ghetti, B., Piccardo, P., Spillantini, M. G., Ichimiya, Y., Porro, M., Perini, F., Kitamoto, T., Tateishi, J., Seiler, C., Frangione, B., Bugiani, O., Giaccone, G., Prelli, F., Goedert, M., Dlouhy, S. R., and Tagliavini, F. (1996) Vascular variant of prion protein cerebral amyloidosis with τ-positive neurofibrillary tangles: the phenotype of the stop codon 145 mutation in PRNP, Proc. Natl. Acad. Sci. USA, 93, 744–748.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Govaerts, C., Wille, H., Prusiner, S. B., and Cohen, F. E. (2004) Evidence for assembly of prions with left-handed β-helices into trimers, Proc. Natl. Acad. Sci. USA, 101, 8342–8347.PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Der-Sarkissian, A., Jao, C. C., Chen, J., and Langen, R. (2003) Structural organization of α-synuclein fibrils studied by site-directed spin labeling, J. Biol. Chem., 278, 37530–37535.PubMedCrossRefGoogle Scholar
  30. 30.
    Petkova, A. T., Ishii, Y., Balbach, J. J., Antzutkin, O. N., Leapman, R. D., Delaglio, F., and Tycko, R. (2002) A structural model for Alzheimer’s β-amyloid fibrils based on experimental constraints from solid state NMR, Proc. Natl. Acad. Sci. USA, 99, 16742–16747.PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Sunde, M., Serpell, L. C., Bartlam, M., Fraser, P. E., Pepys, M. B., and Blake, C. C. (1997) Common core structure of amyloid fibrils by synchrotron X-ray diffraction, J. Mol. Biol., 273, 729–739.PubMedCrossRefGoogle Scholar
  32. 32.
    Luhrs, T., Ritter, C., Adrian, M., Riek-Loher, D., Bohrmann, B., Dobeli, H., Schubert, D., and Riek, R. (2005) 3D structure of Alzheimer’s amyloid-β (1–42) fibrils, Proc. Natl. Acad. Sci. USA, 102, 17342–17347.PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Wasmer, C., Lange, A., Van Melckebeke, H., Siemer, A. B., Riek, R., and Meier, B. H. (2008) Amyloid fibrils of the HET-s (218–289) prion form a β-solenoid with a triangular hydrophobic core, Science, 319, 1523–1526.PubMedCrossRefGoogle Scholar
  34. 34.
    Gajdusek, D. C. (1988) Transmissible and non-transmissible amyloidoses: autocatalytic posttranslational conversion of host precursor proteins to β-pleated sheet configurations, J. Neuroimmunol., 20, 95–110.PubMedCrossRefGoogle Scholar
  35. 35.
    Come, J. H., Fraser, P. E., and Lansbury, P. T., Jr. (1993) A kinetic model for amyloid formation in the prion diseases: importance of seeding, Proc. Natl. Acad. Sci. USA, 90, 5959–5963.PubMedCentralPubMedCrossRefGoogle Scholar
  36. 36.
    Kelly, J. W. (2000) Mechanisms of amyloidogenesis, Nat. Struct. Biol., 7, 824–826.PubMedCrossRefGoogle Scholar
  37. 37.
    Eghiaian, F., Daubenfeld, T., Quenet, Y., van Audenhaege, M., Bouin, A. P., van der Rest, G., Grosclaude, J., and Rezaei, H. (2007) Diversity in prion protein oligomerization pathways results from domain expansion as revealed by hydrogen/deuterium exchange and disulfide linkage, Proc. Natl. Acad. Sci. USA, 104, 7414–7419.PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Rezaei, H., Eghiaian, F., Perez, J., Doublet, B., Choiset, Y., Haertle, T., and Grosclaude, J. (2005) Sequential generation of two structurally distinct ovine prion protein soluble oligomers displaying different biochemical reactivities, J. Mol. Biol., 347, 665–679.PubMedCrossRefGoogle Scholar
  39. 39.
    Singh, J., Sabareesan, A. T., Mathew, M. K., and Udgaonkar, J. B. (2012) Development of the structural core and of conformational heterogeneity during the conversion of oligomers of the mouse prion protein to worm-like amyloid fibrils, J. Mol. Biol., 423, 217–231.PubMedCrossRefGoogle Scholar
  40. 40.
    Aguzzi, A., and Polymenidou, M. (2004) Mammalian prion biology: one century of evolving concepts, Cell, 116, 313–327.PubMedCrossRefGoogle Scholar
  41. 41.
    Vassallo, N., and Herms, J. (2003) Cellular prion protein function in copper homeostasis and redox signaling at the synapse, J. Neurochem., 86, 538–544.PubMedCrossRefGoogle Scholar
  42. 42.
    Tsiroulnikov, K., Rezaei, H., Dalgalarrondo, M., Chobert, J. M., Grosclaude, J., and Haertle, T. (2006) Cu(II) induces small-size aggregates with amyloid characteristics in two alleles of recombinant ovine prion proteins, Biochim. Biophys. Acta, 1764, 1218–1226.PubMedCrossRefGoogle Scholar
  43. 43.
    Wong, E., Thackray, A. M., and Bujdoso, R. (2004) Copper induces increased β-sheet content in the scrapie-susceptible ovine prion protein PrPVRQ compared with the resistant allelic variant PrPARR, Biochem. J., 380, 273–282.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Roucou, X., Gains, M., and LeBlanc, A. C. (2004) Neuroprotective functions of prion protein, J. Neurosci. Res., 75, 153–161.PubMedCrossRefGoogle Scholar
  45. 45.
    Kawahara, M., Kuroda, Y., Arispe, N., and Rojas, E. (2000) Alzheimer’s β-amyloid, human islet amylin, and prion protein fragment evoke intracellular free calcium elevations by a common mechanism in a hypothalamic GnRH neuronal cell line, J. Biol. Chem., 275, 14077–14083.PubMedCrossRefGoogle Scholar
  46. 46.
    Moore, R. C., Lee, I. Y., Silverman, G. L., Harrison, P. M., Strome, R., Heinrich, C., Karunaratne, A., Pasternak, S. H., Chishti, M. A., Liang, Y., Mastrangelo, P., Wang, K., Smit, A. F., Katamine, S., Carlson, G. A., Cohen, F. E., Prusiner, S. B., Melton, D. W., Tremblay, P., Hood, L. E., and Westaway, D. (1999) Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel, J. Mol. Biol., 292, 797–817.PubMedCrossRefGoogle Scholar
  47. 47.
    Collinge, J., Whittington, M. A., Sidle, K. C., Smith, C. J., Palmer, M. S., Clarke, A. R., and Jefferys, J. G. (1994) Prion protein is necessary for normal synaptic function, Nature, 370, 295–297.PubMedCrossRefGoogle Scholar
  48. 48.
    Jeffrey, M., Goodsir, C., McGovern, G., Barmada, S. J., Medrano, A. Z., and Harris, D. A. (2009) Prion protein with an insertional mutation accumulates on axonal and dendritic plasmalemma and is associated with distinctive ultrastructural changes, Am. J. Pathol., 175, 1208–1217.PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Stys, P. K., You, H., and Zamponi, G. W. (2012) Copper-dependent regulation of NMDA receptors by cellular prion protein: implications for neurodegenerative disorders, J. Physiol., 590, 1357–1368.PubMedCentralPubMedCrossRefGoogle Scholar
  50. 50.
    Maglio, L. E., Martins, V. R., Izquierdo, I., and Ramirez, O. A. (2006) Role of cellular prion protein on LTP expression in aged mice, Brain Res., 1097, 11–18.PubMedCrossRefGoogle Scholar
  51. 51.
    Khosravani, H., Zhang, Y., Tsutsui, S., Hameed, S., Altier, C., Hamid, J., Chen, L., Villemaire, M., Ali, Z., Jirik, F. R., and Zamponi, G. W. (2008) Prion protein attenuates excitotoxicity by inhibiting NMDA receptors, J. Gen. Physiol., 131, i5.PubMedCrossRefGoogle Scholar
  52. 52.
    Gimbel, D. A., Nygaard, H. B., Coffey, E. E., Gunther, E. C., Lauren, J., Gimbel, Z. A., and Strittmatter, S. M. (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein, J. Neurosci., 30, 6367–6374.PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    Gunther, E. C., and Strittmatter, S. M. (2010) β-Amyloid oligomers and cellular prion protein in Alzheimer’s disease, J. Mol. Med. (Berl.), 88, 331–338.CrossRefGoogle Scholar
  54. 54.
    Lauren, J., Gimbel, D. A., Nygaard, H. B., Gilbert, J. W., and Strittmatter, S. M. (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers, Nature, 457, 1128–1132.PubMedCentralPubMedCrossRefGoogle Scholar
  55. 55.
    Um, J. W., and Strittmatter, S. M. (2013) Amyloid-β induced signaling by cellular prion protein and Fyn kinase in Alzheimer disease, Prion, 7, 37–41.PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Bukau, B., and Horwich, A. L. (1998) The Hsp70 and Hsp60 chaperone machines, Cell, 92, 351–366.PubMedCrossRefGoogle Scholar
  57. 57.
    Carrell, R. W., and Lomas, D. A. (1997) Conformational disease, Lancet, 350, 134–138.PubMedCrossRefGoogle Scholar
  58. 58.
    Polyakova, O. V., Roitel, O., Asryants, R. A., Poliakov, A. A., Branlant, G., and Muronetz, V. I. (2005) Misfolded forms of glyceraldehyde-3-phosphate dehydrogenase interact with GroEL and inhibit chaperonin-assisted folding of the wild-type enzyme, Protein Sci., 14, 921–928.PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    Welch, W. J., and Gambetti, P. (1998) Chaperoning brain diseases, Nature, 392, 23–24.PubMedCrossRefGoogle Scholar
  60. 60.
    Dulle, J. E., Bouttenot, R. E., Underwood, L. A., and True, H. L. (2013) Soluble oligomers are sufficient for transmission of a yeast prion but do not confer phenotype, J. Cell. Biol, 203, 197–204.PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F., and Caughey, B. (2005) The most infectious prion protein particles, Nature, 437, 257–261.PubMedCentralPubMedCrossRefGoogle Scholar
  62. 62.
    Simoneau, S., Rezaei, H., Sales, N., Kaiser-Schulz, G., Lefebvre-Roque, M., Vidal, C., Fournier, J. G., Comte, J., Wopfner, F., Grosclaude, J., Schatzl, H., and Lasmezas, C. I. (2007) In vitro and in vivo neurotoxicity of prion protein oligomers, PLoS Pathog., 3, e125.PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    Huang, P., Lian, F., Wen, Y., Guo, C., and Lin, D. (2013) Prion protein oligomer and its neurotoxicity, Acta Biochim. Biophys. Sin. (Shanghai), 45, 442–451.CrossRefGoogle Scholar
  64. 64.
    Novitskaya, V., Bocharova, O. V., Bronstein, I., and Baskakov, I. V. (2006) Amyloid fibrils of mammalian prion protein are highly toxic to cultured cells and primary neurons, J. Biol. Chem., 281, 13828–13836.PubMedCrossRefGoogle Scholar
  65. 65.
    Bailey, C. K., Andriola, I. F., Kampinga, H. H., and Merry, D. E. (2002) Molecular chaperones enhance the degradation of expanded polyglutamine repeat androgen receptor in a cellular model of spinal and bulbar muscular atrophy, Hum. Mol. Genet., 11, 515–523.PubMedCrossRefGoogle Scholar
  66. 66.
    Hageman, J., Rujano, M. A., van Waarde, M. A., Kakkar, V., Dirks, R. P., Govorukhina, N., Oosterveld-Hut, H. M., Lubsen, N. H., and Kampinga, H. H. (2010) A DNAJB chaperone subfamily with HDAC-dependent activities suppresses toxic protein aggregation, Mol. Cell, 37, 355–369.PubMedCrossRefGoogle Scholar
  67. 67.
    Waudby, C. A., Knowles, T. P., Devlin, G. L., Skepper, J. N., Ecroyd, H., Carver, J. A., Welland, M. E., Christodoulou, J., Dobson, C. M., and Meehan, S. (2010) The interaction of αB-crystallin with mature α-synuclein amyloid fibrils inhibits their elongation, Biophys. J., 98, 843–851.PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    DebBurman, S. K., Raymond, G. J., Caughey, B., and Lindquist, S. (1997) Chaperone-supervised conversion of prion protein to its protease-resistant form, Proc. Natl. Acad. Sci. USA, 94, 13938–13943.PubMedCentralPubMedCrossRefGoogle Scholar
  69. 69.
    Shorter, J., and Lindquist, S. (2004) Hsp104 catalyzes formation and elimination of self-replicating Sup35 prion conformers, Science, 304, 1793–1797.PubMedCrossRefGoogle Scholar
  70. 70.
    Paushkin, S. V., Kushnirov, V. V., Smirnov, V. N., and Ter-Avanesyan, M. D. (1996) Propagation of the yeast prionlike [psi+] determinant is mediated by oligomerization of the SUP35-encoded polypeptide chain release factor, EMBO J., 15, 3127–3134.PubMedCentralPubMedGoogle Scholar
  71. 71.
    Kryndushkin, D. S., Alexandrov, I. M., Ter-Avanesyan, M. D., and Kushnirov, V. V. (2003) Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104, J. Biol. Chem., 278, 49636–49643.PubMedCrossRefGoogle Scholar
  72. 72.
    Naletova, I. N., Muronetz, V. I., and Schmalhausen, E. V. (2006) Unfolded, oxidized, and thermoinactivated forms of glyceraldehyde-3-phosphate dehydrogenase interact with the chaperonin GroEL in different ways, Biochim. Biophys. Acta, 1764, 831–838.PubMedCrossRefGoogle Scholar
  73. 73.
    Stockel, J., and Hartl, F. U. (2001) Chaperonin-mediated de novo generation of prion protein aggregates, J. Mol. Biol., 313, 861–872.PubMedCrossRefGoogle Scholar
  74. 74.
    Kiselev, G. G., Naletova, I. N., Sheval, E. V., Stroylova, Y. Y., Schmalhausen, E. V., Haertle, T., and Muronetz, V. I. (2011) Chaperonins induce an amyloid-like transformation of ovine prion protein: the fundamental difference in action between eukaryotic TRiC and bacterial GroEL, Biochim. Biophys. Acta, 1814, 1730–1738.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  • Y. Y. Stroylova
    • 1
  • G. G. Kiselev
    • 2
  • E. V. Schmalhausen
    • 1
  • V. I. Muronetz
    • 1
    • 2
    Email author
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.Faculty of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia

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