Advertisement

Biochemistry (Moscow)

, Volume 83, Issue 10, pp 1184–1195 | Cite as

Prions and Non-infectious Amyloids of Mammals – Similarities and Differences

  • A. P. GalkinEmail author
  • M. E. Velizhanina
  • Yu. V. Sopova
  • A. A. Shenfeld
  • S. P. Zadorsky
Review
  • 99 Downloads

Abstract

Amyloids are highly ordered aggregates of protein fibrils exhibiting cross-β structure formed by intermolecular hydrogen bonds. Pathological amyloid deposition is associated with the development of several socially significant incurable human diseases. Of particular interest are infectious amyloids, or prions, that cause several lethal neurodegenerative diseases in humans and can be transmitted from one organism to another. Because of almost complete absence of criteria for infectious and non-infectious amyloids, there is a lack of consensus, especially, in the definition of similarities and differences between prions and non-infectious amyloids. In this review, we formulated contemporary molecular-biological criteria for identification of prions and non-infectious amyloids and focused on explaining the differences between these two types of molecules.

Keywords

protein aggregates fibrils amyloids prions infectivity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Eisenberg, D., and Jucker, M. (2012) The amyloid state of proteins in human diseases, Cell, 148, 1188–1203.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Nizhnikov, A. A., Antonets, K. S., and Inge-Vechtomov, S. G. (2015) Amyloids: from pathogenesis to function, Biochemistry (Moscow), 80, 1127–1144.CrossRefGoogle Scholar
  3. 3.
    Fowler, D. M., Koulov, A. V., Balch, W. E., and Kelly, J. W. (2007) Functional amyloid - from bacteria to humans, Trends Biochem. Sci., 32, 217–224.CrossRefPubMedGoogle Scholar
  4. 4.
    Bleem, A., and Daggett, V. (2017) Structural and functional diversity among amyloid proteins: agents of disease, building blocks of biology, and implications for molecular engineering, Biotechnol. Bioeng., 114, 7–20.CrossRefPubMedGoogle Scholar
  5. 5.
    Prusiner, S. B. (2013) Biology and genetics of prions causing neurodegeneration, Annu. Rev. Genet., 47, 601–623.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    MacLea, K. S. (2017) What makes a prion: infectious proteins from animals to yeast, Int. Rev. Cell. Mol. Biol., 329, 227–276.CrossRefPubMedGoogle Scholar
  7. 7.
    Kajava, A. V., Baxa, U., and Steven, A. C. (2010) Beta arcades: recurring motifs in naturally occurring and disease-related amyloid fibrils, FASEB J., 24, 1311–1319.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Sipe, J. D., Benson, M. D., Buxbaum, J. N., Ikeda, S., Merlini, G., Saraiva, M. J., and Westermark, P. (2014) Nomenclature 2014: amyloid fibril proteins and clinical classification of the amyloidosis, Amyloid, 21, 221–224.CrossRefPubMedGoogle Scholar
  9. 9.
    Lansbury, P. T., Jr., Costa, P. R., Griffiths, J. M., Simon, E. J., Auger, M., Halverson, K. J., Kocisko, D. A., Hendsch, Z. S., Ashburn, T. T., Spencer, R. G. S., Tider, B., and Griffin, R. G. (1995) Structural model for the beta-amyloid fibril based on interstrand alignment of an antiparallel-sheet comprising a C-terminal peptide, Nat. Struct. Biol., 2, 990–998.CrossRefPubMedGoogle Scholar
  10. 10.
    Shewmaker, F., McGlinchey, R. P., and Wickner, R. B. (2011) Structural insights into functional and pathological amyloid, J. Biol. Chem., 286, 16533–16540.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Syed, A. K., and Boles, B. R. (2014) Fold modulating function: bacterial toxins to functional amyloids, Front Microbiol., 5, 401.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Knowles, T. P., Vendruscolo, M., and Dobson, C. M. (2014) The amyloid state and its association with protein misfolding diseases, Nat. Rev. Mol. Cell Biol., 15, 384–396.CrossRefPubMedGoogle Scholar
  13. 13.
    Wickner, R. B., Shewmaker, F., Edskes, H., Kryndushkin, D., Nemecek, J., McGlinchey, R., Bateman, D., and Winchester, C. L. (2010) Prion amyloid structure explains templating: how proteins can be genes, FEMS Yeast Res., 8, 980–991.CrossRefGoogle Scholar
  14. 14.
    Gu, L., Liu, C., Stroud, J. C., Ngo, S., Jiang, L., and Guo, Z. (2014) Antiparallel triple-strand architecture for prefibrillar Aβ42 oligomers, J. Biol. Chem., 289, 27300–27313.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Van Melckebeke, H., Wasmer, C., Lange, A., Ab, E., Loquet, A., Bockmann, A., and Meier, B. H. (2010) Atomic-resolution three-dimensional structure of HET-s (218–289) amyloid fibrils by solid-state NMR spectroscopy, J. Am. Chem. Soc., 132, 13765–13775.CrossRefPubMedGoogle Scholar
  16. 16.
    Saupe, S. J. (2011) The [Het-s] prion of Podospora anserina and its role in heterokaryon incompatibility, Semin. Cell. Dev. Biol., 22, 460–468.CrossRefPubMedGoogle Scholar
  17. 17.
    Maji, S. K., Perrin, M. H., Sawaya, M. R., Jessberger, S., Vadodaria, K., Rissman, R. A., Singru, P. S., Nilsson, K. P., Simon, R., Schubert, D., Eisenberg, D., Rivier, J., Sawchenko, P., Vale, W., and Riek, R. (2009) Functional amyloids as natural storage of peptide hormones in pitu-itary secretory granules, Science, 325, 328–332.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Ahmed, A. B., and Kajava, A. V. (2013) Breaking the amy-loidogenicity code: methods to predict amyloids from amino acid sequence, FEBS Lett., 587, 1089–1095.CrossRefPubMedGoogle Scholar
  19. 19.
    Chiti, F., and Dobson, C. M. (2006) Protein misfolding, functional amyloid, and human disease, Annu. Rev. Biochem., 75, 333–366.CrossRefPubMedGoogle Scholar
  20. 20.
    Toyama, B. H., and Weissman, J. S. (2011) Amyloid structure: conformational diversity and consequences, Annu. Rev. Biochem., 80, 557–585.CrossRefPubMedGoogle Scholar
  21. 21.
    Eanes, E. D., and Glenner, G. G. (1968) X-ray diffraction studies on amyloid filaments, J. Histochem. Cytochem., 16, 673–677.CrossRefPubMedGoogle Scholar
  22. 22.
    Bonar, L., Cohen, A. S., and Skinner, M. M. (1969) Characterization of the amyloid fibril as a cross-beta protein, Proc. Soc. Exp. Biol. Med., 131, 1373–1375.CrossRefPubMedGoogle Scholar
  23. 23.
    Glenner, G. G., Eanes, E. D., and Page, D. L. (1972) The relation of the properties of Congo Red-stained amyloid fibrils to the β-conformation, J. Histochem. Cytochem., 20, 821–826.CrossRefPubMedGoogle Scholar
  24. 24.
    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.CrossRefPubMedGoogle Scholar
  25. 25.
    LeVine, H., 3rd (1999) Quantification of beta-sheet amyloid fibril structures with thioflavin T, Methods Enzymol., 309, 274–284.CrossRefPubMedGoogle Scholar
  26. 26.
    Prusiner, S. B. (1989) Scrapie prions, Am. Rev. Microbiol., 43, 345–374.CrossRefGoogle Scholar
  27. 27.
    Kushnirov, V. V., Alexandrov, I. M., Mitkevich, O. V., Shkundina, I. S., and Ter-Avanesyan, M. D. (2006) Purification and analysis of prion and amyloid aggregates, Methods, 39, 50–55.CrossRefPubMedGoogle Scholar
  28. 28.
    Khurana, R., Uversky, V. N., Nielsen, L., and Fink, A. L. (2001) Is Congo Red an amyloid-specific dye? J. Biol. Chem., 276, 22715–22721.CrossRefPubMedGoogle Scholar
  29. 29.
    Nilsson, M. R. (2004) Techniques to study amyloid fibril formation in vitro, Methods, 34, 151–160.CrossRefPubMedGoogle Scholar
  30. 30.
    Manning, M., and Colon, W. (2004) Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward beta-sheet structure, Biochemistry, 43, 11248–11254.CrossRefPubMedGoogle Scholar
  31. 31.
    Ryzhova, T. A., Sopova, J. V., Zadorsky, S. P., Siniukova, V. A., Sergeeva, A. V., Galkina, S. A., Nizhnikov, A. A., Shenfeld, A. A., Volkov, K. V., and Galkin, A. P. (2018) Screening for amyloid proteins in the yeast proteome, Curr. Genet., 64, 469–478.CrossRefPubMedGoogle Scholar
  32. 32.
    Prusiner, S. B., and Scott, M. R. (1997) Genetics of prions, Annu. Rev. Genet., 31, 139–175.CrossRefPubMedGoogle Scholar
  33. 33.
    Gajdusek, D. C. (1991) The transmissible amyloidoses: genetical control of spontaneous generation of infectious amyloid proteins by nucleation of configurational change in host precursors: kuru-CJD-GSS-scrapie-BSE, Eur. J. Epidemiol., 7, 567–577.CrossRefPubMedGoogle Scholar
  34. 34.
    Cohen, E., Bieschke, J., Perciavalle, R. M., Kelly, J. W., and Dillin, A. (2006) Opposing activities protect against age-onset proteotoxicity, Science, 313, 1604–1610.CrossRefPubMedGoogle Scholar
  35. 35.
    Prusiner, S. B. (2001) Shattuck lecture -neurodegenera-tive diseases and prions, N. Engl. J. Med., 344, 1516–1526.CrossRefPubMedGoogle Scholar
  36. 36.
    Gajdusek, D. C., Gibbs, C. J., Jr., and Alpers, M. (1966) Experimental transmission of a kuru-like syndrome to chimpanzees, Nature, 209, 794–796.CrossRefPubMedGoogle Scholar
  37. 37.
    Gibbs, C. J., Jr., Gajdusek, D. C., Asher, D. M., Alpers, M. P., Beck, E., Daniel, P. M., and Matthews, W. B. (1968) Creutzfeldt-Jakob disease (spongiform encephalopathy): transmission to the chimpanzee, Science, 161, 388–389.CrossRefPubMedGoogle Scholar
  38. 38.
    Nathanson, N., Wilesmith, J., and Griot, C. (1997) Bovine spongiform encephalopathy (BSE): causes and conse-quences of a common source epidemic, Am. J. Epidemiol., 145, 959–969.CrossRefPubMedGoogle Scholar
  39. 39.
    Ma, J., and Lindquist, S. (1999) De novo generation of a PrPSc-like conformation in living cells, Nat. Cell. Biol., 1, 358–361.CrossRefPubMedGoogle Scholar
  40. 40.
    Pan, K. M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., and Cohen, F. E. (1993) Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins, Proc. Natl. Acad. Sci. USA, 90, 10962–10966.CrossRefPubMedGoogle Scholar
  41. 41.
    Nicotera, P. (2001) A route for prion neuroinvasion, Neuron, 31, 345–348.CrossRefPubMedGoogle Scholar
  42. 42.
    Heikenwalder, M., Julius, C., and Aguzzi, A. (2007) Prions and peripheral nerves: a deadly rendezvous, J. Neurosci., 85, 2714–2725.Google Scholar
  43. 43.
    Makarava, N., Kovacs, G. G., Bocharova, O., Savtchenko, R., Alexeeva, I., Budka, H., Rohwer, R. G., and Baskakov, I. V. (2010) Recombinant prion protein induces a new transmissible prion disease in wild-type animals, Acta Neuropathol., 119, 177–187.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Sun, Y., Makarava, N., Lee, C. I., Laksanalamai, P., Robb, F. T., and Baskakov, I. V. (2008) Conformational stability of PrP amyloid fibrils controls their smallest possible fragment size, J. Mol. Biol., 376, 1155–1167.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Kushnirov, V. V., and Ter-Avanesyan, M. D. (1998) Structure and replication of yeast prions, Cell, 94, 13–16.CrossRefPubMedGoogle Scholar
  46. 46.
    Mena, M. A., Rodriguez-Navarro, J. A., and Yebenes, J. G. (2009) The multiple mechanisms of amyloid deposition, Prion, 3, 5–11.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Chiti, F., and Dobson, C. M. (2017) Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade, Annu. Rev. Biochem., 86, 27–68.CrossRefPubMedGoogle Scholar
  48. 48.
    Liebman, S. W., and Chernoff, Y. O. (2012) Prions in yeast, Genetics, 191, 1041–1072.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Butler, D. A., Scott, M. R., Bockman, J. M., Borchelt, D. R., Taraboulos, A., Hsiao, K. K., Kingsbury, D. T., and Prusiner, S. B. (1988) Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins, J. Virol., 62, 1558–1564.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Joshi, P., Benussi, L., Furlan, R., Ghidoni, R., and Verderio, C. (2015) Extracellular vesicles in Alzheimer’s disease: friends or foes? Focus on Aβ-vesicle interaction, Int. J. Mol. Sci., 16, 4800–4813.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Medina, M., and Avila, J. (2014) The role of extracellular tau in the spreading of neurofibrillary pathology, Front Cell. Neurosci., 8, e113.Google Scholar
  52. 52.
    Eisele, Y. S., Obermuller, U., Heilbronner, G., Baumann, F., Kaeser, S. A., Wolburg, H., Walker, L. C., Staufenbiel, M., Heikenwalder, M., and Jucker, M. (2010) Peripherally applied Aβ-containing inoculates induce cerebral beta-amyloidosis, Science, 330, 980–982.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Morales, R., Duran-Aniotz, C., Castilla, J., Estrada, L. D., and Soto, C. (2012) De novo induction of amyloid-β depo-sition in vivo, Mol. Psychiatry, 17, 1347–1353.CrossRefPubMedGoogle Scholar
  54. 54.
    Rosen, R. F., Fritz, J. J., Dooyema, J., Cintron, A. F., Hamaguchi, T., Lah, J. J., LeVine, H., 3rd, Jucker, M., and Walker, L. C. (2012) Exogenous seeding of cerebral β-amyloid deposition in βAPP-transgenic rats, J. Neurochem., 120, 660–666.CrossRefPubMedGoogle Scholar
  55. 55.
    Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I., and Nussbaum, R. L. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson’s disease, Science, 276, 2045–2047.CrossRefPubMedGoogle Scholar
  56. 56.
    Poulopoulos, M., Levy, O. A., and Alcalay, R. N. (2012) The neuropathology of genetic Parkinson’s disease, Mov. Disord., 27, 831–842.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Goedert, M., Ghetti, B., and Spillantini, M. G. (2012) Frontotemporal dementia: implications for understanding Alzheimer’s disease, Cold Spring Harb. Perspect. Med., 2, a006254.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Danzer, K. M., Kranich, L. R., Ruf, W. P., Cagsal-Getkin, O., Winslow, A. R., Zhu, L., Vanderburg, C. R., and McLean, P. J. (2012) Exosomal cell-to-cell transmission of alpha synuclein oligomers, Mol. Neurodegener., 7, 42.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Luk, K. C., Kehm, V., Carroll, J., Zhang, B., O’ Brien, P., Trojanowski, J. Q., and Lee, V. M. (2012) Pathological α-synuclein transmission initiates Parkinson-like neuro-degeneration in nontransgenic mice, Science, 338, 949–953.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Masuda-Suzukake, M., Nonaka, T., Hosokawa, M., Oikawa, T., Arai, T., Akiyama, H., Mann, D. M., and Hasegawa, M. (2013) Prion-like spreading of pathological α-synuclein in brain, Brain, 136, 1128–1138.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Sacino, A. N., Brooks, M., McKinney, A. B., Thomas, M. A., Shaw, G., Golde, T. E., and Giasson, B. I. (2014) Brain injection of α-synuclein induces multiple proteinopathies, gliosis, and a neuronal injury marker, J. Neurosci., 10, 12368–12378.CrossRefGoogle Scholar
  62. 62.
    Iqbal, K., Liu, F., Gong, C. X., Alonso A. C., and Grundke-Iqbal, I. (2009) Mechanisms of tau-induced neu-rodegeneration, Acta Neuropathol., 118, 53–69.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kfoury, N., Holmes, B. B., Jiang, H., Holtzman, D. M., and Diamond, M. I. (2012) Trans-cellular propagation of tau aggregation by fibrillar species, J. Biol. Chem., 287, 19440–19451.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Lasagna-Reeves, C. A., Castillo-Carranza, D. L., Sengupta, U., Sarmiento, J., Troncoso, J., Jackson, G. R., and Kayed, R. (2012) Identification of oligomers at early stages of tau aggregation in Alzheimer’s disease, FASEB J., 26, 1946–1959.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Jaunmuktane, Z., Mead, S., Ellis, M., Wadsworth, J. D., Nicoll, A. J., Kenny, J., Launchbury, F., Linehan, J., Richard-Loendt, A., Walker, A. S., Rudge, P., Collinge, J., and Brandner, S. (2015) Evidence for human transmission of amyloid-β pathology and cerebral amyloid angiopathy, Nature, 525, 247–250.CrossRefPubMedGoogle Scholar
  66. 66.
    Frontzek, K., Lutz, M. I., Aguzzi, A., Kovacs, G. G., and Budka, H. (2016) Amyloid-β pathology and cerebral amyloid angiopathy are frequent in iatrogenic Creutzfeldt-Jakob disease after dural grafting, Swiss Med. Wkly., 146, w14287.PubMedGoogle Scholar
  67. 67.
    Ridley, R. M., Baker, H. F., Windle, C. P., and Cummings, R. M. (2006) Very-long-term studies of the seeding of beta-amyloidosis in primates, J. Neural. Transm. (Vienna), 113, 1243–1251.CrossRefGoogle Scholar
  68. 68.
    Meyer-Luehmann, M., Coomaraswamy, J., Bolmont, T., Kaeser, S., Schaefer, C., Kilger, E., Neuenschwander, A., Abramowski, D., Frey, P., Jaton, A. L., Vigouret, J. M., Paganetti, P., Walsh, D. M., Mathews, P. M., Ghiso, J., Staufenbiel, M., Walker, L. C., and Jucker, M. (2006) Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host, Science, 313, 1781–1784.CrossRefPubMedGoogle Scholar
  69. 69.
    Bu, X. L., Xiang, Y., Jin, W. S., Wang, J., Shen, L. L., Huang, Z. L., Zhang, K., Liu, Y. H., Zeng, F., Liu, J. H., Sun, H. L., Zhuang, Z. Q., Chen, S. H., Yao, X. Q., Giunta, B., Shan, Y. C., Tan, J., Chen, X. W., Dong, Z. F., Zhou, H. D., Zhou, X. F., Song, W., and Wang, Y. J. (2017) Blood-derived amyloid-β protein induces Alzheimer’s disease pathologies, Mol. Psychiatry, doi: 10.1038/mp.2017.204.Google Scholar
  70. 70.
    Watts, J. C., Condello, C., Stohr, J., Oehler, A., Lee, J., DeArmond, S. J., Lannfelt, L., Ingelsson, M., Giles, K., and Prusiner, S. B. (2014) Serial propagation of distinct strains of Aβ prions from Alzheimer’s disease patients, Proc. Natl. Acad. Sci. USA, 111, 10323–10328.CrossRefPubMedGoogle Scholar
  71. 71.
    Elam, J. S., Taylor, A. B., Strange, R., Antonyuk, S., Doucette, P. A., Rodriguez, J. A., Hasnain, S. S., Hayward, L. J., Valentine, J. S., Yeates, T. O., and Hart, P. J. (2003) Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS, Nat. Struct. Biol., 10, 461–467.CrossRefPubMedGoogle Scholar
  72. 72.
    Stathopulos, P. B., Rumfeldt, J., Scholz, G. A., Irani, R. A., Frey, H. E., Hallewell, R. A., Lepock, J. R., and Meiering, E. M. (2003) Cu/Zn superoxide dismutase mutants associated with amyotrophic lateral sclerosis show enhanced formation of aggregates in vitro, Proc. Natl. Acad. Sci. USA, 100, 7021–7026.CrossRefPubMedGoogle Scholar
  73. 73.
    Chattopadhyay, M., Durazo, A., Sohn, S. H., Strong, C. D., Gralla, E. B., Whitelegge, J. P., and Valentine, J. S. (2008) Initiation and elongation in fibrillation of ALS-linked superoxide dismutase, Proc. Natl. Acad. Sci. USA, 105, 18663–18668.CrossRefPubMedGoogle Scholar
  74. 74.
    Furukawa, Y., Kaneko, K., Watanabe, S., Yamanaka, K., and Nukina, N. (2013) Intracellular seeded aggregation of mutant Cu,Zn-superoxide dismutase associated with amyotrophic lateral sclerosis, FEBS Lett., 587, 2500–2505.CrossRefPubMedGoogle Scholar
  75. 75.
    Grad, L. I., Yerbury, J. J., Turner, B. J., Guest, W. C., Pokrishevsky, E., O’Neill, M. A., Yanai, A., Silverman, J. M., Zeineddine, R., Corcoran, L., Kumita, J. R., Luheshi, L. M., Yousefi, M., Coleman, B. M., Hill, A. F., Plotkin, S. S., Mackenzie, I. R., and Cashman, N. R. (2014) Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and -independent mechanisms, Proc. Natl. Acad. Sci. USA, 111, 3620–3625.CrossRefPubMedGoogle Scholar
  76. 76.
    Westermark, G. T., and Westermark, P. (2009) Serumamyloid A and protein AA: molecular mechanisms of a trans-missible amyloidosis, FEBS Lett., 583, 2685–2690.CrossRefPubMedGoogle Scholar
  77. 77.
    Murakami, T., Ishiguro, N., and Higuchi, K. (2013) Transmission of systemic AA amyloidosis in animals, Vet. Pathol., 51, 363–371.CrossRefPubMedGoogle Scholar
  78. 78.
    Costa, V., and Scorrano, L. (2012) Shaping the role of mitochondria in the pathogenesis of Huntington’s disease, EMBO J., 31, 1853–1864.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Lee, C. Y., Cantle, J. P., and Yang, X. W. (2013) Genetic manipulations of mutant huntingtin in mice: new insights into Huntington’s disease pathogenesis, FEBS J., 280, 4382–4394.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Schilling, G., Becher, M. W., Sharp, A. H., Jinnah, H. A., Duan, K., Kotzuk, J. A., Slunt, H. H., Ratovitski, T., Cooper, J. K., Jenkins, N. A., Copeland, N. G., Price, D. L., Ross, C. A., and Borchelt, D. R. (1999) Intranuclear inclusions and neuritic aggregates in transgenic mice expressing a mutant N-terminal fragment of huntingtin, Hum. Mol. Genet., 8, 397–407.CrossRefPubMedGoogle Scholar
  81. 81.
    Vonsattel, J. P., and DiFiglia, M. (1998) Huntington disease, J. Neuropathol. Exp. Neurol., 57, 369–384.CrossRefPubMedGoogle Scholar
  82. 82.
    Cao, Q., Huang, Y. S., Kan, M. C., and Richter, J. D. (2005) Amyloid precursor proteins anchor CPEB to mem-branes and promote polyadenylation-induced translation, Mol. Cell. Biol., 25, 10930–10939.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Si, K., Choi, Y., White-Grindley, E., Majumdar, A., and Kandel, E. (2010) Aplysia CPEB can form prion-like mul-timers in sensory neurons that contribute to long-term facilitation, Cell, 140, 421–435.CrossRefPubMedGoogle Scholar
  84. 84.
    Majumdar, A., Cesario, W. C., White-Grindley, E., Jiang, H., Ren, F., Khan, M. R., Li, L., Choi, E. M., Kannan, K., Guo, F., Unruh, J., Slaughter, B., and Si, K. (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory, Cell, 148, 515–529.CrossRefPubMedGoogle Scholar
  85. 85.
    Stephan, J. S., Fioriti, L., Lamba, N., Colnaghi, L., Karl, K., Derkatch, I. L., and Kandel, E. R. (2015) The CPEB3 protein is a functional prion that interacts with the actin cytoskeleton, Cell. Rep., 11, 1772–1785.CrossRefPubMedGoogle Scholar
  86. 86.
    Hervas, R., Li, L., Majumdar, A., Fernandez-Ramirez Mdel, C., Unruh, J. R., Slaughter, B. D., Galera-Prat, A., Santana, E., Suzuki, M., Nagai, Y., Bruix, M., Casas-Tinto, S., Menendez, M., Laurents, D. V., Si, K., and Carrion-Vazquez, M. (2016) Molecular basis of Orb2 amy-loidogenesis and blockade of memory consolidation, PLoS Biol., 14, e1002361.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Heinrich, S. U., and Lindquist, S. (2011) Protein-only mechanism induces self-perpetuating changes in the activ-ity of neuronal Aplysia cytoplasmic polyadenylation ele-ment binding protein (CPEB), Proc. Natl. Acad. Sci. USA, 108, 2999–3004.CrossRefPubMedGoogle Scholar
  88. 88.
    Si, K., Giustetto, M., Etkin, A., Hsu, R., Janisiewicz, A. M., Miniaci, M. C., Kim, J. H., Zhu, H., and Kandel, E. R. (2003) A neuronal isoform of CREB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia, Cell, 115, 893–904.CrossRefPubMedGoogle Scholar
  89. 89.
    Hou, F., Sun, L., Zheng, H., Skaug, B., Jiang, Q. X., and Chen, Z. J. (2011) MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response, Cell, 146, 448–461.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Cai, X., Xu, H., and Chen, Z. J. (2017) Prion-like poly-merization in immunity and inflammation, Cold Spr. Harb. Perspect. Biol., 9, a023580.CrossRefGoogle Scholar
  91. 91.
    Kryndushkin, D., Pripuzova, N., Burnett, B. G., and Shewmaker, F. (2013) Non-targeted identification of pri-ons and amyloid-forming proteins from yeast and mammalian cells, J. Biol. Chem., 288, 27100–27111.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Nizhnikov, A. A., Alexandrov, A. I., Ryzhova, T. A., Mitkevich, O. V., Dergalev, A. A., Ter-Avanesyan, M. D., and Galkin, A. P. (2014) Proteomic screening for amyloid proteins, PLoS One, 9, e116003.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Nizhnikov, A. A., Ryzhova, T. A., Volkov, K. V., Zadorsky, S. P., Sopova, J. V., Inge-Vechtomov, S. G., and Galkin, A. P. (2016) Interaction of prions causes heritable traits in Saccharomyces cerevisiae, PLoS Genet., 12, e1006504.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • A. P. Galkin
    • 1
    • 2
    Email author
  • M. E. Velizhanina
    • 2
  • Yu. V. Sopova
    • 1
    • 2
  • A. A. Shenfeld
    • 1
    • 2
  • S. P. Zadorsky
    • 1
    • 2
  1. 1.St. Petersburg Branch of Vavilov Institute of General GeneticsRussian Academy of SciencesSt. PetersburgRussia
  2. 2.Department of Genetics and BiotechnologySt. Petersburg State UniversitySt. PetersburgRussia

Personalised recommendations