Heparin binding confers prion stability and impairs its aggregation

FASEB Journal

Volumn 28, Issue 6, 2014, Pages 2667-2676

  Vieira, Tuane C R G ^a   Cordeiro, Yraima ^b   Caughey, Byron ^c   Silva, Jerson L ^a  

^a Centro Nacional de Ressonância Magnética Nuclear Jiri Jonas Instituto de Bioquímica Médica Leopoldo de Meis Instituto Nacional de Ciência e Tecnologia de Biologia Estrutural e Bioimagem   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Glycosaminoglycan; Neurodegeneration

Indexed keywords

AMYLOID; GLYCOSAMINOGLYCAN; LOW MOLECULAR WEIGHT HEPARIN; PRION PROTEIN; RECOMBINANT PROTEIN;

ANIMAL TISSUE; ARTICLE; ASSAY; BRAIN HOMOGENATE; CIRCULAR DICHROISM; COMPLEX FORMATION; DEGENERATIVE DISEASE; IN VITRO STUDY; KINETICS; LIGHT SCATTERING; MOLECULE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN STABILITY; SCRAPIE; SYRIAN HAMSTER; TEMPERATURE; THERMODYNAMICS;

GLYCOSAMINOGLYCAN; NEURODEGENERATION;

AMYLOID; ANIMALS; CRICETINAE; HEPARIN; HEPARIN, LOW-MOLECULAR-WEIGHT; KINETICS; MICE; PRION DISEASES; PRIONS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PRPC PROTEINS; PRPSC PROTEINS;

EID: 84901833027     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-246777     Document Type: Article

References (80)

1. Cohen, F. E. (1999) Protein misfolding and prion diseases. J. Mol. Biol. 293, 313-320
2. Harrison, P. M., Chan, H. S., Prusiner, S. B., and Cohen, F. E. (1999) Thermodynamics of model prions and its implications for the problem of prion protein folding. J. Mol. Biol. 286, 593-606 (Pubitemid 29090172)
3. Legname, G., Baskakov, I. V., Nguyen, H. O., Riesner, D., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions. Science 305, 673-676 (Pubitemid 39006757)
4. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383
5. Caughey, B. (2001) Interactions between prion protein isoforms: the kiss of death? Trends Biochem. Sci. 26, 235-242
6. DeArmond, S. J., McKinley, M. P., Barry, R. A., Braunfeld, M. B., McColloch, J. R., and Prusiner, S. B. (1985) Identification of prion amyloid filaments in scrapie-infected brain. Cell 41, 221-235 (Pubitemid 15068440)
7. Baskakov, I. V., and Bocharova, O. V. (2005) In vitro conversion of mammalian prion protein into amyloid fibrils displays unusual features. Biochemistry 44, 2339-2348 (Pubitemid 40279538)
8. Wilham, J. M., Orru, C. D., Bessen, R. A., Atarashi, R., Sano, K., Race, B., Meade-White, K. D., Taubner, L. M., Timmes, A., and Caughey, B. (2010) Rapid end-point quantitation of prion seeding activity with sensitivity comparable to bioassays. PLoS Pathog. 6, e1001217
9. Govaerts, C., Wille, H., Prusiner, S. B., and Cohen, F. E. (2004) Evidence for assembly of prions with left-handed beta-helices into trimers. Proc. Natl. Acad. Sci. U.S.A. 101, 8342-8347 (Pubitemid 38736577)
10. Schatzl, H. M., Da Costa, M., Taylor, L., Cohen, F. E., and Prusiner, S. B. (1997) Prion protein gene variation among primates. J. Mol. Biol. 265, 257
11. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M. A., Brentani, R. R., Foguel, D., and Silva, J. L. (2001) DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J. Biol. Chem. 276, 49400-49409
12. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O., and Tagliavini, F. (1993) Neurotoxicity of a prion protein fragment. Nature 362, 543-546 (Pubitemid 23113029)
13. Adrover, M., Pauwels, K., Prigent, S., de Chiara, C., Xu, Z., Chapuis, C., Pastore, A., and Rezaei, H. (2010) Prion fibrillization is mediated by a native structural element that comprises helices H2 and H3. J. Biol. Chem. 285, 21004-21012
14. Cobb, N. J., Sonnichsen, F. D., McHaourab, H., and Surewicz, W. K. (2007) Molecular architecture of human prion protein amyloid: a parallel, in-register beta-structure. Proc. Natl. Acad. Sci. U.S.A. 104, 18946-18951
15. Hafner-Bratkovic, I., Bester, R., Pristovsek, P., Gaedtke, L., Veranic, P., Gaspersic, J., Mancek-Keber, M., Avbelj, M., Polymenidou, M., Julius, C., Aguzzi, A., Vorberg, I., and Jerala, R. (2011) Globular domain of the prion protein needs to be unlocked by domain swapping to support prion protein conversion. J. Biol. Chem. 286, 12149-12156
16. Smirnovas, V., Baron, G. S., Offerdahl, D. K., Raymond, G. J., Caughey, B., and Surewicz, W. K. (2011) Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 18, 504-506
17. Telling, G. C., Scott, M., Mastrianni, J., Gabizon, R., Torchia, M., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (1995) Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83, 79-90
18. Caughey, B., and Baron, G. S. (2006) Prions and their partners in crime. Nature 443, 803-810 (Pubitemid 44622685)
19. Gauczynski, S., Peyrin, J. M., Haik, S., Leucht, C., Hundt, C., Rieger, R., Krasemann, S., Deslys, J. P., Dormont, D., Lasmezas, C. I., and Weiss, S. (2001) The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J. 20, 5863-5875 (Pubitemid 33049262)
20. Gomes, M. P., Millen, T. A., Ferreira, P. S., e Silva, N. L., Vieira, T. C., Almeida, M. S., Silva, J. L., and Cordeiro, Y. (2008) Prion protein complexed to N2a cellular RNAs through its N-terminal domain forms aggregates and is toxic to murine neuroblastoma cells. J. Biol. Chem. 283, 19616-19625
21. Deleault, N. R., Lucassen, R. W., and Supattapone, S. (2003) RNA molecules stimulate prion protein conversion. Nature 425, 717-720 (Pubitemid 37314314)
22. Wong, C., Xiong, L. W., Horiuchi, M., Raymond, L., Wehrly, K., Chesebro, B., and Caughey, B. (2001) Sulfated glycans and elevated temperature stimulate PrP(Sc)-dependent cell-free formation of protease-resistant prion protein. EMBO J. 20, 377-386 (Pubitemid 32126974)
23. Hijazi, N., Kariv-Inbal, Z., Gasset, M., and Gabizon, R. (2005) PrPSc incorporation to cells requires endogenous glycosaminoglycan expression. J. Biol. Chem. 280, 17057-17061 (Pubitemid 41389168)
24. Iozzo, R. V. (1998) Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67, 609-652
25. Deleault, N. R., Geoghegan, J. C., Nishina, K., Kascsak, R., Williamson, R. A., and Supattapone, S. (2005) Protease-resistant prion protein amplification reconstituted with partially purified substrates and synthetic polyanions. J. Biol. Chem. 280, 26873-26879 (Pubitemid 41040721)
26. Ben Zaken, O., Tzaban, S., Tal, Y., Horonchik, L., Esko, J. D., Vlodavsky, I., and Taraboulos, A. (2003) Cellular heparan sulfate participates in the metabolism of prions. J. Biol. Chem. 278, 40041-40049 (Pubitemid 37248570)
27. Ancsin, J. B. (2003) Amyloidogenesis: historical and modern observations point to heparan sulfate proteoglycans as a major culprit. Amyloid 10, 67-79
28. Horonchik, L., Tzaban, S., Ben Zaken, O., Yedidia, Y., Rouvinski, A., Papy-Garcia, D., Barritault, D., Vlodavsky, I., and Taraboulos, A. (2005) Heparan sulfate is a cellular receptor for purified infectious prions. J. Biol. Chem. 280, 17062-17067 (Pubitemid 41389169)
29. Gonzalez-Iglesias, R., Pajares, M. A., Ocal, C., Espinosa, J. C., Oesch, B., and Gasset, M. (2002) Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges. J. Mol. Biol. 319, 527-540 (Pubitemid 34729477)
30. Shyng, S. L., Lehmann, S., Moulder, K. L., and Harris, D. A. (1995) Sulfated glycans stimulate endocytosis of the cellular isoform of the prion protein, PrPC, in cultured cells. J. Biol. Chem. 270, 30221-30229
31. Caughey, B., and Raymond, G. J. (1993) Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells. J. Virol. 67, 643-650 (Pubitemid 23032040)
32. Perez, M., Wandosell, F., Colaco, C., and Avila, J. (1998) Sulphated glycosaminoglycans prevent the neurotoxicity of a human prion protein fragment. Biochem. J. 335, 369-374 (Pubitemid 28491072)
33. Gabizon, R., Meiner, Z., Halimi, M., and Ben Sasson, S. A. (1993) Heparin-like molecules bind differentially to prion-proteins and change their intracellular metabolic fate. J. Cell. Physiol. 157, 319-325 (Pubitemid 23332776)
34. Lindahl, U. (2007) Heparan sulfate-protein interactions: a concept for drug design? Thromb. Haemost. 98, 109-115
35. Holmes, B. B., Devos, S. L., Kfoury, N., Li, M., Jacks, R., Yanamandra, K., Ouidja, M. O., Brodsky, F. M., Marasa, J., Bagchi, D. P., Kotzbauer, P. T., Miller, T. M., Papy-Garcia, D., and Diamond, M. I. (2013) Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc. Natl. Acad. Sci. U.S.A. 110, E3138-E3147
36. Vieira, T. C., Reynaldo, D. P., Gomes, M. P., Almeida, M. S., Cordeiro, Y., and Silva, J. L. (2011) Heparin binding by murine recombinant prion protein leads to transient aggregation and formation of RNA-resistant species. J. Am. Chem. Soc. 133, 334-344
37. Weiss, S., Proske, D., Neumann, M., Groschup, M. H., Kretzschmar, H. A., Famulok, M., and Winnacker, E. L. (1997) RNA aptamers specifically interact with the prion protein PrP. J. Virol. 71, 8790-8797 (Pubitemid 27446463)
38. Zahn, R., von, S. C., and Wuthrich, K. (1997) Human prion proteins expressed in Escherichia coli and purified by high-affinity column refolding. FEBS Lett. 417, 400-404
39. Chesebro, B., Race, B., Meade-White, K., Lacasse, R., Race, R., Klingeborn, M., Striebel, J., Dorward, D., McGovern, G., and Jeffrey, M. (2010) Fatal transmissible amyloid encephalopathy: a new type of prion disease associated with lack of prion protein membrane anchoring. PLoS Pathog. 6, e1000800
40. Vascellari, S., Orru, C. D., Hughson, A. G., King, D., Barron, R., Wilham, J. M., Baron, G. S., Race, B., Pani, A., and Caughey, B. (2012) Prion seeding activities of mouse scrapie strains with divergent PrPSc protease sensitivities and amyloid plaque content using RT-QuIC and eQuIC. PLoS One 7, e48969
41. Nielsen, L., Khurana, R., Coats, A., Frokjaer, S., Brange, J., Vyas, S., Uversky, V. N., and Fink, A. L. (2001) Effect of environmental factors on the kinetics of insulin fibril formation: elucidation of the molecular mechanism. Biochemistry 40, 6036-6046 (Pubitemid 32466306)
42. Jarrett, J. T., and Lansbury, P. T., Jr. (1993) Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058 (Pubitemid 23180480)
43. Caughey, B. (2000) Transmissible spongiform encephalopathies, amyloidoses and yeast prions: common threads? Nat. Med. 6, 751-754
44. Kaneko, K., Peretz, D., Pan, K. M., Blochberger, T. C., Wille, H., Gabizon, R., Griffith, O. H., Cohen, F. E., Baldwin, M. A., and Prusiner, S. B. (1995) Prion protein (PrP) synthetic peptides induce cellular PrP to acquire properties of the scrapie isoform. Proc. Natl. Acad. Sci. U.S.A. 92, 11160-11164
45. Gu, Y., Fujioka, H., Mishra, R. S., Li, R., and Singh, N. (2002) Prion peptide 106-126 modulates the aggregation of cellular prion protein and induces the synthesis of potentially neurotoxic transmembrane PrP. J. Biol. Chem. 277, 2275-2286 (Pubitemid 34968815)
46. Honda, H., Sasaki, K., Minaki, H., Masui, K., Suzuki, S. O., Doh-Ura, K., and Iwaki, T. (2012) Protease-resistant PrP and PrP oligomers in the brain in human prion diseases after intraventricular pentosan polysulfate infusion. Neuropathology 32, 124-132
47. Yokoyama, T., Takeuchi, A., Yamamoto, M., Kitamoto, T., Ironside, J. W., and Morita, M. (2011) Heparin enhances the cell-protein misfolding cyclic amplification efficiency of variant Creutzfeldt-Jakob disease. Neurosci. Lett. 498, 119-123
48. Cordeiro, Y., Kraineva, J., Ravindra, R., Lima, L. M., Gomes, M. P., Foguel, D., Winter, R., and Silva, J. L. (2004) Hydration and packing effects on prion folding and beta-sheet conversion: high pressure spectroscopy and pressure perturbation calorimetry studies. J. Biol. Chem. 279, 32354-32359 (Pubitemid 39014688)
49. Van der Kamp, M. W., and Daggett, V. (2010) Pathogenic mutations in the hydrophobic core of the human prion protein can promote structural instability and misfolding. J. Mol. Biol. 404, 732-748
50. Silva, J. L., Vieira, T. C., Gomes, M. P., Bom, A. P., Lima, L. M., Freitas, M. S., Ishimaru, D., Cordeiro, Y., and Foguel, D. (2010) Ligand binding and hydration in protein misfolding: insights from studies of prion and p53 tumor suppressor proteins. Acc. Chem. Res. 43, 271-279
51. Sharp, K. A., and Honig, B. (1990) Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19, 301-332 (Pubitemid 20205627)
52. Ermonval, M., Mouillet-Richard, S., Codogno, P., Kellermann, O., and Botti, J. (2003) Evolving views in prion glycosylation: functional and pathological implications. Biochimie (Paris) 85, 33-45 (Pubitemid 36625979)
53. Cortijo-Arellano, M., Ponce, J., Durany, N., and Cladera, J. (2008) Amyloidogenic properties of the prion protein fragment PrP(185-208): comparison with Alzheimer's peptide Abeta(1-28), influence of heparin and cell toxicity. Biochem. Biophys. Res. Commun. 368, 238-242
54. Kaneko, K., Wille, H., Mehlhorn, I., Zhang, H., Ball, H., Cohen, F. E., Baldwin, M. A., and Prusiner, S. B. (1997) Molecular properties of complexes formed between the prion protein and synthetic peptides. J. Mol. Biol. 270, 574-586 (Pubitemid 27313797)
55. Orrù, C. D., Wilham, J. M., Vascellari, S., Hughson, A. G., and Caughey, B. (2012) New generation QuIC assays for prion seeding activity. Prion 6, 147-152
56. Lee, K. S., and Caughey, B. (2007) A simplified recipe for prions. Proc. Natl. Acad. Sci. U.S.A. 104, 9551-9552
57. Deleault, N. R., Harris, B. T., Rees, J. R., and Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. U.S.A. 104, 9741-9746 (Pubitemid 47175337)
58. Deleault, N. R., Piro, J. R., Walsh, D. J., Wang, F., Ma, J., Geoghegan, J. C., and Supattapone, S. (2012) Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proc. Natl. Acad. Sci. U.S.A. 109, 8546-8551
59. Murayama, Y., Yoshioka, M., Masujin, K., Okada, H., Iwamaru, Y., Imamura, M., Matsuura, Y., Fukuda, S., Onoe, S., Yokoyama, T., and Mohri, S. (2010) Sulfated dextrans enhance in vitro amplification of bovine spongiform encephalopathy PrP(Sc) and enable ultrasensitive detection of bovine PrP(Sc). PLoS One 5, e13152
60. Abid, K., Morales, R., and Soto, C. (2010) Cellular factors implicated in prion replication. FEBS Lett. 584, 2409-2414
61. Turnbaugh, J. A., Unterberger, U., Saa, P., Massignan, T., Fluharty, B. R., Bowman, F. P., Miller, M. B., Supattapone, S., Biasini, E., and Harris, D. A. (2012) The N-terminal, polybasic region of PrP(C) dictates the efficiency of prion propagation by binding to PrP(Sc). J. Neurosci. 32, 8817-8830
62. Solforosi, L., Bellon, A., Schaller, M., Cruite, J. T., Abalos, G. C., and Williamson, R. A. (2007) Toward molecular dissection of PrPC-PrPSc interactions. J. Biol. Chem. 282, 7465-7471 (Pubitemid 47093641)
63. Kuwata, K., Nishida, N., Matsumoto, T., Kamatari, Y. O., Ho-sokawa- Muto, J., Kodama, K., Nakamura, H. K., Kimura, K., Kawasaki, M., Takakura, Y., Shirabe, S., Takata, J., Kataoka, Y., and Katamine, S. (2007) Hot spots in prion protein for pathogenic conversion. Proc. Natl. Acad. Sci. U.S.A. 104, 11921-11926 (Pubitemid 47185606)
64. Morris, A. M., Watzky, M. A., and Finke, R. G. (2009) Protein aggregation kinetics, mechanism, and curve-fitting: a review of the literature. Biochim. Biophys. Acta 1794, 375-397
65. Prusiner, S. B. (1991) Molecular biology of prion diseases. Science 252, 1515-1522
66. Ladogana, A., Casaccia, P., Ingrosso, L., Cibati, M., Salvatore, M., Xi, Y. G., Masullo, C., and Pocchiari, M. (1992) Sulphate polyanions prolong the incubation period of scrapie-infected hamsters. J. Gen. Virol. 73, 661-665
67. Martins, P. M. (2013) True and apparent inhibition of amyloid fibril formation. Prion 7, 136-139
68. Adjou, K. T., Simoneau, S., Sales, N., Lamoury, F., Dormont, D., Papy-Garcia, D., Barritault, D., Deslys, J. P., and Lasmezas, C. I. (2003) A novel generation of heparan sulfate mimetics for the treatment of prion diseases. J. Gen. Virol. 84, 2595-2603 (Pubitemid 37063149)
69. Larramendy-Gozalo, C., Barret, A., Daudigeos, E., Mathieu, E., Antonangeli, L., Riffet, C., Petit, E., Papy-Garcia, D., Barritault, D., Brown, P., and Deslys, J. P. (2007) Comparison of CR36, a new heparan mimetic, and pentosan polysulfate in the treatment of prion diseases. J. Gen. Virol. 88, 1062-1067 (Pubitemid 46359579)
70. Kisilevsky, R., Lemieux, L. J., Fraser, P. E., Kong, X., Hultin, P. G., and Szarek, W. A. (1995) Arresting amyloidosis in vivo using small-molecule anionic sulphonates or sulphates: implications for Alzheimer's disease. Nat. Med. 1, 143-148
71. Zhu, H., Yu, J., and Kindy, M. S. (2001) Inhibition of amyloidosis using low-molecular-weight heparins. Mol. Med. 7, 517-522 (Pubitemid 33701957)
72. Rumjon, A., Coats, T., and Javaid, M. M. (2012) Review of eprodisate for the treatment of renal disease in AA amyloidosis. Int. J. Nephrol. Renovasc. Dis. 5, 37-43
73. Parry, A., Baker, I., Stacey, R., and Wimalaratna, S. (2007) Long term survival in a patient with variant Creutzfeldt-Jakob disease treated with intraventricular pentosan polysulphate. J. Neurol. Neurosurg. Psychiatry 78, 733-734 (Pubitemid 46998846)
74. Whittle, I. R., Knight, R. S., and Will, R. G. (2006) Unsuccessful intraventricular pentosan polysulphate treatment of variant Creutzfeldt-Jakob disease. Acta Neurochir. (Wien) 148, 677-679; discussion 679
75. Terada, T., Tsuboi, Y., Obi, T., Doh-ura, K., Murayama, S., Kitamoto, T., Yamada, T., and Mizoguchi, K. (2010) Less protease-resistant PrP in a patient with sporadic CJD treated with intraventricular pentosan polysulphate. Acta Neurol. Scand. 121, 127-130
76. Caughey, B., Caughey, W. S., Kocisko, D. A., Lee, K. S., Silveira, J. R., and Morrey, J. D. (2006) Prions and transmissible spongiform encephalopathy (TSE) chemotherapeutics: a common mechanism for anti-TSE compounds? Acc. Chem. Res. 39, 646-653
77. Leveugle, B., Ding, W., Laurence, F., Dehouck, M. P., Scanameo, A., Cecchelli, R., and Fillit, H. (1998) Heparin oligosaccharides that pass the blood-brain barrier inhibit beta-amyloid precursor protein secretion and heparin binding to beta-amyloid peptide. J. Neurochem. 70, 736-744 (Pubitemid 28079364)
78. Dudas, B., Rose, M., Cornelli, U., Pavlovich, A., and Hanin, I. (2008) Neuroprotective properties of glycosaminoglycans: potential treatment for neurodegenerative disorders. Neurodegener. Dis. 5, 200-205 (Pubitemid 351347850)
79. Ma, Q., Dudas, B., Hejna, M., Cornelli, U., Lee, J. M., Lorens, S., Mervis, R., Hanin, I., and Fareed, J. (2002) The blood-brain barrier accessibility of a heparin-derived oligosaccharides C3. Thromb. Res. 105, 447-453 (Pubitemid 34621263)
80. Kong, Q., Mills, J. L., Kundu, B., Li, X., Qing, L., Surewicz, K., Cali, I., Huang, S., Zheng, M., Swietnicki, W., Sonnichsen, F. D., Gambetti, P., and Surewicz, W. K. (2013) Thermodynamic stabilization of the folded domain of prion protein inhibits prion infection in vivo. Cell. Rep. 4, 248-254