PrP interactions with nucleic acids and glycosaminoglycans in function and disease

Frontiers in Bioscience

Volumn 15, Issue 1, 2010, Pages 132-150

  Silva, Jerson L ^a   Gomes, Mariana P B ^a   Vieira, Tuane C R G ^a   Cordeiro, Yraima ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Aggregation; DNA; Encephalopathy; Glycosaminoglycan; Prion protein; Review; RNA

Indexed keywords

GLYCOSAMINOGLYCAN; NUCLEIC ACID; PRION PROTEIN;

ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; PRION; PRION DISEASE; PROTEIN BINDING; PROTEIN CONFORMATION; REVIEW;

ANIMALS; GLYCOSAMINOGLYCANS; HUMANS; MODELS, MOLECULAR; NUCLEIC ACIDS; PRION DISEASES; PRIONS; PROTEIN BINDING; PROTEIN CONFORMATION; PRPC PROTEINS; PRPSC PROTEINS;

EID: 77951237351     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3611     Document Type: Article

References (170)

1. S.B. Prusiner: Prions. Proc Natl Acad Sci U S A 95, 13363-13383 (1998).
2. A. Aguzzi and M. Polymenidou: Mammalian prion biology: one century of evolving concepts. Cell 116, 313- 327 (2004). (Pubitemid 38167320)
3. H.G. Creutzfeldt: Über eine eigenartige herdförmige erkrankung des zentralnervensystems. Z Ges Neurol Psychiatr 57, 1-19 (1920).
4. A. Jakob: Über eigenartige erkrankungen des zentralnervensystems mit bemerkenswertem anatomischem befunde (spastische pseudoskleroseencephalomyelopathie mit disseminierten degenerationsherden). Z Ges Neurol Psychiatr 64, 147- 228 (1921).
5. D.C. GAJDUSEK and V. ZIGAS: Degenerative disease of the central nervous system in New Guinea; the endemic occurrence of kuru in the native population. N Engl J Med 257, 974-978 (1957).
6. T. Alper, W.A. Cramp, D.A. Haig and M.C. Clarke: Does the agent of scrapie replicate without nucleic acid? Nature 214, 764-766 (1967).
7. J.S. Griffith: Self-replication and scrapie. Nature 215, 1043-1044 (1967).
8. S.B. Prusiner, D.F. Groth, S.P. Cochran, F.R. Masiarz, M.P. McKinley and H.M. Martinez: Molecular properties, partial purification, and assay by incubation period measurements of the hamster scrapie agent. Biochemistry 19, 4883-4891 (1980).
9. S.B. Prusiner: Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144 (1982). (Pubitemid 12089840)
10. S.B. Prusiner, D.F. Groth, D.C. Bolton, S.B. Kent and L.E. Hood: Purification and structural studies of a major scrapie prion protein. Cell 38, 127-134 (1984). (Pubitemid 15216542)
11. B. Caughey and B. Chesebro: Transmissible spongiform encephalopathies and prion protein interconversions. Adv Virus Res 56, 277-311 (2001).
12. B. Oesch, D. Westaway, M. Walchli, M.P. McKinley, S.B. Kent, R. Aebersold, R.A. Barry, P. Tempst, D.B. Teplow, L.E. Hood and : A cellular gene encodes scrapie PrP 27-30 protein. Cell 40, 735-746 (1985). (Pubitemid 15240279)
13. N.R. Cashman, R. Loertscher, J. Nalbantoglu, I. Shaw, R.J. Kascsak, D.C. Bolton and P.E. Bendheim: Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 61, 185-192 (1990).
14. N. Stahl, D.R. Borchelt, K. Hsiao and S.B. Prusiner: Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51, 229-240 (1987).
15. P.M. Rudd, T. Endo, C. Colominas, D. Groth, S.F. Wheeler, D.J. Harvey, M.R. Wormald, H. Serban, S.B. Prusiner, A. Kobata and R.A. Dwek: Glycosylation differences between the normal and pathogenic prion protein isoforms. Proc Natl Acad Sci U S A 96, 13044-13049 (1999).
16. P.M. Rudd, M.R. Wormald, D.R. Wing, S.B. Prusiner and R.A. Dwek: Prion glycoprotein: structure, dynamics, and roles for the sugars. Biochemistry 40, 3759-3766 (2001). (Pubitemid 32280412)
17. R. Riek, S. Hornemann, G. Wider, R. Glockshuber and K. Wuthrich: NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett 413, 282-288 (1997). (Pubitemid 27353285)
18. J.H. Viles, F.E. Cohen, S.B. Prusiner, D.B. Goodin, P.E. Wright and H.J. Dyson: Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc Natl Acad Sci U S A 96, 2042-2047 (1999). (Pubitemid 29117864)
19. D.R. Brown, K. Qin, J.W. Herms, A. Madlung, J. Manson, R. Strome, P.E. Fraser, T. Kruck, A. von Bohlen, W. Schulz-Schaeffer, A. Giese, D. Westaway and H. Kretzschmar: The cellular prion protein binds copper in vivo. Nature 390, 684- 687 (1997). (Pubitemid 28016355)
20. D.G. Donne, J.H. Viles, D. Groth, I. Mehlhorn, T.L. James, F.E. Cohen, S.B. Prusiner, P.E. Wright and H.J. Dyson: Structure of the recombinant full-length hamster prion protein PrP(29-231): the N terminus is highly flexible. Proc Natl Acad Sci U S A 94, 13452-13457 (1997).
21. D.A. Lysek, C. Schorn, L.G. Nivon, V. Esteve-Moya, B. Christen, L. Calzolai, C. von Schroetter, F. Fiorito, T. Herrmann, P. Guntert and K. Wuthrich: Prion protein NMR structures of cats, dogs, pigs, and sheep. Proc Natl Acad Sci U S A 102, 640-645 (2005). (Pubitemid 40282718)
22. L. Calzolai, D.A. Lysek, D.R. Perez, P. Guntert and K. Wuthrich: Prion protein NMR structures of chickens, turtles, and frogs. Proc Natl Acad Sci U S A 102, 651-655 (2005). (Pubitemid 40282720)
23. R. Zahn, A. Liu, T. Luhrs, R. Riek, C. von Schroetter, G.F. Lopez, M. Billeter, L. Calzolai, G. Wider and K. Wuthrich: NMR solution structure of the human prion protein. Proc Natl Acad Sci U S A 97, 145-150 (2000). (Pubitemid 30055798)
24. J.C. Watts and D. Westaway: The prion protein family: diversity, rivalry, and dysfunction. Biochim Biophys Acta 1772, 654-672 (2007). (Pubitemid 46880210)
25. H. Bueler, M. Fischer, Y. Lang, H. Bluethmann, H.P. Lipp, S.J. DeArmond, S.B. Prusiner, M. Aguet and C. Weissmann: Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582 (1992).
26. A. Aguzzi and M. Heikenwalder: Pathogenesis of prion diseases: current status and future outlook. Nat Rev Microbiol 4, 765-775 (2006). (Pubitemid 44420127)
27. A. Aguzzi, C. Sigurdson and M. Heikenwaelder: Molecular mechanisms of prion pathogenesis. Annu Rev Pathol 3, 11-40 (2008). (Pubitemid 351488275)
28. V.R. Martins, R. Linden, M.A. Prado, R. Walz, A.C. Sakamoto, I. Izquierdo and R.R. Brentani: Cellular prion protein: on the road for functions. FEBS Lett 512, 25-28 (2002). (Pubitemid 34164444)
29. E. Graner, A.F. Mercadante, S.M. Zanata, O.V. Forlenza, A.L. Cabral, S.S. Veiga, M.A. Juliano, R. Roesler, R. Walz, A. Minetti, I. Izquierdo, V.R. Martins and R.R. Brentani: Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res Mol Brain Res 76, 85-92 (2000). (Pubitemid 30133236)
30. E. Graner, A.F. Mercadante, S.M. Zanata, V.R. Martins, D.G. Jay and R.R. Brentani: Laminin-induced PC-12 cell differentiation is inhibited following laser inactivation of cellular prion protein. FEBS Lett 482, 257-260 (2000).
31. S. Gauczynski, J.M. Peyrin, S. Haik, C. Leucht, C. Hundt, R. Rieger, S. Krasemann, J.P. Deslys, D. Dormont, C.I. Lasmezas and S. Weiss: The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J 20, 5863-5875 (2001). (Pubitemid 33049262)
32. V. Ellis, M. Daniels, R. Misra and D.R. Brown: Plasminogen activation is stimulated by prion protein and regulated in a copper-dependent manner. Biochemistry 41, 6891-6896 (2002). (Pubitemid 34575659)
33. A. Barret, L. Forestier, J.P. Deslys, R. Julien and P.F. Gallet: Glycosylation-related gene expression in prion diseases: PrPSc accumulation in scrapie infected GT1 cells depends on beta-1, 4-linked GalNAc-4-SO4 hyposulfation. J Biol Chem 280, 10516-10523 (2005). (Pubitemid 40395911)
34. S.M. Zanata, M.H. Lopes, A.F. Mercadante, G.N. Hajj, L.B. Chiarini, R. Nomizo, A.R. Freitas, A.L. Cabral, K.S. Lee, M.A. Juliano, E. de Oliveira, S.G. Jachieri, A. Burlingame, L. Huang, R. Linden, R.R. Brentani and V.R. Martins: Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J 21, 3307-3316 (2002). (Pubitemid 34760563)
35. G.I. Keshet, O. Bar-Peled, D. Yaffe, U. Nudel and R. Gabizon: The cellular prion protein colocalizes with the dystroglycan complex in the brain. J Neurochem 75, 1889- 1897 (2000).
36. K. Nieznanski, H. Nieznanska, K.J. Skowronek, K.M. Osiecka and D. Stepkowski: Direct interaction between prion protein and tubulin. Biochem Biophys Res Commun 334, 403-411 (2005). (Pubitemid 40982382)
37. A. Aguzzi, F. Baumann and J. Bremer: The prion's elusive reason for being. Annu Rev Neurosci 31, 439-477 (2008).
38. J.L. Silva, L.M. Lima, D. Foguel and Y. Cordeiro: Intriguing nucleic-acid-binding features of mammalian prion protein. Trends Biochem Sci 33, 132-140 (2008).
39. K.M. Pan, M. Baldwin, J. Nguyen, M. Gasset, A. Serban, D. Groth, I. Mehlhorn, Z. Huang, R.J. Fletterick, F.E. Cohen and S.B. Prusiner: Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci U S A 90, 10962-10966 (1993).
40. S.B. Prusiner, M.P. McKinley, K.A. Bowman, D.C. Bolton, P.E. Bendheim, D.F. Groth and G.G. Glenner: Scrapie prions aggregate to form amyloid-like birefringent rods. Cell 35, 349-358 (1983). (Pubitemid 14202913)
41. Z. Huang, S.B. Prusiner and F.E. Cohen: Scrapie prions: a three-dimensional model of an infectious fragment. Fold Des 1, 13-19 (1996). (Pubitemid 126748154)
42. L.M. Herrmann and B. Caughey: The importance of the disulfide bond in prion protein conversion. Neuroreport 9, 2457-2461 (1998). (Pubitemid 28387130)
43. C. Govaerts, H. Wille, S.B. Prusiner and F.E. Cohen: Evidence for assembly of prions with left-handed betahelices into trimers. Proc Natl Acad Sci U S A 101, 8342- 8347 (2004). (Pubitemid 38736577)
44. H. Bueler, A. Aguzzi, A. Sailer, R.A. Greiner, P. Autenried, M. Aguet and C. Weissmann: Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347 (1993). (Pubitemid 23201147)
45. D.A. Kocisko, J.H. Come, S.A. Priola, B. Chesebro, G.J. Raymond, P.T. Lansbury and B. Caughey: Cell-free formation of protease-resistant prion protein. Nature 370, 471-474 (1994). (Pubitemid 24263553)
46. D.A. Kocisko, S.A. Priola, G.J. Raymond, B. Chesebro, P.T. Lansbury, Jr. and B. Caughey: Species specificity in the cell-free conversion of prion protein to proteaseresistant forms: a model for the scrapie species barrier. Proc Natl Acad Sci U S A 92, 3923-3927 (1995).
47. C. Weissmann: The state of the prion. Nat Rev Microbiol 2, 861-871 (2004). (Pubitemid 39561804)
48. Y. Cordeiro, F. Machado, L. Juliano, M.A. Juliano, R.R. Brentani, D. Foguel and J.L. Silva: DNA converts cellular prion protein into the beta-sheet conformation and inhibits prion peptide aggregation. J Biol Chem 276, 49400-49409 (2001).
49. G.C. Telling, M. Scott, J. Mastrianni, R. Gabizon, M. Torchia, F.E. Cohen, S.J. DeArmond and S.B. Prusiner: Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83, 79-90 (1995).
50. B. Caughey, K. Brown, G.J. Raymond, G.E. Katzenstein and W. Thresher: Binding of the proteasesensitive form of PrP (prion protein) to sulfated glycosaminoglycan and congo red [corrected]. J Virol 68, 2135-2141 (1994). (Pubitemid 24091890)
51. B. Caughey and G.S. Baron: Prions and their partners in crime. Nature 443, 803-810 (2006). (Pubitemid 44622685)
52. N.R. Deleault, R.W. Lucassen and S. Supattapone: RNA molecules stimulate prion protein conversion. Nature 425, 717-720 (2003). (Pubitemid 37314314)
53. I.V. Baskakov, G. Legname, S.B. Prusiner and F.E. Cohen: Folding of prion protein to its native alpha-helical conformation is under kinetic control. Journal of Biological Chemistry 276, 19687-19690 (2001).
54. A.C. Apetri and W.K. Surewicz: Atypical effect of salts on the thermodynamic stability of human prion protein. J Biol Chem 278, 22187-22192 (2003). (Pubitemid 36830263)
55. Y. Cordeiro, J. Kraineva, R. Ravindra, L.M. Lima, M.P. Gomes, D. Foguel, R. Winter and J.L. Silva: 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 (2004). (Pubitemid 39014688)
56. Y. Cordeiro, J. Kraineva, M.P. Gomes, M.H. Lopes, V.R. Martins, L.M. Lima, D. Foguel, R. Winter and J.L. Silva: The amino-terminal PrP domain is crucial to modulate prion misfolding and aggregation. Biophys J 89, 2667-2676 (2005). (Pubitemid 41401056)
57. Y. Cordeiro, J. Kraineva, R. Winter and J.L. Silva: Volume and energy folding landscape of prion protein revealed by pressure. Braz J Med Biol Res 38, 1195-1201 (2005). (Pubitemid 41167283)
58. A. De Simone, G.G. Dodson, C.S. Verma, A. Zagari and F. Fraternali: Prion and water: tight and dynamical hydration sites have a key role in structural stability. Proc Natl Acad Sci U S A 102, 7535-7540 (2005). (Pubitemid 40741006)
59. A. De Simone, G.G. Dodson, F. Fraternali and A. Zagari: Water molecules as structural determinants among prions of low sequence identity. FEBS Lett 580, 2488-2494 (2006).
60. A.F. Hill, M. Antoniou and J. Collinge: Proteaseresistant prion protein produced in vitro lacks detectable infectivity. J Gen Virol 80 (Pt 1), 11-14 (1999). (Pubitemid 29041673)
61. S.B. Prusiner, D. Groth, A. Serban, N. Stahl and R. Gabizon: Attempts to restore scrapie prion infectivity after exposure to protein denaturants. Proc Natl Acad Sci U S A 90, 2793-2797 (1993). (Pubitemid 23113503)
62. G.M. Shaked, G. Fridlander, Z. Meiner, A. Taraboulos and R. Gabizon: Protease-resistant and detergent-insoluble prion protein is not necessarily associated with prion infectivity. J Biol Chem 274, 17981-17986 (1999).
63. G.P. Saborio, B. Permanne and C. Soto: Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813 (2001). (Pubitemid 32588105)
64. R. Lucassen, K. Nishina and S. Supattapone: In vitro amplification of protease-resistant prion protein requires free sulfhydryl groups. Biochemistry 42, 4127-4135 (2003). (Pubitemid 36418306)
65. G. Legname, I.V. Baskakov, H.O. Nguyen, D. Riesner, F.E. Cohen, S.J. DeArmond and S.B. Prusiner: Synthetic mammalian prions. Science 305, 673-676 (2004). (Pubitemid 39006757)
66. K. Kaneko, L. Zulianello, M. Scott, C.M. Cooper, A.C. Wallace, T.L. James, F.E. Cohen and S.B. Prusiner: Evidence for protein X binding to a discontinuous epitope on the cellular prion protein during scrapie prion propagation. Proc Natl Acad Sci U S A 94, 10069-10074 (1997).
67. B. Caughey and D.A. Kocisko: Prion diseases - A nucleicacid accomplice? Nature 425, 673-674 (2003).
68. Y. Cordeiro and J.L. Silva: The hypothesis of the catalytic action of nucleic acid on the conversion of prion protein. Protein Pept Lett 12, 251-255 (2005). (Pubitemid 40428415)
69. M.P. Gomes, T.A. Millen, P.S. Ferreira, N.L. Silva, T.C. Vieira, M.S. Almeida, J.L. Silva and Y. Cordeiro: Prion protein complexed to N2a cellular RNAs through its Nterminal domain forms aggregates and is toxic to murine neuroblastoma cells. J Biol Chem 283, 19616-19625 (2008).
70. L. Horonchik, S. Tzaban, O. Ben Zaken, Y. Yedidia, A. Rouvinski, D. Papy-Garcia, D. Barritault, I. Vlodavsky and A. Taraboulos: Heparan sulfate is a cellular receptor for purified infectious prions. J Biol Chem 280, 17062-17067 (2005). (Pubitemid 41389169)
71. I. Capila and R.J. Linhardt: Heparin-protein interactions. Angew Chem Int Ed Engl 41, 391-412 (2002).
72. R. Virchow: Zur cellulosefrage. Virchows Arch Pathol Anat Physiol 6, 416-426 (1854).
73. A.D. Snow and R. Kisilevsky: Temporal Relationship Between Glycosaminoglycan Accumulation and Amyloid Deposition During Experimental Amyloidosis - A Histochemical-Study. Laboratory Investigation 53, 37-44 (1985). (Pubitemid 15237710)
74. I.D. Young, J.P. Willmer and R. Kisilevsky: The Ultrastructural- Localization of Sulfated Proteoglycans Is Identical in the Amyloids of Alzheimers-Disease and Aa, Al, Senile Cardiac and Medullary Carcinoma-Associated Amyloidosis. Acta Neuropathologica 78, 202-209 (1989). (Pubitemid 19160925)
75. I.D. Young, L. Ailles, S. Narindrasorasak, R. Tan and R. Kisilevsky: Localization of the Basement-Membrane Heparan-Sulfate Proteoglycan in Islet Amyloid Deposits in Type-Ii Diabetes-Mellitus. Archives of Pathology & Laboratory Medicine 116, 951-954 (1992).
76. A.D. Snow, R. Kisilevsky, J. Willmer, S.B. Prusiner and S.J. DeArmond: Sulfated Glycosaminoglycans in Amyloid Plaques of Prion Diseases. Acta Neuropathologica 77, 337-342 (1989). (Pubitemid 19070175)
77. P.A. McBride, M.I. Wilson, P. Eikelenboom, A. Tunstall and M.E. Bruce: Heparan sulfate proteoglycan is associated with amyloid plaques and neuroanatomically targeted PrP pathology throughout the incubation period of scrapie-infected mice. Exp Neurol 149, 447-454 (1998). (Pubitemid 28115083)
78. C. Wong, L.W. Xiong, M. Horiuchi, L. Raymond, K. Wehrly, B. Chesebro and B. Caughey: Sulfated glycans and elevated temperature stimulate PrP(Sc)-dependent cell-free formation of protease-resistant prion protein. EMBO J 20, 377-386 (2001). (Pubitemid 32126974)
79. T. Pan, B.S. Wong, T. Liu, R. Li, R.B. Petersen and M.S. Sy: Cell-surface prion protein interacts with glycosaminoglycans. Biochem J 368, 81-90 (2002). (Pubitemid 35463411)
80. R.G. Warner, C. Hundt, S. Weiss and J.E. Turnbull: Identification of the heparan sulfate binding sites in the cellular prion protein. J Biol Chem 277, 18421-18430 (2002). (Pubitemid 34952388)
81. R. Gabizon, Z. Meiner, M. Halimi and S.A. Ben Sasson: Heparin-like molecules bind differentially to prionproteins and change their intracellular metabolic fate. J Cell Physiol 157, 319-325 (1993). (Pubitemid 23332776)
82. O. Ben Zaken, S. Tzaban, Y. Tal, L. Horonchik, J.D. Esko, I. Vlodavsky and A. Taraboulos: Cellular heparan sulfate participates in the metabolism of prions. J Biol Chem 278, 40041-40049 (2003). (Pubitemid 37248570)
83. N. Hijazi, Z. Kariv-Inbal, M. Gasset and R. Gabizon: PrPSc incorporation to cells requires endogenous glycosaminoglycan expression. J Biol Chem 280, 17057- 17061 (2005). (Pubitemid 41389168)
84. A.D. Snow, T.N. Wight, D. Nochlin, Y. Koike, K. Kimata, S.J. DeArmond and S.B. Prusiner: Immunolocalization of heparan sulfate proteoglycans to the prion protein amyloid plaques of Gerstmann-Straussler syndrome, Creutzfeldt-Jakob disease and scrapie. Lab Invest 63, 601-611 (1990).
85. B. Caughey, D. Ernst and R.E. Race: Congo red inhibition of scrapie agent replication. J Virol 67, 6270- 6272 (1993). (Pubitemid 23277541)
86. S.L. Shyng, S. Lehmann, K.L. Moulder and D.A. Harris: Sulfated glycans stimulate endocytosis of the cellular isoform of the prion protein, PrPC, in cultured cells. J Biol Chem 270, 30221-30229 (1995).
87. M. Perez, F. Wandosell, C. Colaco and J. Avila: Sulphated glycosaminoglycans prevent the neurotoxicity of a human prion protein fragment. Biochem J 335 (Pt 2), 369-374 (1998). (Pubitemid 28491072)
88. N.R. Deleault, J.C. Geoghegan, K. Nishina, R. Kascsak, R.A. Williamson and S. Supattapone: Protease-resistant prion protein amplification reconstituted with partially purified substrates and synthetic polyanions. J Biol Chem 280, 26873-26879 (2005). (Pubitemid 41040721)
89. M. Cortijo-Arellano, J. Ponce, N. Durany and J. Cladera: 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 (2008).
90. B. Klajnert, M. Cortijo-Arellano, M. Bryszewska and J. Cladera: Influence of heparin and dendrimers on the aggregation of two amyloid peptides related to Alzheimer's and prion diseases. Biochem Biophys Res Commun 339, 577-582 (2006). (Pubitemid 41739706)
91. S. Chen, A. Mange, L. Dong, S. Lehmann and M. Schachner: Prion protein as trans-interacting partner for neurons is involved in neurite outgrowth and neuronal survival. Mol Cell Neurosci 22, 227-233 (2003). (Pubitemid 36379186)
92. T. Kinnunen, M. Kaksonen, J. Saarinen, N. Kalkkinen, H.B. Peng and H. Rauvala: Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J Biol Chem 273, 10702-10708 (1998). (Pubitemid 28227685)
93. C. Hundt, J.M. Peyrin, S. Haik, S. Gauczynski, C. Leucht, R. Rieger, M.L. Riley, J.P. Deslys, D. Dormont, C.I. Lasmezas and S. Weiss: Identification of interaction domains of the prion protein with its 37-kDa/67-kDa laminin receptor. EMBO J 20, 5876-5886 (2001). (Pubitemid 33049263)
94. S. Gauczynski, D. Nikles, S. El Gogo, D. Papy-Garcia, C. Rey, S. Alban, D. Barritault, C.I. Lasmezas and S. Weiss: The 37-kDa/67-kDa laminin receptor acts as a receptor for infectious prions and is inhibited by polysulfated glycanes. J Infect Dis 194, 702-709 (2006). (Pubitemid 44297858)
95. C. Leucht, S. Simoneau, C. Rey, K. Vana, R. Rieger, C.I. Lasmezas and S. Weiss: The 37 kDa/67 kDa laminin receptor is required for PrP(Sc) propagation in scrapieinfected neuronal cells. EMBO Rep 4, 290-295 (2003). (Pubitemid 36511726)
96. M. Praus, G. Kettelgerdes, M. Baier, H.G. Holzhutter, P.R. Jungblut, M. Maissen, G. Epple, W.D. Schleuning, E. Kottgen, A. Aguzzi and R. Gessner: Stimulation of plasminogen activation by recombinant cellular prion protein is conserved in the NH2-terminal fragment PrP23- 110. Thromb Haemost 89, 812-819 (2003). (Pubitemid 36603422)
97. L.A. Fransson, M. Belting, F. Cheng, M. Jonsson, K. Mani and S. Sandgren: Novel aspects of glypican glycobiology. Cell Mol Life Sci 61, 1016-1024 (2004). (Pubitemid 38656128)
98. K. Mani, F. Cheng and L.A. Fransson: Heparan sulfate degradation products can associate with oxidized proteins and proteasomes. J Biol Chem 282, 21934-21944 (2007). (Pubitemid 47201817)
99. M. Belting, S. Persson and L.A. Fransson: Proteoglycan involvement in polyamine uptake. Biochem J 338 (Pt 2), 317-323 (1999).
100. K. Ding, K. Mani, F. Cheng, M. Belting and L.A. Fransson: Copper-dependent autocleavage of glypican-1 heparan sulfate by nitric oxide derived from intrinsic nitrosothiols. J Biol Chem 277, 33353-33360 (2002). (Pubitemid 34987556)
101. G.L. Millhauser: Copper and the prion protein: methods, structures, function, and disease. Annu Rev Phys Chem 58, 299-320 (2007). (Pubitemid 46877592)
102. K. Mani, F. Cheng, B. Havsmark, M. Jonsson, M. Belting and L.A. Fransson: Prion, amyloid beta-derived Cu(II) ions, or free Zn(II) ions support S-nitroso-dependent autocleavage of glypican-1 heparan sulfate. J Biol Chem 278, 38956-38965 (2003). (Pubitemid 37229067)
103. F. Cheng, J. Lindqvist, C.L. Haigh, D.R. Brown and K. Mani: Copper-dependent co-internalization of the prion protein and glypican-1. J Neurochem 98, 1445-1457 (2006). (Pubitemid 44200436)
104. P.C. Pauly and D.A. Harris: Copper stimulates endocytosis of the prion protein. J Biol Chem 273, 33107- 33110 (1998). (Pubitemid 29005676)
105. A.D. Cardin and H.J. Weintraub: Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9, 21-32 (1989). (Pubitemid 19046087)
106. M. Sobel, D.F. Soler, J.C. Kermode and R.B. Harris: Localization and characterization of a heparin binding domain peptide of human von Willebrand factor. J Biol Chem 267, 8857-8862 (1992).
107. H. Margalit, N. Fischer and S.A. Ben Sasson: Comparative analysis of structurally defined heparin binding sequences reveals a distinct spatial distribution of basic residues. J Biol Chem 268, 19228-19231 (1993). (Pubitemid 23270692)
108. J.R. Fromm, R.E. Hileman, J.M. Weiler and R.J. Linhardt: Interaction of fibroblast growth factor-1 and related peptides with heparan sulfate and its oligosaccharides. Arch Biochem Biophys 346, 252-262 (1997). (Pubitemid 27439043)
109. J.R. Fromm, R.E. Hileman, E.E. Caldwell, J.M. Weiler and R.J. Linhardt: Differences in the interaction of heparin with arginine and lysine and the importance of these basic amino acids in the binding of heparin to acidic fibroblast growth factor. Arch Biochem Biophys 323, 279- 287 (1995).
110. A. Abedini, S.M. Tracz, J.H. Cho and D.P. Raleigh: Characterization of the heparin binding site in the Nterminus of human pro-islet amyloid polypeptide: implications for amyloid formation. Biochemistry 45, 9228- 9237 (2006). (Pubitemid 44156386)
111. J. Hallgren, S. Backstrom, S. Estrada, M. Thuveson and G. Pejler: Histidines are critical for heparin-dependent activation of mast cell tryptase. J Immunol 173, 1868-1875 (2004). (Pubitemid 38971621)
112. A. Sebollela, T.C. Cagliari, G.S. Limaverde, A. Chapeaurouge, M.H. Sorgine, T. Coelho-Sampaio, C.H. Ramos and S.T. Ferreira: Heparin-binding sites in granulocyte-macrophage colony-stimulating factor. Localization and regulation by histidine ionization. J Biol Chem 280, 31949-31956 (2005). (Pubitemid 41291945)
113. R.A. Pixley, Y. Lin, I. Isordia-Salas and R.W. Colman: Fine mapping of the sequences in domain 5 of high molecular weight kininogen (HK) interacting with heparin and zinc. J Thromb Haemost 1, 1791-1798 (2003).
114. F. Wopfner, G. Weidenhofer, R. Schneider, A. von Brunn, S. Gilch, T.F. Schwarz, T. Werner and H.M. Schatzl: Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein. J Mol Biol 289, 1163-1178 (1999). (Pubitemid 29296697)
115. L.G. Goldfarb, P. Brown, W.R. McCombie, D. Goldgaber, G.D. Swergold, P.R. Wills, L. Cervenakova, H. Baron, C.J. Gibbs Jr. and D.C. GAJDUSEK: Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc Natl Acad Sci U S A 88, 10926-10930 (1991). (Pubitemid 21915952)
116. S. Yu, S. Yin, C. Li, P. Wong, B. Chang, F. Xiao, S.C. Kang, H. Yan, G. Xiao, P. Tien and M.S. Sy: Aggregation of prion protein with insertion mutations is proportional to the number of inserts. Biochem J 403, 343-351 (2007). (Pubitemid 46596591)
117. R. Gonzalez-Iglesias, M.A. Pajares, C. Ocal, J.C. Espinosa, B. Oesch and M. Gasset: Prion protein interaction with glycosaminoglycan occurs with the formation of oligomeric complexes stabilized by Cu(II) bridges. J Mol Biol 319, 527-540 (2002). (Pubitemid 34729477)
118. D.B. Brimacombe, A.D. Bennett, F.S. Wusteman, A.C. Gill, J.C. Dann and C.J. Bostock: Characterization and polyanion-binding properties of purified recombinant prion protein. Biochem J 342 Pt 3, 605-613 (1999). (Pubitemid 29452645)
119. S. Yin, S. Yu, C. Li, P. Wong, B. Chang, F. Xiao, S.C. Kang, H. Yan, G. Xiao, J. Grassi, P. Tien and M.S. Sy: Prion proteins with insertion mutations have altered Nterminal conformation and increased ligand binding activity and are more susceptible to oxidative attack. J Biol Chem 281, 10698-10705 (2006). (Pubitemid 43855491)
120. S. Yin, N. Pham, S. Yu, C. Li, P. Wong, B. Chang, S.C. Kang, E. Biasini, P. Tien, D.A. Harris and M.S. Sy: Human prion proteins with pathogenic mutations share common conformational changes resulting in enhanced binding to glycosaminoglycans. Proc Natl Acad Sci U S A 104, 7546-7551 (2007). (Pubitemid 47185943)
121. S. Yu, S. Yin, N. Pham, P. Wong, S.C. Kang, R.B. Petersen, C. Li and M.S. Sy: Ligand binding promotes prion protein aggregation-role of the octapeptide repeats. FEBS J 275, 5564-5575 (2008).
122. D. Shukla, J. Liu, P. Blaiklock, N.W. Shworak, X. Bai, J.D. Esko, G.H. Cohen, R.J. Eisenberg, R.D. Rosenberg and P.G. Spear: A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99, 13- 22 (1999). (Pubitemid 29468626)
123. B. Casu and U. Lindahl: Structure and biological interactions of heparin and heparan sulfate. Adv Carbohydr Chem Biochem 57, 159-206 (2001). (Pubitemid 34121000)
124. M.O. Ouidja, E. Petit, M.E. Kerros, Y. Ikeda, C. Morin, G. Carpentier, D. Barritault, J. Brugere-Picoux, J.P. Deslys, K. Adjou and D. Papy-Garcia: Structure-activity studies of heparan mimetic polyanions for anti-prion therapies. Biochem Biophys Res Commun 363, 95-100 (2007). (Pubitemid 47440153)
125. S. Vasan, P.Y. Mong and A. Grossman: Interaction of prion protein with small highly structured RNAs: detection and characterization of PrP-oligomers. Neurochem Res 31, 629-637 (2006). (Pubitemid 43886411)
126. N.R. Deleault, B.T. Harris, J.R. Rees and S. Supattapone: Formation of native prions from minimal components in vitro. Proc Natl Acad Sci U S A 104, 9741- 9746 (2007). (Pubitemid 47175337)
127. N. Daude, M. Marella and J. Chabry: Specific inhibition of pathological prion protein accumulation by small interfering RNAs. J Cell Sci 116, 2775-2779 (2003). (Pubitemid 36857228)
128. M.V. Karpuj, K. Giles, S. Gelibter-Niv, M.R. Scott, V.R. Lingappa, F.C. Szoka, D. Peretz, W. Denetclaw and S.B. Prusiner: Phosphorothioate oligonucleotides reduce PrP levels and prion infectivity in cultured cells. Mol Med 13, 190-198 (2007). (Pubitemid 46944962)
129. P.K. Nandi: Interaction of prion peptide HuPrP106- 126 with nucleic acid. Arch Virol 142, 2537-2545 (1997).
130. A. Rhie, L. Kirby, N. Sayer, R. Wellesley, P. Disterer, I. Sylvester, A. Gill, J. Hope, W. James and A. Tahiri-Alaoui: Characterization of 2'-fluoro-RNA aptamers that bind preferentially to disease-associated conformations of prion protein and inhibit conversion. J Biol Chem 278, 39697-39705 (2003). (Pubitemid 37248531)
131. W.Q. Zou, J. Zheng, D.M. Gray, P. Gambetti and S.G. Chen: Antibody to DNA detects scrapie but not normal prion protein. Proc Natl Acad Sci U S A 101, 1380-1385 (2004). (Pubitemid 38182697)
132. C. Gabus, S. Auxilien, C. Pechoux, D. Dormont, W. Swietnicki, M. Morillas, W. Surewicz, P. Nandi and J.L. Darlix: The prion protein has DNA strand transfer properties similar to retroviral nucleocapsid protein. J Mol Biol 307, 1011-1021 (2001). (Pubitemid 33031273)
133. C. Gabus, E. Derrington, P. Leblanc, J. Chnaiderman, D. Dormont, W. Swietnicki, M. Morillas, W.K. Surewicz, D. Marc, P. Nandi and J.L. Darlix: The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J Biol Chem 276, 19301-19309 (2001).
134. J.L. Silva, L.M. Lima, D. Foguel and Y. Cordeiro: Response to Radulescu and Brenig: Infectious nucleic acids in prion disease: halfway there. Trends Biochem Sci 34, 5-6 (2009).
135. P.K. Nandi and E. Leclerc: Polymerization of murine recombinant prion protein in nucleic acid solution. Arch Virol 144, 1751-1763 (1999). (Pubitemid 29490035)
136. P.K. Nandi, E. Leclerc, J.C. Nicole and M. Takahashi: DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid. J Mol Biol 322, 153-161 (2002). (Pubitemid 36132675)
137. P.K. Nandi and J.C. Nicole: Nucleic acid and prion protein interaction produces spherical amyloids which can function in vivo as coats of spongiform encephalopathy agent. J Mol Biol 344, 827-837 (2004). (Pubitemid 39469223)
138. L.M. Lima, Y. Cordeiro, L.W. Tinoco, A.F. Marques, C.L. Oliveira, S. Sampath, R. Kodali, G. Choi, D. Foguel, I. Torriani, B. Caughey and J.L. Silva: Structural insights into the interaction between prion protein and nucleic acid. Biochemistry 45, 9180-9187 (2006). (Pubitemid 44156381)
139. A. Mange, C. Crozet, S. Lehmann and F. Beranger: Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin. J Cell Sci 117, 2411-2416 (2004). (Pubitemid 38807507)
140. S. Yin, X. Fan, S. Yu, C. Li and M.S. Sy: Binding of recombinant but not endogenous prion protein to DNA causes DNA internalization and expression in mammalian cells. J Biol Chem 283, 25446-25454 (2008).
141. D.A. Kocisko, A. Vaillant, K.S. Lee, K.M. Arnold, N. Bertholet, R.E. Race, E.A. Olsen, J.M. Juteau and B. Caughey: Potent antiscrapie activities of degenerate phosphorothioate oligonucleotides. Antimicrob Agents Chemother 50, 1034-1044 (2006). (Pubitemid 43327809)
142. D.J. King, J.G. Safar, G. Legname and S.B. Prusiner: Thioaptamer interactions with prion proteins: sequencespecific and non-specific binding sites. J Mol Biol 369, 1001-1014 (2007). (Pubitemid 46754057)
143. S. Weiss, D. Proske, M. Neumann, M.H. Groschup, H.A. Kretzschmar, M. Famulok and E.L. Winnacker: RNA aptamers specifically interact with the prion protein PrP. J Virol 71, 8790-8797 (1997). (Pubitemid 27446463)
144. V. Adler, B. Zeiler, V. Kryukov, R. Kascsak, R. Rubenstein and A. Grossman: Small, highly structured RNAs participate in the conversion of human recombinant PrP(Sen) to PrP(Res) in vitro. J Mol Biol 332, 47-57 (2003). (Pubitemid 36999730)
145. S. Sekiya, K. Noda, F. Nishikawa, T. Yokoyama, P.K. Kumar and S. Nishikawa: Characterization and application of a novel RNA aptamer against the mouse prion protein. J Biochem 139, 383-390 (2006). (Pubitemid 43667102)
146. N.M. Sayer, M. Cubin, A. Rhie, M. Bullock, A. Tahiri-Alaoui and W. James: Structural determinants of conformationally selective, prion-binding aptamers. J Biol Chem 279, 13102-13109 (2004). (Pubitemid 38445888)
147. J.C. Geoghegan, P.A. Valdes, N.R. Orem, N.R. Deleault, R.A. Williamson, B.T. Harris and S. Supattapone: Selective incorporation of polyanionic molecules into hamster prions. J Biol Chem 282, 36341-36353 (2007).
148. F.F. Costa: Non-coding RNAs: new players in eukaryotic biology. Gene 357, 83-94 (2005). (Pubitemid 41297574)
149. D. Kampa, J. Cheng, P. Kapranov, M. Yamanaka, S. Brubaker, S. Cawley, J. Drenkow, A. Piccolboni, S. Bekiranov, G. Helt, H. Tammana and T.R. Gingeras: Novel RNAs identified from an in-depth analysis of the transcriptome of human chromosomes 21 and 22. Genome Res 14, 331-342 (2004). (Pubitemid 38380391)
150. M.E. Dinger, T.R. Mercer and J.S. Mattick: RNAs as extracellular signaling molecules. J Mol Endocrinol 40, 151-159 (2008). (Pubitemid 351586824)
151. A. Bera and P.K. Nandi: Biological polyamines inhibit nucleic-acid-induced polymerisation of prion protein. Arch Virol 152, 655-668 (2007). (Pubitemid 46452235)
152. M.P. Gomes, Y. Cordeiro and J.L. Silva: The peculiar interaction between mammalian prion protein and RNA. Prion 2, 64-66 (2008).
153. R. Linden, V.R. Martins, M.A. Prado, M. Cammarota, I. Izquierdo and R.R. Brentani: Physiology of the prion protein. Physiol Rev 88, 673-728 (2008). (Pubitemid 351520090)
154. H. Tjong and H.X. Zhou: DISPLAR: an accurate method for predicting DNA-binding sites on protein surfaces. Nucleic Acids Res 35, 1465-1477 (2007). (Pubitemid 46592869)
155. A. Bera, A.C. Roche and P.K. Nandi: Bending and unwinding of nucleic acid by prion protein. Biochemistry 46, 1320-1328 (2007). (Pubitemid 46208479)
156. P. Tompa and P. Csermely: The role of structural disorder in the function of RNA and protein chaperones. FASEB J 18, 1169-1175 (2004). (Pubitemid 39006878)
157. N.R. Cashman and B. Caughey: Prion diseases-close to effective therapy? Nat Rev Drug Discov 3, 874-884 (2004).
158. C. Korth, B.C. May, F.E. Cohen and S.B. Prusiner: Acridine and phenothiazine derivatives as pharmacotherapeutics for prion disease. Proc Natl Acad Sci U S A 98, 9836-9841 (2001). (Pubitemid 32769390)
159. S.J. Collins, V. Lewis, M. Brazier, A.F. Hill, A. Fletcher and C.L. Masters: Quinacrine does not prolong survival in a murine Creutzfeldt-Jakob disease model. Ann Neurol 52, 503-506 (2002).
160. D.A. Kocisko, G.S. Baron, R. Rubenstein, J. Chen, S. Kuizon and B. Caughey: New inhibitors of scrapieassociated prion protein formation in a library of 2000 drugs and natural products. J Virol 77, 10288-10294 (2003). (Pubitemid 37129672)
161. Y. Cordeiro, L.M. Lima, M.P. Gomes, D. Foguel and J.L. Silva: Modulation of prion protein oligomerization, aggregation, and beta-sheet conversion by 4, 4'-dianilino- 1, 1'-binaphthyl-5, 5'-sulfonate (bis-ANS). J Biol Chem 279, 5346-5352 (2004).
162. R.H. Kimberlin and C.A. Walker: Suppression of scrapie infection in mice by heteropolyanion 23, dextran sulfate, and some other polyanions. Antimicrob Agents Chemother 30, 409-413 (1986). (Pubitemid 16017319)
163. C.F. Farquhar and A.G. Dickinson: Prolongation of scrapie incubation period by an injection of dextran sulphate 500 within the month before or after infection. J Gen Virol 67 (Pt 3), 463-473 (1986). (Pubitemid 16158586)
164. H. Diringer and B. Ehlers: Chemoprophylaxis of scrapie in mice. J Gen Virol 72 (Pt 2), 457-460 (1991).
165. A. Ladogana, P. Casaccia, L. Ingrosso, M. Cibati, M. Salvatore, Y.G. Xi, C. Masullo and M. Pocchiari: Sulphate polyanions prolong the incubation period of scrapieinfected hamsters. J Gen Virol 73 (Pt 3), 661-665 (1992).
166. N.V. Todd, J. Morrow, K. Doh-ura, S. Dealler, S. O'Hare, P. Farling, M. Duddy and N.G. Rainov: Cerebroventricular infusion of pentosan polysulphate in human variant Creutzfeldt-Jakob disease. J Infect 50, 394- 396 (2005). (Pubitemid 40692023)
167. K.T. Adjou, S. Simoneau, N. Sales, F. Lamoury, D. Dormont, D. Papy-Garcia, D. Barritault, J.P. Deslys and C.I. Lasmezas: A novel generation of heparan sulfate mimetics for the treatment of prion diseases. J Gen Virol 84, 2595-2603 (2003). (Pubitemid 37063149)
168. O. Schonberger, L. Horonchik, R. Gabizon, D. Papy-Garcia, D. Barritault and A. Taraboulos: Novel heparan mimetics potently inhibit the scrapie prion protein and its endocytosis. Biochem Biophys Res Commun 312, 473-479 (2003). (Pubitemid 37445196)
169. C. Larramendy-Gozalo, A. Barret, E. Daudigeos, E. Mathieu, L. Antonangeli, C. Riffet, E. Petit, D. Papy-Garcia, D. Barritault, P. Brown and J.P. Deslys: Comparison of CR36, a new heparan mimetic, and pentosan polysulfate in the treatment of prion diseases. J Gen Virol 88, 1062-1067 (2007). (Pubitemid 46359579)
170. S. Beaudoin, B. Vanderperre, C. Grenier, I. Tremblay, F. Leduc and X. Roucou: A large ribonucleoprotein particle induced by cytoplasmic PrP shares striking similarities with the chromatoid body, an RNA granule predicted to function in posttranscriptional gene regulation. Biochim Biophys Acta 1793, 335-345 (2009).