Effects of metal binding on solubility and resistance of physiological prions depend on tissues and glycotypes

Journal of Cellular Biochemistry

Volumn 114, Issue 12, 2013, Pages 2690-2698

  Kuczius, Thorsten ^a   Kelsch, Reinhard ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

COPPER; DETERGENT SOLUBILITY; METAL BINDING; PHYSIOLOGICAL PRION PROTEIN; ZINC

Indexed keywords

COPPER; PRION PROTEIN; TRITON X 100; ZINC;

ARTICLE; BRAIN; HUMAN; HUMAN CELL; HUMAN TISSUE; METAL BINDING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN STRUCTURE; THROMBOCYTE; TISSUE SPECIFICITY;

COPPER; DETERGENT SOLUBILITY; METAL BINDING; PHYSIOLOGICAL PRION PROTEIN; ZINC;

COPPER; GLYCOSYLATION; HUMANS; METALS; OCTOXYNOL; ORGAN SPECIFICITY; PRION DISEASES; PRIONS; PROTEIN ISOFORMS; PROTEOLYSIS; PRPSC PROTEINS; SOLUBILITY; ZINC;

EID: 84885596976     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24616     Document Type: Article

References (57)

1. Atarashi R, Moore RA, Sim VL, Hughson AG, Dorward DW, Onwubiko HA, Priola SA, Caughey B,. 2007. Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat Methods 4: 645-650.
2. Bednar RA, Gaul SL, Hamill TG, Egbertson MS, Shafer JA, Hartman GD, Gould RJ, Bednar B,. 1998. Identification of low molecular weight GP IIb/IIIa antagonists that bind preferentially to activated platelets. J Pharmacol Exp Ther 285: 1317-1326.
3. Beringue V, Mallinson G, Kaisar M, Tayebi M, Sattar Z, Jackson G, Anstee D, Collinge J, Hawke S,. 2003. Regional heterogeneity of cellular prion protein isoforms in the mouse brain. Brain 126: 2065-2073.
4. Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R, Fraser PE, Kruck T, von Bohlen A, Schulz-Schaeffer W, Giese A, Westaway D, Kretzschmar H,. 1997a. The cellular prion protein binds copper in vivo. Nature 390: 684-687.
5. Brown DR, Schulz-Schaeffer WJ, Schmidt B, Kretzschmar HA,. 1997b. Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp Neurol 146: 104-112.
6. Brown DR, Wong BS, Hafiz F, Clive C, Haswell SJ, Jones IM,. 1999. Normal prion protein has an activity like that of superoxide dismutase. Biochem J 344 (Pt 1): 1-5.
7. Brown LR, Harris DA,. 2003. Copper and zinc cause delivery of the prion protein from the plasma membrane to a subset of early endosomes and the Golgi. J Neurochem 87: 353-363.
8. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, Suttie A, McCardle L, Chree A, Hope J, Birkett C, Cousens S, Fraser H, Bostock CJ,. 1997. Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature 389: 498-501.
9. Cervenakova L, Yakovleva O, McKenzie C, Kolchinsky S, McShane L, Drohan WN, Brown P,. 2003. Similar levels of infectivity in the blood of mice infected with human-derived vCJD and GSS strains of transmissible spongiform encephalopathy. Transfusion 43: 1687-1694.
10. Cordeiro Y, Kraineva J, Gomes MP, Lopes MH, Martins VR, Lima LM, Foguel D, Winter R, Silva JL,. 2005. The amino-terminal PrP domain is crucial to modulate prion misfolding and aggregation. Biophys J 89: 2667-2676.
11. Danks DM,. 1989. Disorders of copper transport. In:, Srciber CR, Beaudet AL, Sly WS, Valley D, editors. The metabolic basis of inherited disease, 6th edition. New York, USA: McGraw-Hill, Inc. pp 1411-1431.
12. Demart S, Fournier JG, Creminon C, Frobert Y, Lamoury F, Marce D, Lasmezas C, Dormont D, Grassi J, Deslys JP,. 1999. New insight into abnormal prion protein using monoclonal antibodies. Biochem Biophys Res Commun 265: 652-657.
13. ++ in rat brain regions. Can J Biochem 51: 87-92.
14. Dubernard V, Arbeille BB, Lemesle MB, Legrand C,. 1997. Evidence for an alpha-granular pool of the cytoskeletal protein alpha-actinin in human platelets that redistributes with the adhesive glycoprotein thrombospondin-1 during the exocytotic process. Arterioscler Thromb Vasc Biol 17: 2293-2305.
15. Gaggelli E, Bernardi F, Molteni E, Pogni R, Valensin D, Valensin G, Remelli M, Luczkowski M, Kozlowski H,. 2005. Interaction of the human prion PrP(106-126) sequence with copper(II), manganese(II), and zinc(II): NMR and EPR studies. J Am Chem Soc 127: 996-1006.
16. 1H NMR solution structure of the palladium2+ bound single octarepeat. Dalton Trans 21: 509-518.
17. Gasset M, Baldwin MA, Fletterick RJ, Prusiner SB,. 1993. Perturbation of the secondary structure of the scrapie prion protein under conditions that alter infectivity. Proc Natl Acad Sci USA 90: 1-5.
18. Goldfarb LG, Brown P, McCombie WR, Goldgaber D, Swergold GD, Wills PR, Cervenakova L, Baron H, Gibbs CJ Jr., Gajdusek DC,. 1991. Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc Natl Acad Sci USA 88: 10926-10930.
19. Hopt A, Korte S, Fink H, Panne U, Niessner R, Jahn R, Kretzsschmar H, Herms J,. 2003. Methods for studying synaptosomal copper release. J Neurosci Methods 128: 159-172.
20. Hornshaw MP, McDermott JR, Candy JM,. 1995. Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem Biophys Res Commun 207: 621-629.
21. Jobling MF, Huang X, Stewart LR, Barnham KJ, Curtain C, Volitakis I, Perugini M, White AR, Cherny RA, Masters CL, Barrow CJ, Collins SJ, Bush AI, Cappai R,. 2001. Copper and zinc binding modulates the aggregation and neurotoxic properties of the prion peptide PrP106-126. Biochemistry 40: 8073-8084.
22. Kanaani J, Prusiner SB, Diacovo J, Baekkeskov S, Legname G,. 2005. Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J Neurochem 95: 1373-1386.
23. Kuczius T, Buschmann A, Zhang W, Karch H, Becker K, Peters G, Groschup MH,. 2004. Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding. Biol Chem 385: 739-747.
24. Kuczius T, Karch H, Groschup MH,. 2009. Differential solubility of prions is associated in manifold phenotypes. Mol Cell Neurosci 42: 226-233.
25. Kuczius T, Kleinert J, Karch H, Sibrowski W, Kelsch R,. 2011a. Cellular prion proteins in human platelets show a phenotype different to those in brain tissues. J Cell Biochem 112: 954-962.
26. Kuczius T, Koch R, Keyvani K, Karch H, Grassi J, Groschup MH,. 2007. Regional and phenotype heterogeneity of cellular prion proteins in the human brain. Eur J Neurosci 25: 2649-2655.
27. Kuczius T, Wohlers J, Karch H, Groschup MH,. 2011b. Subtyping of human cellular prion proteins and their differential solubility. Exp Neurol 227: 188-194.
28. Laplanche JL, Hachimi KH, Durieux I, Thuillet P, Defebvre L, Delasnerie-Lauprêtre N, Peoc'h K, Foncin JF, Destée A,. 1999. Prominent psychiatric features and early onset in an inherited prion disease with a new insertional mutation in the prion protein gene. Brain 122: 2375-2386.
29. Lee SH, Huang JW, Hung KY, Leu LJ, Kan YT, Yang CS, Chung Wu D, Huang CL, Chen PY, Chen JS, Chen WY,. 2000. Trace Metals' abnormalities in hemodialysis patients: Relationship with medications. Artif Organs 24: 841-844.
30. Leliveld SR, Dame RT, Wuite GJ, Stitz L, Korth C,. 2006. The expanded octarepeat domain selectively binds prions and disrupts homomeric prion protein interactions. J Biol Chem 281: 3268-3275.
31. Leliveld SR, Stitz L, Korth C,. 2008. Expansion of the octarepeat domain alters the misfolding pathway but not the folding pathway of the prion protein. Biochemistry 47: 6267-6278.
32. Llewelyn CA, Hewitt PE, Knight RS, Amar K, Cousens S, Mackenzie J, Will RG,. 2004. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 363: 417-421.
33. Milne DB, Johnson PE,. 1993. Assessment of copper status: Effect of age and gender on reference ranges in healthy adults. Clin Chem 39: 883-887.
34. Morel N, Simon S, Frobert Y, Volland H, Mourton-Gilles C, Negro A, Sorgato MC, Créminon C, Grassi J,. 2004. Selective and efficient immunoprecipitation of the disease-associated form of the prion protein can be mediated by nonspecific interactions between monoclonal antibodies and scrapie-associated fibrils. J Biol Chem 279: 30143-30149.
35. Mouillet-Richard S, Ermonval M, Chebassier C, Laplanche JL, Lehmann S, Launay JM, Kellermann O,. 2000. Signal transduction through prion protein. Science 289: 1925-1928.
36. Ono S, Cherian MG,. 1999. Regional distribution of metallothionein, zinc and copper in the brain of different strains of rats. Biol Trace Elem Res 69: 151-159.
37. Owen F, Poulter M, Collinge J, Leach M, Shah T, Lofthouse R, Chen YF, Crow TJ, Harding AE, Hardy J,. 1991. Insertions in the prion protein gene in atypical dementias. Exp Neurol 112: 240-242.
38. Owen F, Poulter M, Lofthouse R, Collinge J, Crow TJ, Risby D, Baker HF, Ridley RM, Hsiao K, Prusiner SB,. 1989. Insertion in prion protein gene in familial Creutzfeldt-Jakob disease. Lancet 1: 51-52.
39. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Melhorn I, Huang Z, Fletterick RJ, Cohen FE, Prusiner SB,. 1993. Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 90: 10962-10966.
40. Pauly PC, Harris DA,. 1998. Copper stimulates endocytosis of the prion protein. J Biol Chem 273: 33107-33110.
41. Peden AH, Head MW, Ritchie DL, Bell JE, Ironside JW,. 2004. Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 364: 527-529.
42. Pushie MJ, Rauk A, Jirik FR, Vogel HJ,. 2009. Can copper binding to the prion protein generate a misfolded form of the protein ? Biometals 22: 159-175.
43. Pushie MJ, Ross AR, Vogel HJ,. 2007. Mass spectrometric determination of the coordination geometry of potential copper(II) surrogates for the mammalian prion protein octarepeat region. Anal Chem 79: 5659-5667.
44. Qin K, Yang DS, Yang Y, Chishti MA, Meng LJ, Kretzschmar HA, Yip CM, Fraser PE, Westaway D,. 2000. Copper(II)-induced conformational changes and protease resistance in recombinant and cellular PrP. Effect of protein age and deamidation. J Biol Chem 275: 19121-19131.
45. Quaglio E, Chiesa R, Harris DA,. 2001. Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J Biol Chem 276: 11432-11438.
46. Renner C, Fiori S, Fiorino F, Landgraf D, Deluca D, Mentler M, Granter K, Parak FG, Kretzschmar H, Moroder L,. 2004. Micellar environments induce structuring of the N-terminal tail of the prion protein. Biopolymers 73: 421-433.
47. Schmitt-Ulms G, Legname G, Baldwin MA, Ball HL, Bradon N, Bosque PJ, Crossin KL, Edelman GM, DeArmond SJ, Cohen FE, Prusiner SB,. 2001. Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J Mol Biol 314: 1209-1225.
48. Soto C, Saborio GP, Anderes L,. 2002. Cyclic amplification of protein misfolding: Application to prion-related disorders and beyond. Trends Neurosci 25: 390-394.
49. Stöckel J, Safar J, Wallace AC, Cohen FE, Prusiner SB,. 1998. Prion protein selectively binds copper(II) ions. Biochemistry 37: 7185-7193.
50. Van Gool WA, Hensels GW, Hoogerwaard EM, Wiezer JH, Wesseling P, Bolhuis PA,. 1995. Hypokinesia and presenile dementia in a Dutch family with a novel insertion in the prion protein gene. Brain 118: 1565-1571.
51. Viles JH, Cohen FE, Prusiner SB, Goodin DB, Wright PE, Dyson HJ,. 1999. Copper binding to the prion protein: Structural implications of four identical cooperative binding sites. Proc Natl Acad Sci USA 96: 2042-2047.
52. Wadsworth JDF, Hill AF, Joiner S, Jackson GS, Clarke AR, Collinge J,. 1999. Strain-specific prion-protein conformation determined by metal ions. Nat Cell Biol 1: 55-59.
53. 2+ coordination modes. J Am Chem Soc 129: 15440-15441.
54. Watanabe Y, Hiraoka W, Igarashi M, Ito K, Shimoyama Y, Horiuchi M, Yamamori T, Yasui H, Kuwabara M, Inagaki F, Inanami O,. 2010. A novel copper(II) coordination at His186 in full-length murine prion protein. Biochem Biophys Res Commun 394: 522-528.
55. Wlostowski T,. 1992. Postnatal changes in subcellular distribution of copper, zinc and metallothionein in the liver of bank vole (Clethrionomys glareolus): A possible involvement of metallothionein and copper in cell proliferation. Comp Biochem Physiol C 103: 35-41.
56. Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, Lopez Garcia F, Billeter M, Calzolai L, Wider G, Wuthrich K,. 2000. NMR solution structure of the human prion protein. Proc Natl Acad Sci USA 97: 145-150.
57. Zhu F, Davies P, Thompsett AR, Kelly SM, Tranter GE, Hecht L, Isaacs NW, Brown DR, Barron LD,. 2008. Raman optical activity and circular dichroism reveal dramatic differences in the influence of divalent copper and manganese ions on prion protein folding. Biochemistry 47: 2510-2517.