Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding

References

Aronoff-Spencer, E., Burns, C.S., Avdievich, N.I., Gerfen, G.J., Peisach, J., Antholine, W.E., Ball, H.L., Cohen, F.E., Prusiner, S.B. and Millhauser, G.L. (2000). Identification of the Cu²⁺ binding sites in the N-terminal domain of the prion protein by EPR and CD spectroscopy. Biochemistry39, 13760–13771.10.1021/bi001472tSearch in Google Scholar

Bajorath, J., Hinrichs, W., and Saenger, W. (1988). The enzymatic activity of proteinase K is controlled by calcium. Eur. J. Biochem.176, 441–447.10.1111/j.1432-1033.1988.tb14301.xSearch in Google Scholar

Belosi, B., Gaggelli, E., Guerrini, R., Kozlowski, H., Luczkowski, M., Mancini, F.M., Remelli, M., Valensin, D. and Valensin, G. (2004). Copper binding to the neurotoxic peptide PrP106–126: thermodynamic and structural studies. Chem Bio Chem5, 349–359.10.1002/cbic.200300786Search in Google Scholar

Betzel, C., Pal, G.P., and Saenger, W. (1988). Three-dimensional structure of proteinase K at 0.15-nm resolution. Eur. J. Biochem.178, 155–171.10.1111/j.1432-1033.1988.tb14440.xSearch in Google Scholar

Brown, D.R., Qin, K., Herms, J.W., Madlung, A., Manson, J., Strome, R., Fraser, P.E., Kruck, T., von Bohlen, A., Schulz-Schaffer, W. et al. (1997a). The cellular prion protein binds copper in vivo. Nature390, 684–687.10.1038/37783Search in Google Scholar

Brown, D.R., Schulz-Schaeffer, W.J., Schmidt, B., and Kretzschmar, H.A. (1997b). Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp. Neurol.146, 104–112.10.1006/exnr.1997.6505Search in Google Scholar

Brown, D.R., Wong, B.S., Hafiz, F., Clive, C., Haswell, S.J., and Jones, I.M. (1999). Normal prion protein has an activity like that of superoxide dismutase. Biochem. J.344, 1–5.10.1042/bj3440001Search in Google Scholar

Buschmann, A., Kuczius, T., Bodemer, W., and Groschup, M.H. (1998). Cellular prion proteins of mammalian species display an intrinsic partial proteinase K resistance. Biochem. Biophys. Res. Commun.253, 693–702.10.1006/bbrc.1998.9838Search in Google Scholar

Cardone, F., Liu, Q.G., Petraroli, R., Ladogana, A., D’Alessandro, M., Arpino, C., Di Bari, M., Macchi, G., and Pocchiari, M. (1999). Prion protein glycotype analysis in familial and sporadic Creutzfeldt-Jakob disease patients. Brain Res. Bull.49, 429–433.10.1016/S0361-9230(99)00077-5Search in Google Scholar

Castilla, J., Gutierrez-Adan, A., Brun, A., Pintado, B., Parra, B., Ramirez, M.A., Salguero, F.J., Diaz San Segundo, F., Rabano, A., Cano, M.J. and Torres, J.M. (2004). Different behavior toward bovine spongiform encephalopathy infection of bovine prion protein transgenic mice with one extra repeat octapeptide insert mutation. J. Neurosci.24, 2156–64.10.1523/JNEUROSCI.3811-03.2004Search in Google Scholar PubMed PubMed Central

Collinge, J., Sidle, K. C. L., Meads, J., Ironside, J., and Hill, A.F. (1996). Molecular analysis of prion strain variation and the aetiology of ‘new variant’ CJD. Nature383, 685–690.10.1038/383685a0Search in Google Scholar

Danks, D.M. (1989). Disorders of copper transport. In: The Metabolic Basis of Inherited Disease, 6^th Edition, C.R. Srciber, A.L. Beaudet, W.S. Sly and D. Valley, eds. (New York, USA: McGraw-Hill, Inc.), pp. 1411–1431.Search in Google Scholar

Deleault, N.R., Lucassen, R.W., and Supattapone, S. (2003). RNA molecules stimulate prion protein conversion. Nature425, 717–720.10.1038/nature01979Search in Google Scholar

Fischer, M., Rulicke, T., Raeber, A., Sailer, A., Moser, M., Oesch, B., Brandner, S., Aguzzi, A. and Weissmann, C. (1996). Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J.15, 1255–1264.10.1002/j.1460-2075.1996.tb00467.xSearch in Google Scholar

Flechsig, E., Shmerling, D., Hegyi, I., Raeber, A.J., Fischer, M., Cozzio, A., von Mering, C., Aguzzi, A. and Weissmann, C. (2000). Prion protein devoid of the octapeptide repeat region restores susceptibility to scrapie in PrP knockout mice. Neuron27, 399–408.10.1016/S0896-6273(00)00046-5Search in Google Scholar

Garnett, A.P. and Viles, J.H. (2003). Copper binding to the octarepeats of the prion protein. Affinity, specificity, folding, and cooperativity: insights from circular dichroism. J. Biol. Chem.278, 6795–6802.10.1074/jbc.M209280200Search in Google Scholar PubMed

Goldfarb, L.G., Brown, P., McCombie, W.R., Goldgaber, D., Swergold, G.D., Wills, P.R., Cervenakova, L., Baron, H., Gibbs Jr., C.J., and Gajdusek, D.C. (1991). Transmissible familial Creutzfeldt-Jakob disease associated with five, seven, and eight extra octapeptide coding repeats in the PRNP gene. Proc. Natl. Acad. Sci. USA88, 10926–10930.10.1073/pnas.88.23.10926Search in Google Scholar PubMed PubMed Central

Groschup, M.H., Kuczius, T., Junghans, F., Sweeney, T., Bodemer, W., and Buschmann, A. (2000). Characterization of BSE and scrapie strains/isolates. Arch. Virol. Suppl.16, 217–226.10.1007/978-3-7091-6308-5_21Search in Google Scholar PubMed

Harmeyer, S., Pfaff, E., and Groschup, M.H. (1998). Synthetic peptide vaccines yield monoclonal antibodies to cellular and pathological prion proteins of ruminants. J. Gen. Virol.79, 937–945.10.1099/0022-1317-79-4-937Search in Google Scholar PubMed

Hijazi, N., Shaked, Y., Rosenmann, H., Ben-Hur, T. and Gabizon, R. (2003). Copper binding to PrPC may inhibit prion disease propagation. Brain Res.993, 192–200.10.1016/j.brainres.2003.09.014Search in Google Scholar PubMed

Hornshaw, M.P., McDermott, J.R., and Candy, J.M. (1995). Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem. Biophys. Res. Commun.207, 621–629.10.1006/bbrc.1995.1233Search in Google Scholar PubMed

Jobling, M.F., Huang, X., Stewart, L.R., Barnham, K.J., Curtain, C., Volitakis, I., Perugini, M., White, A.R., Cherny, R.A., Masters, C.L. et al. (2001). Copper and zinc binding modulatesthe aggregation and neurotoxic properties of the prion peptide PrP106–126. Biochemistry40, 8073–8084.10.1021/bi0029088Search in Google Scholar

Kourie, J.I., Kenna, B.L., Tew, D., Jobling, M.F., Curtain, C.C., Masters, C.L., Barnham, K.J. and Cappai, R. (2003). Copper modulation of ion channels of PrP[106–126] mutant prion peptide fragments. J. Membr. Biol.193, 35–45.10.1007/s00232-002-2005-5Search in Google Scholar

Kuczius, T., Haist, I., and Groschup, M.H. (1998). Molecular Analysis of bovine spongiform encephalopathy and scrapie strain variation. J. Inf. Dis.178, 693–699.10.1086/515337Search in Google Scholar

McKenzie, D., Bartz, J., Mirwald, J., Olander, D., Marsh, R., and Aiken, J. (1998). Reversibility of scrapie inactivation isenhanced by copper. J. Biol. Chem.273, 25545–25547.10.1074/jbc.273.40.25545Search in Google Scholar

Miura, T., Hori-i, A., and Takeuchi, H. (1996). Metal-dependent a-helix formation promoted by the glycine-rich octapeptide region of prion protein. FEBS Lett.396, 248–252.10.1016/0014-5793(96)01104-0Search in Google Scholar

Miura, T., Hori-i, A., Mototani, H., and Takeuchi, H. (1999). Raman spectroscopic study on the copper(II) binding mode of prion octapeptide and its pH dependence. Biochemistry38, 11560–11569.10.1021/bi9909389Search in Google Scholar

Notari, S., Capellari, S., Giese, A., Westner, I., Baruzzi, A., Ghetti, B., Gambetti, P., Kretzschmar, H.A., and Parchi, P. (2004). Effects of different experimental conditions on the PrPSc core generated by protease digestion: implications for strain typing and molecular classification of CJD. J. Biol. Chem.279, 16797–16804.10.1074/jbc.M313220200Search in Google Scholar

Pan, K.M., Baldwin, M., Nguyen, J., Gasset, M., Serban, A., Groth, D., Melhorn, I., Huang, Z., Fletterick, R.J., Cohen, F.E., and Prusiner, S.B. (1993). Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins.Proc. Natl. Acad. Sci. USA90, 10962–10966.10.1073/pnas.90.23.10962Search in Google Scholar

Parchi, P., Capellari S., Chen S.G., Petersen, R.B., Gambetti, P., Kopp, N., Brown, P., Kitamoto, T., Tateishi, J., Giese, A., and Kretzschmar, H. (1997). Typing prion isoforms. Nature386, 232–234.10.1038/386232a0Search in Google Scholar

Pattison, I.H., Jones, K.M., and Jebbett, J.N. (1971). Detection of the scrapie agent in tissues of normal mice with special reference to the possibility of accidental laboratory contamination. Res. Vet. Sci.12, 30–39.10.1016/S0034-5288(18)34235-8Search in Google Scholar

Pauly, P.C., and Harris, D.A. (1998). Copper stimulates endocytosis of the prion protein. J. Biol. Chem.273, 33107–33110.10.1074/jbc.273.50.33107Search in Google Scholar PubMed

Qin, K., Yang, D.S., Yang, Y., Chishti, M.A., Meng, L.J., Kretzschmar, H.A., Yip, C.M., Fraser, P.E., and 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, 19121–19131.10.1074/jbc.275.25.19121Search in Google Scholar PubMed

Quaglio, E., Chiesa, R., and Harris D.A. (2001). Copper converts the cellular prion protein into a protease-resistant species that is distinct from the scrapie isoform. J. Biol. Chem.276, 11432–11438.10.1074/jbc.M009666200Search in Google Scholar PubMed

Renner, C., Fiori, S., Fiorino, F., Landgraf, D., Deluca, D., Mentler, M., Granter, K., Parak, F.G., Kretzschmar, H., and Moroder, L. (2004). Micellar environments induce structuring of the N-terminal tail of the prion protein. Biopolymers73, 421–433.10.1002/bip.20015Search in Google Scholar PubMed

Stöckel, J., Safar, J., Wallace A.C., Cohen, F.E., and Prusiner, S.B. (1998). Prion protein selectively binds copper(II) ions. Biochemistry37, 7185–7193.10.1021/bi972827kSearch in Google Scholar PubMed

Sweeney, T., Kuczius, T., McElroy, M., Gomez Parada, M., Groschup, M.H., and Parada, M.G. (2000). Molecular analysis of Irish sheep scrapie cases. J. Gen. Virol.81, 1621–1627.10.1099/0022-1317-81-6-1621Search in Google Scholar PubMed

Viles, J.H., Cohen, F.E., Prusiner, S.B., Goodin, D.B., Wright, P.E., and Dyson, H.J. (1999). Copper binding to the prion protein: structural implications of four identical cooperative binding sites. Proc. Natl. Acad. Sci. USA96, 2042–2047.10.1073/pnas.96.5.2042Search in Google Scholar PubMed PubMed Central

Wadsworth, J.D.F., Hill, A.F., Joiner, S., Jackson, G.S., Clarke, A.R., and Collinge, J. (1999). Strain-specific prion-protein conformation determined by metal ions. Nat. Cell Biol.1, 55–59.10.1038/9030Search in Google Scholar PubMed

Whittal, R.M., Ball, H.L., Cohen, F.E., Burlingame, A.L., Prusiner, S.B., and Baldwin, M.A. (2000). Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry. Protein Sci.9, 332–343.10.1110/ps.9.2.332Search in Google Scholar PubMed PubMed Central

Winklhofer, K.F., Heske, J., Heller, U., Reintjes, A., Muranyi, W., Moarefi, I., and Tatzelt, J. (2003). Determinants of the in vivo folding of the prion protein. A bipartite function of helix 1 in folding and aggregation. J. Biol. Chem.278, 14961–14970.10.1074/jbc.M209942200Search in Google Scholar PubMed

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, 35–41.10.1016/0742-8413(92)90009-VSearch in Google Scholar

Zou, W.Q., and Cashman, N.R. (2002). Acidic pH and detergents enhance in vitro conversion of human brain PrPC to a PrPSc-like form. J. Biol. Chem.277, 43942–43947.10.1074/jbc.M203611200Search in Google Scholar PubMed