Copper binding to octarepeat peptides of the prion protein monitored by mass spectrometry

Protein Science

Volumn 9, Issue 2, 2000, Pages 332-343

  Whittal, Randy M ^a   Ball, Haydn L ^b   Cohen, Fred E ^a,b,c   Burlingame, Alma L ^a,b   Prusiner, Stanley B ^b   Baldwin, Michael A ^a,b  

^a Dept of Pharmaceutical Chemistry ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Circular dichroism; Copper binding; Dissociation constants; Electrospray ionization mass spectrometry; Prion protein; PrP; PrP peptides

Indexed keywords

COPPER ION; PRION PROTEIN; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; DISSOCIATION CONSTANT; MASS SPECTROMETRY; PH; PRIORITY JOURNAL; PROTEIN BINDING;

EID: 0033996803     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.9.2.332     Document Type: Article

References (55)

1. Anderson RGW, Kamen BA, Rothberg KG, Lacey SW. 1992. Potocylosis: Sequestration and transport of small molecules by caveolae. Science 255:410-411.
2. Atwood CS, Moir RD, Huang X. Scarpa RC. Bacarra NME, Romano DM, Hartshorn MA, Tanzi RE, Bush AI. 1998. Dramatic aggregation of Alzheimer Aβ by Cu(II) is induced by conditions representing physiological acidosis. J Biol Chem 273:12817-12826.
3. Brown DR, Qin K, Herms JW, Madlung A, Manson J, Strome R, Fraser PE, Kruck T, von Bohlen A, Schulz-Schaeffer W, et al. 1997a. The cellular prion protein binds copper in vivo. Nature 390:684-687.
4. 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.
5. Büeler H, Aguzzi A, Sailer A, Greiner R-A, Autenried P, Aguet M, Weissmann C. 1993. Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
6. Collinge J, Whittington MA, Sidle KC, Smith CJ, Palmer MS, Clarke AR, Jefferys JGR. 1994. Prion protein is necessary for normal synaptic function. Nature 370:295-297.
7. Cudkowicz ME, Brown RHJ. 1996. An update on superoxide dismutase 1 in familial amyotrophic lateral sclerosis. J Neurol Sci 139:10-15.
8. Donne DG, Viles JH, Groth D, Mehlhorn I, James TL, Cohen FE, Prusiner SB, Wright PE, Dyson HJ. 1997. Structure of the recombinant full-length hamster prion protein PrP(29-231): The N terminus is highly flexible. Proc Natl Acad Sci USA 94:13452-13457.
9. Freskgard PO, Martensson LG, Jonasson P, Jonsson BH, Carlsson U. 1994. Assignment of the contribution of the tryptophan residues to the circular dichroism spectrum of human carbonic anhydrase II. Biochemistry 33: 14281-14288.
10. Gabriel J-M, Oesch B, Kretzschmar H, Scott M, Prusiner SB. 1992. Molecular cloning of a candidate chicken prion protein. Proc Natl Acad Sci USA 89:9097-9101.
11. Harris DA, Falls DL, Johnson FA, Fischbach GD. 1991. A prion-like protein from chicken brain copurifies with an acetylcholine receptor-inducing activity. Proc Natl Acatl Sci USA 88:7664-7668.
12. Herms JW, Kretzschmar HA, Titz, S. Keller BU. 1995. Patch-clamp analysis of synaptic transmission to cerebellar purkinje cells of prion protein knockout mice. Eur J Neurosci 7:2508-2512.
13. Hornshaw MP, McDermott, JR, Candy JM. 1995a. Copper binding to the N-terminal tandem repeat regions of mammalian and avian prion protein. Biochem Biophys Res Commun 207:621-629.
14. Hornshaw MP, McDermott JR, Candy JM, Lakey JH. 1995b. Copper binding to the N-terminal tandem repeat region of mammalian and avian prion protein: Structural studies using synthetic peptides. Biochem Biophys Res Commun 214:993-999.
15. Hughes MN. 1981. The inorganic chemistry of biological processes, 2nd ed. Chichester UK: J. Wiley.
16. James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, Donne DG, Kaneko K, Groth D, Mehlhorn I. Prusiner SB, Cohen FE. 1997. Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc Natl Acad Sci USA 94:10086-10091.
17. Kebarle P, Tang L. 1993. From ions in solution to ions in the gas phase. Anal Chem 65:972A-984A.
18. Kimberlin RH, Millson GC, Bountiff L, Collis, SC. 1974. A comparison of the biochemical changes induced in mouse brain by cuprizone toxicity and by scrapie infection. J Comp Path 84:263-270.
19. Last AM, Robinson CV. 1999. Protein folding and interactions revealed by mass spectrometry. Curr Opin Chem Biol 3:564-570.
20. Lei QP, Cui X, Kurtz DM Jr, Amster IJ, Chernushevich IV, Standing KG. 1998. Electrospray mass spectrometry of non-heme iron-containing proteins. Anal Chem 70:1838-1846.
21. Lipp HP, Stagliar-Bozicevic M, Fischer M, Wolfer DP. 1998. A 2-year longitudinal study of swimming navigation in mice devoid of the prion protein: No evidence for neurological anomalies or spatial learning impairments. Behav Brain Res 95:47-54.
22. Lledo P-M, Tremblay P, DeArmond SJ, Prusiner SB, Nicoll RA. 1996. Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc Natl Acad Sci USA 93:2403-2407.
23. Loo JA. 1997. Studying noncovalent protein complexes by electrospray ionization mass spectrometry. Mass Spectrom Rev 16:1-23.
24. Marcotte EM, Eisenberg D. 1999. Chicken prion tandem repeats form a stable, protease-resistant domain. Biochemistry 38:667-676.
25. McKenzie D, Bartz J, Mirwald J, Olander D, Marsh R, Aiken J. 1998. Reversibility of scrapie inactivation is enhanced by copper. J Biol Chem 273: 25545-25547.
26. Mineo C, Anderson RGW. 1996. A vacuolar-type proton ATPase mediates acidification of plasmalemmal vesicles during potocytosis. Exp Cell Res 224: 237-242.
27. Miura T, Hori-i A, Mototani H, Takeuchi H. 1999. Raman spectroscopic study on the copper(II) binding mode of prion octapeptide and its pH dependence. Biochemistry 38:11560-11569.
28. Miura T, Hori-i A, Takeuchi H. 1996. Metal-dependent α-helix formation promoted by the glycine-rich octapeptide region of prion protein. FEBS Lett 396:248-252.
29. Multhaup G, Schlicksupp A, Hesse L, Beher D, Ruppert T, Masters CL, Beyreuther K. 1996. The amyloid precursor protein of Alzheimer's disease in the reduction of copper(II) to copper(I). Science 271:1406-1409.
30. Muramoto T, Scott M, Cohen FE, Prusiner SB. 1996. Recombinant scrapie-like prion protein of 106 amino acids is soluble. Proc Natl Acad Sci USA 95:15457-15462.
31. Nishida N, Katamine S, Shigematsu K, Nakatani A, Sakamoto N, Hasegawa S, Nakaoke R, Atarashi R, Kataoka Y, Miyamoto T. 1997. Prion protein is necessary for latent learning and long-term memory retention. Cell Mol Neurobiol 17:537-545.
32. Oesch B, Westaway D, Wälchli M, McKinley MP, Kent SBH, Aebersold R, Barry RA, Tempst P, Teplow DB, Hood LE, et al. 1985. A cellular gene encodes scrapie PrP 27-30 protein. Cell 40:735-746.
33. 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.
34. Pan K-M, Stahl N, Prusiner SB. 1992. Purification and properties of the cellular prion protein from Syrian hamster brain. Protein Sci 1:1343-1352.
35. Parge HE, Hallewell RA, Tainer JA. 1992 Atomic structures of wild-type and thermostable mutant recomhinant human Cu,Zn superoxide dismutase. Proc Acad Natl Sci USA 89:6109-6113.
36. Pattison IH, Jebbett JN. 1971. Clinical and histological observations on cuprizone toxicity and scrapie in mice. Res Vet Sci 12:378-380.
37. Pauly PC, Harris DA. 1998. Copper stimulates endocytosis of the prion protein. J Biol Chem 273:33107-33110.
38. Potier N, Donald LJ, Chernushevich I, Ayed A, Ens W, Arrowsmith CH, Standing KG, Duckworth HW. 1998. Study of a noncovalent trp repressor: DNA operator complex by electrospray ionization time-of-flight mass spectrometry. Protein Sci 7:1388-1395.
39. Prusiner SB, Groth D, Serban A, Koehler R, Foster D, Torchia M, Burton D, Yang S-L, DeArmond SJ. 1993. Ablation of the prion protein (PrP) gene in mice prevents scrapie and facilitates production of anti-PrP antibodies. Proc Natl Acad Sci USA 90:10608-10612.
40. Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, Wüthrich K. 1996. NMR structure of the mouse prion protein domain PrP( 121-231 ). Nature 382:180-182.
41. Riek R, Hornemann S, Wider G, Glockshuber R, Wüthrich K. 1997. NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett 413:282-288.
42. Shyng S-L, Huber MT, Harris DA. 1993. A prion protein cycles between the cell surface and an endocytic compartment in cultured neuroblastoma cells. J Biol Chem 21:15922-15928.
43. Smith CJ, Drake AF, Banfield BA, Bloomberg GB, Palmer MS, Clarke AR, Collinge J. 1997. Conformational properties of the prion octa-repeat and Hydrophobic sequences. FEBS Lett 405:378-384.
44. Stöckel J. Safar J, Wallace AC, Cohen FE, Prusiner SB. 1998. Prion protein selectively binds copper (II) ions. Biochemistry 37:7185-7193.
45. Sulkowski E. 1985. Purification of proteins by IMAC. Trends Biotechnol 3:1-7.
46. Sulkowski E. 1989. The saga of IMAC and MIT. Bioessays 10:170-175.
47. Supattapone S, Bosque P, Muramoto T, Wille H, Aagaard C, Peretz D, Nguyen H-OB, Heinrich C, Torchia M, Safar J, et al. 1999. Prion protein of 106 residues creates an artificial transmission barrier for prion replication in transgenic mice. Cell 96:869-878.
48. Taraboulos A, Raeber AJ, Borchelt DR, Serban D, Prusiner SB. 1992. Synthesis and trafficking of prion proteins in cultured cells. Mol Biol Cell 3:851-863.
49. Taraboulos A, Scott M, Semenov A, Avrahami D, Laszlo L, Prusiner SB. 1995. Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibits formation of the scrapie isoform. J Cell Biol 129:121-132.
50. Tobler I, Gaus SE, Deboer T, Achermann P, Fischer M, Rülicke T, Moser M, Oesch B, McBride PA, Manson JC. 1996. Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380:639-642.
51. Veenstra TD, Johnson KL, Tomlinson AJ, Craig TA, Kumar R, Naylor S. 1998. Zinc-induced conformational changes in the DNA-binding domain of the vitamin D receptor determined by electrospray ionization mass spectrometry. J Am Soc Mass Spectrom 9:8-14.
52. Vey M, Pilkuhn S, Wille H, Nixon R, DeArmond SJ, Smart EJ, Anderson RG, Taraboulos A, Prusiner SB. 1996. Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains. Proc Natl Acad Sci USA 93:14945-14949.
53. 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.
54. Volz J, Bosch FU, Wunderlin M, Schuhmacher M, Melchers K, Bensch K, Steinhilber W, Schafer KP, Toth G, Penke B, Przybylski M. 1998. Molecular characterization of metal-binding polypeptide domains by electrospray ionization mass spectrometry and metal chelate affinity chromatography. J Chromatogr A 800:29-37.
55. Yu XL, Wojciechowski M, Fenselau C. 1993. Assessment of metals in reconstituted metallothioneins by electrospray mass spectrometry. Anal Chem 65:1355-1359.