Stability and conformational properties of doppel, a prion-like protein, and its single-disulphide mutant

Biochemical Journal

Volumn 373, Issue 2, 2003, Pages 485-494

  Whyte, Sheena M ^a   Sylvester, Ian D ^b   Martin, Stephen R ^a   Gill, Andrew C ^b   Wopfner, Franziska ^c   Schätzl, Hermann M ^c   Dodson, Guy G ^a   Bayley, Peter M ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c Gene Center   (Germany)

Author keywords

Amyloid protein; Prion protein; Protein unfolding; Thermodynamic stability; Transmissible spongiform encephalopathy; Urea denaturation

Indexed keywords

DISEASES; SPECTROSCOPIC ANALYSIS; UREA;

DOPPEL;

PROTEINS;

MUTANT PROTEIN; PRION PROTEIN; PROTEIN; PROTEIN DOPPEL; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; DISULFIDE BOND; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; ULTRAVIOLET SPECTROSCOPY;

ANIMALS; CIRCULAR DICHROISM; DISULFIDES; HEAT; MASS SPECTROMETRY; MICE; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEPTIDE FRAGMENTS; PRIONS; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SPECTROPHOTOMETRY, ULTRAVIOLET; THERMODYNAMICS; TRANSFORMATION, GENETIC; UREA;

MURINAE;

EID: 0042346286     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021911     Document Type: Article

References (60)

1. Brown, D. R., Qin, K., Herms, J. W., Madlung, A., Manson, J., Strome, R., Fraser, P. E., Kruck, T., von Bohlen, A., Schulz-Schaeffer, W. et al. (1997) The cellular priori protein binds copper in vivo. Nature (London) 390, 684-687
2. Brown, D. R. and Mohn, C. M. (1999) Astrocytic glutamate uptake and prion protein expression. Glia 25, 282-292
3. Mouillet-Richard, S., Ermonval, M., Chebassier, C., Laplanche, J. L., Lehmann, S., Launay, J. M. and Kellermann, O. (2000) Signal transduction through prion protein. Science (Washington, D.C) 289, 1925-1928
4. Prusiner, S. B., Scott, M. R., DeArmond, S. J. and Cohen, F. E. (1998) Prion protein biology. Cell (Cambridge, Mass.) 93, 337-348
5. Weissmann, C. (1996) The Ninth Datta Lecture. Molecular biology of transmissible spongiform encephalopathies. FEBS Lett. 389, 3-11
6. Horwich, A. L. and Weissman, J. S. (1997) Deadly conformations - protein misfolding in prion disease. Cell (Cambridge, Mass.) 89, 499-510
7. Horiuchi, M. and Caughey, B. (1999) Prion protein interconversions and the transmissible spongiform encephalopathies. Structure Fold Design 7, R231-240
8. Stahl, N., Baldwin, M. A., Teplow, D. B., Hood, L., Gibson, B. W., Burlingame, A. L. and Prusiner, S. B. (1993) Structural studies of the scrapie prion protein using mass spectrometry and amino acid sequencing. Biochemistry 32, 1991-2002
9. Pan, K. M., Baldwin, M., Nguyen, J., Gassel, M., Serban, A., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., Cohen, F. E. et al. (1993) Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins. Proc. Natl. Acad. Sci. U.S.A. 90, 10962-10966
10. Caughey, B. W., Dong, A., Bhat, K. S., Ernst, D., Hayes, S. F. and Caughey, W. S. (1991) Secondary structure analysis of the scrapie-associated protein PrP 27-30 in water by infrared spectroscopy. Biochemistry 30, 7672-7680
11. Safar, J., Roller, P. P., Gajdusek, D. C. and Gibbs, Jr, C. J. (1993) Thermal stability and conformational transitions of scrapie amyloid (prion) protein correlate with infectivity. Protein Sci. 2, 2206-2216
12. Moore, R. C., Lee, I. Y., Silverman, G. L., Harrison, P. M., Strome, R., Heinrich, C., Karunaratne, A., Pasternak, S. H., Chishti, M. A., Liang, Y. et al. (1999) Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J. Mol. Biol. 292, 797-817
13. Behrens, A., Genoud, N., Naumann, H., Rulicke, T., Janett, F., Heppner, F. L., Ledermann, B. and Aguzzi, A. (2002) Absence of the prion protein homologue Doppel causes male sterility. EMBO J. 21, 3652-3658
14. Sakaguchi, S., Katamine, S., Nishida, N., Moriuchi, R., Shigematsu, K., Sugimoto, T., Nakatani, A., Kataoka, Y., Houtani, T., Shirabe, S. et al. (1996) Loss of cerebellar Purkinje cells in aged mice homozygous for a disrupted PrP gene. Nature (London) 380, 528-531
15. Shmerling, D., Hegyi, I., Fischer, M., Blattler, T., Brandner, S., Gotz, J., Rulicke, T., Flechsig, E., Cozzio, A., von Mering, C. et al. (1998) Expression of amino-terminally truncated PrP in the mouse leading to ataxia and specific cerebellar lesions. Cell (Cambridge, Mass.) 93, 203-214
16. Nishida, N., Tremblay, P., Sugimoto, T., Shigematsu, K., Shirabe, S., Petromilli, C., Erpel, S. P., Nakaoke, R., Atarashi, R., Houtani, T. et al. (1999) A mouse prion protein transgene rescues mice deficient for the prion protein gene from purkinje cell degeneration and demyelination. Lab. Invest. 79, 689-697
17. Peoc'h, K., Guerin, C., Brandel, J. P., Launay, J. M. and Laplanche, J. L. (2000) First report of polymorphisms in the prion-like protein gene (PRND): implications for human prion diseases. Neurosci. Lett. 286, 144-148
18. Behrens, A., Brandner, S., Genoud, N. and Aguzzi, A. (2001) Normal neurogenesis and scrapie pathogenesis in neural grafts lacking the prion protein homologue Doppel. Embo Rep. 2, 347-352
19. Tuzi, N. L., Gall, E., Melton, D. and Manson, J. C. (2002) Expression of doppel in the CNS of mice does not modulate transmissible spongiform encephalopathy disease. J. Gen. Virol. 83, 705-711
20. Moore, R. C., Mastrangelo, P., Bouzamondo, E., Heinrich, C., Legname, G., Prusiner, S. B., Hood, L., Westaway, D., DeArmond, S. J. and Tremblay, P. (2001) Doppel-induced cerebellar degeneration in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 98, 15288-15293
21. Peoc'h, K., Serres, C., Frobert, Y., Martin, C., Lehmann, S., Chasseigneaux, S., Sazdovitch, V., Grassi, J., Jouannet, P., Launay, J. M. and Laplanche, J. L. (2002) The human 'prion-like' protein Doppel is expressed in both Sertoli cells and spermatozoa. J. Biol. Chem. 277, 43071-43078
22. c do not share the same membrane microenvironment. FEBS Lett. 530, 85-88
23. Legname, G., Nelken, P., Guan, Z., Kanyo, Z. F., DeArmond, S. J. and Prusiner, S. B. (2002) Prion and doppel proteins bind to granule cells of the cerebellum. Proc. Natl. Acad. Sci. U.S.A. 99, 16285-16290
24. Mastrangelo, P., Serpell, L., Dafforn, T., Lesk, A., Fraser, P. and Westaway, D. (2002) A cluster of familial Creutzfeldt-Jakob disease mutations recapitulate conserved residues in Doppel: a case of molecular mimicry? FEBS Lett. 532, 21-26
25. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O. and Tagliavini, F. (1993) Neurotoxicity of a prion protein fragment. Nature (London) 362, 543-546
26. Mo, H., Moore, R. C., Cohen, F. E., Westaway, D., Prusiner, S. B., Wright, P. E. and Dyson, H. J. (2001) Two different neurodegenerative diseases caused by proteins with similar structures. Proc. Natl. Acad. Sci. U.S.A. 98, 2352-2357
27. Lu, K., Wang, W., Xie, Z., Wong, B. S., Li, R., Petersen, R. B., Sy, M. S. and Chen, S. G. (2000) Expression and structural characterization of the recombinant human doppel protein. Biochemistry 39, 13575-13583
28. Nicholson, E. M., Mo, H., Prusiner, S. B., Cohen, F. E. and Marqusee, S. (2002) Differences between the prion protein and its homolog Doppel: a partially structured state with implications for scrapie formation. J. Mol. Biol. 316, 807-815
29. 0/0 mice predisposed to Purkinje cell loss. J. Biol. Chem. 275, 26834-26841
30. Morillas, M., Vanik, D. L. and Surewicz, W. K. (2001) On the mechanism of α-helix to β-sheet transition in the recombinant prion protein. Biochemistry 40, 6982-6987
31. 90-231. Biochemistry 39, 424-431
32. Swietnicki, W., Petersen, R., Gambetti, P. and Surewicz, W. K. (1997) pH-dependent stability and conformation of the recombinant human prion protein PrP(90-231). J. Biol. Chem. 272, 27517-27520
33. Hornemann, S. and Glockshuber, R. (1998) A scrapie-like unfolding intermediate of the prion protein domain PrP(121-231) induced by acidic pH. Proc. Natl. Acad. Sci. U.S.A. 95, 6010-6014
34. Whyte, S. M., Martin, S., Sylvester, I., Gill, A., Hope, J., Wopfner, F., Schaetzl, H. M., Dodson, G. and Bayley, P. M. (2002) Studies of the conformation and stability of the Protein Doppel. Biophys. J. 82, 332a
35. Bayley, P. M., Findlay, W. A. and Martin, S. R. (1996) Target recognition by calmodulin: dissecting the kinetics and affinity of interaction using short peptide sequences. Protein Sci. 5, 1215-1228
36. Savitzky, A. and Golay, M. J. E. (1964) Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 36, 1627-1639
37. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326
38. Sreerama, N. and Woody, R. W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287, 252-260
39. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131, 266-280
40. Masino, L., Martin, S. R. and Bayley, P. M. (2000) Ligand binding and thermodynamic stability of a multidomain protein, calmodulin. Protein Sci. 9, 1519-1529
41. Myers, J. K., Pace, C. N. and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148
42. Becktel, W. J. and Schellman, J. A. (1987) Protein stability curves. Biopolymers 26, 1859-1877
43. Robertson, A. D. and Murphy, K. P. (1997) Protein structure and the energetics of protein stability. Chem. Rev. 97, 1251-1268
44. Riek, R., Hornemann, S., Wider, G., Billeter, M., Glockshuber, R. and Wuthrich, K. (1996) NMR structure of the mouse prion protein domain PrP(121-321). Nature (London) 382, 180-182
45. James, T. L., Liu, H., Ulyanov, N. B., Farr-Jones, S., Zhang, H., Donne, D. G., Kaneko, K., Groth, D., Mehlhorn, I., Prusiner, S. B. and Cohen, F. E. (1997) Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc. Natl. Acad. Sci. U.S.A. 94, 10086-10091
46. Lopez Garcia, F., Zahn, R., Riek, R. and Wuthrich, K. (2000) NMR structure of the bovine prion protein. Proc. Natl. Acad. Sci. U.S.A. 97, 8334-8339
47. Zahn, R., Liu, A., Luhrs, T., Riek, R., von Schroetter, C., Lopez Garcia, F., Billeter, M., Calzolai, L., Wider, G. and Wuthrich, K. (2000) NMR solution structure of the human prion protein. Proc. Natl. Acad. Sci. U.S.A. 97, 145-150
48. Kuwajima, K. and Sugai, S (1978) Equilibrium and kinetics of the thermal unfolding of α-lactalbumin. The relation to its folding mechanism. Biophys. Chem. 8, 247-254
49. Swietnicki, W., Petersen, R. B., Gambetti, P. and Surewicz, W. K. (1998) Familial mutations and the thermodynamic stability of the recombinant human prion protein. J. Biol. Chem. 273, 31048-31052
50. Rezaei, H., Choiset, Y., Eghiaian, F., Treguer, E., Mentre, P., Debey, P., Grosclaude, J. and Haertle, T. (2002) Amyloidogenic unfolding intermediates differentiate sheep prion protein variants. J. Mol. Biol. 322, 799-814
51. Zahn, R., Guntert, P., von Schroetter, C. and Wuthrich, K. (2003) NMR structure of a variant human prion protein with two disulfide bridges. J. Mol. Biol. 326, 225-234
52. c directly interacts with proteins involved in signaling pathways J. Biol. Chem. 276, 44604-44612
53. 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. Neuron 27, 399-408
54. Baskakov, I. V., Legname, G., Prusiner, S. B. and Cohen, F. E. (2001) Folding of prion protein to its native α-helical conformation is under kinetic control. J. Biol. Chem. 276, 19687-19690
55. Liemann, S. and Glockshuber, R. (1999) Influence of amino acid substitutions related to inherited human prion diseases on the thermodynamic stability of the cellular prion protein. Biochemistry 38, 3258-3267
56. Zhang, H., Kaneko, K., Nguyen, J. T., Livshits, T. L., Baldwin, M. A., Cohen, F. E., James, T. L. and Prusiner, S. B. (1995) Conformational transitions in peptides containing two putative α-helices of the prion protein. J. Mol. Biol. 250, 514-526
57. Kaneko, K., Ball, H. L., Wille, H., Zhang, H., Groth, D., Torchia, M., Tremblay, P., Safar, J., Prusiner, S. B., DeArmond, S. J. et al. (2000) A synthetic peptide initiates Gerstmann-Straussler-Scheinker (GSS) disease in transgenic mice. J. Mol. Biol. 295, 997-1007
58. Zulianello, L., Kaneko, K., Scott, M., Erpel, S., Han, D., Cohen, F. E. and Prusiner, S. B. (2000) Dominant-negative inhibition of prion formation diminished by deletion mutagenesis of the prion protein. J. Virol. 74, 4351-4360
59. Horiuchi, M., Baron, G. S., Xiong, L. W. and Caughey, B. (2001) Inhibition of interactions and interconversions of prion protein isoforms by peptide fragments from the C-terminal folded domain. J. Biol. Chem. 276, 15489-15497
60. Eberl, H. and Glockshuber, R. (2002) Folding and intrinsic stability of deletion variants of PrP(121-231), the folded C-terminal domain of the prion protein. Biophys. Chem. 96, 293-303