New insights into the mechanisms of protein misfolding and aggregation in amyloidogenic diseases derived from pressure studies

Biochemistry

Volumn 43, Issue 36, 2004, Pages 11361-11370

  Foguel, Débora ^a   Silva, Jerson L ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOIDS; INSOLUBLE AGGREGATES; PROTEIN INTERACTION;

AGGLOMERATION; BIOTECHNOLOGY; DISEASES; DRUG PRODUCTS; HIGH PRESSURE EFFECTS; HYDROSTATIC PRESSURE; PATHOLOGY; THERMODYNAMICS;

PROTEINS;

AMYLOID; PROTEIN; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN;

ALZHEIMER DISEASE; AMYLOIDOSIS; BIOTECHNOLOGY; CELL INCLUSION; CONFORMATIONAL TRANSITION; DISSOCIATION; DRUG INDUSTRY; DYNAMICS; FIBRINOLYSIS; HYDROSTATIC PRESSURE; HYPERBARISM; PARKINSON DISEASE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FOLDING DISORDER; PROTEIN INTERACTION; PROTEIN MISFOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; THERMODYNAMICS; TUMOR;

ALZHEIMER DISEASE; AMYLOID; AMYLOIDOSIS; HYDROSTATIC PRESSURE; NEOPLASMS; PARKINSON DISEASE; PRION DISEASES; PROTEIN FOLDING;

EID: 4444362186     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048864a     Document Type: Review

References (76)

1. Horwich, A. (2002) Protein aggregation in disease: a role for folding intermediates forming specific multimeric interactions, J. Clin. Invest. 110, 1221-1232.
2. Caughey, B., and Lansbury, P. T. (2003) Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders, Annu. Rev. Neurosci. 26, 267-298.
3. Hernandez-Boussard, T., Rodriguez-Tome, P., Montesano, R., and Hainaut, P. (1999) IARC p53 mutation database: a relational database to compile and analyze p53 mutations in human tumors and cell lines, Hum. Mutat. 14, 1-8.
4. Prusiner, S. B. (1998) Prions, Proc. Natl. Acad. Sci. U.S.A. 95, 13363-13383.
5. Ferrão-Gonzales, A. D., Souto, S. O., Suva, J. L., and Foguel, D. (2000) The preaggregated state of an amyloidogenic protein: hydrostatic pressure converts native transthyretin into the amyloidogenic state, Proc. Natl. Acad. Sci. U.S.A. 97, 6445-6450.
6. Ferrão-Gonzales, A. D., Palmieri, L., Valory, M., Silva, J. L., Lashuel, H., Kelly, J. W., and Foguel, D. (2003) Hydration and packing are crucial to amyloidogenesis as revealed by pressure studies on transthyretin variants that either protect or worsen amyloid disease, J. Mol. Biol. 328, 963-974.
7. Marchal, S., Shehi, E., Harricane, M. C., Fusi, P., Heitz, F., Tortora, P., and Lange, R. (2003) Structural instability and fibrillar aggregation of non-expanded human ataxin-3 revealed under high pressure and temperature, J. Biol. Chem. 278, 31554-31563.
8. Foguel, D., Suarez, M. C., Ferrao-Gonzales, A. D., Porto, T. C., Palmieri, L., Einsiedler, C. M., Andrade, L. R., Lashuel, H. A., Lansbury, P. T., Kelly, J. W., and Silva, J. L. (2003) Dissociation of amyloid fibrils of α-synuclein and transthyretin by pressure reveals their reversible nature and the formation of water-excluded cavities, Proc. Natl. Acad. Sci. U.S.A. 100, 9831-9836.
9. Ishimaru, D., Andrade, L. R., Teixeira, L. S., Quesado, P. A., Maiolino, L. M., Lopez, P. M., Cordeiro, Y., Costa, L. T., Heckl, W. M., Weissmuller, G., Foguel, D., and Silva, J. L. (2003) Fibrillar aggregates of the tumor suppressor p53C core domain, Biochemistry 42, 9022-9027.
10. Niraula, T. N., Konno, T., Li, H., Yamada, H., Akasaka, K., and Tachibana, H. (2004) Pressure-dissociable reversible assembly of intrinsically denatured lysozyme is a precursor for amyloid fibrils, Proc. Natl. Acad. Sci. U.S.A. 23, 4089-4093.
11. Silva, J. L., and Weber, G. (1993) Pressure stability of proteins, Annu. Rev. Phys. Chem. 44, 89-113.
12. Mozhaev, V. V., Heremans, K., Frank, J., Masson, P., and Balny, C. (1996) High-pressure effects on protein structure and function, Proteins 24, 81-91.
13. Silva, J. L., Foguel, D., and Royer, C. A. (2001) Pressure provides new insights into protein folding, dynamics and structure, Trends Biochem. Sci. 26, 612-618.
14. Niraula, T. N., Haraoka, K., Ando, Y., Li, H., Yamada, H., and Akasaka, K. (2002) Decreased thermodynamic stability as a crucial factor for familial amyloidotic polyneuropathy, J. Mol. Biol. 320, 333-342.
15. Kuwata, K., Li, H., Yamada, H., Legname, G., Prusiner, S. B., Akasaka, K., and James, T. L. (2002) Locally disordered conformer of the hamster prion protein: a crucial intermediate to PrPSc? Biochemistry 41, 12277-12283.
16. Torrent, J., Alvarez-Martinez, M. T., Heitz, F., Liautard, J. P., Balny, C., and Lange, R. (2003) Alternative prion structural changes revealed by high pressure, Biochemistry 42, 1318-1325.
17. Cordeiro, Y., Kraineva, J., Ravindra, R., Lima, L. M. T. R., Gomes, M. P. B., Foguel, D., Winter, R., and Silva, J. L. (2004) Hydration and packing effects on prion folding and β-sheet conversion: High-pressure spectroscopy and pressure perturbation calorimetry studies, J. Biol. Chem. 279, 32354-32359.
18. Ishimaru, D., Maia, L. F., Maiolino, L. M., Quesado, P. A., Lopez, P. C., Almeida, F. C., Valente, A. P., and Silva, J. L. (2003) Conversion of wild-type p53C core domain into a conformation that mimics a hot-spot mutant, J. Mol. Biol. 333, 443-451.
19. Smeller, L., Rubens, P., and Heremans, K. (1999) Pressure effect on the temperature-induced unfolding and tendency to aggregate of myoglobin, Biochemistry 38, 3816-3820.
20. Meersman, F., Smeller, L., and Heremans, K. (2002) Comparative Fourier transform infrared spectroscopy study of cold-, pressure-, and heat-induced unfolding and aggregation of myoglobin, Biophys. J. 82, 2635-2644.
21. Foguel, D., Robinson, C. R., Sousa, P. C., Jr., Silva, J. L., and Robinson, A. S. (1999) Hydrostatic pressure rescues native protein from aggregates, Biotechnol. Bioeng. 63, 552-558.
22. Lefebvre, B. G., and Robinson, A. S. (2003) Pressure treatment of tailspike aggregates rapidly produces on-pathway folding intermediates, Biotechnol. Bioeng. 82, 595-604.
23. Webb, J. N., Webb, S. D., Cleland, J. L., Carpenter, J. F., and Randolph, T. W. (2001) Partial molar volume, surface area, and hydration changes for equilibrium unfolding and formation of aggregation transition state: high-pressure and cosolute studies on recombinant human IFN-γ, Proc. Natl. Acad. Sci. U.S.A. 98, 7259-7264.
24. Gorovits, B. M., and Horowitz, P. M. (1998) High hydrostatic pressure can reverse aggregation of protein folding intermediates and facilitate acquisition of native structure, Biochemistry 37, 6132-6135.
25. Dzwolak, W., Ravindra, R., Lendermann, J., and Winter, R. (2003) Aggregation of bovine insulin probed by DSC/PPC calorimetry and FTK spectroscopy, Biochemistry 42, 11347-11355.
26. Royer, C. A. (2002) Revisiting volume changes in pressure-induced protein unfolding, Biochim. Biophys. Acta 1595, 201-209.
27. Oliveira, A. C., Caspar, L. P., Da Poian, A. T., and Silva, J. L. (1994) Arc repressor will not denature under pressure in the absence of water, J. Mol. Biol. 240, 184-187.
28. Chalikian, T. V. (2003) Volumetric properties of proteins, Annu. Rev. Biophys. Biomol. Struct. 32, 207-235.
29. Foguel, D., and Silva, J. L. (1994) Cold denaturation of a repressor-operator complex: the role of entropy in protein-DNA recognition, Proc. Natl. Acad. Sci. U.S.A. 91, 8244-8247.
30. Nash, D. P., and Jonas, J. (1997) Structure of pressure-assisted cold denatured lysozyme and comparison with lysozyme folding intermediates, Biochemistry 36, 14375-14383.
31. Hummer, G., Garde, S., Garcia, A. E., Paulaitis, M. E., and Pratt, L. R. (1998) The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins, Proc. Natl. Acad. Sci. U.S.A. 95, 1552-1555.
32. Hillson, N., Onuchic, J. N., and Garcia, A. E. (1999) Pressure-induced protein-folding/unfolding kinetics, Proc. Natl. Acad. Sci. U.S.A. 96, 14848-14853.
33. 1H NMR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 90, 1776-1780.
34. Akasaka, K. (2003) Highly fluctuating protein structures revealed by variable-pressure nuclear magnetic resonance, Biochemistry 42, 10875-10885.
35. Fourme, R., Ascone, I., Kahn, R., Mezouar, M., Bouvier, P., Girard, E., Lin, T., and Johnson, J. E. (2002) Opening the high-pressure domain beyond 2 kbar to protein and virus crystallography: technical advance, Structure 10, 1409-1414.
36. Inoue, K., Yamada, H., Akasaka, K., Herrmann, C., Kremer, W., Maurer, T., Doker, R., and Kalbitzer, H. R. (2000) Pressure-induced local unfolding of the Ras binding domain of RalGDS, Nat. Struct. Biol. 7, 547-550.
37. Lima, L. M. T. R., Foguel, D., and Silva, J. L. (2000) DNA tightens the dimeric DNA-binding domain of human papillomavirus E2 protein without changes in volume, Proc. Natl. Acad. Sci. U.S.A. 97, 14289-14294.
38. Zong, Q., Osmulski, P. A., and Hager, L. P. (1995) High-pressure-assisted reconstitution of recombinant chloroperoxidase, Biochemistry 34, 12420-12425.
39. Silva, J. L., Oliveira, A. C., Gomes, A. M. O., Lima, L. M., Mohana-Borges, R., Pacheco, A. B., and Foguel, D. (2002) Pressure induces folding intermediates that are crucial for protein-DNA recognition and virus assembly, Biochim. Biophys. Acta 1595, 250-265.
40. Silva, J. L., Luan, P., Glaser, M., Voss, E. W., and Weber, G. (1992) Effects of hydrostatic pressure on a membrane-enveloped virus: high immunogenicity of the pressure-inactivated virus, J. Virol. 65, 2111-2117.
41. Oliveira, A. C., Ishimaru, D., Gonçalves, R. B., Smith, T. J., Mason, P., Sa-Carvalho, D., and Silva, J. L. (1999) Low temperature and pressure stability of picornaviruses: implications for virus uncoating, Biophys. J. 76, 1270-1279.
42. Tian, S. M., Ruan, K. C., Qian, J. F., Shao, G. Q., and Balny, C. (2000) Effects of hydrostatic pressure on the structure and biological activity of infectious bursal disease virus, Eur. J. Biochem. 267, 4486-4494.
43. Caspar, L. P., Silva, A. C., Gomes, A. M. O., Ano Bom, A. P. D., Schwarcz, W. D., Mestecky, J., Novak, M. J., Foguel, D., and Silva, J. L. (2002) Hydrostatic pressure induces the fusion-active state of enveloped viruses, J. Biol. Chem. 277, 8433-8439.
44. Panda, M., Gorovits, B. M., and Horowitz, P. M. (2000) Productive and nonproductive intermediates in the folding of denatured rhodanese, J. Biol. Chem. 275, 63-70.
45. St John, R. J., Carpenter, J. F., and Randolph, T. W. (1999) High-pressure refolding of recombinant human growth hormone from insoluble aggregates, Proc. Natl. Acad. Sci. U.S.A. 96, 13029-13033.
46. King, J., Haase-Pettingell, C., Robinson, A. S., Speed, M., and Mitraki, A. (1996) Thermolabile folding intermediates: inclusion body precursors and chaperonin substrates, FASEB J. 10, 57-66.
47. Clark, E. D. (2001) Protein refolding for industrial processes, Curr. Opin. Biotechnol. 12, 202-207.
48. Carrio, M. M., and Villaverde, A. (2002) Construction and deconstruction of bacterial inclusion bodies, J. Biotechnol. 96, 3-12.
49. Dobson, C. M. (2003) Protein folding and misfolding, Nature 426, 884-890.
50. Kelly, J. W. (1998) The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways, Curr. Opin. Struct. Biol. 8, 101-106.
51. Soto, C. (2001) Protein misfolding and disease; protein refolding and therapy. FEBS Lett. 498, 204-207.
52. Damas, A. M., and Saraiva, M. J. (2000) TTR amyloidosis-structural features leading to protein aggregation and their implications on therapeutic strategies, J. Struct. Biol. 130, 290-299.
53. Blake, C. C., Geisow, M. J., Oatley, S. J., Rerat, B., and Rerat, C. (1978) Structure of prealbumin: secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 Å, J. Mol. Biol. 121, 339-356.
54. Lai, Z., Colon, W., and Kelly, J. W. (1996) The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid. Biochemistry 35, 6470-6482.
55. Lashuel, H. A., Lai, Z., and Kelly, J. W. (1998) Characterization of the transthyretin acid denaturation pathways by analytical ultracentrifugation: implications for wild-type, V30M, and L55P amyloid fibril formation, Biochemistry 37, 17851-17864.
56. Prives, C., and Hall, P. A. (1999) The p53 pathway, J. Pathol. 187, 112-126.
57. Bullock, A. N., and Fersht, A. R. (2001) Rescuing the function of mutant p53C, Nat. Rev. Cancer 1, 68-76.
58. Wong, K. B., DeDecker, B. S., Freund, S. M., Proctor, M. R., Bycroft, M., and Fersht, A. R. (1999) Hot-spot mutants of p53 core domain evince characteristic local structural changes, Proc. Natl. Acad. Sci. U.S.A. 96, 8438-8442.
59. Chene, P. (1998) In vitro analysis of the dominant negative effect of p53 mutants, J. Mol. Biol. 281, 205-209.
60. Milner, J., and Medcalf, E. A. (1991) Cotranslation of activated mutant p53 with wild-type drives the wild-type p53 protein into the mutant conformation, Cell 65, 765-774.
61. Ostermeyer, A. G., Runko, E., Winkfield, B., Ahn, B., and Moll, U. M. (1996) Cytoplasmically sequestered wild-type p53 protein in neuroblastoma is relocated to the nucleus by a C-terminal peptide, Proc. Natl. Acad. Sci. U.S.A. 93, 15190-15194.
62. Foster, B. A., Coffey, H. A., Morin, M. J., and Rastinejad, F. (1999) Pharmacological rescue of mutant p53 conformation and function, Science 286, 2507-2510.
63. Weber, G. (1992) Protein Interactions, Chapman and Hall, New York.
64. Lai, Z., McCulloch, J., Lashuel, H. A., and Kelly, J. W. (1997) Guanidine hydrochloride-induced denaturation and refolding of transthyretin exhibits a marked hysteresis: equilibria with high kinetic barriers, Biochemistry 36, 10230-10239.
65. Sinclair, J. F., Ziegler, M. M., and Baldwin, T. O. (1994) Kinetic partitioning during protein folding yields multiple native states, Nat. Struct. Biol. 1, 320-326.
66. Schuler, B., Rachel, R., and Seckler, R. (1999) Formation of fibrous aggregates from a non-native intermediate: the isolated P22 tailspike β-helix domain, J. Biol. Chem. 274, 18589-18596.
67. Weber, G. (1986) Phenomenological description of the association of protein subunits subjected to conformational drift. Effects of dilution and of hydrostatic pressure, Biochemistry 25, 3626-3231.
68. Silva, J. L., Miles, E. W., and Weber, G. (1986) Pressure dissociation and conformational drift of the β dimer of tryptophan synthase, Biochemistry 25, 5780-5786.
69. Sacchettini, J. C., and Kelly, J. W. (2002) Therapeutic strategies for human amyloid diseases, Nat. Rev. Drug Discovery I, 267-275.
70. Cohen, F. E., and Kelly, J. W. (2003) Therapeutic approaches to protein-misfolding diseases, Nature 426, 905-909.
71. Spillantini, M. G., Schmidt, M. L., Lee, V. M. Y., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) α-Synuclein in Lewy bodies, Nature 388, 839-840.
72. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M. A., Brentani, R. R., Foguel, D., and Silva, J. L. (2001) DNA converts cellular prion protein into the β-sheet conformation and inhibits prion peptide aggregation, J. Biol. Chem. 276, 49400-49409.
73. Deleault, N. R., Lucassen, R. W., and Supattapone, S. (2003) RNA molecules stimulate prion protein conversion, Nature 425, 717-720.
74. Cordeiro, Y., Lima, L. M. T. R., Gomes, M. P., Foguel, D., and Silva, J. L. (2004) Modulation of prion protein oligomerization, aggregation, and β-sheet conversion by 4,4′-dianilino-1,1′-binaphthyl-5, 5′-sulfonate (bis-ANS), J. Biol. Chem. 279, 5346-5352.
75. Torrent, J., Alvarez-Martinez, M. T., Harricane, M. C., Heitz, F., Liautard, J. P., Balny, C., and Lange, R. (2004) High-pressure induces scrapie-like prion protein misfolding and amyloid fibril formation, Biochemistry 43, 7162-7170.
76. Martins, S. M., Chapeaurouge, A., and Ferreira, S. T. (2003) Folding intermediates of the prion protein stabilized by hydrostatic pressure and low temperature, J. Biol. Chem. 278, 50449-50455.