Misfolding and amyloid aggregation of apomyoglobin

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 14287-14300

  Iannuzzi, Clara ^a   Maritato, Rosa ^a   Irace, Gaetano ^a   Sirangelo, Ivana ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Amyloid aggregation; Apomyoglobin folding; Apomyoglobin misfolding

Indexed keywords

AMYLOID; APOMYOGLOBIN; APOPROTEIN; MYOGLOBIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; MUTATION RATE; OLIGOMERIZATION; PH MEASUREMENT; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN MISFOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN UNFOLDING; REVIEW; ROOM TEMPERATURE; SUBSTITUTION REACTION; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PH; PROTEIN TERTIARY STRUCTURE; PROTEINOSIS;

AMYLOID; ANIMALS; APOPROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; MUTATION; MYOGLOBIN; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84880155073     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140714287     Document Type: Review

References (83)

1. Stefani, M.; Dobson, C.M. Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 2003, 81, 678-699.
2. Stefani, M. Protein misfolding and aggregation: Newexamples in medicine and biology of the dark side of the protein world. Biochim. Biophys. Acta 2004, 1739, 5-25.
3. Sipe, J.D.; Benson, M.D.; Buxbaum, J.N.; Ikeda, S.; Merlini, G.; Saraiva, M.J.; Westermark, P. Amyloid fibril protein nomenclature: 2010 recommendations of the nomenclature committee of the International Society of Amyloidosis. Amyloid 2010, 17, 101-104.
4. Lansbury, P.T. Evolution of amyloid: What normal protein folding may tell us about fibrillogenesis and disease. Proc. Natl. Acad. Sci. USA 1999, 96, 3342-3344.
5. Merlini, G.; Bellotti, V. Molecular mechanisms of amyloidosis. N. Engl. J. Med. 2003, 349, 583-596.
6. Sunde, M.; Blake, C.C. From the globular to the fibrous state: Protein structure and structural conversion in amyloid formation. Quart. Rev. Biophys. 1998, 31, 1-39.
7. Makin, O.S.; Atkins, E.; Sikorski, P.; Johansson, J.; Serpell, L.C. Molecular basis for amyloid fibril formation and stability. Proc. Natl. Acad. Sci. USA 2005, 102, 315-320.
8. Makin, O.S.; Serpell, L.C. Structures for amyloid fibrils. FEBS J. 2005, 272, 5950-5961.
9. Jahn, T.R.; Makin, O.S.; Morris, K.L.; Marshall, K.E.; Tian, P.; Sikorski, P.; Serpell, L.C. The common architecture of cross-beta amyloid. J. Mol. Biol. 2010, 395, 717-727.
10. Sorrentino, A.; Giosafatto, C.V.; Sirangelo, I.; de Simone, C.; di Pierro, P.; Porta, R.; Mariniello, L. Higher susceptibility to amyloid fibril formation of the recombinant ovine prion protein modified by transglutaminase. Biochim. Biophys. Acta 2012, 1822, 1509-1515.
11. Rochet, J.C.; Lansbury, P.J. Amyloid fibrillogenesis: Themes and variations. Curr. Opin. Struct. Biol. 2000, 10, 60-68.
12. Hurle, M.R.; Helms, L.R.; Li, L.; Chan, W.; Wetzel, R. A role for destabilizing amino acid replacements in light-chain amyloidosis. Proc. Natl. Acad. Sci. USA 1994, 91, 5446-5450.
13. Goedert, M.; Ghetti, B.; Spillantini, M.G. Tau gene mutations in frontotemporal dementia and parkinsonism linked to chromosome 17 (FTDP-17). Their relevance for understanding the neurogenerative process. Ann. N. Y. Acad. Sci. 2000, 920, 74-83.
14. Quintas, A.; Vaz, D.C.; Cardoso, I.; Saraiva, M.J.; Brito, R.M. Tetramer dissociation and monomer partial unfolding precedes protofibril formation in amyloidogenic transthyretin variants. J. Biol. Chem. 2001, 276, 27202-27213.
15. Canet, D.; Last, A.M.; Tito, P.; Sunde, M.; Spencer, A.; Archer, D.B.; Redfield, C.; Robinson, C.V.; Dobson, C.M. Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme. Nat. Struct. Biol. 2002, 9, 308-315.
16. Niraula, T.N.; Haraoka, K.; Ando, Y.; Li, H.; Yamada, H.; Akasaka, K. Decreased thermodynamic stability as a crucial factor for familial amyloidotic polyneuropathy. J. Mol. Biol. 2002, 320, 333-342.
17. Konno, T. Amyloid-induced aggregation and precipitation of soluble proteins: An electrostatic contribution of the Alzheimer's beta (25-35) amyloid fibril. Biochemistry 2001, 40, 2148-2154.
18. Chiti, F.; Calamai, M.; Taddei, N.; Stefani, M.; Ramponi, G.; Dobson, C.M. Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc. Natl. Acad. Sci. USA 2002, 99, 16419-16426.
19. Chiti, F.; Stefani, M.; Taddei, N.; Ramponi, G.; Dobson, C.M. Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 2003, 424, 805-808.
20. Tjernberg, L.; Hosia, W.; Bark, N.; Thyberg, J.; Johansson, J. Charge attraction and beta propensity are necessary for amyloid fibril formation from tetrapeptides. J. Biol. Chem. 2002, 277, 43243-43246.
21. Ciani, B.; Hutchinson, E.G.; Sessions, R.B.; Woolfson, D.N. A designed system for assessing how sequence affects alpha to beta conformational transitions in proteins. J. Biol. Chem. 2002, 277, 10150-10155.
22. Monsellier, E.; Ramazzotti, M.; de Laureto, P.P.; Tartaglia, G.G.; Taddei, N.; Fontana, A.; Vendruscolo, M.; Chiti, F. The distribution of residues in a polypeptide sequence is a determinant of aggregation optimized by evolution. Biophys. J. 2007, 93, 4382-4391.
23. Tartaglia, G.G.; Pawar, A.P.; Campioni, S.; Dobson, C.M.; Chiti, F.; Vendruscolo, M. Prediction of aggregation-prone regions in structured proteins. J. Mol. Biol. 2008, 380, 425-443.
24. Uversky, V.N.; Fink, A.L. Conformational constraints for amyloid fibrillation: The importance of being unfolded. Biochim. Biophys. Acta 2004, 1698, 131-153.
25. Bousset, L.; Thomson, N.H.; Radford, S.E.; Melki, R. The yeast prion Ure2p retains its native alpha-helical conformation upon assembly into protein fibrils in vitro. EMBO J. 2002, 21, 2903-2911.
26. Chow, M.K.M.; Ellisdon, A.M.; Cabrita, L.D.; Bottomley, S.P. Polyglutamine expansion in ataxin-3 does not affect protein stability: Implications for misfolding and disease. J. Biol. Chem. 2004, 279, 47643-47651.
27. Pedersen, J.S.; Christensen, G.; Otze, D.E. Modulation of S6 fibrillation by unfolding rates and gatekeeper residues. J. Mol. Biol. 2004, 341, 575-588.
28. Plakoutsi, G.; Taddei, N.; Stefani, M.; Chiti, F. Aggregation of the Acylphosphatase from Sulfolobus solfataricus: The folded and partially unfolded states can both be precursors for amyloid formation. J. Biol. Chem. 2004, 279, 14111-14119.
29. Chiti, F.; Webster, P.; Taddei, N.; Clark, A.; Stefani, M.; Ramponi, G.; Dobson, C.M. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl. Acad. Sci USA 1999, 96, 3590-3594.
30. Dobson, C.M. The structural basis of protein folding and its links with human disease. Philos. Trans. R. Soc. Lond. B. 2001, 356, 133-145.
31. Dobson, C.M. Protein folding and misfolding. Nature 2003, 426, 884-890.
32. Bucciantini, M.; Giannoni, E.; Chiti, F.; Baroni, F.; Formigli, L.; Zurdo, J.; Taddei, N.; Ramponi, G.; Dobson, C.M.; Stefani, M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 2002, 416, 507-511.
33. Stefani, M. Structural features and cytotoxicity of amyloid oligomers: Implications in Alzheimer's disease and other diseases with amyloid deposits. Prog. Neurobiol. 2012, 99, 226-245.
34. Chiti, F.; Dobson, C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 2006, 75, 333-366.
35. Wiseman, R.L.; Powers, E.T.; Kelly, J.W. Partitioning conformational intermediates between competing refolding and aggregation pathways: Insights into transthyretin amyloid disease. Biochemistry 2005, 44, 16612-16623.
36. Lashuel, H.A.; Hartley, D.M.; Petre B.M.; Wall, J.S.; Simon, M.N.; Walz, T.; Lansbury, P.T., Jr. Mixtures of wild-type and a pathogenic (E22G) form of Abeta40 in vitro accumulate protofibrils, including amyloid pores. J. Mol. Biol. 2003, 332, 795-808.
37. Poirier, M.A.; Li, H.; Macosko, J.; Cail, S.; Amzel, M.; Ross, C.A. Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrillization. J. Biol. Chem. 2002, 277, 41032-41037.
38. Serpell, L.C.; Sunde, M.; Benson, M.D.; Tennent, G.A.; Pepys, M.B.; Fraser, P.E. The protofilament substructure of amyloid fibrils. J. Mol. Biol. 2000, 300, 1033-1039.
39. Maliskauskas, M.; Zamotin, V.; Jass, J.; Noppe, W.; Dobson, C.M.; Morozova-Roche, L.A. Amyloid protofilaments from the calcium-binding protein equine lysozyme: Formation of ring and linear structures depends on pH and metal ion concentration. J. Mol. Biol. 2003, 330, 879-890.
40. Hatters, D.M.; MacPhee, C.E.; Lawrence, L.J.; Sawyer, W.H.; Howlett, G.J. Human apolipoprotein C-II forms twisted amyloid ribbons and closed loops. Biochemistry 2000, 39, 8276-8283.
41. Porat, Y.; Kolusheva, S.; Jelinek, R.; Gazil, E. The human islet amyloid polypeptide forms transient membrane-active prefibrillar assemblies. Biochemistry 2003, 42, 10971-10977.
42. Ding, T.T.; Lee, S.J.; Rochet, J.C.; Lansbury, P.T., Jr. Annular alpha-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry 2002, 41, 10209-10217.
43. Relini, A.; Torrasa, S.; Rolandi, R.; Gliozzi, A.; Rosano, C.; Canale, C.; Bolognesi, M.; Plakoutsi, G.; Bucciantini, M.; Chiti, F., et al. Monitoring the process of HypF fibrillization and liposome permeabilization by protofibrils. J. Mol. Biol. 2004, 338, 943-957.
44. Lee, C.C.; Nayak, A.; Sethuraman, A.; Belfort, G.; McRae, G.J. A three-stage kinetic model of amyloid fibrillation. Biophys. J. 2007, 92, 3448-3458.
45. Harper, J.D.; Lansbury, P.T., Jr. Models of amyloid seeding in Alzheimer's disease and scrapie: Mechanistic truths and physiological consequences of the time dependent solubility of amyloid proteins. Annu. Rev. Biochem. 1997, 66, 385-407.
46. Serpell, L.C.; Sunde, M.; Blake, C.C. The molecular basis of amyloidosis. Cell. Mol. Life Sci. 1997, 53, 871-887.
47. Bhak, G.; Choe, Y.J.; Paik, S.R. Mechanism of amyloidogenesis: Nucleation-dependent fibrillation versus double-concerted fibrillation. BMB Rep. 2009, 42, 541-551.
48. Nguyen, H.D.; Hall, H.K. Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proc. Natl. Acad. Sci. USA 2004, 101, 16180-16185.
49. Harper, J.D.; Lieber, C.M.; Lansbury, P.T., Jr. Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-beta protein. Chem. Biol. 1997, 4, 951-959.
50. Stefani, M. Protein folding and misfolding on surfaces. Int. J. Mol. Sci. 2008, 9, 2515-2542.
51. Necula, M.; Kayed, R.; Milton, S.; Glabe, C. Small molecules inhibitors distinguish between amyloid beta oligomerization and fibrillization pathways. J. Biol. Chem. 2007, 28, 10311-10324.
52. Uversky, V.N. Mysterious oligomerization of the amyloidogenic proteins. FEBS J. 2010, 277, 2940-2953.
53. Baldwin, R.L.; Rose, G.D. Is protein folding hierarchic? II. Folding intermediates and transition states. Trends Biochem. Sci. 1999, 24, 77-83.
54. Aurora, R.; Creamer, T.P.; Srinivasan, R.; Rose, G.D. Local interactions in protein folding: Lessons from the alpha-helix. J. Biol. Chem. 1997, 272, 1413-1416.
55. Baldwin, R.L. In search of the energetic role of peptide hydrogen bonds. J. Biol. Chem. 2003, 278, 17581-17588.
56. Kauzmann, W. Some factors in the interpretation of protein denaturation. Adv. Protein Chem. 1959, 14, 1-63.
57. Tanford, C. The Hydrophobic Effect; Wiley: New York, NY, USA, 1973; pp. 120-125.
58. Dill, K.A. Theory for the folding and stability of globular proteins. Biochemistry 1985, 24, 1501-1509.
59. Kim, P.S.; Baldwin, R.L. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 1990, 59, 631-660.
60. Hughson, F.M.; Wright, P.E.; Baldwin, R.L. Structural characterization of a partly folded apomyoglobin intermediate. Science 1990, 249, 1544-1548.
61. Kay, M.S.; Baldwin, R.L. Packing interactions in the apomyglobin folding intermediate. Nat. Struct. Biol. 1996, 3, 439-445.
62. Barrick, D.; Baldwin, R.L. Stein and Moore award address the molten globule state intermediate of apomyoglobin and the process of protein folding. Protein Sci. 1993, 2, 869-876.
63. Sirangelo, I.; Bismuto, E.; Tavassi, S.; Irace, G. Apomyoglobin folding intermediates characterized by the hydrophobic fluorescent probe 8-anilino-1-naphthalene sulfonate. Biochem. Biophys. Acta 1998, 1385, 69-77.
64. Sirangelo, I.; Dal Piaz, F.; Malmo, C.; Casillo, M.; Birolo, L.; Pucci, P.; Marino, G.; Irace, G. Hexafluoroisopropanol and acid destabilized forms of apomyoglobin exhibit structural differences. Biochemistry 2003, 42, 312-319.
65. Sirangelo, I.; Iannuzzi, C.; Malmo, C.; Irace, G. Tryptophanyl substitutions in apomyoglobin affect conformation and dynamic properties of AGH subdomain. Biopolymers 2003, 70, 649-654.
66. Uzawa, T.; Akiyama, S.; Kimura, T.; Takahashi, S.; Ishimori, K.; Morishima, I.; Fujisawa, T. Collapse and search dynamics of apomyoglobin folding revealed by submillisecond observations of alphahelical content and compactness. Proc. Natl. Acad. Sci. USA 2004, 101, 1171-1176.
67. Jennings, P.A.; Wright, P.E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 1993, 262, 892-896.
68. Sirangelo, I.; Malmo, C.; Casillo, M.; Mezzogiorno, A.; Papa, M.; Irace, G. Tryptophanyl substitutions in apomyoglobin determine protein aggregation and amyloid-like fibril formation at physiological pH. J. Biol. Chem. 2002, 277, 45887-45891.
69. Sirangelo, I.; Malmo, C.; Iannuzzi, C.; Mezzogiorno, A.; Bianco, M.R.; Papa, M.; Irace, G. Fibrillogenesis and cytotoxic activity of the amyloid-forming apomyoglobin mutant W7FW14F. J. Biol. Chem. 2004, 279, 13183-13189.
70. Sirangelo, I.; Tavassi, S.; Martelli, P.L.; Casadio, R.; Irace, G. The effect of tryptophanyl substitution on folding and structure of myoglobin. Eur. J. Biochem. 2000, 267, 3937-3945.
71. Fändrich, M.; Forge, V.; Buder, K.; Kittler, M.; Dobson, C.M.; Diekmann, S. Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments. Proc. Natl. Acad. Sci. USA 2003, 100, 15463-15468.
72. Vilasi, S.; Sarcina, R.; Maritato, R.; de Simone, A.; Irace, G.; Sirangelo, I. Heparin induces harmless fibril formation in amyloidogenic W7FW14F apomyoglobin and amyloid aggregation in wild-type protein in vitro. PLoS One 2011, 6, e22076.
73. Infusini, G.; Iannuzzi, C.; Vilasi, S.; Birolo, L.; Pagnozzi, D.; Pucci, P.; Irace, G.; Sirangelo, I. Resolution of the effects induced by W→F substitutions on the conformation and dynamics of the amyloid-forming apomyoglobin mutant W7FW14F. Eur. Biophys. J. 2012, 41, 615-627.
74. Iannuzzi, C.; Vilasi, S.; Portaccio, M.; Irace, G.; Sirangelo, I. Heme binding inhibits the fibrillization of amyloidogenic apomyoglobin and determines lack of aggregate cytotoxicity. Protein Sci. 2007, 16, 507-516.
75. Chow, C.C.; Chow, C.; Raghunathan, V.; Huppert, T.J.; Kimball, E.B.; Cavagnero, S. Chain length dependence of apomyoglobin folding: Structural evolution from misfolded sheets to native helices. Biochemistry 2003, 42, 7090-7099.
76. Ribeiro, E.A., Jr.; Ramos, C.H.I. Circular permutation and deletion of myoglobin indicate that the correct position of its N-terminus is required foe native stability and solubility but not for nativelike heme binding and folding. Biochemistry 2005, 44, 4699-4709.
77. Nishimura, C.; Dyson, H.J.; Wright, P. Identification of native and non-native structure in kinetic folding intermediates of apomyoglobin. J. Mol. Biol. 2006, 355, 139-156.
78. Nishimura, C.; Dyson, H.J.; Wright, P.E. Energetic frustration of apomyoglobin folding: Role of the B helix. J. Mol. Biol. 2010, 396, 1319-1328.
79. Infusini, G.; Iannuzzi, C.; Vilasi, S.; Maritato, R.; Birolo, L.; Pagnozzi, D.; Pucci, P.; Irace, G.; Sirangelo, I. W-F substitutions in apomyoglobin increase the local flexibility of the N-terminal region causing amyloid aggregation: A H/D exchange study. Protein Pept. Lett. 2013, in press.
80. Fandrich, M.; Fletcher, M.A.; Dobson, C.M. Amyloid fibrils from muscle myoglobin. Nature 2001, 410, 165-166.
81. Waltho, J.P.; Feher, V.A.; Merutka, G.; Dyson, H.J.; Wright, P.E. Peptide models of protein folding initiation sites. 1. Secondary structure formation by peptides corresponding to the G- and H-helices of myoglobin. Biochemistry 1993, 32, 6337-6347.
82. Picotti, P.; de Franceschi, G.; Frare, E.; Spolaore, B.; Zambonin, M.; Chiti, F.; de Laureto, P.P.; Fontana, A. Amyloid fibril formation and disaggregation of fragment 1-29 of apomyoglobin: Insights into the effect of pH on protein fibrillogenesis. J. Mol. Biol. 2007, 367, 1237-1245.
83. Fabiani, E.; Stadler, A.M.; Madern, D.; Koza, M.M.; Tehei, M.; Hirai, M.; Zaccai, G. Dynamics of apomyoglobin in the a-to-b transition and of partially unfolded aggregated protein. Eur. Biophys. J. 2009, 38, 237-244.