Heme binding inhibits the fibrillization of amyloidogenic apomyoglobin and determines lack of aggregate cytotoxicity

Protein Science

Volumn 16, Issue 3, 2007, Pages 507-516

  Iannuzzi, Clara ^a   Vilasi, Silvia ^a   Portaccio, Marianna ^a   Irace, Gaetano ^a   Sirangelo, Ivana ^a  

^a SECOND UNIVERSITY OF NAPLES   (Italy)

Author keywords

Amyloid cytotoxicity; Amyloid fibril; Apomyoglobin aggregation; Fibrillization inhibition

Indexed keywords

AMYLOID; APOMYOGLOBIN; HEME;

ARTICLE; CELL STRUCTURE; CELL VIABILITY; CIRCULAR DICHROISM; CYTOTOXICITY; INFRARED SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; ULTRAVIOLET RADIATION; WILD TYPE;

AMYLOID; ANIMALS; APOPROTEINS; CIRCULAR DICHROISM; HEME; HYDROGEN-ION CONCENTRATION; MICE; MICROSCOPY, ATOMIC FORCE; MYOGLOBIN; NIH 3T3 CELLS; PROTEIN BINDING; PROTEIN CONFORMATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; ULTRAVIOLET RAYS;

EID: 33847257041     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062471107     Document Type: Article

References (69)

1. Bismuto, E., Sirangelo, I., and Irace, G. 1992. Salt-induced refolding of myoglobin at acidic pH: Molecular properties of a partly folded intermediate. Arch. Biochem. Biophys. 298: 624-629.
2. Booth, D.R., Sunde, M., Bellotti, V., Robinson, C.V., Hutchinson, W.L., Fraser, P.E., Hawkins, P.N., Dobson, C.M., Radford, S.E., Blake, C.C., et al. 1997. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis. Nature 385: 787-793.
3. Bousset, L., Thomson, N.H., Radford, S.E., and Melki, R. 2002. The yeast prion Ure2p retains its native α-helical conformation upon assembly into protein fibrils in vitro. EMBO J. 21: 2903-2911.
4. Bousset, L., Briki, F., Doucet, J., and Melki, R. 2003. The native-like conformation of Ure2p in fibrils assembled under physiologically relevant conditions switches to an amyloid-like conformation upon heat-treatment of the fibrils. J. Struct. Biol. 141: 132-142.
5. Bucciantini, M., Giannoni, E., Chiti, F., Baroni, F., Formigli, L., Zurdo, J., Taddei, N., Ramponi, G., Dobson, C.M., and Stefani, M. 2002. Inherent toxicity of aggregates implies a common mechanism for protein misfolding disease. Nature 416: 507-511.
6. Chiti, F., Webster, P., Taddei, N., Clark, A., Stefani, M., Ramponi, G., and Dobson, C.M. 1999. Designing conditions for in vitro formation of amyloid protofilaments and fibrils. Proc. Natl. Acad. Sci. 96: 3590-3594.
7. Chow, C.C., Chow, C., Raghunathan, V., Huppert, T.J., Kimball, E.B., and Cavagnero, S. 2003. Chain length dependence of apomyoglobin folding: Structural evolution from misfolded sheets to native helices. Biochemistry 42: 7090-7099.
8. Dobson, C.M. 2001. The structural basis of protein folding and its links with human disease. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356: 133-145.
9. Dobson, C.M. 2003. Protein folding and misfolding. Nature 426: 884-890.
10. Dzwolak, W., Kato, M., Shimizu, A., and Taniguchi, Y. 2002. Fourier transform infrared spectroscopy in high-pressure studies on proteins. Biochim. Biophys. Acta 1595: 131-144.
11. Dzwolak, W., Ravindra, R., Lendermann, J., and Winter, R. 2003. Aggregation of bovine insulin probed by DSC/PPC calorimetry and FTIR spectroscopy. Biochemistry 42: 11347-11355.
12. Edelhoch, H. 1967. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6: 1948-1954.
13. Eisenberg, D., Schwarz, E., Komarony, M., and Wall, R. 1984. Analysis of membrane and surface protein sequences with the hydrophobic moment plot. J. Mol. Biol. 179: 125-142.
14. Evans, S.V. and Brayer, G.D. 1988. Horse heart metmyoglobin. A 2.8-A resolution three-dimensional structure determination. J. Biol. Chem. 263: 4263-4268.
15. Fandrich, M., Fletcher, M.A., and Dobson, C.M. 2001. Amyloid fibrils from muscle myoglobin. Nature 410: 165-166.
16. Fandrich, M., Forge, V., Buder, K., Kittler, M., Dobson, C.M., and Diekmann, S. 2003. Myoglobin forms amyloid fibrils by association of unfolded polypeptide segments. Proc. Natl. Acad. Sci. 100: 15463-15468.
17. Fink, A.L. 1998. Protein aggregation: Folding aggregates, inclusion bodies and amyloid. Fold. Des. 3: R9-R23.
18. Geddes, A.J., Parjer, K.D., Akins, E.D., and Beighton, E. 1968. "Cross-β" conformation in proteins. J. Mol. Biol. 32: 343-358.
19. Goto, Y. and Fink, A.L. 1990. Phase diagram for acidic conformational states of apomyoglobin. J. Mol. Biol. 214: 803-805.
20. Goto, Y., Calciano, L.J., and Fink, A.L. 1990. Acid-induced folding of proteins. Proc. Natl. Acad. Sci. 87: 573-577.
21. Hansen, M.B., Nielsen, S.E., and Berg, K. 1989. Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill. J. Immunol. Methods 119: 203-210.
22. Hartley, D.M., Walsh, D.M., Ye, C.P.P., Diehl, T., Vasquez, S., Vassilev, P.M., Teplow, D.B., and Selkoe, D.J. 1999. Protofibrillar intermediates of amyloid β-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 19: 8876-8884.
23. Hsu, M.C. and Woody, R.W. 1971. The origin of the heme Cotton effects in myoglobin and haemoglobin. J. Am. Chem. Soc. 93: 3515-3525.
24. Hughson, F.M., Barrick, D., and Baldwin, R.L. 1990. Structural characterization of a partly folded apomyoglobin intermediate. Science 249: 1544-1548.
25. Jackson, M. and Mantsch, H.H. 1991. Protein secondary structure from FT-IR spectroscopy: Correlation with dihedral angles from three-dimensional Ramachandran plots. Can. J. Chem. 69: 1639-1642.
26. Jahn, T.R. and Radford, S.E. 2005. The yin and yang of protein folding. FEBS J. 272: 5962-5970.
27. Jennings, P.A. and Wright, P.E. 1993. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262: 892-896.
28. Jimenez, J.L., Guijarro, J.I., Orlova, E., Zurdo, J., Dobson, C.M., Sunde, M., and Saibil, H.R. 1999. Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J. 18: 815-821.
29. Kataoka, M., Nishii, I., Fujisawa, T., Ueki, T., Tokunaga, F., and Goto, Y. 1995. Structural characterization of the molten globule and native states of apomyoglobin by solution X-ray scattering. J. Mol. Biol. 249: 215-228.
30. Kayed, R., Head, E., Thompson, J.L.,McIntire, T.M.,Milton, S.C., Cotman, C.W., and Glabe, C.G. 2003. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300: 486-489.
31. Kelly, J.W. 1998. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8: 101-106.
32. 1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. 95: 6448-6453.
33. Lashuel, A., Hartley, D., Petre, B.M., Walz, T., and Lansbury Jr., P.T. 2002a. Neurodegenerative disease: Amyloid pores from pathogenic mutations. Nature 418: 291.
34. Lashuel, H.A., Petre, B.M., Wall, J., Simon, M., Nowak, R.J., Walz, T., and Lansbury Jr., P.T. 2002b. α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322: 1089-1102.
35. Lashuel, H.A., Hartley, D.M., Petre, B.M., Wall, J.S., Simon, M.N., Walz, T., and Lansbury, P.T. 2003. Mixtures of wild-type and a pathogenic (E22G) form of Ab40 in vitro accumulate protofibrils. including amyloid pores. J. Mol. Biol. 332: 795-808.
36. Laurine, E., Gregoire, C., Fandrich, M., Engemann, S., Marchal, S., Thion, L., Mohr, M., Monsarrat, B., Michel, B., Dobson, C.M., et al. 2003. Lithostathine quadruple-helical filaments form proteinase K-resistant deposits in Creutzfeldt-Jakob disease. J. Biol. Chem. 278: 51770-51778.
37. Malisauskas, M., Zamotin, V., Jass, J., Noppe, W., Dobson, C.M., and Morozova-Roche, L.A. 2003. 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. 330: 879-890.
38. Malmo, C., Vilasi, S., Iannuzzi, C., Tacchi, S., Cametti, C., Irace, G., and Sirangelo, I. 2006. Tetracycline inhibits W7FW14F apomyoglobin fibril extension and keeps the amyloid protein in a pre-fibrillar, highly cytotoxic state. FASEB J. 20: 346-347.
39. Marcon, G., Plakoutsi, G., Canale, C., Relini, A., Taddei, N., Dobson, C.M., Ramponi, G., and Chiti, F. 2005. Amyloid formation from HypF-N under conditions in which the protein is initially in its native state. J. Mol. Biol. 347: 323-335.
40. Nevskaya, N.A. and Chirgadze, Y.N. 1976. Infrared spectra and resonance interactions of amide-I and II vibration of α-helix. Biopolymers 15: 637-648.
41. Perutz, M.F., Finch, J.T., Berriman, J., and Lesk, A. 2002. Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. 99: 5591-5595.
42. Petkova, A.T., Ishii, Y., Balbach, J.J., Antzutkin, O.N., Leapman, R.D., Delaglio, F., and Tycko, R. 2002. A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl. Acad. Sci. 99: 16742-16747.
43. Pieri, P., Bucciantini, M., Nosi, D., Formigli, L., Savistchenko, J., Melki, R., and Stefani, M. 2006. The yeast prion Ure2p native-like assemblies are toxic to mammalian cells regardless of their aggregation state. J. Biol. Chem. 281: 15337-15344.
44. Plakoutsi, G., Taddei, N., Stefani, M., and Chiti, F. 2004. Aggregation of the Acylphosphatase from Sulfolobus solfataricus: The folded and partially unfolded states can both be precursors for amyloid formation. J. Biol. Chem. 279: 14111-14119.
45. Ramirez-Alvarado, M., Merkel, J.S., and Regan, L. 2000. A systematic exploration of the influence of the protein stability on amyloid fibril formation in vitro. Proc. Natl. Acad. Sci. 97: 8979-8984.
46. Relini, A., Torrasa, S., Rolandi, R., Ghiozzi, A., Rosano, C., Canale, C., Bolognesi, M., Plakoutski, G., Bucciantini, M., Chiti, F., et al. 2004. Monitoring the process of HypF fibrillization and liposome permeabilization by protofibrils. J. Mol. Biol. 338: 943-957.
47. Sambashivan, S., Liu, Y., Sawaya, M.R., Gingery, M., and Eisenberg, D. 2005. Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and native-like structure. Nature 437: 266-269.
48. Shirahama, T. and Cohen, A.S. 1967. High-resolution electron microscopic analysis of the amyloid fibril. J. Cell Biol. 33: 679-708.
49. Shirahama, T., Benson, M.D., Cohen, A.S., and Tanaka, A. 1973. Fibrillar assemblage of variable segments of immunoglobulin light chains: An electron microscopic study. J. Immunol. 110: 21-30.
50. Sigurdsson, E.M., Wisniewski, T., and Frangione, B. 2002. Infectivity of amyloid diseases. Trends Mol. Med. 8: 411-413.
51. Singer, S.J. and Dewji, N.N. 2006. Evidence that Perutz's double-β-stranded subunit structure for β-amyloids also applies to their channel-forming structures in membranes. Proc. Natl. Acad. Sci. 103: 1546-1550.
52. Sirangelo, I., Bismuto, E., and Irace, G. 1994. Solvent and thermal denaturation of the acidic compact state of apomyoglobin. FEBS Lett. 338: 11-15.
53. Sirangelo, I., Tavassi, S., Martelli, P.L., Casadio, R., and Irace, G. 2000. The effect of tryptophanyl substitution on folding and structure of myoglobin. Eur. J. Biochem. 267: 3937-3945.
54. Sirangelo, I., Malmo, C., Casillo, M., Mezzogiorno, A., Papa, M., and Irace, G. 2002. Tryptophanyl substitutions in apomyoglobin determine protein aggregation and amyloid-like fibril formation at physiological pH. J. Biol. Chem. 277: 45887-45891.
55. Sirangelo, I., Malmo, C., Iannuzzi, C., Mezzogiorno, A., Bianco, M.R., Papa, M., and Irace, G. 2004. Fibrillogenesis and cytotoxic activity of the amyloid-forming apomyoglobin mutant W7FW14F. J. Biol. Chem. 279: 13183-13189.
56. Smith, D.P., Jones, S., Serpell, L.C., Sunde, M., and Radford, S.E. 2003. A systematic investigation into the effect of protein destabilization on b 2-microglobulin amyloid formation. J. Mol. Biol. 330: 943-954.
57. Sreerama, N. and Woody, R.W. 2000. Estimation of protein secondary structure from dichroism circular spectra: Comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem. 287: 252-260.
58. Stefani, M. and Dobson, C.M. 2003. Protein aggregation and aggregate toxicity: New insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81: 678-699.
59. Sunde, M. and Blake, C.C. 1997. The structure of amyloid fibrils by electron microscopy and X-ray diffraction. Adv. Protein Chem. 50: 123-159.
60. Sunde, M. and Blake, C.C. 1998. From the globular to the fibrous state: Protein structure and structural conversion in amyloid formation. Q. Rev. Biophys. 31: 1-39.
61. Sunde, M., Serpell, L.C., Bartlam, M., Fraser, P.E., Pepys, M.B., and Blake, C.C. 1997. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273: 729-739.
62. Teale, F.W. 1959. Cleavage of the heme-protein link by acid methylethylketone. Biochim. Biophys. Acta 35: 543.
63. Torok, M., Milton, S., Kayed, R., Wu, P., McIntire, T., Glabe, C.G., and Langen, R. 2002. Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 277: 40810-40815.
64. Uversky, V.N. and Fink, A.L. 2001. Evidence for a partially folded intermediate in a synuclein fibril formation. J. Biol. Chem. 276: 10737-10744.
65. Uversky, V.N. and Fink, A.L. 2004. Conformational constraints for amyloid fibrillation: The importance of being unfolded. Biochim. Biophys. Acta 1698: 131-153.
66. Vilasi, S., Dosi, R., Iannuzzi, C., Malmo, C., Parente, A., Irace,G., and Sirangelo, I. 2006. Kinetics of amyloid aggregation of mammal apomyoglobins and correlation with their amino acid sequences. FEBS Lett. 580: 1681-1684.
67. Westermark, P., Benson, M.D., Buxbaum, J.N., Cohen, A.S., Frangione, B., Iked, S., Masters, C.L., Merlini, G., Saraiva, M.J., and Sipe, J.D. 2002. Amyloid fibril protein nomenclature-2002. Amyloid 9: 197-200.
68. Wetzel, R. 2002. Ideas of order for amyloid fibril structure. Structure 10: 1031-1036.
69. Zandomeneghi, G., Krebs, M.R.H., McCammon, M.G., and Fandrich, M. 2004. FTIR reveals differences between native β-sheet proteins and amyloid fibrils. Protein Sci. 13: 3314-3321.