Inclusion bodies: Specificity in their aggregation process and amyloid-like structure

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 10, 2008, Pages 1815-1825

  Morell, Montse ^a   Bravo, Ramona ^b   Espargaró, Alba ^a   Sisquella, Xavier ^b   Avilés, Francesc X ^a   Fernàndez Busquets, Xavier ^b   Ventura, Salvador ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

Author keywords

Amyloid fibrils; Conformational diseases; Inclusion bodies; Protein aggregation; Protein folding

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; PROTEIN VP1;

ANIMAL CELL; ARTICLE; CELL INCLUSION; EUKARYOTIC CELL; FOOT AND MOUTH DISEASE VIRUS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTIC CELL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN STRUCTURE; STRUCTURAL PROTEOMICS; ULTRASTRUCTURE;

AMYLOID BETA-PROTEIN; ESCHERICHIA COLI; INCLUSION BODIES; KINETICS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; PEPTIDE FRAGMENTS; PROTEIN BINDING; SUBSTRATE SPECIFICITY;

FOOT-AND-MOUTH DISEASE VIRUS; MIRIDAE; PROKARYOTA;

EID: 51049095117     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.06.007     Document Type: Article

References (60)

1. Chiti F., and Dobson C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75 (2006) 333-366
2. Wickner S., Maurizi M.R., and Gottesman S. Posttranslational quality control: folding, refolding, and degrading proteins. Science 286 (1999) 1888-1893
3. Kopito R.R. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10 (2000) 524-530
4. Ventura S., and Villaverde A. Protein quality in bacterial inclusion bodies. Trends Biotechnol. 24 (2006) 179-185
5. Speed M.A., Wang D.I., and King J. Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat. Biotechnol. 14 (1996) 1283-1287
6. Jones E.M., and Surewicz W.K. Fibril conformation as the basis of species-and strain-dependent seeding specificity of mammalian prion amyloids. Cell 121 (2005) 63-72
7. Bukau B., Weissman J., and Horwich A. Molecular chaperones and protein quality control. Cell 125 (2006) 443-451
8. Luheshi L.M., Tartaglia G.G., Brorsson A.C., Pawar A.P., Watson I.E., Chiti F., Vendruscolo M., Lomas D.A., Dobson C.M., and Crowther D.C. Systematic in vivo analysis of the intrinsic determinants of amyloid beta pathogenicity. PLoS Biol. 5 (2007) e290
9. Rajan R.S., Illing M.E., Bence N.F., and Kopito R.R. Specificity in intracellular protein aggregation and inclusion body formation. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 13060-13065
10. Johnston J.A., Ward C.L., and Kopito R.R. Aggresomes: a cellular response to misfolded proteins. J. Cell Biol. 143 (1998) 1883-1898
11. Garcia-Fruitos E., Gonzalez-Montalban N., Morell M., Vera A., Ferraz R., Aris A., Ventura S., and Villaverde A. Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb. Cell Fact. 4 (2005) 27
12. Nelson R., and Eisenberg D. Structural models of amyloid-like fibrils. Adv. Protein Chem. 73 (2006) 235-282
13. Ami D., Natalello A., Taylor G., Tonon G., and Maria Doglia S. Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochim. Biophys. Acta 1764 (2006) 793-799
14. Carrio M., Gonzalez-Montalban N., Vera A., Villaverde A., and Ventura S. Amyloid-like properties of bacterial inclusion bodies. J. Mol. Biol. 347 (2005) 1025-1037
15. Schrodel A., and de Marco A. Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC Biochem. 6 (2005) 10
16. Wurth C., Guimard N.K., and Hecht M.H. Mutations that reduce aggregation of the Alzheimer's Abeta42 peptide: an unbiased search for the sequence determinants of Abeta amyloidogenesis. J. Mol. Biol. 319 (2002) 1279-1290
17. Garcia-Fruitos E., Gonzalez-Montalban N., Morell M., Vera A., Ferraz R.M., Aris A., Ventura S., and Villaverde A. Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb. Cell Fact. 4 (2005) 27
18. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
19. Carrio M.M., Cubarsi R., and Villaverde A. Fine architecture of bacterial inclusion bodies. FEBS Lett. 471 (2000) 7-11
20. de Groot N.S., and Ventura S. Effect of temperature on protein quality in bacterial inclusion bodies. FEBS Lett. (2006)
21. Sabate R., Gallardo M., and Estelrich J. An autocatalytic reaction as a model for the kinetics of the aggregation of beta-amyloid. Biopolymers 71 (2003) 190-195
22. Idicula-Thomas S., and Balaji P.V. Correlation between the structural stability and aggregation propensity of proteins. In. Silico Biol. 7 (2007) 0023
23. Ventura S. Sequence determinants of protein aggregation: tools to increase protein solubility. Microb. Cell Fact. 4 (2005) 11
24. Pfleger K.D., and Eidne K.A. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat. Methods 3 (2006) 165-174
25. Heim R., Cubitt A.B., and Tsien R.Y. Improved green fluorescence. Nature 373 (1995) 663-664
26. Anikovsky M., Dale L., Ferguson S., and Petersen N. Resonance energy transfer in cells: a new look at fixation effect and receptor aggregation on cell membrane. Biophys. J. (2008)
27. Conchillo-Sole O., de Groot N.S., Aviles F.X., Vendrell J., Daura X., and Ventura S. AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8 (2007) 65
28. Fernandez-Escamilla A.M., Rousseau F., Schymkowitz J., and Serrano L. Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 22 (2004) 1302-1306
29. Sharpe S., Yau W.M., and Tycko R. Expression and purification of a recombinant peptide from the Alzheimer's beta-amyloid protein for solid-state NMR. Protein Expr. Purif. 42 (2005) 200-210
30. West M.W., Wang W., Patterson J., Mancias J.D., Beasley J.R., and Hecht M.H. De novo amyloid proteins from designed combinatorial libraries. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 11211-11216
31. Wigley W.C., Stidham R.D., Smith N.M., Hunt J.F., and Thomas P.J. Protein solubility and folding monitored in vivo by structural complementation of a genetic marker protein. Nature Biotechnol. 19 (2001) 1131-1136
32. Wang W., and Hecht M.H. Rationally designed mutations convert de novo amyloid-like fibrils into soluble monomeric beta-sheet proteins. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 2760-2765
33. Hammarstrom P., Sekijima Y., White J.T., Wiseman R.L., Lim A., Costello C.E., Altland K., Garzuly F., Budka H., and Kelly J.W.Y. D18G transthyretin is monomeric, aggregation prone, and not detectable in plasma and cerebrospinal fluid: a prescription for central nervous system amyloidosis?. Biochemistry 42 (2003) 6656-6663
34. de Groot N.S., and Ventura S. Effect of temperature on protein quality in bacterial inclusion bodies. FEBS Lett. 580 (2006) 6471-6476
35. Baxa U., Speransky V., Steven A.C., and Wickner R.B. Mechanism of inactivation on prion conversion of the Saccharomyces cerevisiae Ure2 protein. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 5253-5260
36. Hamada D., Tsumoto K., Sawara M., Tanaka N., Nakahira K., Shiraki K., and Yanagihara I. Effect of an amyloidogenic sequence attached to yellow fluorescent protein. Proteins (2008)
37. Sondheimer N., and Lindquist S. Rnq1: an epigenetic modifier of protein function in yeast. Mol. Cell 5 (2000) 163-172
38. Wilson L.M., Mok Y.F., Binger K.J., Griffin M.D., Mertens H.D., Lin F., Wade J.D., Gooley P.R., and Howlett G.J. A structural core within apolipoprotein C-II amyloid fibrils identified using hydrogen exchange and proteolysis. J. Mol. Biol. 366 (2007) 1639-1651
39. Ban T., Yamaguchi K., and Goto Y. Direct observation of amyloid fibril growth, propagation, and adaptation. Acc. Chem. Res. 39 (2006) 663-670
40. Mukai H., Isagawa T., Goyama E., Tanaka S., Bence N.F., Tamura A., Ono Y., and Kopito R.R. Formation of morphologically similar globular aggregates from diverse aggregation-prone proteins in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10887-10892
41. Kim S., Nollen E.A., Kitagawa K., Bindokas V.P., and Morimoto R.I. Polyglutamine protein aggregates are dynamic. Nat. Cell Biol. 4 (2002) 826-831
42. Arimon M., Diez-Perez I., Kogan M.J., Durany N., Giralt E., Sanz F., and Fernandez-Busquets X. Fine structure study of Abeta1-42 fibrillogenesis with atomic force microscopy. FASEB J. 19 (2005) 1344-1346
43. Fink A.L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des. 3 (1998) R9-23
44. Hiramatsu H., and Kitagawa T. FT-IR approaches on amyloid fibril structure. Biochim. Biophys. Acta 1753 (2005) 100-107
45. Sabate R., and Saupe S.J. Thioflavin T fluorescence anisotropy: an alternative technique for the study of amyloid aggregation. Biochem. Biophys. Res. Commun. 360 (2007) 135-138
46. Espargaro A., Castillo V., de Groot N.S., and Ventura S. The in vivo and in vitro aggregation properties of globular proteins correlate with their conformational stability: the SH3 case. J. Mol. Biol. 378 (2008) 1116-1131
47. Hinz J., Gierasch L.M., and Ignatova Z. Orthogonal cross-seeding: an approach to explore protein aggregates in living cells. Biochemistry 47 (2008) 4196-4200
48. Bulone D., Masino L., Thomas D.J., San Biagio P.L., and Pastore A. The interplay between PolyQ and protein context delays aggregation by forming a reservoir of protofibrils. PLoS. ONE 1 (2006) e111
49. Kryndushkin D.S., Alexandrov I.M., Ter-Avanesyan M.D., and Kushnirov V.V. Yeast [PSI+] prion aggregates are formed by small Sup35 polymers fragmented by Hsp104. J. Biol. Chem. 278 (2003) 49636-49643
50. Takahashi R.H., Almeida C.G., Kearney P.F., Yu F., Lin M.T., Milner T.A., and Gouras G.K. Oligomerization of Alzheimer's beta-amyloid within processes and synapses of cultured neurons and brain. J. Neurosci. 24 (2004) 3592-3599
51. Bagriantsev S., and Liebman S. Modulation of Abeta42 low-n oligomerization using a novel yeast reporter system. BMC Biol. 4 (2006) 32
52. Perutz M.F., and Windle A.H. Cause of neural death in neurodegenerative diseases attributable to expansion of glutamine repeats. Nature 412 (2001) 143-144
53. Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases. Nat. Cell Biol. 6 (2004) 1054-1061
54. Krebs M.R., Morozova-Roche L.A., Daniel K., Robinson C.V., and Dobson C.M. Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein Sci. 13 (2004) 1933-1938
55. Mitsui K., Nakayama H., Akagi T., Nekooki M., Ohtawa K., Takio K., Hashikawa T., and Nukina N. Purification of polyglutamine aggregates and identification of elongation factor-1alpha and heat shock protein 84 as aggregate-interacting proteins. J. Neurosci. 22 (2002) 9267-9277
56. Hazeki N., Tsukamoto T., Yazawa I., Koyama M., Hattori S., Someki I., Iwatsubo T., Nakamura K., Goto J., and Kanazawa I. Ultrastructure of nuclear aggregates formed by expressing an expanded polyglutamine. Biochem. Biophys. Res. Commun. 294 (2002) 429-440
57. Saudou F., Finkbeiner S., Devys D., and Greenberg M.E. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95 (1998) 55-66
58. Walsh D.M., and Selkoe D.J. A beta oligomers-a decade of discovery. J. Neurochem. 101 (2007) 1172-1184
59. Lindner A.B., Madden R., Demarez A., Stewart E.J., and Taddei F. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 3076-3081
60. Solomon A., Richey T., Murphy C.L., Weiss D.T., Wall J.S., Westermark G.T., and Westermark P. Amyloidogenic potential of foie gras. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 10998-11001