Prevention of Amyloid-like Aggregation As a Driving Force of Protein Evolution

Overview

Journal EMBO Rep

Specialty Molecular Biology

Date 2007 Aug 2

PMID 17668004

Citations 110

Authors

Elodie Monsellier

Fabrizio Chiti

Affiliations

Soon will be listed here.

Abstract

Uncontrolled protein aggregation is a constant challenge in all compartments of living organisms. The failure of a peptide or protein to remain soluble often results in pathology. So far, more than 40 human diseases have been associated with the formation of extracellular fibrillar aggregates - known as amyloid fibrils - or structurally related intracellular deposits. It is well known that molecular chaperones and elaborate quality control mechanisms exist in the cell to counteract aggregation. However, an increasing number of reports during the past few years indicate that proteins have also evolved structural and sequence-based strategies to prevent aggregation. This review describes these strategies and the selection pressures that exist on protein sequences to combat their uncontrolled aggregation. We will describe the different types of mechanism evolved by proteins that adopt different conformational states including normally folded proteins, intrinsically disordered polypeptide chains, elastomeric systems and multimodular proteins.

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References

Broome B, Hecht M . Nature disfavors sequences of alternating polar and non-polar amino acids: implications for amyloidogenesis. J Mol Biol. 2000; 296(4):961-8. DOI: 10.1006/jmbi.2000.3514. View

Bouchard M, Zurdo J, Nettleton E, Dobson C, Robinson C . Formation of insulin amyloid fibrils followed by FTIR simultaneously with CD and electron microscopy. Protein Sci. 2000; 9(10):1960-7. PMC: 2144465. DOI: 10.1110/ps.9.10.1960. View

Schwartz R, Istrail S, King J . Frequencies of amino acid strings in globular protein sequences indicate suppression of blocks of consecutive hydrophobic residues. Protein Sci. 2001; 10(5):1023-31. PMC: 2374206. DOI: 10.1110/ps.33201. View

Richardson J, Richardson D . Natural beta-sheet proteins use negative design to avoid edge-to-edge aggregation. Proc Natl Acad Sci U S A. 2002; 99(5):2754-9. PMC: 122420. DOI: 10.1073/pnas.052706099. View

Uversky V . Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 2002; 11(4):739-56. PMC: 2373528. DOI: 10.1110/ps.4210102. View

Canet D, Last A, Tito P, Sunde M, Spencer A, Archer D . Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme. Nat Struct Biol. 2002; 9(4):308-15. DOI: 10.1038/nsb768. View

Steward A, Adhya S, Clarke J . Sequence conservation in Ig-like domains: the role of highly conserved proline residues in the fibronectin type III superfamily. J Mol Biol. 2002; 318(4):935-40. DOI: 10.1016/S0022-2836(02)00184-5. View

Bousset L, Thomson N, Radford S, Melki R . The yeast prion Ure2p retains its native alpha-helical conformation upon assembly into protein fibrils in vitro. EMBO J. 2002; 21(12):2903-11. PMC: 126058. DOI: 10.1093/emboj/cdf303. View

Tompa P . Intrinsically unstructured proteins. Trends Biochem Sci. 2002; 27(10):527-33. DOI: 10.1016/s0968-0004(02)02169-2. View

10.

Mandel-Gutfreund Y, Gregoret L . On the significance of alternating patterns of polar and non-polar residues in beta-strands. J Mol Biol. 2002; 323(3):453-61. DOI: 10.1016/s0022-2836(02)00973-7. View

11.

Hammarstrom P, Jiang X, Hurshman A, Powers E, Kelly J . Sequence-dependent denaturation energetics: A major determinant in amyloid disease diversity. Proc Natl Acad Sci U S A. 2002; 99 Suppl 4:16427-32. PMC: 139904. DOI: 10.1073/pnas.202495199. View

12.

Chiti F, Calamai M, Taddei N, Stefani M, Ramponi G, Dobson C . Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proc Natl Acad Sci U S A. 2002; 99 Suppl 4:16419-26. PMC: 139903. DOI: 10.1073/pnas.212527999. View

13.

Stefani M, Dobson C . Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med (Berl). 2003; 81(11):678-99. DOI: 10.1007/s00109-003-0464-5. View

14.

Laurine E, Gregoire C, Fandrich M, Engemann S, Marchal S, Thion L . Lithostathine quadruple-helical filaments form proteinase K-resistant deposits in Creutzfeldt-Jakob disease. J Biol Chem. 2003; 278(51):51770-8. DOI: 10.1074/jbc.M306767200. View

15.

Dobson C . Protein folding and misfolding. Nature. 2003; 426(6968):884-90. DOI: 10.1038/nature02261. View

16.

Hamada D, Yanagihara I, Tsumoto K . Engineering amyloidogenicity towards the development of nanofibrillar materials. Trends Biotechnol. 2004; 22(2):93-7. DOI: 10.1016/j.tibtech.2003.12.003. View

17.

Xia Y, Levitt M . Simulating protein evolution in sequence and structure space. Curr Opin Struct Biol. 2004; 14(2):202-7. DOI: 10.1016/j.sbi.2004.03.001. View

18.

Uversky V, Fink A . Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta. 2004; 1698(2):131-53. DOI: 10.1016/j.bbapap.2003.12.008. View

19.

Pedersen J, Christensen G, Otzen D . Modulation of S6 fibrillation by unfolding rates and gatekeeper residues. J Mol Biol. 2004; 341(2):575-88. DOI: 10.1016/j.jmb.2004.06.020. View

20.

Rajagopal K, Schneider J . Self-assembling peptides and proteins for nanotechnological applications. Curr Opin Struct Biol. 2004; 14(4):480-6. DOI: 10.1016/j.sbi.2004.06.006. View