Evolutionary selection for protein aggregation

Biochemical Society Transactions

Volumn 40, Issue 5, 2012, Pages 1032-1037

  De Groot, Natalia Sanchez ^a   Torrent, Marc ^a   Villar Piqué, Anna ^b   Lang, Benjamin ^a   Ventura, Salvador ^b   Gsponer, Jörg ^c   Babu, M Madan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Amyloid; Chaperone; Evolution; Protein aggregation

Indexed keywords

PROTEOME;

AMINO ACID SEQUENCE; HUMAN; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

PROTEIN BINDING; PROTEIN FOLDING; PROTEINS; SELECTION, GENETIC;

EID: 84866692230     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20120160     Document Type: Review

References (75)

1. Chiti, F. and Dobson, C.M. (2006) Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366
2. Buxbaum, J.N. and Linke, R.P. (2012) A molecular history of the amyloidoses. J. Mol. Biol. 421, 142-159
3. Gregersen, N., Bross, P., Vang, S. and Christensen, J.H. (2006) Protein misfolding and human disease. Annu. Rev. Genomics Hum. Genet. 7, 103-124
4. Olzscha, H., Schermann, S.M., Woerner, A.C., Pinkert, S., Hecht, M.H., Tartaglia, G.G., Vendruscolo, M., Hayer-Hartl, M., Hartl, F.U. and Vabulas, R.M. (2011) Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144, 67-78
5. Xu, J., Reumers, J., Couceiro, J.R., De Smet, F., Gallardo, R., Rudyak, S., Cornelis, A., Rozenski, J., Zwolinska, A., Marine, J.C. et al. (2011) Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nat. Chem. Biol. 7, 285-295
6. Eisenberg, D. and Jucker, M. (2012) The amyloid state of proteins in human diseases. Cell 148, 1188-1203
7. Eichner, T. and Radford, S.E. (2011) A diversity of assembly mechanisms of a generic amyloid fold. Mol. Cell 43, 8-18
8. Fowler, D.M., Koulov, A.V., Balch, W.E. and Kelly, J.W. (2007) Functional amyloid: from bacteria to humans. Trends Biochem. Sci. 32, 217-224
9. Gershenson, A. and Gierasch, L.M. (2011) Protein folding in the cell: challenges and progress. Curr. Opin. Struct. Biol. 21, 32-41
10. Hartl, F.U., Bracher, A. and Hayer-Hartl, M. (2011) Molecular chaperones in protein folding and proteostasis. Nature 475, 324-332
11. De Baets, G., Reumers, J., Delgado Blanco, J., Dopazo, J., Schymkowitz, J. and Rousseau, F. (2011) An evolutionary trade-off between protein turnover rate and protein aggregation favors a higher aggregation propensity in fast degrading proteins. PLoS Comput. Biol. 7, e1002090
12. Chiti, F., Stefani, M., Taddei, N., Ramponi, G. and Dobson, C.M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 424, 805-808
13. Ventura, S., Zurdo, J., Narayanan, S., Parreno, M., Mangues, R., Reif, B., Chiti, F., Giannoni, E., Dobson, C.M., Aviles, F.X. and Serrano, L. (2004) Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case. Proc. Natl. Acad. Sci. U.S.A. 101, 7258-7263
14. Buell, A.K., Tartaglia, G.G., Birkett, N.R., Waudby, C.A., Vendruscolo, M., Salvatella, X., Welland, M.E., Dobson, C.M. and Knowles, T.P. (2009) Position-dependent electrostatic protection against protein aggregation. ChemBioChem 10, 1309-1312
15. Monsellier, E., Ramazzotti, M., Taddei, N. and Chiti, F. (2008) Aggregation propensity of the human proteome. PLoS Comput. Biol. 4, e1000199
16. Rousseau, F., Serrano, L. and Schymkowitz, J.W. (2006) How evolutionary pressure against protein aggregation shaped chaperone specificity. J. Mol. Biol. 355, 1037-1047
17. Broome, B.M. and Hecht, M.H. (2000) Nature disfavors sequences of alternating polar and non-polar amino acids: implications for amyloidogenesis. J. Mol. Biol. 296, 961-968
18. Lim, W.A. and Sauer, R.T. (1991) The role of internal packing interactions in determining the structure and stability of a protein. J. Mol. Biol. 219, 359-376
19. Monsellier, E., Ramazzotti, M., de Laureto, P.P., Tartaglia, G.G., Taddei, N., Fontana, A., Vendruscolo, M. and Chiti, F. (2007) The distribution of residues in a polypeptide sequence is a determinant of aggregation optimized by evolution. Biophys. J. 93, 4382-4391
20. Sanchez, I.E., Tejero, J., Gomez-Moreno, C., Medina, M. and Serrano, L. (2006) Point mutations in protein globular domains: contributions from function, stability and misfolding. J. Mol. Biol. 363, 422-432
21. Pechmann, S., Levy, E.D., Tartaglia, G.G. and Vendruscolo, M. (2009) Physicochemical principles that regulate the competition between functional and dysfunctional association of proteins. Proc. Natl. Acad. Sci. U.S.A. 106, 10159-10164
22. Castillo, V. and Ventura, S. (2009) Amyloidogenic regions and interaction surfaces overlap in globular proteins related to conformational diseases. PLoS Comput. Biol. 5, e1000476
23. Bershtein, S., Mu, W. and Shakhnovich, E.I. (2012) Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc. Natl. Acad. Sci. U.S.A. 109, 4857-4862
24. Vidal, O., Longin, R., Prigent-Combaret, C., Dorel, C., Hooreman, M. and Lejeune, P. (1998) Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J. Bacteriol. 180, 2442-2449
25. Claessen, D., Rink, R., de Jong, W., Siebring, J., de Vreugd, P., Boersma, F.G., Dijkhuizen, L. and Wosten, H.A. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev. 17, 1714-1726
26. Kenney, J.M., Knight, D., Wise, M.J. and Vollrath, F. (2002) Amyloidogenic nature of spider silk. Eur. J. Biochem. 269, 4159-4163
27. Smith, J.F., Knowles, T.P., Dobson, C.M., Macphee, C.E. and Welland, M.E. (2006) Characterization of the nanoscale properties of individual amyloid fibrils. Proc. Natl. Acad. Sci. U.S.A. 103, 15806-15811
28. Blum, E.S., Abraham, M.C., Yoshimura, S., Lu, Y. and Shaham, S. (2012) Control of nonapoptotic developmental cell death in Caenorhabditis elegans by a polyglutamine-repeat protein. Science 335, 970-973
29. Fowler, D.M., Koulov, A.V., Alory-Jost, C., Marks, M.S., Balch, W.E. and Kelly, J.W. (2006) Functional amyloid formation within mammalian tissue. PLoS Biol. 4, e6
30. Gilks, N., Kedersha, N., Ayodele, M., Shen, L., Stoecklin, G., Dember, L.M. and Anderson, P. (2004) Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 15, 5383-5398
31. Maji, S.K., Perrin, M.H., Sawaya, M.R., Jessberger, S., Vadodaria, K., Rissman, R.A., Singru, P.S., Nilsson, K.P., Simon, R., Schubert, D. et al. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules. Science 325, 328-332
32. Li, J., McQuade, T., Siemer, A.B., Napetschnig, J., Moriwaki, K., Hsiao, Y.S., Damko, E., Moquin, D., Walz, T., McDermott, A. et al. (2012) The RIP1/RIP3 necrosome forms a functional amyloid signalling complex required for programmed necrosis. Cell 150, 339-350
33. Torrent, M., Valle, J., Nogues, M.V., Boix, E. and Andreu, D. (2011) The generation of antimicrobial peptide activity: a trade-off between charge and aggregation? Angew. Chem. Int. Ed. 50, 10686-10689
34. Torrent, M., Andreu, D., Nogues, V.M. and Boix, E. (2011) Connecting peptide physicochemical and antimicrobial properties by a rational prediction model. PLoS ONE 6, e16968
35. Kagan, B.L., Jang, H., Capone, R., Teran Arce, F., Ramachandran, S., Lal, R. and Nussinov, R. (2012) Antimicrobial properties of amyloid peptides. Mol. Pharm. 9, 708-717
36. Torrent, M., Sanchez, D., Buzon, V., Nogues, M.V., Cladera, J. and Boix, E. (2009) Comparison of the membrane interaction mechanism of two antimicrobial RNases: RNase 3/ECP and RNase 7. Biochim. Biophys. Acta 1788, 1116-1125
37. Shorter, J. and Lindquist, S. (2005) Prions as adaptive conduits of memory and inheritance. Nat. Rev. Genet. 6, 435-450
38. Wiltzius, J.J., Landau, M., Nelson, R., Sawaya, M.R., Apostol, M.I., Goldschmidt, L., Soriaga, A.B., Cascio, D., Rajashankar, K. and Eisenberg, D. (2009) Molecular mechanisms for protein-encoded inheritance. Nat. Struct. Mol. Biol. 16, 973-978
39. Halfmann, R., Alberti, S. and Lindquist, S. (2010) Prions, protein homeostasis, and phenotypic diversity. Trends Cell Biol. 20, 125-133
40. Suzuki, G., Shimazu, N. and Tanaka, M. (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress. Science 336, 355-359
41. Majumdar, A., Cesario, W.C., White-Grindley, E., Jiang, H., Ren, F., Khan, M.R., Li, L., Choi, E.M., Kannan, K., Guo, F. et al. (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148, 515-529
42. Conchillo-Sole, O., de Groot, N.S., Aviles, F.X., Vendrell, J., Daura, X. and Ventura, S. (2007) AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8, 65
43. Chen, Y. and Dokholyan, N.V. (2008) Natural selection against protein aggregation on self-interacting and essential proteins in yeast, fly, and worm. Mol. Biol. Evol. 25, 1530-1533
44. de Groot, N.S. and Ventura, S. (2010) Protein aggregation profile of the bacterial cytosol. PLoS ONE 5, e9383
45. Gsponer, J. and Babu, M.M. (2009) The rules of disorder or why disorder rules. Prog. Biophys. Mol. Biol. 99, 94-103
46. Kurnik, M., Hedberg, L., Danielsson, J. and Oliveberg, M. (2012) Folding without charges. Proc. Natl. Acad. Sci. U.S.A. 109, 5705-5710
47. Masino, L., Nicastro, G., Calder, L., Vendruscolo, M. and Pastore, A. (2011) Functional interactions as a survival strategy against abnormal aggregation. FASEB J. 25, 45-54
48. Chiti, F. and Dobson, C.M. (2009) Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-22
49. Tzotzos, S. and Doig, A.J. (2010) Amyloidogenic sequences in native protein structures. Protein Sci. 19, 327-348
50. Pastore, A. and Temussi, P.A. (2012) The two faces of Janus: functional interactions and protein aggregation. Curr. Opin. Struct. Biol. 22, 30-37
51. Dehay, B. and Bertolotti, A. (2006) Critical role of the proline-rich region in huntingtin for aggregation and cytotoxicity in yeast. J. Biol. Chem. 281, 35608-35615
52. Hurshman Babbes, A.R., Powers, E.T. and Kelly, J.W. (2008) Quantification of the thermodynamically linked quaternary and tertiary structural stabilities of transthyretin and its disease-associated variants: the relationship between stability and amyloidosis. Biochemistry 47, 6969-6984
53. Munch, C. and Bertolotti, A. (2010) Exposure of hydrophobic surfaces initiates aggregation of diverse ALS-causing superoxide dismutase-1 mutants. J. Mol. Biol. 399, 512-525
54. Harper, J.D. and Lansbury, Jr, P.T. (1997) 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. 66, 385-407
55. Pappu, R.V., Wang, X., Vitalis, A. and Crick, S.L. (2008) A polymer physics perspective on driving forces and mechanisms for protein aggregation. Arch. Biochem. Biophys. 469, 132-141
56. Cohen, S.I., Vendruscolo, M., Dobson, C.M. and Knowles, T.P. (2012) From macroscopic measurements to microscopic mechanisms of protein aggregation. J. Mol. Biol. 421, 160-171
57. Wickner, S., Maurizi, M.R. and Gottesman, S. (1999) Posttranslational quality control: folding, refolding, and degrading proteins. Science 286, 1888-1893
58. Balch, W.E., Morimoto, R.I., Dillin, A. and Kelly, J.W. (2008) Adapting proteostasis for disease intervention. Science 319, 916-919
59. Tartaglia, G.G., Pechmann, S., Dobson, C.M. and Vendruscolo, M. (2007) Life on the edge: a link between gene expression levels and aggregation rates of human proteins. Trends Biochem. Sci. 32, 204-206
60. Krohn, M., Lange, C., Hofrichter, J., Scheffler, K., Stenzel, J., Steffen, J., Schumacher, T., Bruning, T., Plath, A.S., Alfen, F. et al. (2011) Cerebral amyloid-β proteostasis is regulated by the membrane transport protein ABCC1 in mice. J. Clin. Invest. 121, 3924-3931
61. Roth, D.M. and Balch, W.E. (2011) Modeling general proteostasis: proteome balance in health and disease. Curr. Opin. Cell Biol. 23, 126-134
62. Chen, B., Retzlaff, M., Roos, T. and Frydman, J. (2011) Cellular strategies of protein quality control. Cold Spring Harbor Perspect. Biol. 3, a004374
63. Kaganovich, D., Kopito, R. and Frydman, J. (2008) Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095
64. Bandyopadhyay, A., Saxena, K., Kasturia, N., Dalal, V., Bhatt, N., Rajkumar, A., Maity, S., Sengupta, S. and Chakraborty, K. (2012) Chemical chaperones assist intracellular folding to buffer mutational variations. Nat. Chem. Biol. 8, 238-245
65. Williams, T.A. and Fares, M.A. (2010) The effect of chaperonin buffering on protein evolution. Genome Biol. Evol. 2, 609-619
66. Tokuriki, N. and Tawfik, D.S. (2009) Chaperonin overexpression promotes genetic variation and enzyme evolution. Nature 459, 668-673
67. Rousseau, E., Kojima, R., Hoffner, G., Djian, P. and Bertolotti, A. (2009) Misfolding of proteins with a polyglutamine expansion is facilitated by proteasomal chaperones. J. Biol. Chem. 284, 1917-1929
68. Murray, A.N., Solomon, J.P., Wang, Y.J., Balch, W.E. and Kelly, J.W. (2010) Discovery and characterization of a mammalian amyloid disaggregation activity. Protein Sci. 19, 836-846
69. Glover, J.R. and Lindquist, S. (1998) Hsp104, Hsp70, and Hsp40: a novel chaperone system that rescues previously aggregated proteins. Cell 94, 73-82
70. Taylor, R.C. and Dillin, A. (2011) Aging as an event of proteostasis collapse. Cold Spring Harbor Perspect. Biol. 3, a004440
71. Rubinsztein, D.C. (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature 443, 780-786
72. Lindner, A.B., Madden, R., Demarez, A., Stewart, E.J. and Taddei, F. (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl. Acad. Sci. U.S.A. 105, 3076-3081
73. Calamini, B., Silva, M.C., Madoux, F., Hutt, D.M., Khanna, S., Chalfant, M.A., Saldanha, S.A., Hodder, P., Tait, B.D., Garza, D. et al. (2012) Small-molecule proteostasis regulators for protein conformational diseases. Nat. Chem. Biol. 8, 185-196
74. Sivakolundu, S.G., Nourse, A., Moshiach, S., Bothner, B., Ashley, C., Satumba, J., Lahti, J. and Kriwacki, R.W. (2008) Intrinsically unstructured domains of Arf and Hdm2 form bimolecular oligomeric structures in vitro and in vivo. J. Mol. Biol. 384, 240-254
75. Drummond, D.A. and Wilke, C.O. (2008) Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134, 341-352