Sequence determinants of protein aggregation: Tools to increase protein solubility

Microbial Cell Factories

Volumn 4, Issue , 2005, Pages

  Ventura, Salvador ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; BACTERIAL PROTEIN; POLYPEPTIDE; RECOMBINANT PROTEIN;

BACTERIAL CELL; BIOTECHNOLOGY; CELL INCLUSION; ESCHERICHIA COLI; NONHUMAN; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; SEQUENCE ANALYSIS; SOLUBILIZATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 26844498710     PISSN: 14752859     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-4-11     Document Type: Review

References (106)

1. Smith A: Protein misfolding. Nature 2003, 426:883.
2. Dobson CM: Protein folding and misfolding. Nature 2003, 426:884-890.
3. Rochet JC, Lansbury PT Jr: Amyloid fibrillogenesis: themes and variations. Curr Opin Struct Biol 2000, 10:60-68.
4. Cohen FE, Kelly JW: Therapeutic approaches to protein-misfolding diseases. Nature 2003, 426:905-909.
5. Morimoto R, Tissieres A, Georgopoulos C: The Biology of Heat Shock Proteins and Molecular Chaperones. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY; 1994.
6. Weibezahn J, Tessarz P, Schlieker C, Zahn R, Maglica Z, Lee S, Zentgraf H, Weber-Ban EU, Dougan DA, Tsai FT, Mogk A, Bukau B: Thermotolerance requires refolding of aggregated proteins by substrate translocation through the central pore of ClpB. Cell 2004, 119:653-65.
7. Marston FA: The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem J 1986, 40:1-12.a2.
8. Georgiou G, Telford JN, Shuler ML, Wilson DB: Localization of inclusion bodies in Escherichia coli overproducing beta-lactamase or alkaline phosphatase. Appl Environ Microbiol 1986, 52:1157-61.
9. Georgiou G, Valax P: Expression of correctly folded proteins in Escherichia coli. Curr Opin Biotechnol 1996, 7:190-197.
10. Baneyx F: Recombinant protein expression in Escherichia coli. Curr Opin Biotechnol 1999, 10:411-421.
11. Georgiou G, Valax P: Isolating inclusion bodies from bacteria. Methods Enzymol 1999, 309:48-58.
12. Stefani M: Protein misfolding and aggregation: new examples in medicine and biology of the dark side of the protein world. Biochim Biophys Acta 2004, 1739:5-25.
13. Ross CA, Poirier MA: Protein aggregation and neurodegenerative disease. Nat Med 2004, 10:S10-7.
14. Dobson CM: Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 2004, 15:3-16.
15. Ohnishi S, Takano K: Amyloid fibrils from the viewpoint of protein folding. Cell Mol Life Sci 2004, 61:511-24.
16. Lee HG, Petersen RB, Zhu X, Honda K, Aliev G, Smith MA, Perry G: Will preventing protein aggregates live up to its promise as prophylaxis against neurodegenerative diseases? Brain Pathol 2003, 13:630-8.
17. Cabrita LD, Bottomley SP: Protein expression and refolding - A practical guide to getting the most out of inclusion bodies. Biotechnol Annu Rev 2004, 10:31-50.
18. Fahnert B, Lilie H, Neubauer P: Inclusion bodies: formation and utilisation. Adv Biochem Eng Biotechnol 2004, 89:93-142.
19. Villaverde A, Carrio MM: Protein aggregation in recombinant bacteria: biological role of inclusion bodies. Biotechnol Lett 2003, 25:1385-95.
20. Dobson CM: Protein-misfolding diseases: Getting out of shape. Nature 2002, 418:729-730.
21. Ventura S, Lacroix E, Serrano L: Insights into the origin of the tendency of the PI3-SH3 domain to form amyloid fibrils. J Mol Biol 2002, 322:1147-58.
22. Williams DC, Van Frank RM, Muth WL, Burnett JP: Cytoplasmic inclusion bodies in Escherichia coli producing biosynthetic human insulin proteins. Science 1982, 215:687-9.
23. Kundu B, Guptasarma P: Use of a hydrophobic dye to indirectly probe the structural organization and conformational plasticity of molecules in amorphous aggregates of carbonic anhydrase. Biochem Biophys Res Commun 2002, 293:572-7.
24. Chiti F, Calamai M, Taddei N, Stefani M, Ramponi G, Dobson CM: 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.
25. Chiti F, Stefani M, Taddei N, Ramponi G, Dobson CM: Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 2003, 424:805-8.
26. Chiti F, Taddei N, Baroni F, Capanni C, Stefani M, Ramponi G, Dobson CM: Kinetic partitioning of protein folding and aggregation. Nat Struct Biol 2002, 9:137-43.
27. Carrio M, Gonzalez-Montalban N, Vera A, Villaverde A, Ventura S: Amyloid-like properties of bacterial inclusion bodies. J Mol Biol 2005, 347:1025-1037.
28. Clark ED: Protein refolding for industrial processes. Curr Opin Biotechnol 2001, 12:202-7.
29. Corchero JL, Viaplana E, Benito A, Villaverde A: The position of the heterologous domain can influence the solubility and proteolysis of b-galactosidase fusion proteins. J Biotechnol 1996, 48:191-200.
30. Rinas U, Bailey JE: Protein compositional analysis of inclusion bodies produced in recombinant Escherichia coli. Appl Microbiol Biotechnol 1992, 37:609-614.
31. Hoffmann F, Rinas U: Roles of heat-shock chaperones in the production of recombinant proteins in Escherichia coli. Advan Bioche Eng Biotechnol 2004, 89:143-61.
32. De la Torre JC: Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 2004, 3:184-90.
33. Harper JD, Lieber CM, Lansbury PT Jr: Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-beta protein. Chem Biol 1997, 4:951-9.
34. Jarrett JT, Lansbury PT Jr: Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 1992, 31:12345-52.
35. Kocisko DA, Priola SA, Raymond GJ, Chesebro B, Lansbury PT Jr, Caughey B: Species specificity in the cell-free conversion of prion protein to protease-resistant forms: a model for the scrapie species barrier. Proc Natl Acad Sci U S A 1995, 92:3923-7.
36. Saraiva MJ, Birken S, Costa PP, Goodman DS: Amyloid fibril protein in familial amyloidotic polyneuropathy, Portuguese type. Definition of molecular abnormality in transthyretin (prealbumin). J Clin Invest 1984, 74:104-19.
37. MacPhee CE, Dobson CM: Formation of mixed fibrils demonstrates the generic nature and potential utility of amyloid nanostructures. J Am Chem Soc 2000, 122:12707-12713.
38. Krebs MR, Morozova-Roche LA, Daniel K, Robinson CV, Dobson CM: Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein Sci 2004, 13:1933-8.
39. Gordon CL, King J: Temperature-sensitive mutations in the phage P22 coat protein which interfere with polypeptide chain folding. J Biol Chem 1993, 268:9358-68.
40. Teschke CM, King J.: Folding of the phage P22 coat protein in vitro. Biochemistry 1993, 32:10839-47.
41. Speed MA, Wang DI, King J: Multimeric intermediates in the pathway to the aggregated inclusion body state for P22 tailspike polypeptide chains. Protein Sci 1995, 4:900-8.
42. Speed MA, Morshead T, Wang DI, King J: Conformation of P22 tailspike folding and aggregation intermediates probed by monoclonal antibodies. Protein Sci 1997, 6:99-108.
43. Speed MA, Wang DI, King J: Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat Biotechnol 1996, 14:1283-7.
44. Kopito RR: Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 2000, 10:524-30.
45. Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu YZ, Gohler H, Wanker EE, Bates GP, Housman DE, Thompson LM: The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 2000, 97:6763-6768.
46. Rajan RS, Illing ME, Bence NF, Kopito RR: Specificity in intracellular protein aggregation and inclusion body formation. Proc Natl Acad Sci USA 2001, 98:13060-5.
47. Pallares I, Vendrell J, Aviles FX, Ventura S: Amyloid fibril formation by a partially structured intermediate state of alpha-chymotrypsin. J Mol Biol 2004, 342:321-31.
48. Litvinovich SV, Brew SA, Aota S, Akiyama SK, Haudenschild C, Ingham KC: Formation of amyloid-like fibrils by self-association of a partially unfolded fibronectin type III module. J Mol Biol 1998, 280:245-58.
49. Villegas V, Zurdo J, Filimonov VV, Aviles FX, Dobson CM, Serrano L: Protein engineering as a strategy to avoid formation of amyloid fibrils. Protein Sci 2000, 9:1700-1708.
50. Fandrich M, Fletcher MA, Dobson CM: Amyloid fibrils from muscle myoglobin. Nature 2001, 410:165-166.
51. Schein CH: Optimizing protein folding to the native state in bacteria. Curr Opin Biotechnol 1991, 2:746-50.
52. Carrio MM, Villaverde A: Construction and deconstruction of bacterial inclusion bodies. J Biotechnol 2002, 96:3-12.
53. Wetzel R: Ideas of order for amyloid fibril structure. Structure 2002, 10:1031-6.
54. Oberg K, Chrunyk BA, Wetzel R, Fink AL: Nativelike secondary structure in interleukin-1-beta inclusion bodies by attenuated total reflectance FT-IR. Biochemistry 1994, 33:2628-2634.
55. Georgiou G, Valax P, Ostermeier M, Horowitz PM: Folding and aggregation of TEM β-lactamase: analogies with the formation of inclusion bodies in Escherichia coli. Protein Sci 1994, 3:1953-1960.
56. Przybycien TM, Dunn JP, Valax P, Georgiou G: Secondary structure characterization of beta-lactamase inclusion bodies. Protein Eng 1994, 7:131-136.
57. Ami D, Bonecchi L, Cali S, Orsini G, Tonon G, Doglia SM: FT-IR study of heterologous protein expression in recombinant Escherichia coli strains. Biochim Biophys Acta 2003, 1624:6-10.
58. Ismail AA, Mantsch HH, Wong PT: Aggregation of chymotrypsinogen: portrait by infrared spectroscopy. Biochim Biophys Acta 1992, 1121:183-8.
59. Goloubinoff P, Mogk A, Zvi AP, Tomoyasu T, Bukau B: Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 1999, 96:13732-7.
60. Umetsu M, Tsumoto K, Ashish K, Nitta S, Tanaka Y, Adschiri T, Kumagai I: Structural characteristics and refolding of in vivo aggregated hyperthermophilic archaeon proteins. FEBS Lett 2004, 557:49-56.
61. Parsell DA, Kowal AS, Singer MA, Lindquist S: Protein disaggregation mediated by heat-shock protein Hsp104. Nature 1994, 372:475-8.
62. Ben-Zvi AP, Goloubinoff P: Mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J Struct Biol 2001, 135:84-93.
63. Carrio MM, Villaverde A: Role of molecular chaperones in inclusion body formation. FEBS Lett 2003, 537:215-21.
64. Gozu M, Lee YH, Ohhashi Y, Hoshino M, Naiki H, Goto Y: Conformational dynamics of beta(2)-microglobulin analyzed by reduction and reoxidation of the disulfide bond. J Biochem (Tokyo) 2003, 33:731-6.
65. Carmichael J, Chatellier J, Woolfson A, Milstein C, Fersht AR, Rubinsztein DC: Bacterial and yeast chaperones reduce both aggregate formation and cell death in mammalian cell models of Huntington's disease. Proc Natl Acad Sci U S A 2000, 97:9701-5.
66. Bucciantini M, Giannoni E, Chiti F, Baroni F, Formigli L, Zurdo J, Taddei N, Ramponi G, Dobson CM, Stefani M: Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 2002, 416:507-11.
67. Ventura S, Zurdo J, Narayanan S, Parreno M, Mangues R, Reif B, Chiti F, Giannoni E, Dobson CM, Aviles FX, Serrano L: Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case. Proc Natl Acad Sci U S A 2004, 101:7258-63.
68. Kelly JW: The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr Opin Struct Biol 1998, 8:101-106.
69. Tjernberg LO, Näslund J, Lindqvist F, Iohansson J, Karlström AR, Thyberg J, Terenius L, Nordstedt C: Arrest of beta-amyloid fibril formation by a pentapeptide ligand. J Biol Chem 1996, 271:8545-85.
70. Patino M, Liu JJ, Glover JR, Lindquist S: Support for the prion hypothesis for inheritance of a phenotypic trait in yeast. Science 1996, 273:622-626.
71. Tenidis K, Waldner M, Bernhagen J, Fischle W, Bergmann M, Weber M, Merkle ML, Voelter W, Brunner H, Kapurniotu A: Identification of a penta- and hexapeptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J Mol Biol 2000, 295:1055-1071.
72. Wurth C, Guimard NK, Hecht MH: Mutations that reduce aggregation of the Alzheimer's Abeta42 peptide: an unbiased search for the sequence determinants of Abeta amyloidogenesis. J Mol Biol 2002, 319:1279-90.
73. McParland VJ, Kad NM, Kalverda AP, Brown A, Kirwin-Jones P, Hunter MG, Sunde M, Radford SE: Partially unfolded states of beta-2-microglobulin and amyloid formation in vitro. Biochemistry 2000, 39:8735-8746.
74. Legname G, Baskakov IV, Nguyen HO, Riesner D, Cohen FE, DeArmond SJ, Prusiner SB: Synthetic mammalian prions. Science 2004, 305:673-676.
75. Lopes DH, Colin C, Degaki TL, de Sousa AC, Vieira MN, Sebollela A, Martinez AM, Bloch C Jr, Ferreira ST, Sogayar MC: Amyloidogenicity and cytotoxicity of recombinant mature human islet amyloid polypeptide (rhIAPP). J Biol Chem 2005, 279:42803-42810.
76. Fink AL: Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold Des 1998, 3:9-23.
77. de la Paz ML, Goldie K, Zurdo J, Lacroix E, Dobson CM, Hoenger A, Serrano L: De novo designed peptide-based amyloid fibrils. Proc Natl Acad Sci USA 2002, 99:16052-16057.
78. Izard J, Parker MW, Chartier M, Duche D, Baty D: A single amino acid substitution can restore the solubility of aggregated colicin A mutants in Escherichia coli. Protein Eng 1994, 7:1495-1500.
79. Wetzel R, Perry LJ, Veilleux C: Mutations in human interferon gamma affecting inclusion body formation identified by a general immunochemical screen. Biotechnology (NY) 1991, 9:731-737.
80. Krueger JK, Stock J, Schutt CE: Evidence that the methylesterase of bacterial chemotaxis may be a serine hydrolase. Biochim Biophys Acta 1992, 1119:322-326.
81. Wetzel R, Chrunyk BA: Inclusion body formation by interleukin-1b depends on the thermal sensitivity of a folding intermediate. FEBS Lett 1994, 350:245-248.
82. Nieba L, Honegger A, Krebber C, Pluckthun A: Disrupting the hydrophobic patches at the antibody variable/constant domain interface: improved in vivo folding and physical characterization of an engineered scFv fragment. Protein Eng 1997, 10:435-444.
83. Chrunyk BA, Wetzel R: Breakdown in the relationship between thermal and thermodynamic stability in an interleukin-1 beta point mutant modified in a surface loop. Protein Eng 1993, 6:733-738.
84. Azriel R, Gazit E: Analysis of the minimal amyloid-forming fragment of the islet amyloidpolypeptide. An experimental support for the key role of the phenylalanine residue in amyloid formation:. J Biol Chem 2001, 276:34156-34161.
85. Salmona M, Malesani P, De Gioia L, Gorla S, Bruschi M, Molinari A, Della Vedova F, Pedrotti B, Marrari MA, Awan T, Bugiani O, Forloni G, Tagliavini F: Molecular determinants of the physicochemical properties of a critical prion protein region comprising residues 106-126. Biochem J 1999, 342:207-214.
86. Conway KA, Lee SJ, Rochet JC, Ding TT, Williamson RE, Lansbury PT Jr: Acceleration of oligomerization, not fibrillization, is a shared property of both alpha-synuclein mutations linked to early-onset Parkinson's disease: Implications for pathogenesis and therapy. Proc Natl Acad Sci USA 2000, 97:571-576.
87. Esler WP, Stimson ER, Ghilardi JR, Lu YA, Felix AM, Vinters HV, Mantyh PW, Lee JP, Maggio JE: Point substitution in the central hydrophobic cluster of a human β-amyloid congener disrupts peptide folding and abolishes plaque competence. Biochemistry 1996, 35:13914-13921.
88. Barghorn S, Zheng-Fischhofer Q, Ackmann M, Biernat J, von Bergen M, Mandelkow EM, Mandelkow E: Structure, microtubule interactions, and paired helical filament aggregation by tau mutants of frontotemporal dementias. Biochemistry 2000, 39:11714-11721.
89. Wigley WC, Stidham RD, Smith NM, Hunt JF, Thomas PJ: Protein solubility and folding monitored in vivo by structural complementation of a genetic marker protein. Nature Biotechnol 2001, 19:1131-136.
90. 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.
91. Hammarstrom P, Sekijima Y, White JT, Wiseman RL, Lim A, Costello CE, Altland K, Garzuly F, Budka H, Kelly JWY: D18G transthyretin is monomeric, aggregation prone, and not detectable in plasma and cerebrospinal fluid: a prescription for central nervous system amyloidosis? Biochemistry 2003, 42:6656-6663.
92. West MW, Wang W, Patterson J, Mancias JD, Beasley JR, Hecht MH: De novo amyloid proteins from designed combinatorial libraries. Proc Natl Acad Sci USA 1999, 96:11211-11216.
93. Wang W, Hecht MH: Rationally designed mutations convert de novo amyloid-like fibrils into soluble monomeric β-sheet proteins. Proc Natl Acad Sci USA 2002, 99:2760-2765.
94. de la Paz ML, Serrano L: Sequence determinants of amyloid fibril formation. Proc Natl Acad Sci U S A 2004, 101:87-92.
95. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, Serrano L: Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 2004, 22:1302-6.
96. Linding R, Schymkowitz J, Rousseau F, Diella F, Serrano L: A comparative study of the relationship between protein structure and beta-aggregation in globular and intrinsically disordered proteins. J Mol Biol 2004, 342:345-53.
97. DuBay KF, Pawar AP, Chiti F, Zurdo J, Dobson CM, Vendruscolo M: Prediction of the absolute aggregation rates of amyloidogenic polypeptide chains. J Mol Biol 2004, 341:1317-26.
98. Vallejo LF, Rinas U: Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 2004, 3:11.
99. Sorensen HP, Mortensen KK: Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb Cell Fact 2005, 4:1.
100. Maloney AP, Callan SM, Murray PG, Tuohy MG: Mitochondrial malate dehydrogenase from the thermophilic, filamentous fungus Talaromyces emersonii. Eur J Biochem 2004, 271:3115-26.
101. Bertoldo C, Armbrecht M, Becker F, Schafer T, Antranikian G, Liebl W: Cloning, sequencing, and characterization of a heat- and alkali-stable type I pullulanase from Anaerobranca gottschalkii. Appl Environ Microbiol 2004, 70:3407-16.
102. Fang TY, Hung XG, Shih TY, Tseng WC: Characterization of the trehalosyl dextrin-forming enzyme from the thermophilic archaeon Sulfolobus solfataricus ATCC 35092. Extremophiles 2004, 8:335-43.
103. Idicula-Thomas S, Balaji PV: Understanding the relationship between the primary structure of proteins and its propensity to be soluble on overexpression in Escherichia coli. Protein Sci 2005, 14:582-92.
104. Yan G, Cheng S, Zhao G, Wu S, Liu Y, Sun W: A single residual replacement improves the folding and stability of recombinant cassava hydroxynitrile lyase in E. coli. Biotechnol Lett 2003, 25:1041-7.
105. Calloni G, Zoffoli S, Stefani M, Dobson CM, Chiti F: Investigating the effects of mutations on protein aggregation in the cell. J Biol Chem 2005, 280:10607-13.
106. Fan D, Li Q, Korando L, Jerome WG, Wang J: A monomeric human apolipoprotein E carboxyl-terminal domain. Biochemistry 2004, 43:5055-64.