Biological role of bacterial inclusion bodies: A model for amyloid aggregation

FEBS Journal

Volumn 278, Issue 14, 2011, Pages 2419-2427

  García Fruitõs, Elena ^a,b   Sabate, Raimon ^a   De Groot, Natalia S ^a   Villaverde, Antonio ^a,b   Ventura, Salvador ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

Author keywords

aggregation; amyloid; FTIR; inclusion bodies; protein folding; protein quality; recombinant proteins

Indexed keywords

AMYLOID; AMYLOID BETA PROTEIN; PRION PROTEIN; RECOMBINANT PROTEIN;

AGING; BACTERIAL CELL; BACTERIAL INCLUSION BODY; BACTERIAL INFECTION; BIOCATALYSIS; BIOLOGICAL ACTIVITY; BIOTECHNOLOGICAL PRODUCTION; CELL ACTIVITY; CELL INCLUSION; CRYSTAL STRUCTURE; CYTOPLASM; ESCHERICHIA COLI; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; STEREOSPECIFICITY;

AMYLOID; ANIMALS; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; INCLUSION BODIES; INDUSTRIAL MICROBIOLOGY; MODELS, BIOLOGICAL; PRIONS; PROTEIN FOLDING; RECOMBINANT PROTEINS; SOLUBILITY;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 79959920280     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08165.x     Document Type: Review

References (74)

1. Ferrer-Miralles N, Domingo-Espin J, Corchero JL, Vazquez E, &, Villaverde A, (2009) Microbial factories for recombinant pharmaceuticals. Microb Cell Fact 8, 17-24.
2. Gasser B, Saloheimo M, Rinas U, Dragosits M, Rodriguez-Carmona E, Baumann K, Giuliani M, Parrilli E, Branduardi P, Lang C, et al. (2008) Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. Microb Cell Fact 7, 11-28.
3. Villaverde A, &, Carriõ MM, (2003) Protein aggregation in recombinant bacteria: biological role of inclusion bodies. Biotechnol Lett 25, 1385-1395. (Pubitemid 37065286)
4. Sorensen HP, &, Mortensen KK, (2005) Advanced genetic strategies for recombinant protein expression in Escherichia coli. J Biotechnol 115, 113-128. (Pubitemid 39656438)
5. Vallejo LF, &, Rinas U, (2004) Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 3, 11-22.
6. Carrio MM, &, Villaverde A, (2001) Protein aggregation as bacterial inclusion bodies is reversible. FEBS Lett 489, 29-33. (Pubitemid 32176000)
7. García-Fruitõs E, Gonzalez-Montalban N, Morell M, Vera A, Ferraz RM, Aris A, Ventura S, &, Villaverde A, (2005) Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb Cell Fact 4, 27-32.
8. Carriõ M, Gonzalez-Montalban N, Vera A, Villaverde A, &, Ventura S, (2005) Amyloid-like properties of bacterial inclusion bodies. J Mol Biol 347, 1025-1037. (Pubitemid 40387450)
9. Gonzalez-Montalban N, García-Fruitõs E, &, Villaverde A, (2007) Recombinant protein solubility-does more mean better? Nat Biotechnol 25, 718-720. (Pubitemid 47052176)
10. García-Fruitõs E, Martinez-Alonso M, Gonzalez-Montalban N, Valli M, Mattanovich D, &, Villaverde A, (2007) Divergent genetic control of protein solubility and conformational quality in Escherichia coli. J Mol Biol 374, 195-205. (Pubitemid 47610779)
11. Martinez-Alonso M, García-Fruitõs E, &, Villaverde A, (2008) Yield, solubility and conformational quality of soluble proteins are not simultaneously favored in recombinant Escherichia coli. Biotechnol Bioeng 101, 1353-1358.
12. García-Fruitõs E, (2010) Inclusion bodies: a new concept. Microb Cell Fact 9, 80-82.
13. Martinez-Alonso M, Gonzalez-Montalban N, García-Fruitõs E, &, Villaverde A, (2009) Learning about protein solubility from bacterial inclusion bodies. Microb Cell Fact 8, 4-8.
14. de Groot NS, Sabate R, &, Ventura S, (2009) Amyloids in bacterial inclusion bodies. Trends Biochem Sci 34, 408-416.
15. Sabate R, Espargaro A, Saupe SJ, &, Ventura S, (2009) Characterization of the amyloid bacterial inclusion bodies of the HET-s fungal prion. Microb Cell Fact 8, 56-65.
16. Carriõ MM, &, Villaverde A, (2002) Construction and deconstruction of bacterial inclusion bodies. J Biotechnol 96, 3-12. (Pubitemid 34876295)
17. Jurgen B, Breitenstein A, Urlacher V, Buttner K, Lin H, Hecker M, Schweder T, &, Neubauer P, (2010) Quality control of inclusion bodies in Escherichia coli. Microb Cell Fact 9, 41-53.
18. Vera A, Aris A, Carriõ M, Gonzalez-Montalban N, &, Villaverde A, (2005) Lon and ClpP proteases participate in the physiological disintegration of bacterial inclusion bodies. J Biotechnol 119, 163-171. (Pubitemid 41219545)
19. Carbonell X, &, Villaverde A, (2002) Protein aggregated into bacterial inclusion bodies does not result in protection from proteolytic digestion. Biotechnology Lett 24, 1939-1944. (Pubitemid 35464912)
20. Martinez-Alonso M, Vera A, &, Villaverde A, (2007) Role of the chaperone DnaK in protein solubility and conformational quality in inclusion body-forming Escherichia coli cells. FEMS Microbiol Lett 273, 187-195. (Pubitemid 47084008)
21. Vera A, Gonzalez-Montalban N, Aris A, &, Villaverde A, (2007) The conformational quality of insoluble recombinant proteins is enhanced at low growth temperatures. Biotechnol Bioeng 96, 1101-1106. (Pubitemid 46648670)
22. Ventura S, &, Villaverde A, (2006) Protein quality in bacterial inclusion bodies. Trends Biotechnol 24, 179-185.
23. Bukau B, Weissman J, &, Horwich A, (2006) Molecular chaperones and protein quality control. Cell 125, 443-451.
24. Carriõ MM, &, Villaverde A, (2005) Localization of chaperones DnaK and GroEL in bacterial inclusion bodies. J Bacteriol 187, 3599-3601. (Pubitemid 40628721)
25. Schlieker C, Tews I, Bukau B, &, Mogk A, (2004) Solubilization of aggregated proteins by ClpB/DnaK relies on the continuous extraction of unfolded polypeptides. FEBS Lett 578, 351-356. (Pubitemid 39601805)
26. Weibezahn J, Bukau B, &, Mogk A, (2004) Unscrambling an egg: protein disaggregation by AAA+ proteins. Microb Cell Fact 3, 1-12.
27. Gonzalez-Montalban N, García-Fruitõs E, Ventura S, Aris A, &, Villaverde A, (2006) The chaperone DnaK controls the fractioning of functional protein between soluble and insoluble cell fractions in inclusion body-forming cells. Microb Cell Fact 5, 26-34.
28. Gonzalez-Montalban N, Natalello A, García-Fruitõs E, Villaverde A, &, Doglia SM, (2008) In situ protein folding and activation in bacterial inclusion bodies. Biotechnol Bioeng 100, 797-802. (Pubitemid 351914005)
29. Martinez-Alonso M, García-Fruitõs E, Ferrer-Miralles N, Rinas U, &, Villaverde A, (2010) Side effects of chaperone gene co-expression in recombinant protein production. Microb Cell Fact 9, 64-69.
30. Martinez-Alonso M, Gomez-Sebastian S, Escribano JM, Saiz JC, Ferrer-Miralles N, &, Villaverde A, (2009) DnaK/DnaJ-assisted recombinant protein production in Trichoplusia ni larvae. Appl Microbiol Biotechnol 86, 633-639.
31. de Marco A, &, Schroedel A, (2005) Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC Biochem 6, 10-20.
32. Hamodrakas SJ, (2011) Protein aggregation and amyloid fibril formation prediction software from primary sequence: towards controlling the formation of bacterial inclusion bodies. FEBS J 278, 2428-2435.
33. Ferrer-Miralles N, Martinez-Alonso M, Villaverde A, &, García-Fruitõs E, (2010) Inclusion Bodies: A New Concept of Biocatalysts. Protein Aggregation. Nova Science Publishers, New York.
34. García-Fruitõs E, Aris A, &, Villaverde A, (2007) Localization of functional polypeptides in bacterial inclusion bodies. Appl Environ Microbiol 73, 289-294. (Pubitemid 46079961)
35. Nahalka J, Dib I, &, Nidetzky B, (2008) Encapsulation of Trigonopsis variabilis D-amino acid oxidase and fast comparison of the operational stabilities of free and immobilized preparations of the enzyme. Biotechnol Bioeng 99, 251-260. (Pubitemid 351158273)
36. Nahalka J, &, Patoprsty V, (2009) Enzymatic synthesis of sialylation substrates powered by a novel polyphosphate kinase (PPK3). Org Biomol Chem 7, 1778-1780.
37. Nahalka J, (2008) Physiological aggregation of maltodextrin phosphorylase from Pyrococcus furiosus and its application in a process of batch starch degradation to alpha-D-glucose-1-phosphate. J Ind Microbiol Biotechnol 35, 219-223.
38. Nahalka J, Vikartovska A, &, Hrabarova E, (2008) A crosslinked inclusion body process for sialic acid synthesis. J Biotechnol 134, 146-153. (Pubitemid 351288947)
39. Steinmann B, Christmann A, Heiseler T, Fritz J, &, Kolmar H, (2010) In vivo enzyme immobilization by inclusion body display. Appl Environ Microbiol 76, 5563-5569.
40. Chiti F, Stefani M, Taddei N, Ramponi G, &, Dobson CM, (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 424, 805-808. (Pubitemid 37021713)
41. de Groot NS, Aviles FX, Vendrell J, &, Ventura S, (2006) Mutagenesis of the central hydrophobic cluster in Abeta42 Alzheimer's peptide. Side-chain properties correlate with aggregation propensities. FEBS J 273, 658-668.
42. Conchillo-Sole O, de Groot NS, Aviles FX, Vendrell J, Daura X, &, Ventura S, (2007) AGGRESCAN: a server for the prediction and evaluation of 'hot spots' of aggregation in polypeptides. BMC Bioinformatics 8, 65-81.
43. Fernandez-Escamilla AM, Rousseau F, Schymkowitz J, &, Serrano L, (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat Biotechnol 22, 1302-1306. (Pubitemid 39336784)
44. Krebs MR, Morozova-Roche LA, Daniel K, Robinson CV, &, Dobson CM, (2004) Observation of sequence specificity in the seeding of protein amyloid fibrils. Protein Sci 13, 1933-1938. (Pubitemid 38822133)
45. Harper JD, Lieber CM, &, Lansbury PT, (1997) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-beta protein. Chem Biol 4, 951-959. (Pubitemid 28050379)
46. Jarrett JT, &, Lansbury PT, (1993) Seeding 'one-dimensional crystallization' of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73, 1055-1058. (Pubitemid 23180480)
47. Chiti F, &, Dobson CM, (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75, 333-366. (Pubitemid 44118036)
48. Sabate R, Espargaro A, de Groot NS, Valle-Delgado JJ, Fernandez-Busquets X, &, Ventura S, (2010) The role of protein sequence and amino acid composition in amyloid formation: scrambling and backward reading of IAPP amyloid fibrils. J Mol Biol 404, 337-352.
49. Uversky VN, &, Fink AL, (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta 1698, 131-153. (Pubitemid 38591469)
50. Jahn TR, &, Radford SE, (2008) Folding versus aggregation: polypeptide conformations on competing pathways. Arch Biochem Biophys 469, 100-117. (Pubitemid 350214559)
51. Gatti-Lafranconi P, Natalello A, Ami D, Doglia SM, &, Lotti M, (2011) Concepts and tools to exploit the potential of bacterial inclusion bodies in protein science and biotechnology. FEBS J 278, 2408-2418.
52. Ecroyd H, &, Carver JA, (2008) Unraveling the mysteries of protein folding and misfolding. IUBMB Life 60, 769-774.
53. Merlini G, &, Bellotti V, (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349, 583-596. (Pubitemid 36951371)
54. Fowler DM, Koulov AV, Balch WE, &, Kelly JW, (2007) Functional amyloid-from bacteria to humans. Trends Biochem Sci 32, 217-224. (Pubitemid 46694328)
55. Sabate R, de Groot NS, &, Ventura S, (2010) Protein folding and aggregation in bacteria. Cell Mol Life Sci 67, 2695-2715.
56. Greenwald J, &, Riek R, (2010) Biology of amyloid: structure, function, and regulation. Structure 18, 1244-1260.
57. Serpell LC, Sunde M, Benson MD, Tennent GA, Pepys MB, &, Fraser PE, (2000) The protofilament substructure of amyloid fibrils. J Mol Biol 300, 1033-1039.
58. Nelson R, &, Eisenberg D, (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16, 260-265.
59. Wang L, Maji SK, Sawaya MR, Eisenberg D, &, Riek R, (2008) Bacterial inclusion bodies contain amyloid-like structure. PLoS Biol 6, e195.
60. Morell M, Bravo R, Espargaro A, Sisquella X, Aviles FX, Fernandez-Busquets X, &, Ventura S, (2008) Inclusion bodies: specificity in their aggregation process and amyloid-like structure. Biochim Biophys Acta 1783, 1815-1825.
61. Dasari M, Espargaro A, Sabate R, Lõpez del Amo J, Fink U, Grelle G, Bieschke J, Ventura S, &, Reif B, (2011) Bacterial inclusion bodies of the alzheimer disease beta-amyloid peptides can be employed to study native like aggregation intermediate states. Chem Bio Chem 12, 407-423.
62. Wasmer C, Benkemoun L, Sabate R, Steinmetz MO, Coulary-Salin B, Wang L, Riek R, Saupe SJ, &, Meier BH, (2009) Solid-state NMR spectroscopy reveals that E. coli inclusion bodies of HET-s(218-289) are amyloids. Angew Chem Int Ed Engl 48, 4858-4860.
63. Thompson LK, (2003) Unraveling the secrets of Alzheimer's beta-amyloid fibrils. Proc Natl Acad Sci USA 100, 383-385. (Pubitemid 36126059)
64. Tycko R, (2006) Molecular structure of amyloid fibrils: insights from solid-state NMR. Q Rev Biophys 39, 1-55. (Pubitemid 44566373)
65. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, &, Meier BH, (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319, 1523-1526. (Pubitemid 351398180)
66. Garrity SJ, Sivanathan V, Dong J, Lindquist S, &, Hochschild A, (2010) Conversion of a yeast prion protein to an infectious form in bacteria. Proc Natl Acad Sci USA 107, 10596-10601.
67. Woulfe J, (2008) Nuclear bodies in neurodegenerative disease. Biochim Biophys Acta 1783, 2195-2206.
68. Kopito RR, (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol 10, 524-530.
69. Lindner AB, Madden R, Demarez A, Stewart EJ, &, Taddei F, (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105, 3076-3081. (Pubitemid 351723670)
70. de Groot NS, &, Ventura S, (2006) Effect of temperature on protein quality in bacterial inclusion bodies. FEBS Lett 580, 6471-6476. (Pubitemid 44750943)
71. Espargaro A, Sabate R, &, Ventura S, (2008) Kinetic and thermodynamic stability of bacterial intracellular aggregates. FEBS Lett 582, 3669-3673.
72. Castillo V, Espargaro A, Gordo V, Vendrell J, &, Ventura S, (2010) Deciphering the role of the thermodynamic and kinetic stabilities of SH3 domains on their aggregation inside bacteria. Proteomics 10, 4172-4185.
73. Ignatova Z, &, Gierasch LM, (2004) Monitoring protein stability and aggregation in vivo by real-time fluorescent labeling. Proc Natl Acad Sci USA 101, 523-528. (Pubitemid 38084669)
74. Kim W, Kim Y, Min J, Kim DJ, Chang YT, &, Hecht MH, (2006) A high-throughput screen for compounds that inhibit aggregation of the Alzheimer's peptide. ACS Chem Biol 1, 461-469.