Designing non-classical inclusion bodies

Ribosomal Proteins and Protein Engineering: Design, Selection and Applications

Volumn , Issue , 2010, Pages 1-20

  Peternel, Špela ^a  

^a NATIONAL INSTITUTE OF CHEMISTRY   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77957148932     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (110)

1. Grabherr R, Nilsson E, Striedner G, Bayer K: Stabilizing plasmid copy number to improve recombinant protein production. Biotechnol. Bioeng. 2002, 77: 142-147.
2. Hoffmann F, Rinas U: Stress induced by recombinant protein production in Escherichia coli. Adv. Biochem. Eng. Biotechnol. 2004, 89: 73-92.
3. Garber CC, Witte DL: Quality for tomorrow: by design or by checking? Clin. Chem. 1997, 43: 864-865.
4. Westgard JO: Nothing but the Truth about Quality; Essays on Quality Management in the Healthcare Laboratory; Quality By Design. Washington, DC: American Association for Clinical Chemistry (AACC); 2004.
5. Itakura K, Hirose T, Crea R, Riggs AD, Heyneker HL, Bolivar F et al.: Expression in Escherichia coli of a chemically synthesized gene for the hormone somatostatin. Science 1977, 198: 1056-1063.
6. Graumann K., Premstaller A.: Manufacturing of recombinant therapeutic proteins in microbial systems. Biotechnology Journal 2006, 2006: 164-186.
7. Schmidt FR: Recombinant expression systems in the pharmaceutical industry. Appl. Microbiol. Biotechnol. 2004, 65: 363-372.
8. Terpe K: Overview of bacterial expression systems for heterologous protein production: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 2006, 72: 211-222.
9. Villaverde A, Carrio MM: Protein aggregation in recombinant bacteria: biological role of inclusion bodies. Biotechnol. Lett. 2003, 25: 1385-1395.
10. Baneyx F, Mujacic M: Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol. 2004, 22: 1399-1408.
11. de Groot NS, Espargaro A, Morell M, Ventura S: Studies on bacterial inclusion bodies. Future Microbiol. 2008, 3: 423-435.
12. Smith A: Protein misfolding. Nature 2003, 426: 883.
13. Bowden GA, Paredes AM, Georgiou G: Structure and morphology of protein inclusion bodies in Escherichia coli. Biotechnology (N Y) 1991, 9: 725-730.
14. Arie JP, Miot M, Sassoon N, Betton JM: Formation of active inclusion bodies in the periplasm of Escherichia coli. Mol. Microbiol. 2006, 62: 427-437.
15. Williams DC, Van Frank RM, Muth WL, Burnett JP: Cytoplasmic inclusion bodies in Escherichia coli producing biosynthetic human insulin proteins. Science 1982, 215: 687-689.
16. Carrio MM, Cubarsi R, Villaverde A: Fine architecture of bacterial inclusion bodies. FEBS Lett. 2000, 471: 7-11.
17. Peternel S, Jevsevar S, Bele M, Gaberc-Porekar V, Menart V: New properties of inclusion bodies with implications for biotechnology. Biotechnol. Appl. Biochem. 2008, 49: 239-246.
18. Singh SM, Panda AK: Solubilization and refolding of bacterial inclusion body proteins. J. Biosci. Bioeng. 2005, 99: 303-310.
19. Carrio MM, Cubarsi R, Villaverde A: Fine architecture of bacterial inclusion bodies. Febs. Lett. 2000, 471: 7-11.
20. Carrio MM, Corchero JL, Villaverde A: Dynamics of in vivo protein aggregation: building inclusion bodies in recombinant bacteria. FEMS Microbiol. Lett. 1998, 169: 9-15.
21. Hart RA, Rinas U, Bailey JE: Protein composition of Vitreoscilla hemoglobin inclusion bodies produced in Escherichia coli. J. Biol. Chem. 1990, 265: 12728-12733.
22. Carrio MM, Villaverde A: Construction and deconstruction of bacterial inclusion bodies. J. Biotechnol. 2002, 96: 3-12.
23. Rinas U, Bailey JE: Protein compositional analysis of inclusion bodies produced in recombinant Escherichia coli. Appl. Microbiol. Biotechnol. 1992, 37: 609-614.
24. Valax P, Georgiou G: Molecular characterization of beta-lactamase inclusion bodies produced in Escherichia coli. 1. Composition. Biotechnol. Prog. 1993, 9: 539-547.
25. Carrio MM, Corchero JL, Villaverde A: Proteolytic digestion of bacterial inclusion body proteins during dynamic transition between soluble and insoluble forms. Biochim. Biophys. Acta 1999, 1434: 170-176.
26. Rinas U, Hoffmann F, Betiku E, Estape D, Marten S: Inclusion body anatomy and functioning of chaperone-mediated in vivo inclusion body disassembly during high-level recombinant protein production in Escherichia coli. J. Biotechnol. 2007, 127: 244-257.
27. Marston FA: The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem. J. 1986, 240: 1-12.
28. Sorensen HP, Mortensen KK: Advanced genetic strategies for recombinant protein expression in Escherichia coli. J. Biotechnol. 2005, 115: 113-128.
29. Worrall DM, Goss NH: The formation of biologically active beta-galactosidase inclusion bodies in Escherichia coli. Aust. J. Biotechnol. 1989, 3: 28-32.
30. Strandberg L, Enfors SO: Factors influencing inclusion body formation in the production of a fused protein in Escherichia coli. Appl. Environ. Microbiol. 1991, 57: 1669-1674.
31. Sorensen HP, Mortensen KK: Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb. Cell Fact. 2005, 4: 1.
32. Makrides SC: Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol. Rev. 1996, 60: 512-538.
33. De Marco A, Vigh L, Diamant S, Goloubinoff P: Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid-or benzyl alcohol-overexpressed molecular chaperones. Cell Stress Chaperones. 2005, 10: 329-339.
34. Mogk A, Deuerling E, Vorderwulbecke S, Vierling E, Bukau B: Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 2003, 50: 585-595.
35. Rinas U, Tsai LB, Lyons D, Fox GM, Stearns G, Fieschko J et al.: Cysteine to serine substitutions in basic fibroblast growth factor: effect on inclusion body formation and proteolytic susceptibility during in vitro refolding. Biotechnology (N Y) 1992, 10: 435-440.
36. De M, V, Stier G, Blandin S, De Marco A: The solubility and stability of recombinant proteins are increased by their fusion to NusA. Biochem Biophys. Res. Commun. 2004, 322: 766-771.
37. Ventura S: Sequence determinants of protein aggregation: tools to increase protein solubility. Microb. Cell Fact. 2005, 4: 11.
38. de Groot NS, Espargaro A, Morell M, Ventura S: Studies on bacterial inclusion bodies. Future Microbiol 2008, 3: 423-435.
39. Ventura S, Villaverde A: Protein quality in bacterial inclusion bodies. Trends Biotechnol. 2006, 24: 179-185.
40. Tokatlidis K, Dhurjati P, Millet J, Beguin P, Aubert JP: High activity of inclusion bodies formed in Escherichia coli overproducing Clostridium thermocellum endoglucanase D. FEBS Lett. 1991, 282: 205-208.
41. Garcia-Fruitos E, Carrio MM, Aris A, Villaverde A: Folding of a misfolding-prone beta-galactosidase in absence of DnaK. Biotechnol. Bioeng. 2005, 90: 869-875.
42. Garcia-Fruitos E, Gonzalez-Montalban N, Morell M, Vera A, Ferraz RM, Aris A et al.: Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb. Cell Fact. 2005, 4: 27.
43. Jevsevar S, Gaberc-Porekar V, Fonda I, Podobnik B, Grdadolnik J, Menart V: Production of nonclassical inclusion bodies from which correctly folded protein can be extracted. Biotechnol. Prog. 2005, 21: 632-639.
44. Peternel S, Bele M, Gaberc-Porekar V, Komel R: Contraction of inclusion bodies with implications in biotechnology. Acta Chim. Slov. 2008, 55: 608-612.
45. Peternel S, Grdadolnik J, Gaberc-Porekar V, Komel R: Engineering inclusion bodies for non denaturing extraction of functional proteins. Microb. Cell Fact. 2008, 7: 34.
46. Ami D, Natalello A, Taylor G, Tonon G, Maria DS: Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochim. Biophys. Acta 2006, 1764: 793-799.
47. Oberg K, Chrunyk BA, Wetzel R, Fink AL: Nativelike secondary structure in interleukin-1 beta inclusion bodies by attenuated total reflectance FTIR. Biochemistry 1994, 33: 2628-2634.
48. Ami D, Natalello A, Gatti-Lafranconi P, Lotti M, Doglia SM: Kinetics of inclusion body formation studied in intact cells by FT-IR spectroscopy. FEBS Lett. 2005, 579: 3433-3436.
49. Doglia SM, Ami D, Natalello A, Gatti-Lafranconi P, Lotti M: Fourier transform infrared spectroscopy analysis of the conformational quality of recombinant proteins within inclusion bodies. Biotechnol. J. 2008, 3: 193-201.
50. Gonzalez-Montalban N, Natalello A, Garcia-Fruitos E, Villaverde A, Doglia SM: In situ protein folding and activation in bacterial inclusion bodies. Biotechnol. Bioeng. 2008, 100: 797-802.
51. Vera A, Gonzalez-Montalban N, Aris A, Villaverde A: The conformational quality of insoluble recombinant proteins is enhanced at low growth temperatures. Biotechnol. Bioeng. 2007, 96: 1101-1106.
52. de Groot NS, Ventura S: Protein activity in bacterial inclusion bodies correlates with predicted aggregation rates. J. Biotechnol. 2006, 125: 110-113.
53. Baneyx F: Recombinant protein expression in Escherichia coli. Curr. Opin. Biotechnol. 1999, 10: 411-421.
54. Grossman TH, Kawasaki ES, Punreddy SR, Osburne MS: Spontaneous cAMP-dependent derepression of gene expression in stationary phase plays a role in recombinant expression instability. Gene 1998, 209: 95-103.
55. Carbonell X, Corchero JL, Cubarsi R, Vila P, Villaverde A: Control of Escherichia coli growth rate through cell density. Microbiol. Res. 2002, 157: 257-265.
56. Jevsevar S, Palcic J, Jalen S, Pavko A: Influence of the Media Composition on Behavior of the pET Expression Systems. Acta Chim. Slov. 2007, 54: 360-365.
57. Fotadar U, Zaveloff P, Terracio L: Growth of Escherichia coli at elevated temperatures. J. Basic. Microbiol. 2005, 45: 403-404.
58. Mujacic M, Cooper KW, Baneyx F: Cold-inducible cloning vectors for low-temperature protein expression in Escherichia coli: application to the production of a toxic and proteolytically sensitive fusion protein. Gene 1999, 238: 325-332.
59. Sorensen HP, Mortensen KK: Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb. Cell Fact. 2005, 4: 1.
60. Weickert MJ, Doherty DH, Best EA, Olins PO: Optimization of heterologous protein production in Escherichia coli. Curr. Opin. Biotechnol. 1996, 7: 494-499.
61. Garcia-Fruitos E, Aris A, Villaverde A: Localization of functional polypeptides in bacterial inclusion bodies. Appl. Environ. Microbiol. 2007, 73: 289-294.
62. de Groot NS, Ventura S: Effect of temperature on protein quality in bacterial inclusion bodies. FEBS Lett. 2006, 580: 6471-6476.
63. Yin J, Li G, Ren X, Herrler G: Select what you need: a comparative evaluation of the advantages and limitations of frequently used expression systems for foreign genes. J. Biotechnol. 2007, 127: 335-347.
64. Gasser B, Saloheimo M, Rinas U, Dragosits M, Rodriguez-Carmona E, Baumann K et al.: Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. Microb. Cell Fact. 2008, 7: 11.
65. Vallejo LF, Rinas U: Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 2004, 3: 11.
66. Khmelnitsky YL, Mozhaev VV, Belova AB, Sergeeva MV, Martinek K: Denaturation capacity: a new quantitative criterion for selection of organic solvents as reaction media in biocatalysis. Eur. J. Biochem. 1991, 198: 31-41.
67. Stathopulos PB, Scholz GA, Hwang YM, Rumfeldt JA, Lepock JR, Meiering EM: Sonication of proteins causes formation of aggregates that resemble amyloid. Protein. Sci. 2004, 13: 3017-3027.
68. Feliu JX, Cubarsi R, Villaverde A: Optimized release of recombinant proteins by ultrasonication of E. coli cells. Biotechnol. Bioeng. 1998, 58: 536-540.
69. Feliu JX, Villaverde A: An optimized ultrasonication protocol for bacterial cell disruption and recovery of beta-galactosidase fusion proteins. Biotechn. Techn. 1994, 8: 509-514.
70. Bernardez Clark ED: Protein refolding for industrial processes. Curr. Opin. Biotechnol 2001, 12: 202-207.
71. Middelberg AP: Preparative protein refolding. Trends Biotechnol. 2002, 20: 437-443.
72. Wong HH, O'Neill BK, Middelberg AP: Centrifugal processing of cell debris and inclusion bodies from recombinant Escherichia coli. Bioseparation 1997, 6: 361-372.
73. Patra AK, Mukhopadhyay R, Mukhija R, Krishnan A, Garg LC, Panda AK: Optimization of inclusion body solubilization and renaturation of recombinant human growth hormone from Escherichia coli. Protein. Expr. Purif. 2000, 18: 182-192.
74. 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.
75. Jungbauer A, Kaar W: Current status of technical protein refolding. J Biotechnol 2007, 128: 587-596.
76. Rudolph R: Successful Protein Folding on an Industrial Scale. In Protein Engineering: Principles and Practice. Edited by Cleland JL, Craik CS. New York: Wiley-Liss, Inc.; 1996: 283-298.
77. Fabian H, Mäntele W: Infrared Spectroscopy of Proteins. In Handbook of vibrational spectroscopy: Applications in Life, Pharmaceutical and Natural Sciences. Edited by Chalmers JM, Griffiths PR. Wiley; 2001: 3399-3425.
78. Prakash S, Matouschek A: Protein unfolding in the cell. Trends Biochem. Sci. 2004, 29: 593-600.
79. Tsumoto K, Umetsu M, Kumagai I, Ejima D, Arakawa T: Solubilization of active green fluorescent protein from insoluble particles by guanidine and arginine. Biochem. Biophys. Res. Commun. 2003, 312: 1383-1386.
80. Umetsu M, Tsumoto K, Nitta S, Adschiri T, Ejima D, Arakawa T et al.: Nondenaturing solubilization of beta2 microglobulin from inclusion bodies by L-arginine. Biochem. Biophys. Res. Commun. 2005, 328: 189-197.
81. Umetsu M, Tsumoto K, Ashish K, Nitta S, Tanaka Y, Adschiri T et al.: Structural characteristics and refolding of in vivo aggregated hyperthermophilic archaeon proteins. FEBS Lett. 2004, 557: 49-56.
82. Swietnicki W: Folding aggregated proteins into functionally active forms. Curr. Opin. Biotechnol. 2006, 17: 367-372.
83. Swartz JR: Advances in Escherichia coli production of therapeutic proteins. Curr. Opin. Biotechnol. 2001, 12: 195-201.
84. Gaberc-Porekar V, Menart V: Perspectives of immobilized-metal affinity chromatography. J Biochem Biophys Methods 2001, 49: 335-360.
85. Gaberc Porekar V, Menart V.: Process for the Purification And/Or Isolation Of Biologically Active Granulocyte Colony Stimulating Factor. Patent: PCT/EP02/13810[WO 03/051922 A1] 2003.
86. Martinez-Alonso M, Gonzalez-Montalban N, Garcia-Fruitos E, Villaverde A: Learning about protein solubility from bacterial inclusion bodies. Microb. Cell Fact. 2009, 8: 4.
87. Martinez-Alonso M, Vera A, Villaverde A: Role of the chaperone DnaK in protein solubility and conformational quality in inclusion body-forming Escherichia coli cells. FEMS Microbiol. Lett. 2007, 273: 187-195.
88. Martinez-Alonso M, Gonzalez-Montalban N, Garcia-Fruitos E, Villaverde A: The Functional quality of soluble recombinant polypeptides produced in Escherichia coli is defined by a wide conformational spectrum. Appl. Environ. Microbiol. 2008, 74: 7431-7433.
89. Schrodel A, De Marco A: Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC Biochem. 2005, 6: 10.
90. Carrio MM, Villaverde A: Protein aggregation as bacterial inclusion bodies is reversible. FEBS Lett. 2001, 489: 29-33.
91. Hoffmann F, Posten C, Rinas U: Kinetic model of in vivo folding and inclusion body formation in recombinant Escherichia coli. Biotechnol. Bioeng. 2001, 72: 315-322.
92. Lilie H, Schwarz E, Rudolph R: Advances in refolding of proteins produced in E. coli. Curr. Opin. Biotechnol. 1998, 9: 497-501.
93. Schlieker C, Bukau B, Mogk A: Prevention and reversion of protein aggregation by molecular chaperones in the E-coli cytosol: implications for their applicability in biotechnology. J. Biotechnol. 2002, 96: 13-21.
94. Speed MA, Wang DIC, King J: Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat. Biotechnol. 1996, 14: 1283-1287.
95. 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.
96. Soto C, Estrada L, Castilla J: Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem. Sci. 2006, 31: 150-155.
97. Harper JD, Lansbury PT, Jr.: 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. 1997, 66: 385-407.
98. Dobson CM: Protein folding and misfolding. Nature 2003, 426: 884-890.
99. Soto C, Estrada L, Castilla J: Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem. Sci. 2006, 31: 150-155.
100. Soto C, Estrada LD: Protein misfolding and neurodegeneration. Arch Neurol 2008, 65: 184-189.
101. Carrell RW, Lomas DA: Conformational disease. Lancet 1997, 350: 134-138.
102. Bandekar J, KRIMM S: Normal mode of the spectrum of the parallel-chain beta-sheet. Biopolymers 1988, 27: 909-921.
103. Cubarsi R, Carrio MM, Villaverde A: A mathematical approach to molecular organization and proteolytic disintegration of bacterial inclusion bodies. Math. Med. Biol. 2005, 22: 209-226.
104. Cubarsi R, Carrio MM, Villaverde A: In situ proteolytic digestion of inclusion body polypeptides occurs as a cascade process. Biochem. Biophys. Res. Commun. 2001, 282: 436-441.
105. Menart V., Gaberc-Porekar V., Jevsevar S.: Process For The Production of a Heterologous Protein. Patent: PCT/EP2003/006134 (WO2004/015124) 2004.
106. Dobson CM: The structural basis of protein folding and its links with human disease. Phil. Trans R. Soc. Lond B 2001, 356: 133-145.
107. Fornai F, Soldani P, Lazzeri G, di Poggio AB, Biagioni F, Fulceri F et al.: Neuronal inclusions in degenerative disorders Do they represent static features or a key to understand the dynamics of the disease? Brain Res. Bull. 2005, 65: 275-290.
108. Soto C, Estrada LD: Protein misfolding and neurodegeneration. Arch. Neurol. 2008, 65: 184-189.
109. Ravikumar B, Rubinsztein DC: Can autophagy protect against neurodegeneration caused by aggregate-prone proteins? Neuroreport 2004, 15: 2443-2445.
110. Kegel KB, Kim M, Sapp E, McIntyre C, Castano JG, Aronin N et al.: Huntingtin expression stimulates endosomal-lysosomal activity, endosome tubulation, and autophagy. J. Neurosci. 2000, 20: 7268-7278.