Analytical approaches for assessing aggregation of protein biopharmaceuticals

Current Pharmaceutical Biotechnology

Volumn 12, Issue 10, 2011, Pages 1530-1536

  García Fruitós, Elena ^a,b   Vazquez, Esther ^a,b   Gonzalez Montalbán, Nuria ^c   Ferrer Miralles, Neus ^a,b   Villaverde, Antonio ^a,b  

^a BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Aggregation; Analytical procedures; Protein drugs; Recombinant proteins; Screening

Indexed keywords

RECOMBINANT PROTEIN;

ANALYTIC METHOD; ATTENUATED TOTAL REFLECTANCE; CIRCULAR DICHROISM; FIELD FLOW FRACTIONATION; FLUORESCENCE MICROSCOPY; GEL ELECTROPHORESIS; GEL PERMEATION CHROMATOGRAPHY; INFRARED SPECTROSCOPY; LIGHT SCATTERING; MICRODIALYSIS; MICROSCOPY; NANOPARTICLE TRACKING ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN QUALITY; REVIEW; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION;

MAMMALIA;

EID: 80052348142     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920111798357339     Document Type: Review

References (109)

1. Ferrer-Miralles, N.; Domingo-Espin, J.; Corchero, J. L.; Vazquez, E.; Villaverde, A. Microbial factories for recombinant pharmaceuticals. Microb. Cell Fact., 2009, 8 (1), 17.
2. Gasser, B.; Saloheimo, M.; Rinas, U.; Dragosits, M.; Rodriguez- Carmona, E.; Baumann, K.; Giuliani, M.; Parrilli, E.; Branduardi, P.; Lang, C.; Porro, D.; Ferrer, P.; Tutino, M. L.; Mattanovich, D.; Villaverde, A. Protein folding and conformational stress in microbial cells producing recombinant proteins: a host comparative overview. Microb. Cell Fact., 2008, 7, 11.
3. Baneyx, F.; Mujacic, M. Recombinant protein folding and misfolding in Escherichia coli. Nat. Biotechnol., 2004, 22 (11), 1399-1408.
4. Sorensen, H. P.; Mortensen, K. K. Soluble expression of recombinant proteins in the cytoplasm of Escherichia coli. Microb. Cell Fact., 2005, 4 (1), 1.
5. Sorensen, H. P.; Mortensen, K. K. Advanced genetic strategies for recombinant protein expression in Escherichia coli. J. Biotechnol., 2005, 115 (2), 113-128.
6. Kolaj, O.; Spada, S.; Robin, S.; Wall, J. G. Use of folding modulators to improve heterologous protein production in Escherichia coli. Microb. Cell Fact., 2009, 8 (1), 9.
7. Martinez-Alonso, M.; Gomez-Sebastian, S.; Escribano, J. M.; Saiz, J. C.; Ferrer-Miralles, N.; Villaverde, A. DnaK/DnaJ-assisted recombinant protein production in Trichoplusia ni larvae. Appl. Microbiol. Biotechnol., 2009, 86(2), 633-639.
8. Martinez-Alonso, M.; Garcia-Fruitos, E.; Ferrer-Miralles, N.; Rinas, U.; Villaverde, A. Side effects of chaperone gene coexpression in recombinant protein production. Microb. Cell Fact., 2010, 9 (1), 64.
9. Martinez-Alonso, M.; Toledo-Rubio, V.; Noad, R.; Unzueta, U.; Ferrer-Miralles, N.; Roy, P.; Villaverde, A. Re-hosting bacterial chaperones for high-quality protein production. Appl. Environ. Microbiol., 2009, 75(24), 7850-7854.
10. de Marco A. Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli. Microb. Cell Fact., 2009, 8, 26.
11. de Marco A.; Deuerling, E.; Mogk, A.; Tomoyasu, T.; Bukau, B. Chaperone-based procedure to increase yields of soluble recombinant proteins produced in E. coli. BMC. Biotechnol., 2007, 7 (1), 32.
12. de Marco A. Protocol for preparing proteins with improved solubility by co-expressing with molecular chaperones in Escherichia coli. Nat. Protoc., 2007, 2 (10), 2632-2639.
13. Villaverde, A.; Carrio, M. M. Protein aggregation in recombinant bacteria: biological role of inclusion bodies. Biotechnol. Lett., 2003, 25 (17), 1385-1395.
14. Speed, M. A.; Wang, D. I.; King, J. Specific aggregation of partially folded polypeptide chains: the molecular basis of inclusion body composition. Nat. Biotechnol., 1996, 14 (10), 1283-1287.
15. Morell, M.; Bravo, R.; Espargaro, A.; Sisquella, X.; Aviles, F. X.; Fernandez-Busquets, X.; Ventura, S. Inclusion bodies: specificity in their aggregation process and amyloid-like structure. Biochim. Biophys. Acta, 2008, 1783 (10), 1815-1825.
16. Marston, F. A. The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem. J., 1986, 240 (1), 1-12.
17. Carrio, M. M.; Villaverde, A. Role of molecular chaperones in inclusion body formation. FEBS Lett., 2003, 537 (1-3), 215-221.
18. Gonzalez-Montalban, N.; Natalello, A.; Garcia-Fruitos, E.; Villaverde, A.; Doglia, S. M. In situ protein folding and activation in bacterial inclusion bodies. Biotechnol. Bioeng., 2008, 100 (4), 797-802.
19. 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 (6), 1101-1106.
20. Ventura, S.; Villaverde, A. Protein quality in bacterial inclusion bodies. Trends Biotechnol., 2006, 24 (4), 179-185.
21. Jurgen, B.; Breitenstein, A.; Urlacher, V.; Buttner, K.; Lin, H.; Hecker, M.; Schweder, T.; Neubauer, P. Quality control of inclusion bodies in Escherichia coli. Microb. Cell Fact., 2010, 9 (1), 41.
22. Carrio, M. M.; Villaverde, A. Construction and deconstruction of bacterial inclusion bodies. J Biotechnol., 2002, 96 (1), 3-12.
23. Carrio, M. M.; Villaverde, A. Protein aggregation as bacterial inclusion bodies is reversible. FEBS Lett., 2001, 489 (1), 29-33.
24. Carrio, M. M.; Corchero, J. L.; Villaverde, A. Proteolytic digestion of bacterial inclusion body proteins during dynamic transition between soluble and insoluble forms. Biochim. Biophys. Acta, 1999, 1434 (1), 170-176.
25. Carrio, M. M.; Corchero, J. L.; Villaverde, A. Dynamics of protein aggregation: building inclusion bodies in recombinant bacteria. FEMS Microbiol. Lett., 1998, 169 (1), 9-15.
26. Bukau, B.; Weissman, J.; Horwich, A. Molecular chaperones and protein quality control. Cell, 2006, 125 (3), 443-451.
27. Neubauer, P.; Fahnert, B.; Lilie, H.; Villaverde, A. In: Inclusions in Prokaryotes. Microbiology Monographs; Shively, J. M., Ed.; Springer: Berlin, 2006; pp 237-292.
28. Garcia-Fruitos, E.; Martinez-Alonso, M.; Gonzalez-Montalban, N.; Valli, M.; Mattanovich, D.; Villaverde, A. Divergent genetic control of protein solubility and conformational quality in Escherichia coli. J. Mol. Biol., 2007, 374, 195-205.
29. Weibezahn, J.; Bukau, B.; Mogk, A. Unscrambling an egg: protein disaggregation by AAA+ proteins. Microb. Cell Fact., 2004, 3 (1), 1.
30. Vallejo, L. F.; Rinas, U. Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb. Cell Fact., 2004, 3 (1), 11.
31. 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, 101 (6), 1353- 1358.
32. de Marco, A.; Schroedel, A. Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC. Biochem., 2005, 6 (1), 10.
33. Haacke, A.; Fendrich, G.; Ramage, P.; Geiser, M. Chaperone overexpression in Escherichia coli: Apparent increased yields of soluble recombinant protein kinases are due mainly to soluble aggregates. Protein Expr. Purif., 2008, 64(2), 185-193.
34. Martinez-Alonso, M.; Gonzalez-Montalban, N.; Garcia-Fruitos, E.; Villaverde, A. Learning about protein solubility from bacterial inclusion bodies. Microb. Cell Fact., 2009, 8 (1), 4.
35. Gonzalez-Montalban, N.; Garcia-Fruitos, E.; Villaverde, A. Recombinant protein solubility-does more mean better? Nat. Biotechnol., 2007, 25 (7), 718-720.
36. de Marco A.; Sevastsyanovich, Y. R.; Cole, J. A. Minimal information for protein functional evaluation (MIPFE) workshop. N. Biotechnol., 2009, 25 (4), 170.
37. Peternel, S.; Grdadolnik, J.; Gaberc-Porekar, V.; Komel, R. Engineering inclusion bodies for non denaturing extraction of functional proteins. Microb. Cell Fact., 2008, 7 (1), 34.
38. Garcia-Fruitos, E.; Villaverde, A. Friendly production of bacterial inclusion bodies. Korean J. Chem. Eng., 2010, 27 (2), 385-389.
39. 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 (2), 632-639.
40. Nahalka, J.; Vikartovska, A.; Hrabarova, E. A crosslinked inclusion body process for sialic acid synthesis. J. Biotechnol., 2008, 134 (1-2), 146-153.
41. Nahalka, J. 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., 2008, 35 (4), 219-223.
42. Nahalka, J.; Nidetzky, B. Fusion to a pull-down domain: a novel approach of producing Trigonopsis variabilisD-amino acid oxidase as insoluble enzyme aggregates. Biotechnol. Bioeng., 2007, 97(3), 454-461.
43. Garcia-Fruitos, E.; Aris, A.; Villaverde, A. Localization of functional polypeptides in bacterial inclusion bodies. Appl. Environ. Microbiol., 2007, 73 (1), 289-294.
44. Garcia-Fruitos, E.; Gonzalez-Montalban, N.; Morell, M.; Vera, A.; Ferraz, R. M.; Aris, A.; Ventura, S.; Villaverde, A. Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb. Cell Fact., 2005, 4, 27.
45. 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 (Pt 4), 239-246.
46. Doglia, S. M.; 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 (2), 193-201.
47. Gonzalez-Montalban, N.; Garcia-Fruitos, E.; Ventura, S.; Aris, A.; Villaverde, A. The chaperone DnaK controls the fractioning of functional protein between soluble and insoluble cell fractions in inclusion body-forming cells. Microb. Cell Fact., 2006, 5, 26.
48. Carrio, M.; Gonzalez-Montalban, N.; Vera, A.; Villaverde, A.; Ventura, S. Amyloid-like properties of bacterial inclusion bodies. J. Mol. Biol., 2005, 347 (5), 1025-1037.
49. Ami, D.; Natalello, A.; Gatti-Lafranconi, P.; Lotti, M.; Doglia, S. M. Kinetics of inclusion body formation studied in intact cells by FT-IR spectroscopy. FEBS Lett., 2005, 579 (16), 3433-3436.
50. de Groot, N. S.; Sabate, R.; Ventura, S. Amyloids in bacterial inclusion bodies. Trends Biochem. Sci., 2009, 34 (8), 408-416.
51. Wang, L.; Maji, S. K.; Sawaya, M. R.; Eisenberg, D.; Riek, R. Bacterial inclusion bodies contain amyloid-like structure. PLoS. Biol., 2008, 6 (8), e195.
52. Sabate, R.; Espargaro, A.; Saupe, S. J.; Ventura, S. Characterization of the amyloid bacterial inclusion bodies of the HET-s fungal prion. Microb. Cell Fact., 2009, 8, 56.
53. Human insulin receives FDA approval. FDA. Drug Bull., 1982, 12 (3), 18-19.
54. Misra, A. Are biosimilars really generics? Expert. Opin. Biol. Ther., 2010, 10 (4), 489-494.
55. Read, E. K.; Park, J. T.; Shah, R. B.; Riley, B. S.; Brorson, K. A.; Rathore, A. S. Process Analytical Technology (PAT) for Biopharmaceutical Products: Part I. Concepts and Applications. Biotechnol. Bioeng., 2010, 105 (2), 276-284.
56. Sahoo, N.; Choudhury, K.; Manchikanti, P. Manufacturing of biodrugs: need for harmonization in regulatory standards. Biodrugs, 2009, 23 (4), 217-229.
57. Wolynes, P. G.; Onuchic, J. N.; Thirumalai, D. Navigating the Folding Routes. Science, 1995, 267 (5204), 1619-1620.
58. Kaltashov, I. A.; Bobst, C. E.; Abzalimov, R. R.; Berkowitz, S. A.; Houde, D. Conformation and Dynamics of Biopharmaceuticals: Transition of Mass Spectrometry-Based Tools from Academe to Industry. J. Am. Soc. Mass Spectrom., 2010, 21 (3), 323-337.
59. Bobst, C. E.; Abzalimov, R. R.; Houde, D.; Kloczewiak, M.; Mhatre, R.; Berkowitz, S. A.; Kaltashov, I. A. Detection and characterization of altered conformations of protein pharmaceuticals using complementary mass spectrometry-based approaches. Anal. Chem., 2008, 80 (19), 7473-7481.
60. Kukrer, B.; Filipe, V.; van, D. E.; Kasper, P. T.; Vreeken, R. J.; Heck, A. J.; Jiskoot, W. Mass spectrometric analysis of intact human monoclonal antibody aggregates fractionated by sizeexclusion chromatography. Pharm. Res., 2010, 27 (10), 2197-2204.
61. Grandori, R.; Santambrogio, C.; Brocca, S.; Invernizzi, G.; Lotti, M. Electrospray-ionization mass spectrometry as a tool for fast screening of protein structural properties. Biotechnol. J., 2009, 4 (1), 73-87.
62. Suchanova, B.; Tuma, R. Folding and assembly of large macromolecular complexes monitored by hydrogen-deuterium exchange and mass spectrometry. Microb. Cell Fact., 2008, 7, 12.
63. Moullintraffort, L.; Bruneaux, M.; Nazabal, A.; Allegro, D.; Giudice, E.; Zal, F.; Peyrot, V.; Barbier, P.; Thomas, D.; Garnier, C. Biochemical and biophysical characterization of the Mg2+-induced 90-kDa heat shock protein oligomers. J. Biol. Chem., 2010, 285 (20), 15100-15110.
64. Bich, C.; Bovet, C.; Rochel, N.; Peluso-Iltis, C.; Panagiotidis, A.; Nazabal, A.; Moras, D.; Zenobi, R. Detection of nucleic acidnuclear hormone receptor complexes with mass spectrometry. J. Am. Soc. Mass Spectrom., 2010, 21 (4), 635-645.
65. Cheng, X.; van Breemen, R. B. Mass spectrometry-based screening for inhibitors of beta-amyloid protein aggregation. Anal. Chem., 2005, 77 (21), 7012-7015.
66. Natalello, A.; Ami, D.; Brocca, S.; Lotti, M.; Doglia, S. M. Secondary structure, conformational stability and glycosylation of a recombinant Candida rugosa lipase studied by Fourier-transform infrared spectroscopy. Biochem. J., 2005, 385 (Pt 2), 511-517.
67. Arrondo, J. L.; Goni, F. M. Structure and dynamics of membrane proteins as studied by infrared spectroscopy. Prog. Biophys. Mol. Biol., 1999, 72 (4), 367-405.
68. Barth, A.; Zscherp, C. What vibrations tell us about proteins. Q. Rev. Biophys., 2002, 35 (4), 369-430.
69. Ami, D.; Bonecchi, L.; Cali, S.; Orsini, G.; Tonon, G.; Doglia, S. M. FT-IR study of heterologous protein expression in recombinant Escherichia coli strains. Biochim. Biophys. Acta, 2003, 1624 (1-3), 6-10.
70. Gross-Selbeck, S.; Margreiter, G.; Obinger, C.; Bayer, K. Fast quantification of recombinant protein inclusion bodies within intact cells by FT-IR spectroscopy. Biotechnol. Prog., 2007, 23 (3), 762-766.
71. Gonzalez-Montalban, N.; Villaverde, A.; Aris, A. Amyloid-linked cellular toxicity triggered by bacterial inclusion bodies. Biochem. Biophys. Res. Commun., 2007, 355 (3), 637-642.
72. Fink, A. L. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des, 1998, 3 (1), R9-23.
73. Ami, D.; Natalello, A.; Taylor, G.; Tonon, G.; Maria, D. S. Structural analysis of protein inclusion bodies by Fourier transform infrared microspectroscopy. Biochim. Biophys. Acta, 2006, 1764 (4), 793-799.
74. Oberg, K.; Chrunyk, B. A.; Wetzel, R.; Fink, A. L. Nativelike secondary structure in interleukin-1 beta inclusion bodies by attenuated total reflectance FTIR. Biochemistry, 1994, 33 (9), 2628- 2634.
75. Lewandowska, A.; Matuszewska, M.; Liberek, K. Conformational properties of aggregated polypeptides determine ClpB-dependence in the disaggregation process. J. Mol. Biol., 2007, 371 (3), 800-811.
76. Wasmer, C.; Benkemoun, L.; Sabate, R.; Steinmetz, M. O.; Coulary- Salin, B.; Wang, L.; Riek, R.; Saupe, S. J.; Meier, B. H. Solidstate NMR spectroscopy reveals that E. coli inclusion bodies of HET-s(218-289) are amyloids. Angew. Chem. Int. Ed Engl., 2009, 48 (26), 4858-4860.
77. Bemporad, F.; Chiti, F. Native-like aggregation of the acylphosphatase from Sulfolobus solfataricus and its biological implications. FEBS Lett., 2009, 583 (16), 2630-2638.
78. Wang, Q.; Johnson, J. L.; Agar, N. Y.; Agar, J. N. Protein aggregation and protein instability govern familial amyotrophic lateral sclerosis patient survival. PLoS. Biol., 2008, 6 (7), e170.
79. Rokney, A.; Shagan, M.; Kessel, M.; Smith, Y.; Rosenshine, I.; Oppenheim, A. B. E. coli transports aggregated proteins to the poles by a specific and energy-dependent process. J. Mol. Biol., 2009, 392 (3), 589-601.
80. Li, L.; Kim, Y. S.; Hwang, D. S.; Seo, J. H.; Jung, H. J.; Du, J.; Cha, H. J. High and compact formation of baculoviral polyhedrininduced inclusion body by co-expression of baculoviral FP25 in Escherichia coli. Biotechnol. Bioeng., 2007, 96 (6), 1183-1190.
81. Garcia-Fruitos, E.; Seras-Franzoso, J.; Vazquez, E.; Villaverde, A. Tunable geometry of bacterial inclusion bodies as substrate materials for tissue engineering. Nanotechnology, 2010, 21 (20), 205101.
82. Garcia-Fruitos, E.; Rodriguez-Carmona, E.; Diez-Gil, C.; Ferraz, R. M.; Vazquez, E.; Corchero, J. L.; Cano-Sarabia, M.; Ratera, I.; Ventosa, N.; Vaciana, J.; Villaverde, A. Surface Cell Growth engineering assisted by a novel bacterial nanomaterial. Adv. Materials, 2009, 21 (42), 4249-4253.
83. de Groot, N. S.; Ventura, S. Protein activity in bacterial inclusion bodies correlates with predicted aggregation rates. J. Biotechnol., 2006, 125 (1), 110-113.
84. Arie, J. P.; Miot, M.; Sassoon, N.; Betton, J. M. Formation of active inclusion bodies in the periplasm of Escherichia coli. Mol. Microbiol., 2006, 62 (2), 427-437.
85. Li, R. Y.; Cheng, C. Y. Investigation of inclusion body formation in recombinant Escherichia coli with a bioimaging system. J. Biosci. Bioeng., 2009, 107 (5), 512-515.
86. Rajan, R. S.; Illing, M. E.; Bence, N. F.; Kopito, R. R. Specificity in intracellular protein aggregation and inclusion body formation. Proc. Natl. Acad. Sci. USA, 2001, 98 (23), 13060-13065.
87. Zuniga, R. N.; Tolkach, A.; Kulozik, U.; Aguilera, J. M. Kinetics of formation and physicochemical characterization of thermallyinduced beta-lactoglobulin aggregates. J. Food Sci., 2010, 75 (5), E261-E268.
88. Wang, L. Towards revealing the structure of bacterial inclusion bodies. Prion., 2009, 3 (3), 139-145.
89. Singh, S. M.; Panda, A. K. Solubilization and refolding of bacterial inclusion body proteins. J. Biosci. Bioeng., 2005, 99 (4), 303-310.
90. Rinas, U.; Boone, T. C.; Bailey, J. E. Characterization of inclusion bodies in recombinant Escherichia coli producing high levels of porcine somatotropin. J. Biotechnol., 1993, 28 (2-3), 313-320.
91. Schrodel, A.; de, M. A. Characterization of the aggregates formed during recombinant protein expression in bacteria. BMC Biochem., 2005, 6, 10.
92. Ivanova, M. I.; Sawaya, M. R.; Gingery, M.; Attinger, A.; Eisenberg, D. An amyloid-forming segment of beta2-microglobulin suggests a molecular model for the fibril. Proc. Natl. Acad. Sci USA, 2004, 101 (29), 10584-10589.
93. Mukai, H.; Isagawa, T.; Goyama, E.; Tanaka, S.; Bence, N. F.; Tamura, A.; Ono, Y.; Kopito, R. R. Formation of morphologically similar globular aggregates from diverse aggregation-prone proteins in mammalian cells. Proc. Natl. Acad. Sci USA, 2005, 102 (31), 10887-10892.
94. Diez-Gil, C.; Krabbenborg, S.; Garcia-Fruitos, E.; Vazquez, E.; Rodriguez-Carmona, E.; Ratera, I.; Ventosa, N.; Seras-Franzoso, J.; Cano-Garrido, O.; Ferrer-Miralles, N.; Villaverde, A.; Veciana, J. The nanoscale properties of bacterial inclusion bodies and their effect on mammalian cell proliferation. Biomaterials, 2010, 31, 5805-5812.
95. McAllister, C.; Karymov, M. A.; Kawano, Y.; Lushnikov, A. Y.; Mikheikin, A.; Uversky, V. N.; Lyubchenko, Y. L. Protein interactions and misfolding analyzed by AFM force spectroscopy. J. Mol. Biol., 2005, 354 (5), 1028-1042.
96. Stine, W. B., Jr.; Dahlgren, K. N.; Krafft, G. A.; LaDu, M. J. characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J. Biol. Chem., 2003, 278 (13), 11612-11622.
97. Khurana, R.; Ionescu-Zanetti, C.; Pope, M.; Li, J.; Nielson, L.; Ramirez-Alvarado, M.; Regan, L.; Fink, A. L.; Carter, S. A. A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy. Biophys. J., 2003, 85 (2), 1135-1144.
98. Arimon, M.; ez-Perez, I.; Kogan, M. J.; Durany, N.; Giralt, E.; Sanz, F.; Fernandez-Busquets, X. Fine structure study of Abeta1-42 fibrillogenesis with atomic force microscopy. FASEB J., 2005, 19 (10), 1344-1346.
99. Alberti, S.; Halfmann, R.; King, O.; Kapila, A.; Lindquist, S. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell, 2009, 137 (1), 146-158.
100. Halfmann, R.; Lindquist, S. Screening for Amyloid Aggregation by Semi-Denaturing Detergent-Agarose Gel Electrophoresis. J. Vis. Exp., 2008, (17).
101. Bondos, S. E.; Bicknell, A. Detection and prevention of protein aggregation before, during, and after purification. Anal. Biochem., 2003, 316 (2), 223-231.
102. Jones, A. J. S. Analysis of Polypeptides and Proteins. Adv. Drug Deliv. Rev., 1993, 10, 29-90.
103. Stulik, K.; Pacakova, V.; Ticha, M. Some potentialities and drawbacks of contemporary size-exclusion chromatography. J. Biochem. Biophys. Methods, 2003, 56 (1-3), 1-13.
104. Ejima, D.; Yumioka, R.; Arakawa, T.; Tsumoto, K. Arginine as an effective additive in gel permeation chromatography. J. Chromatogr. A, 2005, 1094 (1-2), 49-55.
105. Philo, J. S. Methods for Structural Analysis of Protein Pharmaceuticals. In: Analytical Ultracentrifugation., AAPS Press: 2010.
106. Arakawa, T.; Philo, J. S.; Ejima, D.; Sato, H.; Tsumoto, K. Aggregation Analysis of Therapeutic Proteins, Part 3: Principles and Optimization of Field-Flow-Fractionation (FFF). BioProcess Int., 2007, 5 (10), 52-70.
107. Filipe, V.; Hawe, A.; Jiskoot, W. Critical evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates. Pharm. Res., 2010, 27 (5), 796-810.
108. Toledo-Rubio, V.; Vazquez, E.; Platas, G.; Domingo-Espin, J.; Unzueta, U.; Steinkamp, E.; Garcia-Fruitos, E.; Ferrer-Miralles, N.; Villaverde, A. Protein aggregation and soluble aggregate formation screened by a fast microdialysis assay. J. Biomol. Screen, 2010, 15 (4), 453-457.
109. de Marco, A. Minimal information: an urgent need to assess the functional reliability of recombinant proteins used in biological experiments. Microb. Cell Fact., 2008, 7, 20.