Multistep aggregation pathway of human interIeukin-1 receptor antagonist: Kinetic, structural, and morphological characterization

Biophysical Journal

Volumn 96, Issue 1, 2009, Pages 199-208

  Krishnan, Sampathkumar ^a   Raibekas, Andrei A ^a  

^a AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; FLUORESCENT DYE; RECOMBINANT PROTEIN;

ARTICLE; BETA SHEET; INFRARED SPECTROSCOPY; KINETICS; MORPHOLOGY; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; SCANNING ELECTRON MICROSCOPE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE; SCANNING ELECTRON MICROSCOPY; TEMPERATURE;

FLUORESCENT DYES; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; KINETICS; MICROSCOPY, ELECTRON, SCANNING; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TEMPERATURE;

EID: 58849107789     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.10.002     Document Type: Article

References (54)

1. Cleland, J. F., M. F. Powell, and S. J. Shire. 1993. The development of stable protein formulations: a close look at protein aggregation, deamidation, and oxidation. Crit. Rev. Ther. Drug Carrier Syst. 10:307-377.
2. Carpenter, J. F., B. S. Kendrick, B. S. Chang, M. C. Manning, and T. W. Randolph. 1999. Inhibition of stress-induced aggregation of protein therapeutics. Methods Enzymol. 309:236-255.
3. Fink, A. L. 1998. Protein aggregation: folding aggregates, inclusion bodies and amyloid. Fold. Des. 3:R9-R23.
4. Manning, M. C., K. Patel, and R. T. Borchardt. 1989. Stability of protein pharmaceuticals. Pharm. Res. 6:903-918.
5. Koo, E. H., P. T. Lansbury, and J. W. Kelly. 1999. Amyloid diseases: abnormal protein aggregation in neurodegeneration. Proc. Natl. Acad. Sci. USA. 96:9989-9990.
6. Hardy, J., and D. J. Selkoe. 2002. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science. 297:353-356.
7. Kyle, R. A. 1994. Monoclonal proteins and renal disease. Annu. Rev. Med. 45:71-77.
8. Kendrick, B. S., B. S. Chang, T. Arakawa, B. Peterson, T. W. Randolph, et al. 1997. Preferential exclusion of sucrose from recombinant interleukin-1 receptor antagonist: role in restricted conformational mobility and compaction of native state. Proc. Natl. Acad. Sci. USA. 94:11917-11922.
9. Smith, A. V., and C. K. Hall. 2001. Protein refolding versus aggregation: computer simulation on an intermediate-resolution protein model. J.Mol. Biol. 312:187-202.
10. Chi, E. Y., S. Krishnan, T. W. Randolph, and J. F. Carpenter. 2003. Physical stability of proteins in aqueous solution: mechanism and driving forces in nonnative protein aggregation. Pharm. Res. 20:13251336.
11. Krishnan, S., E. Y. Chi, J. N. Webb, et al. 2002. Aggregation of granulocyte colony stimulating factor under physiological conditions: characterization and thermodynamic inhibition. Biochemistry. 41: 6422-6431.
12. Webb, J. N., S. D. Webb, J. L. Cleland, J. F. Carpenter, and T. W. Randolph. 2001. Partial molar volume, surface area, and hydration changes for equilibrium unfolding and formation of aggregation transition state:high-pressure and co-solute studies on recombinant human IFN-gamma. Proc. Natl. Acad. Sci. USA. 98:7259-7264.
13. Wood, S. J., J. Wypych, S. Steavenson, J. C. Louis, M. Citron, et al.1999. α-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J.Biol. Chem. 274:1950919512.
14. Ferrone, F. 1999. Analysis of protein aggregation kinetics. Methods Enzymol. 309:256-274.
15. Kim, Y. S., S. P. Cape, E. Chi, R. Raffen, P. Wilkins-Stevens, et al. 2001. Counteracting effects of renal solutes on amyloid fibril formation by immunoglobulin light chains. J. Biol. Chem. 276:1626-1633.
16. Thirumalai, D., D. K. Klimov, and R. I. Dima. 2003. Emerging ideas on the molecular basis of protein and peptide aggregation. Curr. Opin. Struct. Biol. 13:146-159.
17. Fandrich, M., M. A. Fletcher, and C. M. Dobson. 2001. Amyloid fibrils from muscle myoglobin. Nature. 410:165-166.
18. Vetri, V., C. Canale, A. Relini, F. Librizzi, V. Militello, et al. 2007. Amyloid fibrils formation and amorphous aggregation in concanavalin A. Biophys. Chem. 125:184-190.
19. Nielsen, L., S. Frokjaer, J. Brange, V. N. Uversky, and A. L. Fink. 2001. Probing the mechanism of insulin fibril formation with insulin mutants. Biochemistry. 40:8397-8409.
20. Sambashivan, S., Y. Liu, M. R. Sawaya, M. Gingery, and D. Eisenberg. 2005. Amyloid-like fibrils of ribonuclease A with three-dimensional domain-swapped and native-like structure. Nature. 437:266-269.
21. Hills, R. D. Jr., and C. L. Brooks III. 2007. Hydrophobic cooperativity as a mechanism for amyloid nucleation. J. Mol. Biol. 368:894-901.
22. Raman, B., E. Chatani, M. Kihara, T. Ban, M. Sakai, et al. 2005. Critical balance of electrostatic and hydrophobic interactions is required for β2-microglobulin amyloid fibril growth and stability. Biochemistry. 44:1288-1299.
23. Ruano, M. L. F., I. Garcia-Verdugo, E. Miguel, J. Perez-Gil, and C. Casals. 2000. Self-aggregation of surfactant protein A. Biochemistry. 39:6529-6537.
24. Wang, K., and B. I. Kurganov. 2003. Kinetics of heat- and acidification-induced aggregation of firefly luciferase. Biophys. Chem. 106:97-109.
25. Raibekas, A. A., E. J. Bures, C. C. Siska, T. Kohno, R. F. Latypov, et al. 2005. Anion binding and controlled aggregation of human interleukin-1 receptor antagonist. Biochemistry. 44:9871-9879.
26. Roberts, C. J. 2007. Non-native protein aggregation kinetics. Biotech- nol. Bioeng. 98:927-938.
27. Frieden, C. 2007. Protein aggregation processes: in search of the mechanism. Protein Sci. 16:2334-2344.
28. Liu, J., J. D. Andya, and S. J. Shire. 2006. A critical review of analytical ultracentrifugation and field flow fractionation methods for measuring protein aggregation. AAPS J. 8:E580-E589.
29. Latypov, R. F., T. S. Harvey, D. Liu, P. V. Bondarenko, T. Kohno, et al. 2007. Biophysical characterization of structural properties and folding of interleukin-1 receptor antagonist. J. Mol. Biol. 368:1187-1201.
30. Arend, W. P. 2002. The balance between IL-1 and IL-1ra in disease. Cytokine Growth Factor Rev. 13:323-340.
31. Murzin, A. G., A. M. Lesk, and C. Chothia. 1992. β-trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors interleukins-1 β and 1 α and fibroblast growth factors. J. Mol. Biol. 223:531-543.
32. Vigers, G. P. A., P. Caffes, R. J. Evans, R. C. Thompson, S. P. Eisen-berg, et al. 1994. X-ray structure of interleukin-1 receptor antagonist at 2.0-A resolution. J. Biol. Chem. 269:12874-12879.
33. Schreuder, H. A., J. M. Rondeau, C. Tardif, A. Soffientini, E. Sarubbi, et al. 1995. Refined crystal structure of the interleukin-1 receptor antagonist. Presence of a disulfide link and a cis-proline. Eur. J. Biochem. 227:838-847.
34. Ansevin, A. T., and M. A. Lauffer. 1963. Polymerization-depolymerization of tobacco mosaic virus protein. I. Kinetics. Biophys. J. 3:239-251.
35. Smith, C. E., and M. A. Lauffer. 1967. Polymerization-depolymerization of tobacco mosaic virus protein. VIII. Light-scattering studies. Biochemistry. 6:2457-2465.
36. Jarrett, J. T., and P. T. Lansbury, Jr. 1992. Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry. 31:12345-12352.
37. Dong, A., and W. S. Caughey. 1994. Infrared methods for study of hemoglobin reactions and structures. Methods Enzymol. 232:139-175.
38. Kendrick, B. S., A. Dong, S. D. Allison, M. C. Manning, and J. F. Carpenter. 1996. Quantitation of the area of overlap between second-derivative amide I infrared spectra to determine the structural similarity of a protein in different states. J. Pharm. Sci. 85:155-158.
39. Seefeldt, M. B., Y. S. Kim, K. P. Tolley, J. Seely, J. F. Carpenter, et al. 2005. High pressure studies of aggregation of recombinant human inter-leukin-1 receptor antagonist: thermodynamics, kinetics and application of accelerated formulation studies. Protein Sci. 14:2258-2266.
40. Fogler, H. S. 2006. Collection and analysis of rate data. In Elements of Chemical Reaction Engineering, 4th ed. Prentice Hall, Upper Saddle River, NJ. 277-279.
41. Roy, S., D. Katayama, A. Dong, B. A. Kerwin, T. W. Randolph, et al. 2006. Temperature dependence of benzyl alcohol and 8-anilinonaphtha-lene-1-sulfonate- induced aggregation of recombinant human interleukin-1 receptor antagonist. Biochemistry. 45:3898-3911.
42. Latypov, R. F., D. Liu, K. Gunasekaran, T. S. Harvey, V. I. Razinkov, et al. 2008. Structural and thermodynamic effects of ANS binding to human interleukin-1 receptor antagonist. Protein Sci. 17:652-663.
43. Sehorn, M. G., S. V. Slepenkov, and S. N. Witt. 2002. Characterization of two partially unfolded intermediates of the molecular chaperone DnaK at low pH. Biochemistry. 41:8499-8507.
44. Hoyer, W., T. Antony, D. Cherny, G. Heim, T. M. Jovin, et al. 2002. Dependence of α-synuclein aggregate morphology on solution conditions. J. Mol. Biol. 322:383-393.
45. Kim, Y. S., T. W. Randolph, F. J. Stevens, and J. F. Carpenter. 2002. Kinetics and energetics of assembly, nucleation, and growth of aggre gates and fibrils for an amyloidogenic protein. Insights into transition states from pressure, temperature, and co-solute studies. J. Biol. Chem. 277:27240-27246.
46. Giasson, B. I., K. Uryu, J. Q. Trojanowski, and V. M.-Y. Lee. 1999. Mutant and wild type human α-synucleins assemble into elongated filaments with distinct morphologies in vitro. J. Biol. Chem. 274:7619-7622.
47. Narhi, L., S. J. Wood, S. Steavenson, Y. Jiang, G. M. Wu, et al. 1999. Both familial Parkinson's disease mutations accelerate α-synuclein aggregation. J. Biol. Chem. 274:9843-9846.
48. Guo, B., S. Kao, H. McDonald, A. Asanov, L. L. Combs, et al. 1999. Correlation of second viral coefficients and solubilities useful in protein crystal growth. J. Cryst. Growth. 196:424-433.
49. Haas, C., and J. Drenth. 1999. Understanding protein crystallization on the basis of the phase diagram. J. Cryst. Growth. 196:388-394.
50. Cerda-Costa, N., A. Esteras-Chopo, F. X. Aviles, L. Serrano, and V. Villegas. 2007. Early kinetics of amyloid fibril formation reveals conformational reorganisation of initial aggregates. J. Mol. Biol. 366:1351-1363.
51. Serio, T. R., A. G. Cashikar, A. S. Kowal, G. J. Sawicki, J. J. Moslehi, et al. 2000. Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science. 289:13171321.
52. Chiti, F., N. Taddei, F. Baroni, C. Capanni, M. Stefani, et al. 2002. Kinetic partitioning of protein folding and aggregation. Nat. Struct. Biol. 9:137-143.
53. Meyer, P. S., J. W. Yung, and J. H. Ausubel. 1999. A primer on logistic growth and substitution: the mathematics of the Loglet lab software. Technol. Forecast. Soc. Change. 61:247-271.
54. Anderson, G. M. 2005. Defining our terms. In Thermodynamics of Natural Systems, 2nd ed. Cambridge University Press, New York. 10-30.