Inhibition of antithrombin and bovine serum albumin native state aggregation by heparin

Langmuir

Volumn 30, Issue 1, 2014, Pages 278-287

  Minsky, Burcu Baykal ^a   Zheng, Bingqian ^a   Dubin, Paul L ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION PROCESS; BIOLOGICAL PROCESS; BOVINE SERUM ALBUMINS; ELECTROSTATICALLY DRIVEN; EQUILIBRIUM ASSOCIATION CONSTANT; INHIBITION EFFECT; PROTEIN AGGREGATION; SULFATED POLYSACCHARIDES;

AGGLOMERATION; BODY FLUIDS; CAPILLARY ELECTROPHORESIS; FRACTAL DIMENSION; MAMMALS; POLYSACCHARIDES; PROTEINS;

AGGREGATES;

ANTITHROMBIN; BOVINE SERUM ALBUMIN; HEPARIN; RECOMBINANT PROTEIN;

ANIMAL; ARTICLE; CATTLE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; PH; PROTEIN CONFORMATION; PROTEIN FOLDING; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANTITHROMBINS; CATTLE; HEPARIN; HUMANS; HYDROGEN-ION CONCENTRATION; PROTEIN CONFORMATION; PROTEIN FOLDING; RECOMBINANT PROTEINS; SERUM ALBUMIN, BOVINE; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84892587144     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la4039232     Document Type: Article

References (56)

1. Suk, J. Y.; Zhang, F.; Balch, W. E.; Linhardt, R. J.; Kelly, J. W. Heparin Accelerates Gelsolin Amyloidogenesis† Biochemistry 2006, 45, 2234-2242
2. Bravo, R.; Arimon, M.; Valle-Delgado, J. J.; García, R.; Durany, N.; Castel, S.; Cruz, M.; Ventura, S.; Fernàndez-Busquets, X. Sulfated Polysaccharides Promote the Assembly of Amyloid β1-42 Peptide into Stable Fibrils of Reduced Cytotoxicity J. Biol. Chem. 2008, 283, 32471-32483
3. Nielsen, S. B.; Yde, P.; Giehm, L.; Sundbye, S.; Christiansen, G.; Mathiesen, J.; Jensen, M. H.; Jensen, P. H.; Otzen, D. E. Multiple Roles of Heparin in the Aggregation of p25α J. Mol. Biol. 2012, 421, 601-615
4. Vieira, T. C.; Reynaldo, D. P.; Gomes, M. P.; Almeida, M. S.; Cordeiro, Y.; Silva, J. L. Heparin Binding by Murine Recombinant Prion Protein Leads to Transient Aggregation and Formation of RN-Resistant Species J. Am. Chem. Soc. 2011, 133, 334-344
5. Silva, J. L.; Vieira, T. C.; Gomes, M. P.; Rangel, L. P.; Scapin, S. M.; Cordeiro, Y. Experimental Approaches to the Interaction of the Prion Protein with Nucleic Acids and Glycosaminoglycans: Modulators of the Pathogenic Conversion Methods 2011, 53, 306-317
6. Zhu, H.; Yu, J.; Kindy, M. S. Inhibition of Amyloidosis Using Low-Molecular-Weight Heparins Mol. Med. 2001, 7, 517-522
7. Wilhelmus, M. M.; de Waal, R. M.; Verbeek, M. M. Heat Shock Proteins and Amateur Chaperones in Amyloid-Beta Accumulation and Clearance in Alzheimer's Disease Mol. Neurobiol. 2007, 35, 203-216
8. Vilasi, S.; Sarcina, R.; Maritato, R.; De Simone, A.; Irace, G.; Sirangelo, I. Heparin Induces Harmless Fibril Formation in Amyloidogenic W7FW14F Apomyoglobin and Amyloid Aggregation in Wild-Type Protein In Vitro PLoS ONE 2011, 6
9. Bergamaschini, L.; Rossi, E.; Vergani, C.; De Simoni, M. G. Alzheimer's Disease: Another Target for Heparin Therapy Sci. World J. 2009, 9, 891-908
10. Miura, Y.; Yasuda, K.; Yamamoto, K.; Koike, M.; Nishida, Y.; Kobayashi, K. Inhibition of Alzheimer Amyloid Aggregation with Sulfated Glycopolymers Biomacromolecules 2007, 8, 2129-2134
11. Calamai, M.; Chiti, F.; Dobson, C. M. Amyloid Fibril Formation Can Proceed from Different Conformations of a Partially Unfolded Protein Biophys. J. 2005, 89, 4201-4210
12. Carrotta, R.; Manno, M.; Bulone, D.; Martorana, V.; Biagio, P. L. S. Protofibril Formation of Amyloid β-Protein at Low pH via a Noncooperative Elongation Mechanism J. Biol. Chem. 2005, 280, 30001-30008
13. Jain, S.; Udgaonkar, J. B. Defining the Pathway of Wormlike Amyloid Fibril Formation by the Mouse Prion Protein by Delineation of the Productive and Unproductive Oligomerization Reactions Biochemistry 2011, 50, 1153-1161
14. Park, S.; Saven, J. G. Simulation of pH-Dependent Edge Strand Rearrangement in Human Beta-2-microglobulin Protein Sci. 2006, 15, 200-207
15. Chiti, F.; Bucciantini, M.; Capanni, C.; Taddei, N.; Dobson, C. M.; Stefani, M. Solution Conditions Can Promote Formation of Either Amyloid Protofilaments or Mature Fibrils from the HypF N-Terminal Domain Protein Sci. 2001, 10, 2541-2547
16. Chiti, F.; Dobson, C. M. Amyloid Formation by Globular Proteins under Native Conditions Nat. Chem. Biol. 2009, 5, 15-22
17. Wang, G.; Johnson, A. J.; Kaltashov, I. A. Evaluation of Electrospray Ionization Mass Spectrometry as a Tool for Characterization of Small Soluble Protein Aggregates Anal. Chem. 2011, 84, 1718-1724
18. Zhou, A.; Carrell, R. W. Dimers Initiate and Propagate Serine Protease Inhibitor Polymerisation J. Mol. Biol. 2008, 375, 36-42
19. Vetri, V.; Librizzi, F.; Leone, M.; Militello, V. Thermal Aggregation of Bovine Serum Albumin at Different pH: Comparison with Human Serum Albumin Eur. Biophys. J. 2007, 36, 717-725
20. Holm, N. K.; Jespersen, S. K.; Thomassen, L. V.; Wolff, T. Y.; Sehgal, P.; Thomsen, L. A.; Christiansen, G.; Andersen, C. B.; Knudsen, A. D.; Otzen, D. E. Aggregation and Fibrillation of Bovine Serum Albumin Biochim. Biophys. Acta, Proteins Proteomics 2007, 1774, 1128-1138
21. Militello, V.; Casarino, C.; Emanuele, A.; Giostra, A.; Pullara, F.; Leone, M. Aggregation Kinetics of Bovine Serum Albumin Studied by FTIR Spectroscopy and Light Scattering Biophys. Chem. 2004, 107, 175-187
22. Xu, Y.; Seeman, D.; Yan, Y.; Sun, L.; Post, J.; Dubin, P. L. Effect of Heparin on Protein Aggregation: Inhibition versus Promotion Biomacromolecules 2012, 13, 1642-1651
23. Schreiber, G.; Haran, G.; Zhou, H. X. Fundamental Aspects of Protein-Protein Association Kinetics Chem. Rev. 2009, 109, 839-860
24. Vijayakumar, M.; Wong, K. Y.; Schreiber, G.; Fersht, A. R.; Szabo, A.; Zhou, H. X. Electrostatic Enhancement of Diffusion-Controlled Protein-Protein Association: Comparison of Theory and Experiment on Barnase and Barstar J. Mol. Biol. 1998, 278, 1015-1024
25. Giger, K.; Vanam, R. P.; Seyrek, E.; Dubin, P. L. Suppression of Insulin Aggregation by Heparin Biomacromolecules 2008, 9, 2338-2344
26. Meakin, P. A Historical Introduction to Computer Models for Fractal Aggregates J. Sol-Gel Sci. Technol. 1999, 15, 97-117
27. Kayitmazer, A. B.; Quinn, B.; Kimura, K.; Ryan, G. L.; Tate, A. J.; Pink, D. A.; Dubin, P. L. Protein Specificity of Charged Sequences in Polyanions and Heparins Biomacromolecules 2010, 11, 3325-3331
28. Bourgault, S.; Solomon, J. P.; Reixach, N. l.; Kelly, J. W. Sulfated Glycosaminoglycans Accelerate Transthyretin Amyloidogenesis by Quaternary Structural Conversion Biochemistry 2010, 50, 1001-1015
29. Kayitmazer, A. B.; Seeman, D.; Minsky, B. B.; Dubin, P. L.; Xu, Y. Protein-Polyelectrolyte Interactions Soft Matter 2013, 9, 2553-2583
30. Jones, L. S.; Yazzie, B.; Middaugh, C. R. Polyanions and the Proteome Mol. Cell. Proteomics 2004, 3, 746-769
31. Record, M. T., Jr.; Lohman, M. L.; De Haseth, P. Ion Effects on Ligand-Nucleic Acid Interactions J. Mol. Biol. 1976, 107, 145-158
32. Mascotti, D. P.; Lohman, T. M. Thermodynamic Extent of Counterion Release upon Binding Oligolysines to Single-Stranded Nucleic Acids Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 3142-3146
33. Fenley, M. O.; Russo, C.; Manning, G. S. Theoretical Assessment of the Oligolysine Model for Ionic Interactions in Protein-DNA Complexes J. Phys. Chem. B 2011, 115, 9864-9872
34. Mascotti, D. P.; Lohman, T. M. Thermodynamics of Charged Oligopeptide-Heparin Interactions Biochemistry 1995, 34, 2908-2915
35. Grymonpre, K. R.; Staggemeier, B. A.; Dubin, P. L.; Mattison, K. W. Identification by Integrated Computer Modeling and Light Scattering Studies of an Electrostatic Serum Albumin-Hyaluronic Acid Binding Site Biomacromolecules 2001, 2, 422-429
36. Seyrek, E.; Dubin, P. L.; Tribet, C.; Gamble, E. A. Ionic Strength Dependence of Protein-Polyelectrolyte Interactions Biomacromolecules 2003, 4, 273-282
37. Seyrek, E.; Dubin, P. L.; Henriksen, J. Nonspecific Electrostatic Binding Characteristics of the Heparin-Antithrombin Interaction Biopolymers 2007, 86, 249-259
38. Zhang, C.; Lillie, R.; Cotter, J.; Vaughan, D. Lysozyme Purification from Tobacco Extract by Polyelectrolyte Precipitation J. Chromatogr. A 2005, 1069, 107-112
39. Peram, T.; McDonald, P.; Carter-Franklin, J.; Fahrner, R. Monoclonal Antibody Purification Using Cationic Polyelectrolytes: An Alternative to Column Chromatography Biotechnol. Prog. 2010, 26, 1322-1331
40. Zhao, J. Y.; Ford, C. F.; Glatz, C. E.; Rougvie, M. A.; Gendel, S. M. Polyelectrolyte Precipitation of Beta-Galactosidase Fusions Containing Poly-Aspartic Acid Tails J. Biotechnol. 1990, 14, 273-283
41. Levi, V.; González Flecha, F. L. Reversible Fast-Dimerization of Bovine Serum Albumin Detected by Fluorescence Resonance Energy Transfer Biochim. Biophys. Acta, Proteins Proteomics 2002, 1599, 141-148
42. Rocchia, W.; Alexov, E.; Honig, B. Extending the Applicability of the Nonlinear Poisson-Boltzmann Equation: Multiple Dielectric Constants and Multivalent Ions† J. Phys. Chem. B 2001, 105, 6507-6514
43. Rocchia, W.; Sridharan, S.; Nicholls, A.; Alexov, E.; Chiabrera, A.; Honig, B. Rapid Grid-Based Construction of the Molecular Surface and the Use of Induced Surface Charge to Calculate Reaction Field Energies: Applications to the Molecular Systems and Geometric Objects J. Comput. Chem. 2002, 23, 128-137
44. Tanford, C.; Kirkwood, J. G. Theory of Protein Titration Curves. I. General Equations for Impenetrable Spheres J. Am. Chem. Soc. 1957, 79, 5333-5339
45. Xu, Y.; Yan, Y.; Seeman, D.; Sun, L.; Dubin, P. L. Multimerization and Aggregation of Native-State Insulin: Effect of Zinc Langmuir 2012, 28, 579-586
46. Yan, Y.; Seeman, D.; Zheng, B.; Kizilay, E.; Xu, Y.; Dubin, P. L. pH-Dependent Aggregation and Disaggregation of Native Beta-Lactoglobulin in Low Salt Langmuir 2013, 29, 4584-4593
47. Majhi, P. R.; Ganta, R. R.; Vanam, R. P.; Seyrek, E.; Giger, K.; Dubin, P. L. Electrostatically Driven Protein Aggregation: Beta-Lactoglobulin at Low Ionic Strength Langmuir 2006, 22, 9150-9159
48. Barbosa, L. R.; Ortore, M. G.; Spinozzi, F.; Mariani, P.; Bernstorff, S.; Itri, R. The Importance of Protein-Protein Interactions on the pH-Induced Conformational Changes of Bovine Serum Albumin: A Small-Angle X-ray Scattering Study Biophys. J. 2010, 98, 147-157
49. El Kadi, N.; Taulier, N.; Le Huerou, J. Y.; Gindre, M.; Urbach, W.; Nwigwe, I.; Kahn, P. C.; Waks, M. Unfolding and Refolding of Bovine Serum Albumin at Acid pH: Ultrasound and Structural Studies Biophys. J. 2006, 91, 3397-3404
50. Estey, T.; Kang, J.; Schwendeman, S. P.; Carpenter, J. F. BSA Degradation under Acidic Conditions: A Model for Protein Instability during Release from PLGA Delivery Systems J. Pharm. Sci. 2006, 95, 1626-1639
51. Zhou, A.; Stein, P. E.; Huntington, J. A.; Carrell, R. W. Serpin Polymerization Is Prevented by a Hydrogen Bond Network That Is Centered on His-334 and Stabilized by Glycerol J. Biol. Chem. 2003, 278, 15116-15122
52. Wang, K.; Kurganov, B. I. Kinetics of Heat- and Acidification-Induced Aggregation of Firefly Luciferase Biophys. Chem. 2003, 106, 97-109
53. Kurganov, B. I. Kinetics of Protein Aggregation. Quantitative Estimation of the Chaperone-Like Activity in Test-Systems Based on Suppression of Protein Aggregation Biochemistry (Moscow) 2002, 67, 409-422
54. Olson, S. T.; Bjork, I.; Sheffer, R.; Craig, P. A.; Shore, J. D.; Choay, J. Role of the Antithrombin-Binding Pentasaccharide in Heparin Acceleration of Antithrombin-Proteinase Reactions. Resolution of the Antithrombin Conformational Change Contribution to Heparin Rate Enhancement J. Biol. Chem. 1992, 267, 12528-12538
55. Jho, Y. S.; Safran, S. A.; In, M.; Pincus, P. A. Effect of Charge Inhomogeneity and Mobility on Colloid Aggregation Langmuir 2012, 28, 8329-8336
56. Magazu, S.; Maisano, G.; Mallamace, F.; Micali, N. Growth of Fractal Aggregates in Water Solutions of Macromolecules by Light Scattering Phys. Rev. A 1989, 39, 4195-4200