Effects of calcium binding on structure and autolysis regulation in trypsins. A molecular dynamics investigation

Journal of Chemical Theory and Computation

Volumn 1, Issue 6, 2005, Pages 1286-1297

  Papaleo, Elena ^a   Fantucci, Piercarlo ^a   De Gioia, Luca ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33747770055     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct050092o     Document Type: Article

References (48)

1. Hedstrom, L. Serine protease mechanism and specificity. Chem. Rev. 2002, 102, 4501-4524.
2. Burdette, S. C.; Lippard, S. J. Meeting of the minds: metalloneurochemistry. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 3605-3610.
3. Smalas, A. O.; Heimstad, E. S.; Hordvik, A.; Willassen, N. P.; Male, R. Cold adaptation of enzymes: structural comparison between salmon and bovine trypsins. Proteins 1994, 20, 149-166.
4. Read, R. J.; James, M. N. Refined crystal structure of Streptomyces griseus trypsin at 1.7 Å resolution. J. Mol. Biol. 1988, 200, 523-551.
5. Toth, M. S.; Graf, L.; Toth, M. Trypsinogen stabilization by mutation Arg 117→His: a unifying pathomechanism for hereditary pancreatitis? Biochim. Biophys. Res. Commun. 1999, 264, 505-508.
6. Sipos, T.; Merkel, J. R. An effect of calcium ions on the activity, heat stability and structure of trypsin. Biochemistry 1970, 9, 2766-2775.
7. Gabel, D.; Kasche, V. Autolysis of beta-trypsin. Influence of calcium ions and heat. Acta Chem. Scand. 1973, 27, 1971-1981.
8. Bulaj, G.; Otlewski, J. Denaturation of free and complexed bovine trypsinogen with the calcium ion, dipeptide Ile-Val and basic pancreatic trypsin inhibitor. Eur. J. Biochem. 1994, 223, 939-946.
9. Bulaj, G.; Otlewski, J. Ligand-induced changes in the conformational stability of bovine trypsinogen and their implications for the protein function. J. Mol. Biol. 1995, 247, 701-716.
10. Buono, R. A.; Prestrelski, S. J.; Liebman, M. N.; Byler, D. M. Infrared spectroscopic studies of calcium binding to inhibited beta-trypsins. Biochim. Biophys. Acta 1994, 204, 124-128.
11. Smith, R. L.; Shaw, E. Pseudotrypsin. A modified bovine trypsin produced by limited autodigestion. J. Biol. Chem. 1969, 244, 4704-4712.
12. Maroux, S.; Desnuelle, P. On some autolyzed derivatives of bovine trypsin. Biochim. Biophys. Acta 1969, 181, 59-72.
13. Varallyay, E.; Pal, G.; Patthy, A.; Szilagyi, L.; Graf, L. Two mutations in rat trypsin confer resistance against autolysis. Biochim. Biophys. Res. Commun. 1998, 243, 56-60.
14. Kaslik, G.; Patthy, A.; Balint, M.; Graf, L. Trypsin complexed with alpha 1-proteinase inhibitor has an increased structural flexibility. FEBS Lett. 1995, 370, 179-183.
15. Li, X. F.; Nie, X.; Tang, J. G. Anti-autolysis of trypsin by modification of autolytic site Arg117. Biochim. Biophys. Res. Commun. 1998, 250, 235-239.
16. Outzen, H.; Berglund, G. I.; Smalas, A. O.; Willassen, N. P. Temperature and pH sensitivity of trypsins from Atlantic Salmon in comparison with bovine and porcine trypsin. Comp. Biochem. Physiol. B 1996, 115, 33-45.
17. Hjelmeland, K.; Raa, J. Characteristics of two trypsin type isozymes isolated from the artic fish capelin. Comp. Biochem. Physiol. B 1982, 71, 557-562.
18. Reeck, G. R.; Neurath, H. Pancreatic trypsinogen from the African lungfish. Biochemistry 1972, 11, 503-510.
19. Fontana, A.; Fassina, G.; Vita, C.; Dal Zoppo, D.; Zamai, M.; Zambonin, M. Correlation between sites of limited proteolysis and segmental mobility in thermolysin. Biochemistry 1986, 25, 1847-1951.
20. Novotny, J.; Bruccoleri, R. E. Correlation among sites of limited proteolysis, enzyme accessibility and segmental mobility. FEBS Lett. 1987, 211, 185-189.
21. Norberg, J.; Nilsson, L. Advances in biomolecular simulations: methodology and recent applications. Q. Rev. Biophys. 2003, 36, 257-306.
22. Wang, W.; Donini, O.; Reyes, C. M.; Kollman, P. A. Biomolecular simulations: recent developments in force fields, simulations of enzyme-catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 211-243.
23. Hansson, T.; Oostenbrink, C.; van Gusteren, W. Molecular dynamics simulations. Curr. Opin. Struct. Biol. 2002, 12, 190-196.
24. Heimstad, E. S.; Hansen, L. K.; Smalas, A. O. Comparative molecular dynamics simulation studies of salmon and bovine trypsins in aqueous solution. Protein Eng. 1995, 8, 379-388.
25. Brandsdal, B. O.; Heimstad, E. S.; Sylte, I.; Smalas, A. O. Comparative molecular dynamics of mesophilic and psy-crophilic protein homologues studied by 1.2 ns simulations. J. Biomol. Struct. Dyn. 1999, 17, 493-506.
26. Iyer, L. K.; Qasba, P. K. Molecular dynamics simulation of α-lactalbumin and calcium binding c-type lysozyme. Protein Eng. 1999, 12, 129-139.
27. Cates, S. M.; Teodoro, M. L.; Phillips, G. N. Molecular mechanism of calcium and magnesium binding to paralbumin. Biophys. J. 2002, 82, 1133-1146.
28. Yang, C.; Jas, G. S.; Kuczera, K. Structure, dynamics and interaction with kinase targets: computer simulations of calmodulin. Biochim. Biophys. Acta 2004, 1697, 289-300.
29. Komeiji, Y.; Ueno, Y.; Uebayasi, M. Molecular dynamics simulations revealed Ca (2+)-dependent conformational change of calmodulin. FEBS Lett. 2002, 521, 133-139.
30. Berman, H. M.; Westbrook, J.; Feng, Z.; Gilliland, G.; Bhat, T. N.; Weissing, H.; Shindyalov, I. N.; Bourne, P. E. The Protein Data Bank. Nucleic Acids Res. 2000, 28, 235-242.
31. Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389-3402.
32. Higgins, D.; Thompson, J.; Gibson, T.; Thompson, J. D.; Higgins, D. G.; Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalities and weight matrix choice. Nucleic Acids Res. 1994, 22, 4673-4680.
33. * University of Groningen: Groningen, The Netherlands, 2002. www.gromacs.org.
34. Marquart, M.; Walter, J.; Deisenhofer, J.; Bode, W.; Huber, R. The geometry of the reactive site and of the peptide groups in trypsin, trypsinogen and its complexes with inhibitors. Acta Crystallogr., Sect. B. 1983, 39, 480.
35. Smalas, A. O.; Hordvik, A.; Hansen, L. K.; Hough, E.; Jynge, K. Crystallization and preliminary X-ray crystallographic studies of benzamidine-inhibited trypsin from the North Atlantic Salmon (Salmo salar). J. Mol. Biol. 1990, 214, 355-358.
36. Berendsen, H. J. C.; Postma, J. P. M.; van Gusteren, W. F.; Hermans, J. Interaction models for water in relation to protein hydratation; Reidel: Dordrecht, The Netherlands, 1981; pp 331-342.
37. Berendsen, H. J. C.; Postma, J. P. M.; van Gusteren, W. F.; Di Nola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath. J. Client. Phys. 1984, 81, 3684-3690.
38. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraahje, J. G. E. M. LINCS: a linear constraint solver for molecular interactions. J. Commit. Client. 1997, 18, 1463-1472.
39. Darden, T. A.; York, D. M.; Pedersen, L. G. Particle mesh Ewald. An N log (N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089-10092.
40. Jarvis, R. A.; Patrick, E. A. Clustering using a similarity measure based on shared nearest neighbors. IEE Trans. Commit. 1973, 11, 1025-1034.
41. Kabsch, W.; Sander, C. Dictionary of Protein Secondary Structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22, 2577-2637.
42. Hubbard, S. J.; Thortnon, J. M. NACCESS; 1993.
43. Humphrey, W.; Dalke, A.; Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 1996, 14, 33-38.
44. Tsai, J.; Levitt, M.; Baker, D. Hierarchy of structure loss in MD simulations of src SH3 domain unfolding. J. Mol. Biol. 1999, 291, 215-225.
45. Hess, B. Convergence of sampling in protein simulations. Phys. Rev. E. 2002, 65, 031910/1-031910/10.
46. Smith, L. J.; Daura, X.; van Gusteren, W. F. Assesing equilibration and convergence in biomolecular simulations. Proteins 2002, 48, 487-496.
47. Note that the analysis of single trajectories led to similar results, with some differences in the intensity of the peaks in the rmsf plots.
48. Leiros, H. K.; Willassen, N. P.; Smalas, A. O. Structural comparison of psycrophilic and mesophilic trypsins. Elucidating the molecular basis of cold-adaptation. Eur. J. Biochem. 2000, 267, 1039-1049.