The role of salt bridges on the temperature adaptation of aqualysin I, a thermostable subtilisin-like proteinase

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 12, 2014, Pages 2174-2181

  Jónsdóttir, Lilja B ^a   Ellertsson, Brynjar Ö ^a   Invernizzi, Gaetano ^b   Magnúsdóttir, Manuela ^a   Thorbjarnardóttir, Sigríur H ^a   Papaleo, Elena ^b   Kristjánsson, Magnús M ^a  

^a UNIVERSITY OF ICELAND   (Iceland)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Molecular dynamics; Protease; Protein stability; Salt bridges; Subtilisin like; Thermophilic

Indexed keywords

AQUALYSIN I; SERINE PROTEINASE; SUBTILISIN; UNCLASSIFIED DRUG;

ARTICLE; ENZYME ACTIVITY; GENE MUTATION; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SALT BRIDGE; SITE DIRECTED MUTAGENESIS; TEMPERATURE ACCLIMATIZATION; THERMOSTABILITY;

EID: 84907484440     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.08.011     Document Type: Article

References (68)

1. S.T. Kwon, I. Terada, H. Matsuzawa, and T. Ohta Nucleotide sequence of the gene for aqualysin I (a thermophilic alkaline serine protease) of Thermus aquaticus YT-1 and characteristics of the deduced primary structure of the enzyme Eur. J. Biochem. 173 1988 491 497
2. H. Matsuzawa, K. Tokugawa, M. Hamaoki, M. Mizoguchi, H. Taguchi, I. Terada, S.T. Kwon, and T. Ohta Purification and characterization of aqualysin I (a thermophilic alkaline serine protease) produced by Thermus aquaticus YT-1 Eur. J. Biochem. 171 1988 441 447
3. I. Terada, S.T. Kwon, Y. Miyata, H. Matsuzawa, and T. Ohta Unique precursor structure of an extracellular protease, aqualysin I, with NH2- and COOH-terminal pro-sequences and its processing in Escherichia coli J. Biol. Chem. 265 1990 6576 6581
4. K. Kurosaka, T. Ohta, and H. Matsuzawa A 38 kDa precursor protein of aqualysin I (a thermophilic subtilisin-type protease) with a C-terminal extended sequence: its purification and in vitro processing Mol. Microbiol. 20 1996 385 389
5. R.J. Siezen, and J.A. Leunissen Subtilases: the superfamily of subtilisin-like serine proteases Protein Sci. 6 1997 501 523
6. M.M. Kristjánsson Thermostable subtilases (sutlisin-like serine proteinases) S. Sen, L. Nilsson, Thermostable Proteins. Structural stability and Design 2012 CRC Press Boca Raton 67 104
7. C. Betzel, S. Gourinath, P. Kumar, P. Kaur, M. Perbandt, S. Eschenburg, and T.P. Singh Structure of a serine protease proteinase K from Tritirachium album limber at 0.98 Å resolution Biochemistry 40 2001 3080 3088
8. B.L. Barnett, P.R. Green, L.C. Strickland, J.D. Oliver, and T. Rydel J.F: Sullivan, Aqualysin I: the crystal structure of a serine protease from an extreme thermophile, Thermus aquaticus YT-1 (release date: 28.03.2012) 2014 (in press)
9. J. Arnórsdóttir, M.M. Kristjánsson, and R. Ficner Crystal structure of a subtilisin-like serine proteinase from a psychrotrophic Vibrio species reveals structural aspects of cold adaptation FEBS J. 272 2005 832 845
10. N. Coquelle, E. Fioravanti, M. Weik, F. Vellieux, and D. Madern Activity, stability and structural studies of lactate dehydrogenases adapted to extreme thermal environments J. Mol. Biol. 374 2007 547 562
11. R. Jaenicke, and G. Böhm The stability of proteins in extreme environments Curr. Opin. Struct. Biol. 8 1998 738 748
12. E. Papaleo, M. Tiberti, G. Invernizzi, M. Pasi, and V. Ranzani Molecular determinants of enzyme cold adaptation: comparative structural and computational studies of cold- and warm-adapted enzymes Curr. Protein Pept. Sci. 12 2011 657 683
13. C. Vieille, and G.J. Zeikus Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability Microbiol. Mol. Biol. Rev. 65 2001 1 43
14. P.A. Fields Review: protein function at thermal extremes: balancing stability and flexibility Comp. Biochem. Physiol. A Mol. Integr. Physiol. 129 2001 417 431
15. P.A. Fields, and G.N. Somero Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes Proc. Natl. Acad. Sci. U. S. A. 95 1998 11476 11481
16. K.S. Siddiqui, and R. Cavicchioli Cold-adapted enzymes Annu. Rev. Biochem. 75 2006 403 433
17. M.M. Kristjánsson, and B. Ásgeirsson Properties of extremophilic enzymes and their importance in food science and technology J.R. Whitaker, A.G.J. Voragen, D.W.S. Wong, Handbook of Food and Enzymology 2002 Marcel Decker, Inc. New York 77 100
18. A. Razvi, and J.M. Scholtz Lessons in stability from thermophilic proteins Protein Sci. 15 2006 1569 1578
19. G. Feller Protein stability and enzyme activity at extreme biological temperatures J. Phys. Condens. Matter 22 2010 323101
20. A.H. Elcock The stability of salt bridges at high temperatures: implications for hyperthermophilic proteins J. Mol. Biol. 284 1998 489 502
21. A. Karshikoff, and R. Ladenstein Ion pairs and the thermotolerance of proteins from hyperthermophiles: a "traffic rule" for hot roads Trends Biochem. Sci. 26 2001 550 556
22. S. Kumar, and R. Nussinov How do thermophilic proteins deal with heat? Cell. Mol. Life Sci. 58 2001 1216 1233
23. A. Szilágyi, and P. Závodszky Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey Structure 8 2000 493 504
24. L. Xiao, and B. Honig Electrostatic contributions to the stability of hyperthermophilic proteins J. Mol. Biol. 289 1999 1435 1444
25. E. Maugini, D. Tronelli, F. Bossa, and S. Pascarella Structural adaptation of the subunit interface of oligomeric thermophilic and hyperthermophilic enzymes Comput. Biol. Chem. 33 2009 137 148
26. G. Gianese, F. Bossa, and S. Pascarella Comparative structural analysis of psychrophilic and meso- and thermophilic enzymes Proteins 47 2002 236 249
27. A.G. Gvritishvili, A.V. Gribenko, and G.I. Makhatadze Cooperativity of complex salt bridges Protein Sci. 17 2008 1285 1290
28. E. Papaleo, G. Renzetti, G. Invernizzi, and B. Asgeirsson Dynamics fingerprint and inherent asymmetric flexibility of a cold-adapted homodimeric enzyme. A case study of the Vibrio alkaline phosphatase Biochim. Biophys. Acta 1830 2013 2970 2980
29. H.R. Bosshard, D.N. Marti, and I. Jelesarov Protein stabilization by salt bridges: concepts, experimental approaches and clarification of some misunderstandings J. Mol. Recognit. 17 2004 1 16
30. I. Jelesarov, and A. Karshikoff Defining the role of salt bridges in protein stability Methods Mol. Biol. 490 2009 227 260
31. Z.S. Hendsch, and B. Tidor Do salt bridges stabilize proteins? A continuum electrostatic analysis Protein Sci. 3 1994 211 226
32. P. Phelan, A.A. Gorfe, I. Jelesarov, D.N. Marti, J. Warwicker, and H.R. Bosshard Salt bridges destabilize a leucine zipper designed for maximized ion pairing between helices Biochemistry 41 2002 2998 3008
33. C.V. Sindelar, Z.S. Hendsch, and B. Tidor Effects of salt bridges on protein structure and design Protein Sci. 7 1998 1898 1914
34. S. Kumar, and R. Nussinov Different roles of electrostatics in heat and in cold: adaptation by citrate synthase Chembiochem 5 2004 280 290
35. M. Olufsen, E. Papaleo, A.O. Smalås, and B.O. Brandsdal Ion pairs and their role in modulating stability of cold- and warm-active uracil DNA glycosylase Proteins 71 2008 1219 1230
36. E. Papaleo, M. Olufsen, L. De Gioia, and B.O. Brandsdal Optimization of electrostatics as a strategy for cold-adaptation: a case study of cold- and warm-active elastases J. Mol. Graph. Model. 26 2007 93 103
37. S. Kumar, and R. Nussinov Fluctuations in ion pairs and their stabilities in proteins Proteins 43 2001 433 454
38. S. Kumar, and R. Nussinov Relationship between ion pair geometries and electrostatic strengths in proteins Biophys. J. 83 2002 1595 1612
39. P. Strop, and S.L. Mayo Contribution of surface salt bridges to protein stability Biochemistry 39 2000 1251 1255
40. C.N. Pace, R.W. Alston, and K.L. Shaw Charge-charge interactions influence the denatured state ensemble and contribute to protein stability Protein Sci. 9 2000 1395 1398
41. J.H. Tomlinson, S. Ullah, P.E. Hansen, and M.P. Williamson Characterization of salt bridges to lysines in the protein G B1 domain J. Am. Chem. Soc. 131 2009 4674 4684
42. M.M. Kristjánsson, O.T. Magnússon, H.M. Gudmundsson, G.A. Alfredsson, and H. Matsuzawa Properties of a subtilisin-like proteinase from a psychrotrophic Vibrio species comparison with proteinase K and aqualysin I Eur. J. Biochem. 260 1999 752 760
43. J. Arnórsdottir, R.B. Smáradóttir, O.T. Magnússon, S.H. Thorbjarnardóttir, G. Eggertsson, and M.M. Kristjánsson Characterization of a cloned subtilisin-like serine proteinase from a psychrotrophic Vibrio species Eur. J. Biochem. 269 2002 5536 5546
44. A.G. Sigurdardóttir, J. Arnórsdóttir, S.H. Thorbjarnardóttir, G. Eggertsson, K. Suhre, and M.M. Kristjánsson Characteristics of mutants designed to incorporate a new ion pair into the structure of a cold adapted subtilisin-like serine proteinase Biochim. Biophys. Acta 1794 2009 512 518
45. A.R. Sigtryggsdóttir, E. Papaleo, S.H. Thorbjarnardóttir, and M.M. Kristjánsson Flexibility of cold- and heat-adapted subtilisin-like serine proteinases evaluated with fluorescence quenching and molecular dynamics Biochim. Biophys. Acta 1844 2014 705 712
46. J. Arnórsdóttir, M. Magnúsdóttir, O.H. Fricrossed d signjónsson, and M.M. Kristjánsson The effect of deleting a putative salt bridge on the properties of the thermostable subtilisin-like proteinase, aqualysin I Protein Pept. Lett. 18 2011 545 551
47. G.G. Dodson, D.P. Lane, and C.S. Verma Molecular simulations of protein dynamics: new windows on mechanisms in biology EMBO Rep. 9 2008 144 150
48. R.O. Dror, R.M. Dirks, J.P. Grossman, H. Xu, and D.E. Shaw Biomolecular simulation: a computational microscope for molecular biology Annu. Rev. Biophys. 41 2012 429 452
49. D.E. Shaw, P. Maragakis, K. Lindorff-Larsen, S. Piana, R.O. Dror, M.P. Eastwood, J.A. Bank, J.M. Jumper, J.K. Salmon, Y. Shan, and W. Wriggers Atomic-level characterization of the structural dynamics of proteins Science 330 2010 341 346
50. S. Piana, K. Lindorff-Larsen, and D.E. Shaw How robust are protein folding simulations with respect to force field parameterization? Biophys. J. 100 2011 L47 L49
51. K. Lindorff-larsen, P. Maragakis, S. Piana, M.P. Eastwood, R.O. Dror, and D.E. Shaw Systematic Validation of Protein Force Fields against Experimental Data 7 2012 1 6
52. G. Bussi, D. Donadio, and M. Parrinello Canonical sampling through velocity rescaling J. Chem. Phys. 126 2007 014101
53. B. Hess, H. Bekker, H. Berendsen, and J. Fraaije LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 18 1997 1463 1472
54. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: an Nâlog(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089
55. A. Amadei, A.B. Linssen, and H.J. Berendsen Essential dynamics of proteins Proteins 17 1993 412 425
56. B. Hess Convergence of sampling in protein simulations Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 65 2002 031910
57. B. Hess Similarities between principal components of protein dynamics and random diffusion Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 62 2000 8438 8448
58. M. Tiberti, G. Invernizzi, M. Lambrughi, Y. Inbar, G. Schreiber, and E. Papaleo PyInteraph: a framework for the analysis of interaction networks in structural ensembles of proteins J. Chem. Inf. Model. 54 2014 1537 1551
59. T. Paramo, A. East, D. Garzón, M.B. Ulmschneider, and P.J. Bond Efficient characterisation of protein cavities within molecular simulation trajectories: trjcavity J. Chem. Theory Comput. 10 2014 2151 2164
60. J. Schymkowitz, J. Borg, F. Stricher, R. Nys, F. Rousseau, and L. Serrano The FoldX web server: an online force field Nucleic Acids Res. 33 2005 W382 W388
61. M. Tiberti, and E. Papaleo Dynamic properties of extremophilic subtilisin-like serine-proteases J. Struct. Biol. 174 2011 69 83
62. O. Almog, D.T. Gallagher, J.E. Ladner, S. Strausberg, P. Alexander, P. Bryan, and G.L. Gilliland Structural basis of thermostability. Analysis of stabilizing mutations in subtilisin BPN J. Biol. Chem. 277 2002 27553 27558
63. G.I. Makhatadze, V.V. Loladze, D.N. Ermolenko, X. Chen, and S.T. Thomas Contribution of surface salt bridges to protein stability: guidelines for protein engineering J. Mol. Biol. 327 2003 1135 1148
64. A.-E. Fedøy, N. Yang, A. Martinez, H.-K.S. Leiros, and I.H. Steen Structural and functional properties of isocitrate dehydrogenase from the psychrophilic bacterium Desulfotalea psychrophila reveal a cold-active enzyme with an unusual high thermal stability J. Mol. Biol. 372 2007 130 149
65. H.-K.S. Leiros, A.L. Pey, M. Innselset, E. Moe, I. Leiros, I.H. Steen, and A. Martinez Structure of phenylalanine hydroxylase from Colwellia psychrerythraea 34H, a monomeric cold active enzyme with local flexibility around the active site and high overall stability J. Biol. Chem. 282 2007 21973 21986
66. P.L. Wintrode, and F.H. Arnold Temperature adaptation of enzymes: lessons from laboratory evolution Adv. Protein Chem. 55 2000 161 225
67. F.H. Arnold, P.L. Wintrode, K. Miyazaki, and A. Gershenson How enzymes adapt: lessons from directed evolution Trends Biochem. Sci. 26 2001 100 106
68. K.T. Debiec, A.M. Gronenborn, and L.T. Chong Evaluating the strength of salt bridges: a comparison of current biomolecular force fields J. Phys. Chem. B 118 2014 6561 6569