Equilibrium conformational ensemble of the intrinsically disordered peptide n16N: Linking subdomain structures and function in nacre

Biomacromolecules

Volumn 15, Issue 12, 2014, Pages 4467-4479

  Brown, Aaron H ^a,c   Rodger, P Mark ^b   Evans, John Spencer ^d   Walsh, Tiffany R ^c  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c DEAKIN UNIVERSITY   (Australia)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CALCIUM; CALCIUM CARBONATE; CHITIN; EXPERIMENTS; MINERALS; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES; STABILIZATION;

BIOGENIC MINERALS; CONFORMATIONAL ENSEMBLE; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR MECHANISM; REPLICA EXCHANGE; SECONDARY STRUCTURES; SELECTIVE BINDING; SPECTROSCOPY DATA;

GEMS;

CHITIN; N16N PEPTIDE; PEPTIDE DERIVATIVE; TYROSINE; UNCLASSIFIED DRUG; CALCIUM CARBONATE; INTRINSICALLY DISORDERED PROTEIN; NACRE; PEPTIDE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CONFORMATIONAL ENSEMBLE; CONTROLLED STUDY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MINERALIZATION; MOLECULAR DYNAMICS; NACRE; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; BINDING SITE; CHEMISTRY; CLUSTER ANALYSIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

BINDING SITES; CALCIUM CARBONATE; CHITIN; CLUSTER ANALYSIS; INTRINSICALLY DISORDERED PROTEINS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; NACRE; PEPTIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84916633972     PISSN: 15257797     EISSN: 15264602     Source Type: Journal    
DOI: 10.1021/bm501263s     Document Type: Article

References (101)

1. Nudelman, F.; Gotliv, B. A.; Addadi, L.; Weiner, S. Mollusk shell formation: Mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre J. Struct. Biol. 2006, 153, 176-187
2. Addadi, L.; Raz, S.; Weiner, S. Taking Advantage of Disorder: Amorphous Calcium Carbonate and Its Roles in Biomineralization Adv. Mater. 2003, 15, 959-970
3. Meldrum, F. C. Calcium carbonate in biomineralisation and biomimetic chemistry Int. Mater. Rev. 2003, 48, 187-224
4. Aizenberg, J. New Nanofabrication Strategies: Inspired by Biomineralization MRS Bull. 2010, 35, 323-330
5. Belton, D. J.; Deschaume, O.; Perry, C. C. An overview of the fundamentals of the chemistry of silica with relevance to biosilicification and technological advances FEBS J. 2012, 279, 1710-1720
6. Nudelman, F.; Sommerdijk, N. A. J. M. Biomineralization as an Inspiration for Materials Chemistry Angew. Chem., Int. Ed. 2012, 51, 6582-6596
7. Weiner, S.; Addadi, L. Crystallization Pathways in Biomineralization Annu. Rev. Mater. Res. 2011, 41, 21-40
8. Evans, J. S. "Tuning in" to Mollusk Shell Nacre- and Prismatic-Associated Protein Terminal Sequences. Implications for Biomineralization and the Construction of High Performance Inorganic-Organic Composites Chem. Rev. 2008, 108, 4455-4462
9. Kim, S.; Park, C. B. Bio-Inspired Synthesis of Minerals for Energy, Environment, and Medicinal Applications Adv. Funct. Mater. 2013, 23, 10-25
10. Cheng, Q. F.; Liang, J.; Tang, Z. Y. Bioinspired Layered Materials with Superior Mechanical Performance Acc. Chem. Res. 2014, 47, 1256-1266
11. Young, J. R.; Davis, S. A.; Brown, P. R.; Mann, S. Coccolith Ultrastructure and Biomineralization J. Struct. Biol. 1999, 126, 195-215
12. Villiers, J. P. R. D. Crystal Structures of Aragonite, Strontianite and Witherite Am. Mineral. 1971, 56, 758-768
13. Samata, T.; Hayashi, N.; Kono, M.; Hasegawa, K.; Horita, C.; Akera, S. A new matrix protein family related to the nacreous layer formation of Pinctada fucata FEBS Lett. 1999, 462, 225-229
14. Amos, F. F.; Evans, J. S. AP7, a partially disordered pseudo C-RING protein, is capable of forming stabilized aragonite in vitro Biochemistry 2009, 48, 1332-1339
15. Amos, F. F.; Destine, E.; Ponce, C. B.; Evans, J. S. The N- and C-Terminal Regions of the Pearl-Associated EF Hand Protein, PFMG1, Promote the Formation of the Aragonite Polymorph in Vitro Cryst. Growth Des. 2010, 10, 4211-4216
16. Ponce, C. B.; Evans, J. S. Polymorph Crystal Selection by n16, an Intrinsically Disordered Nacre Framework Protein Cryst. Growth Des. 2011, 11, 4690-4696
17. Seto, J.; Picker, A.; Chen, Y.; Rao, A.; Evans, J. S.; Coelfen, H. Nacre Protein Sequence Compartmentalizes Mineral Polymorphs in Solution Cryst. Growth Des. 2014, 14, 1501-1505
18. Marin, F.; Luquet, G. Molluscan shell proteins CR. Palevol 2004, 3, 469-492
19. Metzler, R. A.; Evans, J. S.; Killian, C. E.; Zhou, D.; Churchill, T. H.; Appathurai, N. P.; Coppersmith, S. N.; Gilbert, P. U. P. A. Nacre protein fragment templates lamellar aragonite growth J. Am. Chem. Soc. 2010, 132, 6329-6334
20. Furuhashi, T.; Schwarzinger, C.; Miksik, I.; Smrz, M.; Beran, A. Molluscan shell evolution with review of shell calcification hypothesis Comp. Biochem. Phys., Part B 2009, 154, 351-371
21. Weiner, S.; Addadi, L. Design strategies in mineralized biological materials J. Mater. Chem. 1997, 7, 689-702
22. Heinemann, F.; Launspach, M.; Gries, K.; Fritz, M. Gastropod nacre: Structure, properties and growth Biological, chemical and physical basics Biophys. Chem. 2011, 153, 126-153
23. Checa, A. G.; Rodriguez-Navarro, A. B. Self-organisation of nacre in the shells of Pterioida (Bivalvia: Mollusca) Biomaterials 2005, 26, 1071-1079
24. Jackson, A. P.; Vincent, J. F.; Turner, R. M. The mechanical design of Nacre Proc. R. Soc. London, Ser. B 1988, 234, 415-440
25. Barber, D. J. The role of interfaces in biomineralization Scr. Metall. Mater. 1994, 31, 989-994
26. Vincent, J. F. V.; Wegst, U. G. K. Design and mechanical properties of insect cuticle Arthropod Struct. Dev. 2004, 33, 187-199
27. Cartwright, J. H. E.; Checa, A. G. The dynamics of nacre self-assembly J. R. Soc. Interface 2007, 4, 491-504
28. Launspach, M.; Rückmann, K.; Gummich, M.; Rademaker, H.; Doschke, H.; Radmacher, M.; Fritz, M. Immobilisation and characterisation of the demineralised, fully hydrated organic matrix of nacre-an atomic force microscopy study Micron 2012, 43, 1351-1363
29. Zhou, X. L.; Miao, H. C.; Li, F. X. Nanoscale structural and functional mapping of nacre by scanning probe microscopy techniques Nanoscale 2013, 5, 11885-11893
30. Falini, G.; Albeck, S.; Weiner, S.; Addadi, L. Control of Aragonite or Calcite Polymorphism by Mollusk Shell Macromolecules Science 1996, 271, 67-69
31. Belcher, A. M.; Wu, X. H.; Christensen, R. J.; Hansma, P. K.; Stucky, G. D.; Morse, D. E. Control of crystal phase switching and orientation by soluble mollusc-shell proteins Nature 1996, 381, 56-58
32. Suzuki, M.; Saruwatari, K.; Kogure, T.; Yamamoto, Y.; Nishimura, T.; Kato, T.; Nagasawa, H. An Acidic Matrix Protein, Pif, Is a Key Macromolecule for Nacre Formation Science 2009, 325, 1388-1390
33. Chang, E. P.; Russ, J. A.; Verch, A.; Kroeger, R.; Estroff, L. A.; Evans, J. S. Engineering of crystal surfaces and subsurfaces by framework biomineralization protein phases Cryst. Eng. Commun. 2014, 16, 7406-7409
34. Perovic, I.; Chang, E. P.; Lui, M.; Rao, A.; Coelfen, H.; Evans, J. S. A nacre protein, n16.3, self-assembles to form protein oligomers that dimensionally limit and organize mineral deposits Biochemistry 2014, 53, 2739-2748
35. Kim, I. W.; DiMasi, E.; Evans, J. S. Identification of Mineral Modulation Sequences within the Nacre-Associated Oyster Shell Protein, n16 Cryst. Growth Des. 2004, 4, 1113-1118
36. Delak, K.; Collino, S.; Evans, J. S. Expected and unexpected effects of amino acid substitutions on polypeptide-directed crystal growth Langmuir 2007, 23, 11951-11955
37. Keene, E. C.; Evans, J. S.; Estroff, L. A. Matrix Interactions in Biomineralization: Aragonite Nucleation by an Intrinsically Disordered Nacre Polypeptide, n16N, Associated with a β-Chitin Substrate Cryst. Growth Des. 2010, 10, 1383-1389
38. Keene, E. C.; Evans, J. S.; Estroff, L. A. Silk Fibroin Hydrogels Coupled with the n16Nβ-Chitin Complex: An in Vitro Organic Matrix for Controlling Calcium Carbonate Mineralization Cryst. Growth Des. 2010, 10, 5169-5175
39. Amos, F. F.; Ponce, C. B.; Evans, J. S. Formation of framework nacre polypeptide supramolecular assemblies that nucleate polymorphs Biomacromolecules 2011, 12, 1883-1890
40. Evans, J. S. "Liquid-like" biomineralization protein assemblies: A key to the regulation of non-classical nucleation CrystEngComm 2013, 15, 8388-8394
41. Collino, S.; Evans, J. S. Molecular specifications of a mineral modulation sequence derived from the aragonite-promoting protein n16 Biomacromolecules 2008, 9, 1909-1918
42. Evans, J. S. Aragonite-associated biomineralization proteins are disordered and contain interactive motifs Bioinformatics 2012, 28, 3182-3185
43. Uversky, V. N. Intrinsically disordered proteins from A to Z Int. J. Biochem. Cell Biol. 2011, 43, 1090-1103
44. Dunker, A. K.; Obradovic, Z. The protein trinity-linking function and disorder Nat. Biotechnol. 2001, 19, 805-806
45. Tompa, P. Intrinsically unstructured proteins Trends Biochem. Sci. 2002, 27, 527-533
46. Linding, R.; Schymkowitz, J.; Rousseau, F.; Diella, F.; Serrano, L. A comparative study of the relationship between protein structure and beta-aggregation in globular and intrinsically disordered proteins J. Mol. Biol. 2004, 342, 345-353
47. Mittag, T.; Forman-Kay, J. D. Atomic-level characterization of disordered protein ensembles Curr. Opin. Struct. Biol. 2007, 17, 3-14
48. Fisher, C. K.; Stultz, C. M. Constructing ensembles for intrinsically disordered proteins Curr. Opin. Struct. Biol. 2011, 21, 426-431
49. Rogers, J. M.; Steward, A.; Clarke, J. Folding and binding of an intrinsically disordered protein: Fast, but not diffusion-limited J. Am. Chem. Soc. 2013, 135, 1415-1422
50. Lindorff-Larsen, K.; Trbovic, N.; Maragakis, P.; Piana, S.; Shaw, D. E. Structure and Dynamics of an Unfolded Protein Examined by Molecular Dynamics Simulations J. Am. Chem. Soc. 2012, 134, 3787-3791
51. Ostermeir, K.; Zacharias, M. Advanced Replica-exchange Sampling to Study the Flexibility and Plasticity of Peptides and Proteins Biochim. Biophys. Acta 2013, 1834, 847-853
52. Tang, Z.; Palafox-Hernandez, J. P.; Law, W.-C.; Hughes, Z. E.; Swihart, M. T.; Prasad, P. N.; Knecht, M. R.; Walsh, T. R. Biomolecular Recognition Principles for Bionanocombinatorics: An Integrated Approach to Elucidate Enthalpic and Entropic Factors ACS Nano 2013, 7, 9632-9646
53. Hansmann, U. H. E. Parallel tempering algorithm for conformational studies of biological molecules Chem. Phys. Lett. 1997, 281, 140-150
54. Trebst, S.; Troyer, M.; Hansmann, U. H. E. Optimized parallel tempering simulations of proteins J. Chem. Phys. 2006, 124, 174903
55. Ball, K. A.; Phillips, A. H.; Wemmer, D. E.; Head-Gordon, T. Differences in β-strand Populations of Monomeric Aβ40 and Aβ42 Biophs. J. 2013, 104, 2714-2724
56. Narayanan, C.; Weinstock, D. S.; Wu, K. P.; Levy, R. M. Investigation of the Polymeric Properties of α-Synuclein and Comparison with NMR Experiments: A Replica Exchange Molecular Dynamics Study J. Chem. Theory Comput. 2012, 8, 3929-3942
57. Wright, L. B.; Walsh, T. R. Efficient conformational sampling of peptides adsorbed onto inorganic surfaces: Insights from a quartz binding peptide Phys. Chem. Chem. Phys. 2013, 15, 4715-4726
58. Schneider, J.; Colombi Ciacchi, L. Specific Material Recognition by Small Peptides Mediated by the Interfacial Solvent Structure J. Am. Chem. Soc. 2012, 134, 2407-2413
59. Mittal, J.; Yoo, T. H.; Georgiou, G.; Truskett, T. M. Structural ensemble of an intrinsically disordered polypeptide J. Phys. Chem. B 2013, 117, 118-124
60. Knott, M.; Best, R. B. A Preformed Binding Interface in the Unbound Ensemble of an Intrinsically Disordered Protein: Evidence from Molecular Simulations PLoS Comp. Biol. 2012, 8, e1002605-1-10
61. Vellore, N. A.; Yancey, J. A.; Collier, G.; Latour, R. A.; Stuart, S. J. Assessment of the Transferrability of a Protein Force Field for the simulation of Peptide-Surface Interactions Langmuir 2010, 26, 7396-7404
62. Wang, F.; Stuart, S. J.; Latour, R. A. Calculation of the Adsorption Free Energy for Solute-surface Interactions using Biased Replica-Exchange Molecular Dynamics Biointerphases 2008, 3, 9-18
63. Notman, R.; Oren, E. E.; Tamerler, C.; Sarikaya, M.; Samudrala, R.; Walsh, T. R. Solution study of engineered quartz-binding peptides using replica exchange molecular dynamics Biomacromolecules 2010, 11, 3266-3274
64. Sethi, A.; Tian, J.; Vu, D. M.; Gnanakaran, S. Identification of Minimally Interacting Modules in an Intrinsically Disordered Protein Biophys. J. 2012, 103, 748-757
65. Terakawa, T.; Takada, S. Multiscale Ensemble Modelling of Intrinsically Disordered Proteins: p53 N-Terminal Domain Biophys. J. 2011, 101, 1450-1458
66. Higo, J.; Nishimura, Y.; Nakamura, H. A Free Energy Lanbgscape for Coupled Foldings and Binding of an Intrinsically Disordered Protein in Explicit Solvent from Detailed All-Atom Simulations J. Am. Chem. Soc. 2011, 133, 10448-10458
67. Moritsugu, K.; Terada, T.; Kidera, A. Disorder-to-Order Transition of an Intrinsically Disordered Region of Sortase Revealed by Multiscale Enhanced Sampling J. Am. Chem. Soc. 2012, 134, 7094-7101
68. Patriksson, A.; van der Spoel, D. A temperature predictor for parallel tempering simulations Phys. Chem. Chem. Phys. 2008, 10, 2073-2077
69. Zhou, R.; Berne, B. J. Can a continuum solvent model reproduce the free energy landscape of a beta -hairpin folding in water? Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 12777-12782
70. Shell, M. S.; Ritterson, R.; Dill, K. A. A test on peptide stability of AMBER force fields with implicit solvation J. Phys. Chem.. B 2008, 112, 6878-6886
71. Battisti, A.; Tenenbaum, A. Molecular dynamics simulation of intrinsically disordered proteins Mol. Simul. 2012, 38, 139-143
72. Bottaro, S.; Lindor-Larsen, K.; Best, R. B. Variational Optimization of an All-Atom Implicit Solvent Force Field To Match Explicit Solvent Simulation Data J. Chem. Theory Comput. 2013, 9, 5641-5652
73. Liu, P.; Kim, B.; Friesner, R. A.; Berne, B. J. Replica exchange with solute tempering: A method for sampling biological systems in explicit water Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 13749-13754
74. Wang, L.; Friesner, R. A.; Berne, B. J. Replica exchange with solute scaling: A more efficient version of replica exchange with solute tempering (REST2) J. Phys. Chem. B 2011, 115, 9431-9438
75. Terakawa, T.; Kameda, T.; Takada, S. On Easy Implementation of a Variant of the Replica Exchange with Solute Tempering in GROMACS J. Comput. Chem. 2011, 32, 1228-1234
76. Wang, L.; Deng, Y.; Knight, J. L.; Wu, Y.; Kim, B.; Sherman, W.; Shelley, J. C.; Lin, T.; Abel, R. Modeling Local Structural Rearrangements Using FEP/REST: Application to Relative Binding Affinity Predictions of CDK2 Inhibitors J. Chem. Theory Comput. 2013, 9, 1282-1293
77. Ponder, J. W.; Ren, P.; Pappu, R. V.; Hart, R. K.; Hodgson, M. E.; Cistola, D. P.; Kundrot, C. E.; Richards, F. M. TINKER, version 5.1; Washington University School of Medicine: St. Louis, MO, 2013.
78. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for highly efficient, load balanced, and scable molecular simulation J. Chem. Theory Comp. 2008, 4, 435-477
79. Earl, D. J.; Deem, M. W. Parallel tempering: Theory, applications, and new perspectives Phys. Chem. Chem. Phys. 2005, 7, 3910-3916
80. Onufriev, A.; Bashford, D.; Case, D. A. Exploring protein native states and large-scale conformational changes with a modified generalized born model Proteins 2004, 55, 383-394
81. Nosé, S. A Molecular-Dynamics Method for Simulations in the Canonical Ensemble Mol. Phys. 1984, 52, 255-268
82. Nosé, S. A Unified Formulation of the Constant Temperature Molecular-Dynamics Methods J. Chem. Phys. 1984, 81, 511-519
83. Hoover, W. G. Canonical Dynamics-Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
84. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
85. van der Spoel, D.; Lindahl, E.; Hess, B.; van Buuren, A. R.; Apol, E.; Meulenhoff, P. J.; Tieleman, D. P.; Sijbers, A. L. T. M.; Feenstra, K. A.; van Drunen, R.; Berendsen, H. J. C. Gromacs User Manual, version 4.5.4; 2010; www.gromacs.org.
86. Piana, S.; Lindorff-Larsen, K.; Shaw, D. E. How Robust Are Protein Folding Simulations with Respect to Force Field Parameterization? Biophys. J. 2011, 100, L47-L49
87. MacKerell, A. D.; Bashford, D.; Bellot, M.; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S. All atom empirical potential for molecular modelling and dynamics studies of proteins J. Phys. Chem. B 1998, 102, 3586-3616
88. Parrinello, M.; Rahman, A. Polymorphic transitions in single crystals: A new molecular dynamics method J. Appl. Phys. 1981, 52, 7182-7190
89. Darden, T.; York, T.; Pedersen, L. Particle Mesh Ewald-An N.Log(N) Method For Ewald Sums In Large Systems J. Chem. Phys. 1993, 98, 10089-10092
90. Hockney, R. W.; Goel, S. P.; Eastwood, J. Quiet high resolution computer models of a plasma J. Comput. Phys. 1974, 14, 148-158
91. Mackerell, A. D.; Feig, M.; Brooks, C. L. Extending the Treatment of Backbone Energetics in Protein Force Fields: Limitations of Gas-phase Quantum Mechanics in Reproducing Protein Conformational Distributions in Molecular Dynamics Simulations J. Comput. Chem. 2004, 25, 1400-1415
92. Daura, X.; Gademann, K.; Jaun, B.; Seebach, D.; van Gunsteren, W. F.; Mark, A. E. Peptide Folding: When Simulation Meets Experiment Angew. Chem., Int. Ed. 1999, 38, 236-240
93. Jedlovszky, P.; Brodholt, J. P.; Bruni, F.; Ricci, M. A.; Soper, A. K.; Vallauri, R. Analysis of the hydrogen-bonded structure of water from ambient to supercritical conditions J. Chem. Phys. 1998, 108, 8528-8540
94. Kohlhoff, K. J.; Robustelli, P.; Cavalli, A.; Salvatella, X.; Vendruscolo, M. Fast and Accurate Predictions of Protein NMR Chemical Shifts from Interatomic Distances J. Am. Chem. Soc. 2009, 131, 13894-13895
95. Shen, Y.; Bax, A. SPARTA+: A modest improvement in empirical NMR chemical shift prediction by means of an artificial neural network J. Biomol. NMR 2010, 48, 13-22
96. Collino, S.; Evans, J. S. Structural features that distinguish kinetically distinct biomineralization polypeptides Biomacromolecules 2007, 8, 1686-1694
97. Goddard, T. D.; Kneller, D. G. SPARKY 3, version 3.110; University of California, San Francisco: San Francisco, CA, 2004.
98. Delaglio, F.; Grzesiek, S.; Vuister, G. W.; Zhu, G.; Pfeifer, J.; Bax, A. J. NMRPipe: A multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 1995, 6, 227-293
99. Suzuki, K.; Suzuki, M.; Taiyoji, M.; Nikaidou, N. Chitin Binding Protein (CBP21) in the Culture Supernatant of Serratia marcescens 2170 Biosci. Biotechnol. Biochem. 1998, 62, 128-135
100. Schnellmann, J.; Zeltins, A.; Blaak, H.; Schrempf, H. The novel lectin-like protein CHB1 is encoded by a chitin-inducible Streptomyces olivaceoviridis gene and binds specifically to crystalline a-chitin of fungi and other organisms Mol. Microbiol. 1994, 13, 807-819
101. Vaaje-Kolstad, G.; Houston, D. R.; Riemen, A. H. K.; Eijsink, V. G. H.; van Alten, D. M. F. Crystal Structure and Binding Properties of the Serratia marcescens Chitin-Binding Protein CBP21 J. Biol. Chem. 2005, 280, 11313-11319