Strain analysis of protein structures and low dimensionality of mechanical allosteric couplings

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 40, 2016, Pages E5847-E5855

  Mitchell, Michael R ^a   Tlusty, Tsvi ^b,c,d   Leibler, Stanislas ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b INSTITUTE FOR ADVANCED STUDY   (United States)

^c Institute for Basic Science   (South Korea)

^d Ulsan National Institute of Science and Technology   (South Korea)

Author keywords

Elasticity; Protein allostery; Protein mechanics; Strain

Indexed keywords

LIGAND; PEPTIDE; PROTEIN;

ALLOSTERISM; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; LIGAND BINDING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; STRESS STRAIN RELATIONSHIP; ALLOSTERIC SITE; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; ESCHERICHIA COLI; HUMAN; MOLECULAR MODEL; MYCOBACTERIUM TUBERCULOSIS;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; CATALYTIC DOMAIN; ESCHERICHIA COLI; HUMANS; LIGANDS; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; PEPTIDES; PROTEINS;

EID: 84989936696     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1609462113     Document Type: Article

References (69)

1. Perutz MF (1970) Stereochemistry of cooperative effects in haemoglobin. Nature 228(5273):726-739.
2. Hill AV (1910) The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 40(suppl):iv-vii.
3. Stryer L (1995) Biochemistry (Freeman, New York), 4th Ed.
4. Van Schaftingen E (1989) A protein from rat liver confers to glucokinase the property of being antagonistically regulated by fructose 6-phosphate and fructose 1-phosphate. Eur J Biochem 179(1):179-184.
5. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: A plausible model. J Mol Biol 12:88-118.
6. Koshland DE, Jr, Némethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5(1):365-385.
7. Kern D, Zuiderweg ER (2003) The role of dynamics in allosteric regulation. Curr Opin Struct Biol 13(6):748-757.
8. Cui Q, Karplus M (2008) Allostery and cooperativity revisited. Protein Sci 17(8):1295-1307.
9. Tsai CJ, Del Sol A, Nussinov R (2009) Protein allostery, signal transmission and dynamics: A classification scheme of allosteric mechanisms. Mol Biosyst 5(3):207-216.
10. Changeux JP (2012) Allostery and the Monod-Wyman-Changeux model after 50 years. Annu Rev Biophys 41:103-133.
11. Motlagh HN, Wrabl JO, Li J, Hilser VJ (2014) The ensemble nature of allostery. Nature 508(7496):331-339.
12. Fraser JS, et al. (2009) Hidden alternative structures of proline isomerase essential for catalysis. Nature 462(7273):669-673.
13. Tomita A, et al. (2009) Visualizing breathing motion of internal cavities in concert with ligand migration in myoglobin. Proc Natl Acad Sci USA 106(8):2612-2616.
14. Rice S, et al. (1999) A structural change in the kinesin motor protein that drives motility. Nature 402(6763):778-784.
15. Choi B, et al. (2005) Artificial allosteric control of maltose binding protein. Phys Rev Lett 94(3):038103.
16. Wang Y, Zocchi G (2010) Elasticity of globular proteins measured from the ac susceptibility. Phys Rev Lett 105(23):238104.
17. Nichols WL, Rose GD, Ten Eyck LF, Zimm BH (1995) Rigid domains in proteins: an algorithmic approach to their identification. Proteins 23(1):38-48.
18. Kelley LA, Gardner SP, Sutcliffe MJ (1997) An automated approach for defining core atoms and domains in an ensemble of NMR-derived protein structures. Protein Eng 10(6):737-741.
19. Wriggers W, Schulten K (1997) Protein domain movements: Detection of rigid domains and visualization of hinges in comparisons of atomic coordinates. Proteins 29(1):1-14.
20. Schneider TR (2002) A genetic algorithm for the identification of conformationally invariant regions in protein molecules. Acta Crystallogr D Biol Crystallogr 58(Pt 2):195-208.
21. Damm KL, Carlson HA (2006) Gaussian-weighted RMSD superposition of proteins: A structural comparison for flexible proteins and predicted protein structures. Biophys J 90(12):4558-4573.
22. Finkelstein A, Ptitsyn O (2002) Protein Physics: A Course of Lectures, Soft Condensed Matter, Complex Fluids and Biomaterials (Elsevier, Amsterdam).
23. Daily MD, Upadhyaya TJ, Gray JJ (2008) Contact rearrangements form coupled networks from local motions in allosteric proteins. Proteins 71(1):455-466.
24. Hinsen K, Thomas A, Field MJ (1999) Analysis of domain motions in large proteins. Proteins 34(3):369-382.
25. Panjkovich A, Daura X (2012) Exploiting protein flexibility to predict the location of allosteric sites. BMC Bioinformatics 13(1):273.
26. Miyashita O, Onuchic JN, Wolynes PG (2003) Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc Natl Acad Sci USA 100(22):12570-12575.
27. Yamato T (1996) Strain tensor field in proteins. J Mol Graph 14(2):105-107, 98-99.
28. Koike K, Kawaguchi K, Yamato T (2008) Stress tensor analysis of the protein quake of photoactive yellow protein. Phys Chem Chem Phys 10(10):1400-1405.
29. Landau L, Lifshitz E, Kosevich A, Pitaevskiǐ L (1986) Theory of Elasticity, Course of Theoretical Physics (Butterworth-Heinemann, Amsterdam).
30. Born M, Huang K (1954) Dynamical Theory of Crystal Lattices (Clarendon, London).
31. Capecchi D, Ruta G, Trovalusci P (2010) From classical to Voigt's molecular models in elasticity. Arch Hist Exact Sci 64(5):525-559.
32. Bagi K (1996) Stress and strain in granular assemblies. Mech Mater 22(3):165-177.
33. Miron S, Munier-Lehmann H, Craescu CT (2004) Structural and dynamic studies on ligand-free adenylate kinase from Mycobacterium tuberculosis revealed a closed conformation that can be related to the reduced catalytic activity. Biochemistry 43(1):67-77.
34. Kerns SJ, et al. (2015) The energy landscape of adenylate kinase during catalysis. Nat Struct Mol Biol 22(2):124-131.
35. Hible G, et al. (2006) Unique GMP-binding site in Mycobacterium tuberculosis guanosine monophosphate kinase. Proteins 62(2):489-500.
36. Kamata K, Mitsuya M, Nishimura T, Eiki JI, Nagata Y (2004) Structural basis for allosteric regulation of the monomeric allosteric enzyme human glucokinase. Structure 12(3):429-438.
37. Mitsuya M, et al. (2009) Discovery of novel 3,6-disubstituted 2-pyridinecarboxamide derivatives as GK activators. Bioorg Med Chem Lett 19(10):2718-2721.
38. Nishimura T, et al. (2009) Identification of novel and potent 2-amino benzamide derivatives as allosteric glucokinase activators. Bioorg Med Chem Lett 19(5):1357-1360.
39. Petit P, et al. (2011) The active conformation of human glucokinase is not altered by allosteric activators. Acta Crystallogr D Biol Crystallogr 67(Pt 11):929-935.
40. Bebernitz GR, et al. (2009) Investigation of functionally liver selective glucokinase activators for the treatment of type 2 diabetes. J Med Chem 52(19):6142-6152.
41. Takahashi K, et al. (2009) The design and optimization of a series of 2-(pyridin-2-yl)-1H-benzimidazole compounds as allosteric glucokinase activators. Bioorg Med Chem 17(19):7042-7051.
42. Pfefferkorn JA, et al. (2011) Designing glucokinase activators with reduced hypoglycemia risk: Discovery of N,N-dimethyl-5-(2-methyl-6-((5-methylpyrazin-2-yl)-carbamoyl)benzofuran-4-yloxy)pyrimidine-2-carboxamide as a clinical candidate for the treatment of type 2 diabetes mellitus. Med Chem Commun 2(9):828-839.
43. Liu S, et al. (2012) Insights into mechanism of glucokinase activation: Observation of multiple distinct protein conformations. J Biol Chem 287(17):13598-13610.
44. Cheruvallath ZS, et al. (2013) Design, synthesis and SAR of novel glucokinase activators. Bioorg Med Chem Lett 23(7):2166-2171.
45. Filipski KJ, et al. (2013) Pyrimidone-based series of glucokinase activators with alternative donor-acceptor motif. Bioorg Med Chem Lett 23(16):4571-4578.
46. Beck T, Miller BG (2013) Structural basis for regulation of human glucokinase by glucokinase regulatory protein. Biochemistry 52(36):6232-6239.
47. Hinklin RJ, et al. (2013) Identification of a new class of glucokinase activators through structure-based design. J Med Chem 56(19):7669-7678.
48. Hinklin RJ, et al. (2014) Discovery of 2-pyridylureas as glucokinase activators. J Med Chem 57(19):8180-8186.
49. Cockrell GM, et al. (2013) New paradigm for allosteric regulation of Escherichia coli aspartate transcarbamoylase. Biochemistry 52(45):8036-8047.
50. Stevens RC, Gouaux JE, Lipscomb WN (1990) Structural consequences of effector binding to the T state of aspartate carbamoyltransferase: Crystal structures of the unligated and ATP- and CTP-complexed enzymes at 2.6-A resolution. Biochemistry 29(33):7691-7701.
51. Ke HM, Lipscomb WN, Cho YJ, Honzatko RB (1988) Complex of N-phosphonacetyl-L-aspartate with aspartate carbamoyltransferase. X-ray refinement, analysis of conformational changes and catalytic and allosteric mechanisms. J Mol Biol 204(3):725-747.
52. Gouaux JE, Stevens RC, Lipscomb WN (1990) Crystal structures of aspartate carbamoyltransferase ligated with phosphonoacetamide, malonate, and CTP or ATP at 2.8-A resolution and neutral pH. Biochemistry 29(33):7702-7715.
53. Grassberger P, Procaccia I (1983) Characterization of strange attractors. Phys Rev Lett 50(5):346-349.
54. Grassberger P, Procaccia I (1983) Measuring the strangeness of strange attractors. Physica D 9(1-2):189-208.
55. Baroni S, et al. (2001) Effect of ibuprofen and warfarin on the allosteric properties of haem-human serum albumin. A spectroscopic study. Eur J Biochem 268(23):6214-6220.
56. Bhattacharya AA, Curry S, Franks NP (2000) Binding of the general anesthetics propofol and halothane to human serum albumin. High resolution crystal structures. J Biol Chem 275(49):38731-38738.
57. Ghuman J, et al. (2005) Structural basis of the drug-binding specificity of human serum albumin. J Mol Biol 353(1):38-52.
58. Wardell M, et al. (2002) The atomic structure of human methemalbumin at 1.9 A. Biochem Biophys Res Commun 291(4):813-819.
59. Fan JS, et al. (2013) Solution structure and dynamics of human hemoglobin in the carbonmonoxy form. Biochemistry 52(34):5809-5820.
60. Berman HM, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28(1):235-242.
61. Ishikura T, Hatano T, Yamato T (2012) Atomic stress tensor analysis of proteins. Chem Phys Lett 539-540:144-150.
62. Gullett PM, Horstemeyer MF, Baskes MI, Fang H (2007) A deformation gradient tensor and strain tensors for atomistic simulations. Model Simul Mater Sci Eng 16(1):015001.
63. Liebschner D, Dauter M, Brzuszkiewicz A, Dauter Z (2013) On the reproducibility of protein crystal structures: five atomic resolution structures of trypsin. Acta Crystallogr D Biol Crystallogr 69(Pt 8):1447-1462.
64. Cock PJA, et al. (2009) Biopython: Freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25(11):1422-1423.
65. Hamelryck T, Manderick B (2003) PDB file parser and structure class implemented in Python. Bioinformatics 19(17):2308-2310.
66. Rice P, Longden I, Bleasby A (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16(6):276-277.
67. Wang X, Snoeyink J (2006) Multiple structure alignment by optimal RMSD implies that the average structure is a consensus. Comput Syst Bioinformatics Conf 2006:79-87.
68. Theiler J (1990) Estimating fractal dimension. J Opt Soc Am A Opt Image Sci Vis 7(6):1055-1073.
69. Sanner MF, Olson AJ, Spehner JC (1996) Reduced surface: An efficient way to compute molecular surfaces. Biopolymers 38(3):305-320.