Dynamics of noncovalent interactions in all-α and all-β class proteins: Implications for the stability of amyloid aggregates

Journal of Chemical Information and Modeling

Volumn 51, Issue 12, 2011, Pages 3208-3216

  Jain, Alok ^a   Sankararamakrishnan, Ramasubbu ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATES; ATOMS; C (PROGRAMMING LANGUAGE); GLYCOPROTEINS; HYDROGEN BONDS; IONS; MOLECULAR DYNAMICS; STABILITY;

AVERAGE LIFETIME; FUNCTIONAL PROTEINS; MOLECULAR DYNAMICS SIMULATIONS; NON-COVALENT INTERACTION; OVERALL STABILITIES; PROTEIN STRUCTURES; SECONDARY STRUCTURES; STRUCTURAL STABILITIES;

PROTEINS;

AMYLOID; BACTERIAL PROTEIN;

ARTICLE; BACTERIUM; CHEMISTRY; MOLECULAR DYNAMICS; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY;

AMYLOID; BACTERIA; BACTERIAL PROTEINS; MOLECULAR DYNAMICS SIMULATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY;

EID: 84555194738     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci200302q     Document Type: Article

References (76)

1. Nooren, I. M. A.; Thornton, J. M. Structural characterisation and functional significance of transient protein-protein interactions J. Mol. Biol. 2003, 325, 991-1018
2. Derewenda, Z. S.; Derewenda, U.; Kobos, P. M. (His)C- H•••O=C< hydrogen bond in the active sites of serine hydrolases J. Mol. Biol. 1994, 241, 83-93
3. Brandl, M.; Lindauer, K.; Meyer, M.; Sühnel, J. C-H...O and C-H...N interactions in RNA structures Theor. Chem. Acc. 1999, 101, 103-113
4. Ghosh, A.; Bansal, M. C-H..O hydrogen bonds in minor groove of A-tracts in DNA double helices J. Mol. Biol. 1999, 294, 1149-1158
5. Manikandan, K.; Ramakumar, S. The occurrence of C-H...O hydrogen bonds in α-helices and helix termini in globular proteins Proteins: Struct., Funct., Bioinf. 2004, 56, 768-781
6. Bhattacharyya, R.; Samanta, U.; Chakrabarti, P. Aromatic-aromatic interactions in and around α-helices Protein Eng. 2002, 15, 91-100
7. Ho, B. K.; Curmi, P. M. G. Twist and shear in β-sheets and β-ribbons J. Mol. Biol. 2002, 317, 291-308
8. Barouch-Bentov, R.; Che, J.; Lee, C. C.; Yang, Y.; Herman, A.; Jia, Y.; Velentza, A.; Watson, J.; Sternberg, L.; Kim, S.; Ziaee, N.; Miller, A.; Jackson, C.; Fujimoto, M.; Young, M.; Batalov, S.; Liu, Y.; Warmuth, M.; Wiltshire, T.; Cooke, M. P.; Sauer, K. A conserved salt bridge in the G loop of multiple protein kinases is important for catalysis and for in vivo lyn function Mol. Cell 2009, 33, 43-52
9. Mahalingam, M.; Martínez-Mayorga, K.; Brown, M. F.; Vogel, R. Two protonation switches control rhodopsin activation in membranes Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 17795-17800
10. Kristiansen, K. Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: Molecular modeling and mutagenesis approaches to receptor structure and function Pharmacol. Ther. 2004, 103, 21-80
11. Stockner, T.; Vogel, H. J.; Tieleman, D. P. A salt-bridge motif involved in ligand binding and large-scale domain motions of the maltose-binding protein Biophys. J. 2005, 89, 3362-3371
12. Dehner, A.; Klein, C.; Hansen, S.; Müller, L.; Buchner, J.; Schwaiger, M.; Kessler, H. Cooperative binding of p53 to DNA: Regulation by protein-protein interactions through a double salt bridge Angew. Chem., Int. Ed. 2005, 44, 5247-5251
13. Brandl, M.; Weiss, M. S.; Jabs, A.; Suhnel, J.; Hilgenfeld, R. C-H...π interactions in proteins J. Mol. Biol. 2001, 307, 357-377
14. Kannan, N.; Vishveshwara, S. Aromatic clusters: A determinant of thermal stability of thermophilic proteins Protein Eng. 2000, 13, 753-761
15. Jeyaprakash, A. A.; Katiyar, S.; Swaminathan, C. P.; Sekar, K.; Surolia, A.; Vijayan, M. Structural basis of the carbohydrate specificities of jacalin: An X-ray and modeling study J. Mol. Biol. 2003, 332, 217-228
16. Jain, A.; Purohit, C. S.; Verma, S.; Sankararamakrishnan, R. Close contacts between carbonyl oxygen atoms and aromatic centers in protein structures: π•••π or lone-pair•••π interactions? J. Phys. Chem. B 2007, 111, 8680-8683
17. Jain, A.; Ramanathan, V.; Sankararamakrishnan, R. Lone pair•••π interactions between water oxygens and aromatic residues: Quantum chemical studies based on high-resolution protein structures and model compounds Protein Sci. 2009, 18, 595-605
18. Pless, S. A.; Hanek, A. P.; Price, K. L.; Lynch, J. W.; Lester, H. A.; Dougherty, D. A.; Lummis, S. C. R. A cation-π interaction at a phenylalanine residue in the glycine receptor binding site is conserved for different agonists Mol. Pharmacol. 2011, 79, 742-748
19. 7 Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 21388-21393
20. Queralt-Rosinach, N.; Mestres, J. A canonical cation-π interaction stabilizes the agonist conformation of estrogen-like nuclear receptors Eur. Biophys. J. 2010, 39, 1471-1475
21. Tantry, S.; Ding, F.-X.; Dumont, M.; Becker, J. M.; Naider, F. Binding of fluorinated phenylalanine α-factor analogues to ste2p: Evidence for a cation-π binding interaction between a peptide ligand and its cognate G protein-coupled receptor Biochemistry 2010, 49, 5007-5015
22. Zacharias, N.; Dougherty, D. A. Cation-π interactions in ligand recognition and catalysis Trends Pharmacol. Sci. 2002, 23, 281-287
23. Waters, M. L. Aromatic interactions in peptides: Impact on structure and function Pept. Sci. 2004, 76, 435-445
24. Gallivan, J. P.; Dougherty, D. A. Cation-π interactions in structural biology Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 9459-9464
25. Santarelli, V. P.; Eastwood, A. L.; Dougherty, D. A.; Horn, R.; Ahern, C. A. A cation-π interaction discriminates among sodium channels that are either sensitive or resistant to tetrodotoxin block J. Biol. Chem. 2007, 282, 8044-8051
26. Liu, Y.; Hu, X. Molecular determinants for binding of ammonium ion in the ammonia transporter AmtBA quantum chemical analysis J. Phys. Chem. A 2005, 110, 1375-1381
27. 3A) and nicotinic acetylcholine receptors:The anomalous binding properties of nicotine Biochemistry 2002, 41, 10262-10269
28. Santarelli, V. P.; Eastwood, A. L.; Dougherty, D. A.; Ahern, C. A.; Horn, R. Calcium block of single sodium channels: Role of a pore-lining aromatic residue Biophys. J. 2007, 93, 2341-2349
29. Cerny, J.; Hobza, P. Non-covalent interactions in biomacromolecules Phys. Chem. Chem. Phys. 2007, 9, 5291-5303
30. Mueller-Dethlefs, K.; Hobza, P. Noncovalent interactions: A challenge for experiment and theory ChemInform 2000, 31, 143-168
31. Salonen, L. M.; Ellermann, M.; Diederich, F. Aromatic rings in chemical and biological recognition: Energetics and structures Angew. Chem., Int. Ed. 2011, 50, 4808-4842
32. Rusconi, F.; Guillonneau, F.; Praseuth, D. Contributions of mass spectrometry in the study of nucleic acid-binding proteins and of nucleic acid-protein interactions Mass Spectrom. Rev. 2002, 21, 305-348
33. Yanes, O.; Villanueva, J.; Querol, E.; Aviles, F. X. Detection of non-covalent protein interactions by 'intensity fading' MALDI-TOF mass spectrometry: Applications to proteases and protease inhibitors Nat. Protoc. 2007, 2, 119-130
34. Luzar, A. Resolving the hydrogen bond dynamics conundrum J. Chem. Phys. 2000, 113, 10663-10675
35. 2O J. Chem. Phys. 2005, 122, 54506-54518
36. Asbury, J. B.; Steinel, T.; Kwak, K.; Corcelli, S. A.; Lawrence, C. P.; Skinner, J. L.; Fayer, M. D. Dynamics of water probed with vibrational echo correlation spectroscopy J. Chem. Phys. 2004, 121, 12431-12446
37. Nicodemus, R. A.; Corcelli, S. A.; Skinner, J. L.; Tokmakoff, A. Collective hydrogen bond reorganization in water studied with temperature-dependent ultrafast infrared spectroscopy J. Phys. Chem. B 2011, 115, 5604-5616
38. Voloshin, V.; Naberukhin, Y. Hydrogen bond lifetime distributions in computer-simulated water J. Struct. Chem. 2009, 50, 78-89
39. Ding, F.; Dokholyan, N. V. Simple but predictive protein models Trends Biotechnol. 2005, 23, 450-455
40. Khandelia, H.; Kaznessis, Y. N. Cation-π interactions stabilize the structure of the antimicrobial peptide indolicidin near membranes:Molecular dynamics simulations J. Phys. Chem. B 2006, 111, 242-250
41. Zhang, R.; Li, H.; Lei, Y.; Han, S. All-atom molecular dynamic simulations and relative NMR spectra study of weak C-H•••O contacts in amide-water systems J. Phys. Chem. B 2005, 109, 7482-7487
42. Guvench, O.; Brooks, C. L. Tryptophan side chain electrostatic interactions determine edge-to-face vs parallel-displaced tryptophan side chain geometries in the designed β-hairpin "trpzip2 J. Am. Chem. Soc. 2005, 127, 4668-4674
43. Chelli, R.; Gervasio, F. L.; Procacci, P.; Schettino, V. Stacking and T-shape competition in aromatic-aromatic amino acid interactions J. Am. Chem. Soc. 2002, 124, 6133-6143
44. Sigala, P. A.; Tsuchida, M. A.; Herschlag, D. Hydrogen bond dynamics in the active site of photoactive yellow protein Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 9232-9237
45. Bernstein, F. C.; Koetzle, T. F.; Williams, G. J. B.; Meyer, J. E. F.; Brice, M. D.; Rodgers, J. R.; Kennard, O.; Shimanouchi, T.; Tasumi, M. The protein data bank: A computer-based archival file for macromolecular structures J. Mol. Biol. 1977, 112, 535-542
46. 2 J. Biol. Chem. 2002, 277, 20059-20069
47. Shimomura, Y.; Takahashi, Y.; Kakuta, Y.; Fukuyama, K. Crystal structure of escherichia coli YfhJ protein, a member of the ISC machinery involved in assembly of iron-sulfur clusters Proteins: Struct., Funct., Bioinf. 2005, 60, 566-569
48. Osawa, T.; Matsubara, Y.; Muramatsu, T.; Kimura, M.; Kakuta, Y. Crystal structure of the alginate (poly α-l-guluronate) lyase from corynebacterium sp. at 1.2 Å resolution J. Mol. Biol. 2005, 345, 1111-1118
49. Teplyakov, A.; Obmolova, G.; Wilson, K.; Kuromizu, K. Crystal structure of apo-neocarzinostatin at 0.15-nm resolution Eur. J. Biochem. 1993, 213, 737-741
50. Andreeva, A.; Howorth, D.; Chandonia, J.-M.; Brenner, S. E.; Hubbard, T. J. P.; Chothia, C.; Murzin, A. G. Data growth and its impact on the SCOP database: New developments Nucleic Acids Res. 2008, 36, D419-D425
51. Murzin, A. G.; Brenner, S. E.; Hubbard, T.; Chothia, C. SCOP: A structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 1995, 247, 536-540
52. Laskowski, R. A.; MacArthur, M. W.; Moss, D. S.; Thornton, J. M. PROCHECK: A program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 1993, 26, 283-291
53. Weiss, M. S.; Brandl, M.; Sühnel, J.; Pal, D.; Hilgenfeld, R. More hydrogen bonds for the (structural) biologist Trends Biochem. Sci. 2001, 26, 521-523
54. Kumar, S.; Ma, B.; Tsai, C.-J.; Nussinov, R. Electrostatic strengths of salt bridges in thermophilic and mesophilic glutamate dehydrogenase monomers Proteins: Struct., Funct., Bioinf. 2000, 38, 368-383
55. Samanta, U.; Pal, D.; Chakrabarti, P. Packing of aromatic rings against tryptophan residues in proteins Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, 55, 1421-1427
56. Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: A package for molecular simulation and trajectory analysis J. Mol. Model. 2001, 7, 306-317
57. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids J. Am. Chem. Soc. 1996, 118, 11225-11236
58. 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
59. Neria, E.; Fischer, S.; Karplus, M. Simulation of activation free energies in molecular systems J. Chem. Phys. 1996, 105, 1902-1921
60. Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.; DiNola, A.; Haak, J. R. Molecular dynamics with coupling to an external bath J. Chem. Phys. 1984, 81, 3684-3690
61. Essmann, U.; Perera, L.; Berkowitz, M. L.; Darden, T.; Lee, H.; Pedersen, L. G. A smooth particle mesh ewald method J. Chem. Phys. 1995, 103, 8577-8593
62. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations J. Comput. Chem. 1997, 18, 1463-1472
63. Miyamoto, S.; Kollman, P. A. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models J. Comput. Chem. 1992, 13, 952-962
64. Sanjeev, B. S.; Vishveshwara, S. Protein-water interactions in ribonuclease A and angiogenin: A molecular dynamics study Proteins: Struct., Funct., Bioinf. 2004, 55, 915-923
65. Wibowo, F. R.; Rauch, C.; Trieb, M.; Wellenzohn, B.; Liedl, K. R. Water-mediated contacts in the trp-repressor operator complex recognition process Biopolymers 2004, 73, 668-681
66. Biot, C.; Buisine, E.; Kwasigroch, J.-M.; Wintjens, R.; Rooman, M. Probing the energetic and structural role of amino acid/nucleobase cation-π interactions in protein-ligand complexes J. Biol. Chem. 2002, 277, 40816-40822
67. Gromiha, M. M.; Santhosh, C.; Ahmad, S. Structural analysis of cation-π interactions in DNA binding proteins Int. J. Biol. Macromol. 2004, 34, 203-211
68. Hong, H.; Szabo, G.; Tamm, L. K. Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening Nat. Chem. Biol. 2006, 2, 627-635
69. Honig, B. H.; Hubbell, W. L. Stability of 'salt bridges' in membrane proteins Proc. Natl. Acad. Sci. U. S. A. 1984, 81, 5412-5416
70. Starr, F. W.; Nielsen, J. K.; Stanley, H. E. Fast and slow dynamics of hydrogen bonds in liquid water Phys. Rev. Lett. 1999, 82, 2294-2297
71. Fändrich, M. On the structural definition of amyloid fibrils and other polypeptide aggregates Cell. Mol. Life Sci. 2007, 64, 2066-2078
72. Toyama, B. H.; Weissman, J. S. Amyloid structure: Conformational diversity and consequences Annu. Rev. Biochem. 2011, 80, 557-585
73. Tsai, H.-H. G.; Zanuy, D.; Haspel, N.; Gunasekaran, K.; Ma, B.; Tsai, C.-J.; Nussinov, R. The stability and dynamics of the human calcitonin amyloid peptide DFNKF Biophys. J. 2004, 87, 146-158
74. Gazit, E. A possible role for π-stacking in the self-assembly of amyloid fibrils FASEB J. 2002, 16, 77-83
75. Sahoo, B.; Nag, S.; Sengupta, P.; Maiti, S. On the stability of the soluble amyloid aggregates Biophys. J. 2009, 97, 1454-1460
76. Pettersen, E. F.; Goddard, T. D.; Huang, C. C.; Couch, G. S.; Greenblatt, D. M.; Meng, E. C.; Ferrin, T. E. UCSF Chimera-A visualization system for exploratory research and analysis J. Comput. Chem. 2004, 25, 1605-1612