Improved model of hydrated calcium ion for molecular dynamics simulations using classical biomolecular force fields

Biopolymers

Volumn , Issue , 2016, Pages 752-763

  Yoo, Jejoong ^a,b   Wilson, James ^a   Aksimentiev, Aleksei ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Illinois at Urbana Champaign   (United States)

Author keywords

AMBER; calcium; CHARMM; force field; molecular dynamics; nucleic acid

Indexed keywords

AMBER; BIOPOLYMERS; CALCIUM; CELL SIGNALING; DNA; ELECTRIC FIELDS; FREE ENERGY; HYDRATION; IONS; LIPID BILAYERS; MOLECULAR DYNAMICS; NUCLEIC ACIDS; OSMOSIS;

CHARMM; CLASSICAL FORCE FIELDS; EXPERIMENTAL VALUES; FORCE FIELDS; LIPID BILAYER MEMBRANES; MOLECULAR DYNAMICS SIMULATIONS; QUANTITATIVE AGREEMENT; SOLID-STATE NANOPORE;

BIOINFORMATICS;

CALCIUM ACETATE; CALCIUM CHLORIDE; CALCIUM ION; CHLORIDE; OXYGEN; PHOSPHATE; WATER;

ARTICLE; BIOMOLECULAR ELECTRONICS; ELECTRIC FIELD; ENERGY; FORCE; HYDRATION; INTERACTIONS WITH DNA; MOLECULAR DYNAMICS; MOLECULAR MODEL; NANOPORE; OSMOTIC PRESSURE; QUANTITATIVE ANALYSIS; SOLID STATE;

EID: 84979037384     PISSN: 00063525     EISSN: 10970282     Source Type: Journal    
DOI: 10.1002/bip.22868     Document Type: Article

References (82)

1. Berridge, M. J. Nature 1993, 361, 315–325.
2. Berridge, M. J.; Bootman, M. D.; Roderick, H. L. Nat Rev Mol Cell Biol 2003, 4, 517–529.
3. Clapham, D. E. Cell 1995, 80, 259–268.
4. Clapham, D. E. Cell 2007, 131, 1047–1058.
5. McLaughlin, S.; Wang, J.; Gambhir, A.; Murray, D. Annu Rev Biophys Biomol Struct 2002, 31, 151–175.
6. McLaughlin, S.; Murray, D. Nature 2005, 438, 605–611.
7. Dolmetsch, R. E.; Lewis, R. S.; Goodnow, C. C.; Healy, J. I. Nature 1997, 386, 855–858.
8. Dolmetsch, R. E.; Xu, K.; Lewis, R. S. Nature 1998, 392, 933–936.
9. Bading, H. Nat Rev Neurosci 2013, 14, 593–608.
10. Dominguez, D. C. Mol Microbiol 2004, 54, 291–297.
11. Nakayama, S.; Kretsinger, R. H. Annu Rev Biophys Biomol Struct 1994, 23, 473–507.
12. Ellenbroek, W. G.; Wang, Y. H. H.; Christian, D. A.; Discher, D. E.; Janmey, P. A.; Liu, A. J Biophys J 2011, 101, 2178–2184.
13. Boettcher, J. M.; Davis-Harrison, R. L.; Clay, M. C.; Nieuwkoop, A. J.; Ohkubo, Y. Z.; Tajkhorshid, E.; Morrissey, J. H.; Rienstra, C. M. Biochemistry 2011, 50, 2264–2273.
14. Wang, Y. H.; Collins, A.; Guo, L.; Smith-Dupont, K. B.; Gai, F.; Svitkina, T.; Janmey, P. A. J Am Chem Soc 2012, 134, 3387–3395.
15. Rau, D. C.; Lee, B.; Parsegian, V. A. Proc Natl Acad Sci USA 1984, 81, 2621–2625.
16. Qiu, X.; Parsegian, V. A.; Rau, D. C. Proc Natl Acad Sci USA 2010, 107, 21482–21486.
17. Celander, D.; Cech, T. Science 1991, 251, 401–407.
18. Draper, D. E.; Grilley, D.; Soto, A. M. Annu Rev Biophys Biomol Struct 2005, 34, 221–243.
19. Sotomayor, M.; Schulten, K. Biophys J 2008, 94, 4621–4633.
20. Bai, Y.; Greenfeld, M.; Travers, K. J.; Chu, V. B.; Lipfert, J.; Doniach, S.; Herschlag, D. J Am Chem Soc 2007, 129, 14981–14988.
21. Pabst, G.; Hodzic, A.; Strancar, J.; Danner, S.; Rappolt, M.; Laggner, P. Biophys J 2007, 93, 2688–2696.
22. Sovago, M.; Wurpel, G. W. H.; Smits, M.; Müller, M.; Bonn, M. J Am Chem Soc 2007, 129, 11079–11084.
23. Åqvist, J. J Phys Chem 1990, 94, 8021–8024.
24. Marchand, S.; Roux, B. Proteins: Struct, Funct, Bioinf 1998, 33, 265–284.
25. Jalilehvand, F.; Spångberg, D.; Lindqvist-Reis, P.; Hermansson, K.; Persson, I.; Sandström, M. J Am Chem Soc 2001, 123, 431–441.
26. Sponer, J.; Leszczynski, J.; Hobza, P. Biopolymers 2001, 61, 3–31.
27. Piquemal, J. P.; Perera, L.; Cisneros, G. A.; Ren, P.; Pedersen, L. G.; Darden, T. A. J Chem Phys 2006, 125, 054511.
28. Ikeda, T.; Boero, M.; Terakura, K. J Chem Phys 2007, 127, 074503.
29. Yoo, J.; Aksimentiev, A. J Phys Chem Lett 2012, 3, 45–50.
30. Yoo, J.; Aksimentiev, A. J Phys Chem B 2012, 116, 12946–12954.
31. Saxena, A.; Sept, D. J Chem Theory Comput 2013, 9, 3538–3542.
32. Saxena, A.; García, A. E. J Phys Chem B 2015, 119, 219–227.
33. Luo, Y.; Roux, B. J Phys Chem Lett 2009, 1, 183–189.
34. Yoo, J.; Aksimentiev, A. J Chem Theory Comput 2016, 12, 430–443.
35. Miller, M.; Lay, W.; Elcock, A. H. J Phys Chem B 2016, In press. DOI: 10.1021/acs.jpcb.6b01902.
36. Lay, W. K.; Miller, M. S.; Elcock, A. H. J Chem Theory Comput 2016, 12, 1401–1407.
37. Best, R. B.; Zhu, X.; Shim, J.; Lopes, P. E. M.; Mittal, J.; Feig, M.; MacKerell, A. D. Jr., J Chem Theory Comput 2012, 8, 3257–3273.
38. Apelblat, A.; Korin, E. J Chem Thermodynamics 2001, 33, 113–120.
39. Robinson, R. A.; Stokes, R. H. Electrolyte Solutions; Butterworths scientific publications, London, 1959.
40. Dill, K. A.; Bromberg, S. Molecular Driving Forces: Statistical Thermodynamics in Biology, Chemistry, Physics, and Nanoscience; Garland Science, New York, 2010.
41. Yoo, J.; Aksimentiev, A. Nucleic Acids Res 2016, 44, 2036–2046.
42. Kumar, S.; Rosenberg, J. M.; Bouzida, D.; Swendsen, R. H.; Kollman, P. A. J Comput Chem 1992, 13, 1011–1021.
43. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. J Chem Phys 1983, 79, 926–935.
44. Fulton, J. L.; Heald, S. M.; Badyal, Y. S.; Simonson, J. M. J Phys Chem A 2003, 107, 4688–4696.
45. Fulton, J. L.; Chen, Y.; Heald, S. M.; Balasubramanian, M. J Chem Phys 2006, 125, 094507.
46. Badyal, Y. S.; Barnes, A. C.; Cuello, G. J.; Simonson, J. M. J Phys Chem A 2004, 108, 11819–11827.
47. Schwenk, C. F.; Loeffler, H. H.; Rode, B. M. J Chem Phys 2001, 115, 10808–10813.
48. Bakó, I.; Hutter, J.; Pálinkás, G. J Chem Phys 2002, 117, 9838–9843.
49. Jiao, D.; King, C.; Grossfield, A.; Darden, T. A.; Ren, P. J Phys Chem B 2006, 110, 18553–18559.
50. Lightstone, F. C.; Schwegler, E.; Allesch, M.; Gygi, F.; Galli, G. ChemPhysChem 2005, 6, 1745–1749.
51. McNally, B.; Singer, A.; Yu, Z.; Sun, Y.; Weng, Z.; Meller, A. Nano Lett 2010, 10, 2237–2244.
52. Ivankin, A.; Henley, R. Y.; Larkin, J.; Carson, S.; Toscano, M. L.; Wanunu, M. ACS Nano 2014, 8, 10774–10781.
53. Maffeo, C.; Bhattacharya, S.; Yoo, J.; Wells, D. B.; Aksimentiev, A. Chem Rev 2012, 112, 6250–6284.
54. Pedersen, U. R.; Leidy, C.; Westh, P.; Peters, G. H. Biochim Biophys Acta Biomembr 2006, 1758, 573–582.
55. Böckmann, R. A.; Grubmüller, H. Angew Chem Int Ed Engl 2004, 43, 1021–1024.
56. Issa, Z. K.; Manke, C. W.; Jena, B. P.; Potoff, J. J. J Phys Chem B 2010, 114, 13249–13254.
57. Berger, O.; Edholm, O.; Jähnig, F. Biophys J 1997, 72, 2002–2013.
58. Luan, B.; Carr, R.; Caffrey, M.; Aksimentiev, A. Proteins: Struct, Funct, Bioinf 2010, 78, 1162.
59. Baker, C. M.; Lopes, P. E. M.; Zhu, X.; Roux, B.; MacKerell, A. D., Jr., J Chem Theory Comput 2010, 6, 1181–1198.
60. Ponder, J. W.; Wu, C.; Ren, P.; Pande, V. S.; Chodera, J. D.; Schnieders, M. J.; Haque, I.; Mobley, D. L.; Lambrecht, D. S.; DiStasio, R. A.; Head-Gordon, M.; Clark, G. N. I.; Johnson, M. E.; Head-Gordon, T. J Phys Chem B 2010, 114, 2549–2564.
61. Li, H.; Ngo, V.; Da Silva, M. C.; Salahub, D. R.; Callahan, K.; Roux, B.; Noskov, S. Y. J Phys Chem B 2015, 119, 9401–9416.
62. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. J Chem Theory Comput 2008, 4, 435–447.
63. Darden, T. A.; York, D.; Pedersen, L. J Chem Phys 1993, 98, 10089–10092.
64. Nose, S.; Klein, M. L. Mol Phys 1983, 50, 1055–1076.
65. Hoover, W. G. Phys Rev A 1985, 31, 1695–1697.
66. Parrinello, M.; Rahman, A. J Appl Phys 1981, 52, 7182–7190.
67. Miyamoto, S.; Kollman, P. A. J Comput Chem 1992, 13, 952–962.
68. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. J Comput Chem 1997, 18, 1463–1472.
69. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. J Comput Chem 2005, 26, 1781–1802.
70. Andersen, H. C. J Comput Phys 1983, 52, 24–34.
71. Martyna, G. J.; Tobias, D. J.; Klein, M. L. J Chem Phys 1994, 101, 4177–4189.
72. MacKerell, A. D., Jr.; Banavali, N. K. J Comput Chem 2000, 21, 105–120.
73. Beglov, D.; Roux, B. J Chem Phys 1994, 100, 9050–9063.
74. Hart, K.; Foloppe, N.; Baker, C. M.; Denning, E. J.; Nilsson, L.; MacKerell, A. D. Jr. J Chem Theory Comput 2012, 8, 348–362.
75. Cornell, W. D.; Cieplak, P.; Bayly, C. I.; Gould, I. R.; Merz, K. M.; Ferguson, D. M.; Spellmeyer, D. C.; Fox, T.; Caldwell, J. W.; Kollman, P. A. J Am Chem Soc 1995, 117, 5179–5197.
76. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Biophys J 2007, 92, 3817–3829.
77. Joung, I. S.; Cheatham, T. E. J Phys Chem B 2008, 112, 9020–9041.
78. van Dijk, M.; Bonvin, A. M. J. J Nucleic Acids Res 2009, 37, W235–W239.
79. Carson, S.; Wilson, J.; Aksimentiev, A.; Wanunu, M. Biophys J 2014, 107, 2381–2393.
80. Aksimentiev, A.; Heng, J. B.; Timp, G.; Schulten, K. Biophys J 2004, 87, 2086–2097.
81. Comer, J.; Dimitrov, V.; Zhao, Q.; Timp, G.; Aksimentiev, A. Biophys J 2009, 96, 593–608.
82. Wells, D. B.; Abramkina, V.; Aksimentiev, A. J Chem Phys 2007, 127, 125101.