Mapping the structural and dynamical features of multiple p53 DNA binding domains: Insights into loop 1 intrinsic dynamics

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Lukman, Suryani ^a   Lane, David P ^b   Verma, Chandra S ^a,c,d  

^a BIOINFORMATICS INSTITUTE   (Singapore)

^b AGENCY FOR SCIENCE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; RIBOSOMAL PROTEIN L1; RIBOSOME PROTEIN; RIBOSOME PROTEIN L3; UNCLASSIFIED DRUG; ZINC ION;

AMINO ACID SEQUENCE; ARTICLE; DNA BINDING MOTIF; DNA TRANSCRIPTION; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN PROCESSING; SIMULATION; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84893122526     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080221     Document Type: Article

References (103)

1. Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408: 307-310. doi:10.1038/35042675. PubMed: 11099028.
2. Li T, Kon N, Jiang L, Tan M, Ludwig T et al. (2012) Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 149: 1269-1283. doi:10.1016/j.cell.2012.04.026. PubMed: 22682249.
3. Vousden KH, Prives C (2009) Blinded by the Light: The Growing Complexity of p53. Cell 137: 413-431. doi:10.1016/j.cell.2009.04.037. PubMed: 19410540.
4. Dai C, Gu W (2010) p53 post-translational modification: deregulated in tumorigenesis. Trends Mol Med 16: 528-536. doi:10.1016/j.molmed.2010.09.002. PubMed: 20932800.
5. Joerger AC, Fersht AR (2008) Structural biology of the tumor suppressor p53. Annu Rev Biochem 77: 557-582. doi:10.1146/annurev.biochem.77.060806.091238. PubMed: 18410249.
6. Okorokov AL, Orlova EV (2009) Structural biology of the p53 tumour suppressor. Curr Opin Struct Biol 19: 197-202. doi:10.1016/j.sbi.2009.02.003. PubMed: 19286366.
7. Cañadillas JM, Tidow H, Freund SM, Rutherford TJ, Ang HC et al. (2006) Solution structure of p53 core domain: structural basis for its instability. Proc Natl Acad Sci U S A 103: 2109-2114. doi:10.1073/pnas. 0510941103. PubMed: 16461916.
8. Loh SN (2010) The missing zinc: p53 misfolding and cancer. Metallomics 2: 442-449. doi:10.1039/c003915b. PubMed: 21072344.
9. Xu X, Ma Z, Wang X, Xiao ZT, Li Y et al. (2012) Water's potential role: Insights from studies of the p53 core domain. J Struct Biol 177: 358-366. doi:10.1016/j.jsb.2011.12.008. PubMed: 22197648.
10. Bista M, Freund SM, Fersht AR (2012) Domain-domain interactions in full-length p53 and a specific DNA complex probed by methyl NMR spectroscopy. Proc Natl Acad Sci U S A 109: 15752-15756. doi:10.1073/pnas.1214176109. PubMed: 22972749.
11. Liu J, Pan Y, Ma B, Nussinov R (2006) "Similarity trap" in protein-protein interactions could be carcinogenic: simulations of p53 core domain complexed with 53BP1 and BRCA1 BRCT domains. Structure 14: 1811-1821. doi:10.1016/j.str.2006.10.009. PubMed: 17161371.
12. Bullock AN, Henckel J, DeDecker BS, Johnson CM, Nikolova PV et al. (1997) Thermodynamic stability of wild-type and mutant p53 core domain. Proc Natl Acad Sci U S A 94: 14338-14342. doi:10.1073/pnas.94.26.14338. PubMed: 9405613.
13. Olivier M, Eeles R, Hollstein M, Khan MA, Harris CC et al. (2002) The IARC TP53 database: new online mutation analysis and recommendations to users. Hum Mutat 19: 607-614. doi:10.1002/humu.10081. PubMed: 12007217.
14. Kawaguchi T, Kato S, Otsuka K, Watanabe G, Kumabe T et al. (2005) The relationship among p53 oligomer formation, structure and transcriptional activity using a comprehensive missense mutation library. Oncogene 24: 6976-6981. doi:10.1038/sj.onc.1208839. PubMed: 16007150.
15. Sakaguchi K, Sakamoto H, Lewis MS, Anderson CW, Erickson JW et al. (1997) Phosphorylation of serine 392 stabilizes the tetramer formation of tumor suppressor protein p53. Biochemistry 36: 10117-10124. doi:10.1021/bi970759w. PubMed: 9254608.
16. Natan E, Hirschberg D, Morgner N, Robinson CV, Fersht AR (2009) Ultraslow oligomerization equilibria of p53 and its implications. Proc Natl Acad Sci U S A 106: 14327-14332. doi:10.1073/pnas.0907840106. PubMed: 19667193.
17. Kitayner M, Rozenberg H, Kessler N, Rabinovich D, Shaulov L et al. (2006) Structural basis of DNA recognition by p53 tetramers. Mol Cell 22: 741-753. doi:10.1016/j.molcel.2006.05.015. PubMed: 16793544.
18. Wang Y, Rosengarth A, Luecke H (2007) Structure of the human p53 core domain in the absence of DNA. Acta Crystallogr D Biol Crystallogr 63: 276-281. doi:10.1107/S0907444906048499. PubMed: 17327663.
19. Ho WC, Fitzgerald MX, Marmorstein R (2006) Structure of the p53 core domain dimer bound to DNA. J Biol Chem 281: 20494-20502. doi:10.1074/jbc. M603634200. PubMed: 16717092.
20. Lubin DJ, Butler JS, Loh SN (2010) Folding of tetrameric p53: oligomerization and tumorigenic mutations induce misfolding and loss of function. J Mol Biol 395: 705-716. doi:10.1016/j.jmb.2009.11.013. PubMed: 19913028.
21. Duan J, Nilsson L (2006) Effect of Zn2+ on DNA recognition and stability of the p53 DNA-binding domain. Biochemistry 45: 7483-7492. doi:10.1021/ bi0603165. PubMed: 16768444.
22. Butler JS, Loh SN (2003) Structure, function, and aggregation of the zinc-free form of the p53 DNA binding domain. Biochemistry 42: 2396-2403. doi:10.1021/bi026635n. PubMed: 12600206.
23. Puca R, Nardinocchi L, Porru M, Simon AJ, Rechavi G et al. (2011) Restoring p53 active conformation by zinc increases the response of mutant p53 tumor cells to anticancer drugs. Cell Cycle 10: 1679-1689. doi:10.4161/cc.10.10. 15642. PubMed: 21508668.
24. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254: 1598-1603. doi:10.1126/science.1749933. PubMed: 1749933.
25. Weber G (1972) Ligand binding and internal equilibria in proteins. Biochemistry 11: 864-878. doi:10.1021/bi00755a028. PubMed: 5059892.
26. Kern D, Zuiderweg ER (2003) The role of dynamics in allosteric regulation. Curr Opin Struct Biol 13: 748-757. doi:10.1016/j.sbi.2003.10.008. PubMed: 14675554.
27. Tsai CJ, del Sol A, Nussinov R (2008) Allostery: absence of a change in shape does not imply that allostery is not at play. J Mol Biol 378: 1-11. doi:10.1016/j.jmb.2008.02.034. PubMed: 18353365.
28. Barakat K, Issack BB, Stepanova M, Tuszynski J (2011) Effects of temperature on the p53-DNA binding interactions and their dynamical behavior: comparing the wild type to the R248Q mutant. PLOS ONE 6: e27651. doi:10.1371/journal.pone.0027651. PubMed: 22110706.
29. Chen JM, Rosal R, Smith S, Pincus MR, Brandt-Rauf PW (2001) Common conformational effects of p53 mutations. J Protein Chem 20: 101-105. doi:10.1023/A:1011065022283. PubMed: 11563689.
30. Pan Y, Ma B, Venkataraghavan RB, Levine AJ, Nussinov R (2005) In the quest for stable rescuing mutants of p53: computational mutagenesis of flexible loop L1. Biochemistry 44: 1423-1432. doi:10.1021/bi047845y. PubMed: 15683227.
31. Merabet A, Houlleberghs H, Maclagan K, Akanho E, Bui TT et al. (2010) Mutants of the tumour suppressor p53 L1 loop as second-site suppressors for restoring DNA binding to oncogenic p53 mutations: structural and biochemical insights. Biochem J 427: 225-236. doi:10.1042/BJ20091888. PubMed: 20113312.
32. Noskov SY, Wright JD, Lim C (2002) Long-Range Effects of Mutating R248 to Q/W in the p53 Core Domain. J Phys Chem B 106: 13047-13057. doi:10.1021/jp022140w.
33. Tan YH, Chen YM, Ye X, Lu Q, Tretyachenko-Ladokhina V et al. (2009) Molecular mechanisms of functional rescue mediated by P53 tumor suppressor mutations. Biophys Chem 145: 37-44. doi:10.1016/j.bpc.2009.08.008. PubMed: 19748724.
34. Lukman S, Grant BJ, Gorfe AA, Grant GH, McCammon JA (2010) The distinct conformational dynamics of K-Ras and H-Ras A59G. PLOS Comput Biol 6: ([MedlinePgn:]) PubMed: 20838576.
35. Grant BJ, Lukman S, Hocker HJ, Sayyah J, Brown JH et al. (2011) Novel allosteric sites on Ras for lead generation. PLOS ONE 6: e25711. doi:10.1371/journal.pone.0025711. PubMed: 22046245.
36. Grant BJ, Rodrigues AP, ElSawy KM, McCammon JA, Caves LS (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22: 2695-2696.
37. Yang L, Song G, Carriquiry A, Jernigan RL (2008) Close correspondence between the motions from principal component analysis of multiple HIV-1 protease structures and elastic network modes. Structure 16: 321-330. doi:10.1016/j.str.2007.12.011. PubMed: 18275822.
38. Petty TJ, Emamzadah S, Costantino L, Petkova I, Stavridi ES et al. (2011) An induced fit mechanism regulates p53 DNA binding kinetics to confer sequence specificity. EMBO J 30: 2167-2176. doi:10.1038/emboj.2011.127. PubMed: 21522129.
39. Emamzadah S, Tropia L, Halazonetis TD (2011) Crystal structure of a multidomain human p53 tetramer bound to the natural CDKN1A (p21) p53-response element. Mol Cancer Res 9: 1493-1499. doi:10.1158/1541-7786.MCR-11-0351. PubMed: 21933903.
40. Cho Y, Gorina S, Jeffrey PD, Pavletich NP (1994) Crystal structure of a p53 tumor suppressor-DNA complex: understanding tumorigenic mutations. Science 265: 346-355. doi:10.1126/science.8023157. PubMed: 8023157.
41. Lilyestrom W, Klein MG, Zhang R, Joachimiak A, Chen XS (2006) Crystal structure of SV40 large T-antigen bound to p53: interplay between a viral oncoprotein and a cellular tumor suppressor. Genes Dev 20: 2373-2382. doi:10.1101/gad.1456306. PubMed: 16951253.
42. Miller SD, Farmer G, Prives C (1995) p53 inhibits DNA replication in vitro in a DNA-binding-dependent manner. Mol Cell Biol 15: 6554-6560. PubMed: 8524220.
43. Bargonetti J, Reynisdóttir I, Friedman PN, Prives C (1992) Site-specific binding of wild-type p53 to cellular DNA is inhibited by SV40 T antigen and mutant p53. Genes Dev 6: 1886-1898. doi:10.1101/gad.6.10.1886. PubMed: 1398068.
44. Joerger AC, Ang HC, Veprintsev DB, Blair CM, Fersht AR (2005) Structures of p53 cancer mutants and mechanism of rescue by second-site suppressor mutations. J Biol Chem 280: 16030-16037. doi:10.1074/jbc.M500179200. PubMed: 15703170.
45. Ang HC, Joerger AC, Mayer S, Fersht AR (2006) Effects of common cancer mutations on stability and DNA binding of full-length p53 compared with isolated core domains. J Biol Chem 281: 21934-21941. doi:10.1074/jbc.M604209200. PubMed: 16754663.
46. Tidow H, Veprintsev DB, Freund SM, Fersht AR (2006) Effects of oncogenic mutations and DNA response elements on the binding of p53 to p53-binding protein 2 (53BP2). J Biol Chem 281: 32526-32533. doi:10.1074/jbc.M604725200. PubMed: 16887812.
47. Bowman GR, Geissler PL (2012) Equilibrium fluctuations of a single folded protein reveal a multitude of potential cryptic allosteric sites. Proc Natl Acad Sci U S A 109: 11681-11686. doi:10.1073/pnas.1209309109. PubMed: 22753506.
48. Csermely P, Palotai R, Nussinov R (2010) Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends Biochem Sci 35: 539-546. doi:10.1016/j.tibs.2010.04.009. PubMed: 20541943.
49. Kwon E, Kim DY, Suh SW, Kim KK (2008) Crystal structure of the mouse p53 core domain in zinc-free state. Proteins 70: 280-283. PubMed: 17876829.
50. Hainaut P, Milner J (1993) Redox modulation of p53 conformation and sequence-specific DNA binding in vitro. Cancer Res 53: 4469-4473. PubMed: 8402615.
51. Hainaut P, Milner J (1993) A structural role for metal ions in the "wild-type" conformation of the tumor suppressor protein p53. Cancer Res 53: 1739-1742. PubMed: 8467489.
52. Holloway DE, Singh UP, Shogen K, Acharya KR (2011) Crystal structure of Onconase at 1.1 A resolution - insights into substrate binding and collective motion. FEBS J 278: 4136-4149. doi:10.1111/j.1742-4658.2011.08320.x. PubMed: 21895975.
53. Fraser JS, van den Bedem H, Samelson AJ, Lang PT, Holton JM et al. (2011) Accessing protein conformational ensembles using room-temperature X-ray crystallography. Proc Natl Acad Sci U S A 108: 16247-16252. doi:10.1073/pnas. 1111325108. PubMed: 21918110.
54. Zheng W, Brooks BR, Thirumalai D (2006) Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc Natl Acad Sci U S A 103: 7664-7669. doi:10.1073/pnas.0510426103. PubMed: 16682636.
55. Tama F, Gadea FX, Marques O, Sanejouand YH (2000) Building-block approach for determining low-frequency normal modes of macromolecules. Proteins 41: 1-7. doi:10.1002/1097-0134(20001001)41:1. PubMed: 10944387.
56. Tzeng SR, Kalodimos CG (2012) Protein activity regulation by conformational entropy. Nature 488: 236-240. doi:10.1038/nature11271. PubMed: 22801505.
57. Kamerzell TJ, Middaugh CR (2008) The complex inter-relationships between protein flexibility and stability. J Pharmacol Sci 97: 3494-3517. doi:10.1002/jps.21269. PubMed: 18186490.
58. Grant BJ, Gheorghe DM, Zheng W, Alonso M, Huber G et al. (2011) Electrostatically biased binding of kinesin to microtubules. PLOS Biol 9: e1001207. PubMed: 22140358.
59. ElSawy KM, Twarock R, Verma CS, Caves LS (2012) Peptide inhibitors of viral assembly: a novel route to broad-spectrum antivirals. J Chem Inf Model 52: 770-776. doi:10.1021/ci200467s. PubMed: 22390317.
60. Pan Y, Nussinov R (2007) Structural basis for p53 binding-induced DNA bending. J Biol Chem 282: 691-699. PubMed: 17085447.
61. Kosztin D, Bishop TC, Schulten K (1997) Binding of the estrogen receptor to DNA. The role of waters. Biophys J 73: 557-570. doi:10.1016/S0006-3495(97) 78093-7. PubMed: 9251777.
62. Arbely E, Natan E, Brandt T, Allen MD, Veprintsev DB et al. (2011) Acetylation of lysine 120 of p53 endows DNA-binding specificity at effective physiological salt concentration. Proc Natl Acad Sci U S A 108: 8251-8256. doi:10.1073/pnas.1105028108. PubMed: 21525412.
63. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R et al. (2006) Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Mol Cell 24: 841-851. doi:10.1016/j.molcel.2006.11.026. PubMed: 17189187.
64. Lickwar CR, Mueller F, Hanlon SE, McNally JG, Lieb JD (2012) Genome-wide protein-DNA binding dynamics suggest a molecular clutch for transcription factor function. Nature 484: 251-255. doi:10.1038/nature10985. PubMed: 22498630.
65. Tafvizi A, Huang F, Fersht AR, Mirny LA, van Oijen AM (2011) A single-molecule characterization of p53 search on DNA. Proc Natl Acad Sci U S A 108: 563-568. doi:10.1073/pnas.1016020107. PubMed: 21178072.
66. Calhoun S, Daggett V (2011) Structural effects of the L145Q, V157F, and R282W cancer-associated mutations in the p53 DNA-binding core domain. Biochemistry 50: 5345-5353. doi:10.1021/bi200192j. PubMed: 21561095.
67. Benson NC, Daggett V (2012) A Comparison of Multiscale Methods for the Analysis of Molecular Dynamics Simulations. J Phys Chem B.
68. Joerger AC, Ang HC, Fersht AR (2006) Structural basis for understanding oncogenic p53 mutations and designing rescue drugs. Proc Natl Acad Sci U S A 103: 15056-15061. doi:10.1073/pnas.0607286103. PubMed: 17015838.
69. Tu C, Tan YH, Shaw G, Zhou Z, Bai Y et al. (2008) Impact of low-frequency hotspot mutation R282Q on the structure of p53 DNA-binding domain as revealed by crystallography at 1.54 angstroms resolution. Acta Crystallogr D Biol Crystallogr 64: 471-477. doi:10.1107/S0907444908003338. PubMed: 18453682.
70. Huyen Y, Jeffrey PD, Derry WB, Rothman JH, Pavletich NP et al. (2004) Structural differences in the DNA binding domains of human p53 and its C. elegans ortholog Cep-1. Structure 12: 1237-1243. doi:10.1016/j.str.2004.05.007. PubMed: 15242600.
71. Ichiye T, Karplus M (1991) Collective motions in proteins: a covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations. Proteins 11: 205-217. doi:10.1002/prot.340110305. PubMed: 1749773.
72. Lukman S, Grant GH, Bui JM (2010) Unraveling evolutionary constraints: a heterogeneous conservation in dynamics of the titin Ig domains. FEBS Lett 584: 1235-1239. doi:10.1016/j.febslet.2010.02.035. PubMed: 20171214.
73. McLure KG, Lee PW (1998) How p53 binds DNA as a tetramer. EMBO J 17: 3342-3350. doi:10.1093/emboj/17.12.3342. PubMed: 9628871.
74. Weinberg RL, Veprintsev DB, Fersht AR (2004) Cooperative binding of tetrameric p53 to DNA. J Mol Biol 341: 1145-1159. doi:10.1016/j.jmb.2004.06.071. PubMed: 15321712.
75. Wang Y, Schwedes JF, Parks D, Mann K, Tegtmeyer P (1995) Interaction of p53 with its consensus DNA-binding site. Mol Cell Biol 15: 2157-2165. PubMed: 7891710.
76. Hubbard S, Thornton J (1993) NACCESS, 2.1. 1. London: Department of Biochemistry and Molecular Biology, University College.
77. Brachmann RK, Yu K, Eby Y, Pavletich NP, Boeke JD (1998) Genetic selection of intragenic suppressor mutations that reverse the effect of common p53 cancer mutations. EMBO J 17: 1847-1859. doi:10.1093/emboj/17.7.1847. PubMed: 9524109.
78. Inga A, Resnick MA (2001) Novel human p53 mutations that are toxic to yeast can enhance transactivation of specific promoters and reactivate tumor p53 mutants. Oncogene 20: 3409-3419. doi:10.1038/sj.onc.1204457. PubMed: 11423991.
79. Zupnick A, Prives C (2006) Mutational analysis of the p53 core domain L1 loop. J Biol Chem 281: 20464-20473. doi:10.1074/jbc.M603387200. PubMed: 16687402.
80. Saller E, Tom E, Brunori M, Otter M, Estreicher A et al. (1999) Increased apoptosis induction by 121F mutant p53. EMBO J 18: 4424-4437. doi:10.1093/emboj/18.16.4424. PubMed: 10449408.
81. Fen CX, Coomber DW, Lane DP, Ghadessy FJ (2007) Directed evolution of p53 variants with altered DNA-binding specificities by in vitro compartmentalization. J Mol Biol 371: 1238-1248. doi:10.1016/j.jmb.2007.05.099. PubMed: 17610896.
82. Dhulesia A, Gsponer J, Vendruscolo M (2008) Mapping of two networks of residues that exhibit structural and dynamical changes upon binding in a PDZ domain protein. J Am Chem Soc 130: 8931-8939. doi:10.1021/ja0752080. PubMed: 18558679.
83. Osborne MJ, Schnell J, Benkovic SJ, Dyson HJ, Wright PE (2001) Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism. Biochemistry 40: 9846-9859. doi:10.1021/bi010621k. PubMed: 11502178.
84. Lukman S, Robinson RC, Wales D, Verma CS (2012) Conformational dynamics of capping protein and interaction partners: simulation studies. Proteins 80: 1066-1077. doi:10.1002/prot.24008. PubMed: 22253039.
85. Berlow RB, Swain M, Dalal S, Sweasy JB, Loria JP (2012) Substrate-Dependent Millisecond Domain Motions in DNA Polymerase beta. J Mol Biol 419: 171-182. doi:10.1016/j.jmb.2012.03.013. PubMed: 22446382.
86. Smirnova IN, Kaback HR (2003) A mutation in the lactose permease of Escherichia coli that decreases conformational flexibility and increases protein stability. Biochemistry 42: 3025-3031. doi:10.1021/bi027329c. PubMed: 12627968.
87. Reuveni S, Granek R, Klafter J (2008) Proteins: coexistence of stability and flexibility. Phys Rev Lett 100: 208101. doi:10.1103/PhysRevLett.100.208101. PubMed: 18518581.
88. Jordan JJ, Menendez D, Sharav J, Beno I, Rosenthal K et al. (2012) Low-level p53 expression changes transactivation rules and reveals superactivating sequences. Proc Natl Acad Sci U S A 109: 14387-14392. doi:10.1073/pnas.1205971109. PubMed: 22908277.
89. Wassman CD, Baronio R, Demir O, Wallentine BD, Chen CK et al. (2013) Computational identification of a transiently open L1/S3 pocket for reactivation of mutant p53. Nat Commun 4: 1407. doi:10.1038/ncomms2361. PubMed: 23360998.
90. Gorfe AA, Grant BJ, McCammon JA (2008) Mapping the nucleotide and isoform-dependent structural and dynamical features of Ras proteins. Structure 16: 885-896. doi:10.1016/j.str.2008.03.009. PubMed: 18547521.
91. Kabsch W, Sander C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637. doi:10.1002/bip.360221211. PubMed: 6667333.
92. Frishman D, Argos P (1995) Knowledge-based protein secondary structure assignment. Proteins 23: 566-579. doi:10.1002/prot.340230412. PubMed: 8749853.
93. Hornak V, Abel R, Okur A, Strockbine B, Roitberg A et al. (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65: 712-725. doi:10.1002/prot.21123. PubMed: 16981200.
94. Case D, Darden T, Cheatham TE, Simmerling CL, Wang J et al. (2010) AMBER 11. University of California, San Francisco.
95. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926. doi:10.1063/1.445869.
96. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32: W665-W667. doi:10.1093/nar/gkh381. PubMed: 15215472.
97. Darden T, York D, Pedersen L (1993) Particle mesh Ewald-an NlogN method for Ewald sums in large systems. J Chem Phys 98: 10089-10092. doi:10.1063/1.464397.
98. Pastor RW, Bernard R Brooks, Szabo A (1988) An analysis of the accuracy of Langevin and molecular dynamics algorithms. Mol Phys 65: 1409-1419. doi:10.1080/00268978800101881.
99. van Gunsteren WF, Berendsen HJC (1977) Algorithms for macromolecular dynamics and constraint dynamics. Molecular Physics 34: 1311-1327.
100. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S et al. (2000) Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 33: 889-897. doi:10.1021/ar000033j. PubMed: 11123888.
101. Srinivasan J, Cheatham TE, Cieplak P, Kollman PA, Case DA (1998) Continuum Solvent Studies of the Stability of DNA, RNA, and Phosphoramidate-DNA Helices. J Am Chem Soc 120: 9401-9409.
102. Connolly ML (1983) Solvent-accessible surfaces of proteins and nucleic acids. Science 221: 709-713. doi:10.1126/science.6879170. PubMed: 6879170.
103. Sanner MF, Olson AJ, Spehner JC (1996) Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38: 305-320. doi:10.1002/(SICI)1097- 0282(199603)38:3. PubMed: 8906967.