Comparing the intrinsic dynamics of multiple protein structures using elastic network models

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 5, 2015, Pages 911-922

  Fuglebakk, Edvin ^a   Tiwari, Sandhya P ^a   Reuter, Nathalie ^a  

^a UNIVERSITY OF BERGEN   (Norway)

Author keywords

Elastic network models; Intrinsic dynamics; Normal mode analysis; Protein dynamics

Indexed keywords

ELASTIC NETWORK MODEL; MATHEMATICAL ANALYSIS; MATHEMATICAL COMPUTING; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; RELIABILITY; REVIEW; STRUCTURE ACTIVITY RELATION; VALIDATION STUDY; CHEMISTRY; KINETICS; MOTION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN UNFOLDING; THERMODYNAMICS;

PROTEIN;

KINETICS; MOLECULAR DYNAMICS SIMULATION; MOTION; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN UNFOLDING; PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 84923139220     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.09.021     Document Type: Review

References (129)

1. P.J. Fleming, and F.M. Richards Protein packing: dependence on protein size, secondary structure and amino acid composition J. Mol. Biol. 299 2000 487 498
2. B. Halle Flexibility and packing in proteins Proc. Natl. Acad. Sci. U. S. A. 99 2002 1274 1279
3. M.M. Tirion Large amplitude elastic motions in proteins from a single-parameter, atomic analysis Phys. Rev. Lett. 77 1996 1905 1908
4. K. Hinsen Analysis of domain motions by approximate normal mode calculations Proteins 33 1998 417 429
5. A.R. Atilgan, S.R. Durell, R.L. Jernigan, M.C. Demirel, O. Keskin, and I. Bahar Anisotropy of fluctuation dynamics of proteins with an elastic network model Biophys. J. 80 2001 505 515
6. B. Brooks, and M. Karplus Normal modes for specific motions of macromolecules: application to the hinge-bending mode of lysozyme Proc. Natl. Acad. Sci. U. S. A. 82 1985 4995 4999
7. N. Go, T. Noguti, and T. Nishikawa Dynamics of a small globular protein in terms of low-frequency vibrational modes Proc. Natl. Acad. Sci. U. S. A. 80 1983 3696 3700
8. M. Levitt, C. Sander, and P.S. Stern Protein normal-mode dynamics: trypsin inhibitor, crambin, ribonuclease and lysozyme J. Mol. Biol. 181 1985
9. T. Noguti, and N. Go Collective variable description of small-amplitude conformational fluctuations in a globular protein Nature 296 1982 776 778
10. B.R. Brooks, and M. Karplus Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor Proc. Natl. Acad. Sci. U. S. A. 80 1983 6571 6575
11. F. Pontiggia, G. Colombo, C. Micheletti, and H. Orland Anharmonicity and self-similarity of the free energy landscape of protein G Phys. Rev. Lett. 98 2007 048102
12. M. Rueda, P. Chacón, and M. Orozco Thorough validation of protein normal mode analysis: a comparative study with essential dynamics Structure 15 2007 565 575
13. L. Skjaerven, A. Martinez, and N. Reuter Principal component and normal mode analysis of proteins; a quantitative comparison using the GroEL subunit Proteins 79 2011 232 243
14. L. Yang, G. Song, A. Carriquiry, and R.L. Jernigan Close correspondence between the motions from principal component analysis of multiple HIV-1 protease structures and elastic network modes Structure 16 2008 321 330
15. O. Marques, and Y.H. Sanejouand Hinge-bending motion in citrate synthase arising from normal mode calculations Proteins 23 1995 557 560
16. K. Hinsen, A. Thomas, and M.J. Field Analysis of domain motions in large proteins Proteins 34 1999 369 382
17. F. Tama, and Y.H. Sanejouand Conformational change of proteins arising from normal mode calculations Protein Eng. 14 2001 1 6
18. W.G. Krebs, V. Alexandrov, C.A. Wilson, N. Echols, H. Yu, and M. Gerstein Normal mode analysis of macromolecular motions in a database framework: developing mode concentration as a useful classifying statistic Proteins 48 2002 682 695
19. J.M. Seckler, N. Leioatts, H. Miao, and A. Grossfield The interplay of structure and dynamics: insights from a survey of HIV-1 reverse transcriptase crystal structures Proteins 81 2013 1792 1801
20. T.L. Rodgers, P.D. Townsend, D. Burnell, M.L. Jones, S.A. Richards, T.C. McLeish, E. Pohl, M.R. Wilson, and M.J. Cann Modulation of global low-frequency motions underlies allosteric regulation: demonstration in CRP/FNR family transcription factors PLoS Biol. 11 2013 e1001651
21. D. Kolan, G. Fonar, and A.O. Samson Elastic network normal mode dynamics reveal the GPCR activation mechanism Proteins 82 2014 579 586
22. M. Laberge, and T. Yonetani Common dynamics of globin family proteins IUBMB life 59 2007 528 534
23. S. Lukman, and G.H. Grant A network of dynamically conserved residues deciphers the motions of maltose transporter Proteins 76 2009 588 597
24. S. Maguid, S. Fernández-Alberti, and J. Echave Exploring the common dynamics of homologous proteins. Application to the globin family Biophys. J. 89 2005 3 13
25. E. Marcos, R. Crehuet, and I. Bahar Changes in dynamics upon oligomerization regulate substrate binding and allostery in amino acid kinase family members PLoS Comput. Biol. 7 2011 e1002201
26. F. Raimondi, M. Orozco, and F. Fanelli Deciphering the deformation modes associated with function retention and specialization in members of the Ras superfamily Structure 18 2010 402 414
27. J.A. Velazquez-Muriel, M. Rueda, I. Cuesta, A. Pascual-Montano, and M. Orozco Comparison of molecular dynamics and superfamily spaces of protein domain deformation BMC Struct. Biol. 9 2009 6
28. W. Zheng, and S. Doniach A comparative study of motor-protein motions by using a simple elastic-network model Proc. Natl. Acad. Sci. U. S. A. 100 2003 13253 13258
29. S.M. Hollup, E. Fuglebakk, W.R. Taylor, and N. Reuter Exploring the factors determining the dynamics of different protein folds Protein Sci. 20 2011 197 209
30. C. Micheletti Comparing proteins by their internal dynamics: exploring structure-function relationships beyond static structural alignments Phys. Life Rev. 2013 10
31. A. Leo-Macias, P. Lopez-Romero, D. Lupyan, D.l Zerbino, and A.R. Ortiz Core deformations in protein families: a physical perspective Biophys. Chem. 115 2005 125 128
32. A. Leo-Macias, P. Lopez-Romero, D. Lupyan, D. Zerbino, and A.R. Ortiz An analysis of core deformations in protein superfamilies Biophys. J. 88 2005 1291 1299
33. S. Nicolay, and Y.-H. Sanejouand Functional modes of proteins are among the most robust Phys. Rev. Lett. 96 2006 4
34. F. Tama, and C.L. Brooks Symmetry, form, and shape: guiding principles for robustness in macromolecular machines Annu. Rev. Biophys. Biomol. Struct. 35 2006 115 133
35. J. Echave, and F.M. Fernndez A perturbative view of protein structural variation Proteins 78 2010 173 180
36. W. Zheng, B.R. Brooks, and D. Thirumalai Allosteric transitions in the chaperonin GroEL are captured by a dominant normal mode that is most robust to sequence variations Biophys. J. 93 2007 2289 2299
37. W. Zheng, B.R. Brooks, and D. Thirumalai Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations Proc. Natl. Acad. Sci. U. S. A. 103 2006 7664 7669
38. I. Bahar, A.R. Atilgan, and B. Erman Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential Fold. Des. 2 1997 173 181
39. K. Moritsugu, and J.C. Smith Coarse-grained biomolecular simulation with REACH: realistic extension algorithm via covariance Hessian Biophys. J. 93 2007 3460 3469
40. K. Moritsugu, V. Kurkal-Siebert, and J.C. Smith REACH coarse-grained normal mode analysis of protein dimer interaction dynamics Biophys. J. 97 2009 1158 1167
41. J.I. Jeong, Y. Jang, and M.K. Kim A connection rule for alpha-carbon coarse-grained elastic network models using chemical bond information J. Mol. Graph. Model. 24 2006 296 306
42. M.H. Kim, S. Seo, J.I. Jeong, B.J. Kim, W.K. Liu, B.S. Lim, J.B. Choi, and M.K. Kim A mass weighted chemical elastic network model elucidates closed form domain motions in proteins Protein Sci. 22 2013 605 613
43. Y. Dehouck, and A.S. Mikhailov Effective harmonic potentials: insights into the internal cooperativity and sequence-specificity of protein dynamics PLoS Comput. Biol. 9 2013 e1003209
44. C. Micheletti, P. Carloni, and A. Maritan Accurate and efficient description of protein vibrational dynamics: comparing molecular dynamics and Gaussian models Proteins 55 2004 635 645
45. R. Mendez, and U. Bastolla Torsional network model: normal modes in torsion angle space better correlate with conformation changes in proteins Phys. Rev. Lett. 104 2010 228103 228104
46. H. Wako, and S. Endo Ligand-induced conformational change of a protein reproduced by a linear combination of displacement vectors obtained from normal mode analysis Biophys. Chem. 159 2011 257 266
47. F. Tama, F.X. Gadea, O. Marques, and Y.H. Sanejouand Building-block approach for determining low-frequency normal modes of macromolecules Proteins 41 2000 1 7
48. K. Hinsen, and G.R. Kneller Solvent effects in the slow dynamics of proteins Proteins 70 2008 1235 1242
49. T. Ichiye, and M. Karplus Collective motions in proteins: a covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations Proteins 11 1991 205 217
50. K. Hinsen, and G.R. Kneller Projection methods for the analysis of complex motions in macromolecules Mol. Simul. 23 2000 275 292
51. N. Leioatts, T.D. Romo, and A. Grossfield Elastic network models are robust to variations in formalism J. Chem. Theory Comput. 8 2012 2424 2434
52. K. Hinsen, A.J. Petrescu, S. Dellerue, M.C. Bellissent-Funel, and G.R. Kneller Harmonicity in slow protein dynamics Chem. Phys. 261 2000 25 37
53. D. Riccardi, Q. Cui, and G.N. Phillips Jr. Evaluating elastic network models of crystalline biological molecules with temperature factors, correlated motions, and diffuse X-Ray scattering Biophys. J. 99 2010 2616 2625
54. K. Hinsen Structural flexibility in proteins: impact of the crystal environment Bioinformatics 24 2008 521 528
55. R. Soheilifard, D.E. Makarov, and G.J. Rodin Critical evaluation of simple network models of protein dynamics and their comparison with crystallographic B-factors Phys. Biol. 5 2008 026008
56. E. Fuglebakk, N. Reuter, and K. Hinsen Evaluation of protein elastic network models based on an analysis of collective motions J. Chem. Theory Comput. 9 2013 5618 5628
57. M.K. Kim, G.S. Chirikjian, and R.L. Jernigan Elastic models of conformational transitions in macromolecules J. Mol. Graph. Model. 21 2002 151 160
58. F. Tama, W. Wriggers, and C.L. Brooks 3rd. Exploring global distortions of biological macromolecules and assemblies from low-resolution structural information and elastic network theory J. Mol. Biol. 321 2002 297 305
59. D. Ming, Y. Kong, M.A. Lambert, Z. Huang, and J. Ma How to describe protein motion without amino acid sequence and atomic coordinates Proc. Natl. Acad. Sci. U. S. A. 99 2002 8620 8625
60. S. Kundu, J.S. Melton, D.C. Sorensen, and G.N. Phillips Jr. Dynamics of proteins in crystals: comparison of experiment with simple models Biophys. J. 83 2002 723 732
61. K. Moritsugu, and J.C. Smith REACH coarse-grained biomolecular simulation: transferability between different protein structural classes Biophys. J. 95 2008 1639 1648
62. M. Delarue, and Y.H. Sanejouand Simplified normal mode analysis of conformational transitions in DNA-dependent polymerases: the elastic network model J. Mol. Biol. 320 2002 1011 1024
63. H. Valadie, J.J. Lacapere, Y.H. Sanejouand, and C. Etchebest Dynamical properties of the MscL of Escherichia coli: a normal mode analysis J. Mol. Biol. 332 2003 657 674
64. F. Tama, M. Valle, J. Frank, and C.L. Brooks Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy Proc. Natl. Acad. Sci. U. S. A. 100 2003 9319 9323
65. N. Reuter, K. Hinsen, and J.-J. Lacapere Transconformations of the SERCA1 Ca-ATPase: a normal mode study Biophys. J. 85 2003 99020
66. E. Fuglebakk, J. Echave, and N. Reuter Measuring and comparing structural fluctuation patterns in large protein datasets Bioinformatics 28 2012 2431 2440
67. A. Amadei, M.A. Ceruso, and A. Di Nola On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins' molecular dynamics simulations Proteins 36 1999 419 424
68. B. Hess Convergence of sampling in protein simulations Phys. Rev. E. 65 2002 031910
69. V. Carnevale, F. Pontiggia, and C. Micheletti Structural and dynamical alignment of enzymes with partial structural similarity J. Phys. Condens. Matter 19 2007 285206 285214
70. C. Berbalk, C.S. Schwaiger, and P. Lackner Accuracy analysis of multiple structure alignments Protein Sci. 18 2009 2027 2035
71. H. Hasegawa, and L. Holm Advances and pitfalls of protein structural alignment Curr. Opin. Struct. Biol. 19 2009 341 348
72. M.A. Marti-Renom, I.N. Shindyalov, and P.E. Bourne J.B. Gu, P.E. 2nd ed. Struct. Bioinformatics 2009 John Wiley and Sons NJ 397 417
73. R.B. Russell, and G.J. Barton Multiple protein sequence alignment from tertiary structure comparison: assignment of global and residue confidence levels Proteins 14 1992 309 323
74. J. Ma, and S. Wang Algorithms, applications, and challenges of protein structure alignment Adv. Protein Chem. Struct. Biol. 94 2014 121 175
75. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
76. A.S. Konagurthu, J.C. Whisstock, P.J. Stuckey, and A.M. Lesk MUSTANG: a multiple structural alignment algorithm Proteins 64 2006 559 574
77. N. Nagano, C.A. Orengo, and J.M. Thornton One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions J. Mol. Biol. 321 2002 741 765
78. H.L. Woodcock, W. Zheng, A. Ghysels, Y. Shao, J. Kong, and B.R. Brooks Vibrational subsystem analysis: a method for probing free energies and correlations in the harmonic limit J. Chem. Phys. 129 2008 214109
79. J. Luo, and T.C. Bruice Envisioning the loop movements and rotation of the two subdomains of dihydrofolate reductase by elastic normal mode analysis J. Biomol. Struct. Dyn. 27 2009 245 258
80. W. Zheng, B.R. Brooks, S. Doniach, and D. Thirumalai Network of dynamically important residues in the open/closed transition in polymerases is strongly conserved Structure 13 2005 565 577
81. P. Maragakis, and M. Karplus Large amplitude conformational change in proteins explored with a plastic network model: adenylate kinase J. Mol. Biol. 352 2005 807 822
82. P.C. Whitford, J.N. Onuchic, and P.G. Wolynes Energy landscape along an enzymatic reaction trajectory: hinges or cracks? HFSP J. 2 2008 61 64
83. Y. Togashi, T. Yanagida, and A.S. Mikhailov Nonlinearity of mechanochemical motions in motor proteins PLoS Comput. Biol. 6 2010 e1000814
84. A. Stein, M. Rueda, A. Panjkovich, M. Orozco, and P. Aloy A systematic study of the energetics involved in structural changes upon association and connectivity in protein interaction networks Structure 19 2011 881 889
85. R. Tehver, J. Chen, and D. Thirumalai Allostery wiring diagrams in the transitions that drive the GroEL reaction cycle J. Mol. Biol. 387 2009 390 406
86. H.N. Motlagh, J.O. Wrabl, J. Li, and V.J. Hilser The ensemble nature of allostery Nature 508 2014 331 339
87. S. Mitternacht, and I.N. Berezovsky Coherent conformational degrees of freedom as a structural basis for allosteric communication PLoS Comput. Biol. 7 2011 e1002301
88. A.E. Garcia Large-amplitude nonlinear motions in proteins Phys. Rev. Lett. 68 1992 2696 2699
89. A. Bakan, and I. Bahar The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding Proc. Natl. Acad. Sci. U. S. A. 106 2009 14349 14354
90. A.R. Katebi, and R.L. Jernigan The critical role of the loops of triosephosphate isomerase for its oligomerization, dynamics, and functionality Protein Sci. 23 2014 213 228
91. A. Zen, C. Micheletti, O. Keskin, and R. Nussinov Comparing interfacial dynamics in protein-protein complexes: an elastic network approach BMC Struct. Biol. 10 2010 26
92. Z. Xu, R. Paparcone, and M.J. Buehler Alzheimer's abeta (1-40) amyloid fibrils feature size-dependent mechanical properties Biophys. J. 98 2010 2053 2062
93. G. Polles, G. Indelicato, R. Potestio, P. Cermelli, R. Twarock, and C. Micheletti Mechanical and assembly units of viral capsids identified via quasi-rigid domain decomposition PLoS Comput. Biol. 9 2013 e1003331
94. M.Y. Niv, and M. Filizola Influence of oligomerization on the dynamics of G-protein coupled receptors as assessed by normal mode analysis Proteins 71 2008 575 586
95. B.A. Hall, J.P. Armitage, and M.S. Sansom Mechanism of bacterial signal transduction revealed by molecular dynamics of Tsr dimers and trimers of dimers in lipid vesicles PLoS Comput. Biol. 8 2012 e1002685
96. N. Kantarci, P. Doruker, and T. Haliloglu Cooperative fluctuations point to the dimerization interface of p53 core domain Biophys. J. 91 2006 421 432
97. C. Chothia, and A.M. Lesk The relation between the divergence of sequence and structure in proteins EMBO J. 5 1986 823 826
98. S. Maguid, S. Fernández-Alberti, G. Parisi, and J. Echave Evolutionary conservation of protein backbone flexibility J. Mol. Evol. 63 2006 448 457
99. S. Maguid, S. Fernández-Alberti, and J. Echave Evolutionary conservation of protein vibrational dynamics Gene 422 2008 7 13
100. J. Echave Evolutionary divergence of protein structure: the linearly forced elastic network model Chem. Phys. Lett. 457 2008 413 416
101. J. Echave Why are the low-energy protein normal modes evolutionarily conserved? Protein Sci. 84 2012 1931 1937
102. V. Carnevale, S. Raugei, C. Micheletti, and P. Carloni Convergent dynamics in the protease enzymatic superfamily J. Am. Chem. Soc. 128 2006 9766 9772
103. C. Atilgan, and A.R. Atilgan Perturbation-response scanning reveals ligand entry-exit mechanisms of ferric binding protein PLoS Comput. Biol. 5 2009 e1000544
104. Z. Nevin Gerek, S. Kumar, and S. Banu Ozkan Structural dynamics flexibility informs function and evolution at a proteome scale Evol. Appl. 6 2013 423 433
105. N. Warren, A. Strom, B. Nicolet, K. Albin, J. Albrecht, B. Bausch, M. Dobbe, M. Dudek, S. Firgens, C. Fritsche, et al. Comparison of the intrinsic dynamics of aminoacyl-tRNA synthetases Protein J. 33 2014 184 198
106. M. Gerstein, and W. Krebs A database of macromolecular motions Nucleic Acids Res. 26 1998 4280 4290
107. M. Davis, and D. Tobi Multiple Gaussian network modes alignment reveals dynamically variable regions: the hemoglobin case Proteins 82 9 2014 2097 2105
108. D. Tobi Dynamics alignment: comparison of protein dynamics in the SCOP database Proteins 80 2012 1167 1176
109. A. Zen, V. Carnevale, A.M. Lesk, and C. Micheletti Correspondences between low-energy modes in enzymes: dynamics-based alignment of enzymatic functional families Protein Sci. 17 2008 918 929
110. S.M. Hollup, G. Salensminde, and N. Reuter WEBnm@: a web application for normal mode analyses of proteins BMC Bioinforma. 6 2005
111. A. Zen, C. de Chiara, A. Pastore, and C. Micheletti Using dynamics-based comparisons to predict nucleic acid binding sites in proteins: an application to OB-fold domains Bioinformatics 25 2009 1876 1883
112. G. Hu, S. Michielssens, S.L. Moors, and A. Ceulemans The harmonic analysis of cylindrically symmetric proteins: a comparison of Dronpa and a DNA sliding clamp J. Mol. Graph. Model. 34 2012 28 37
113. K. Hinsen The Molecular Modeling Toolkit: a new approach to molecular simulations J. Comput. Chem. 21 2000 79 85
114. A. Bakan, L.M. Meireles, and I. Bahar ProDy: protein dynamics inferred from theory and experiments Bioinformatics 27 2011 1575 1577
115. T.D. Romo, and A. Grossfield 31st Annual International Conference of the IEEE EMBS 2009 2332 2335
116. B.J. Grant, A.P.C. Rodrigues, K.M. ElSawy, J.A. McCammon, and L.S.D. Caves Bio3d: an R package for the comparative analysis of protein structures Bioinformatics 22 2006 2695 2696
117. T.L. Rodgers, D. Burnell, P.D. Townsend, E. Pohl, M.J. Cann, M.R. Wilson, and T.C. McLeish ΔΔPT: a comprehensive toolbox for the analysis of protein motion BMC Bioinforma. 14 2013 183
118. K. Suhre, and Y. Sanejouand ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement Nucleic Acids Res. 32 2004 610 614
119. E. Eyal, L.W. Yang, and I. Bahar Anisotropic network model: systematic evaluation and a new web interface Bioinformatics 22 2006 2619 2627
120. S. Seo, and M.K. Kim KOSMOS: a universal morph server for nucleic acids, proteins and their complexes Nucleic Acids Res. 40 2012 W531 W536
121. D.M. Kruger, A. Ahmed, and H. Gohlke NMSim web server: integrated approach for normal mode-based geometric simulations of biologically relevant conformational transitions in proteins Nucleic Acids Res. 40 2012 W310 W316
122. E. Lindahl, C. Azuara, P. Koehl, and M. Delarue NOMAD-Ref: visualization, deformation and refinement of macromolecular structures based on all-atom normal mode analysis Nucleic Acids Res. 34 2006 W52 W56
123. M.T. Zimmermann, A. Kloczkowski, and R.L. Jernigan MAVENs: motion analysis and visualization of elastic networks and structural ensembles BMC Bioinforma. 12 2011
124. A. Bakan, A. Dutta, W. Mao, Y. Liu, C. Chennubhotla, T.R. Lezon, and I. Bahar Evol and ProDy for bridging protein sequence evolution and structural dynamics Bioinformatics 30 18 2014 2681 2683
125. R. Potestio, T. Aleksiev, F. Pontiggia, S. Cozzini, and C. Micheletti ALADYN: a web server for aligning proteins by matching their large-scale motion Nucleic Acids Res. 38 2010 W41 W45
126. C. Toyoshima, H. Nomura, and T. Tsuda Lumenal gating mechanism revealed in calcium pump crystal structures with phosphate analogues Nature 432 2004 361 368
127. P. Gourdon, X.Y. Liu, T. Skjorringe, J.P. Morth, L.B. Moller, B.P. Pedersen, and P. Nissen Crystal structure of a copper-transporting PIB-type ATPase Nature 475 2011 59 64
128. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graph. 14 1996 33 38
129. K.R. Skowronek, F. Guo, Y. Zheng, and N. Nassar The C-terminal basic tail of RhoG assists the guanine nucleotide exchange factor trio in binding to phospholipids J. Biol. Chem. 279 2004 37895 37907