Mutations in DNA-binding loop of NFAT5 transcription factor produce unique outcomes on protein-DNA binding and dynamics

Journal of Physical Chemistry B

Volumn 117, Issue 42, 2013, Pages 13226-13234

  Li, Minghui ^a   Shoemaker, Benjamin A ^a   Thangudu, Ratna R ^a   Ferraris, Joan D ^b   Burg, Maurice B ^b   Panchenko, Anna R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEXATION; CYTOLOGY; PROTEINS; TRANSCRIPTION;

DIFFERENT MECHANISMS; DIMERIC COMPLEXES; NON-SPECIFIC BINDING; NUCLEAR FACTOR OF ACTIVATED T-CELLS; NUCLEAR TRANSLOCATIONS; PROTEIN DYNAMICS; PROTEIN-DNA BINDING; TRANSCRIPTIONAL ACTIVATORS;

DNA;

DNA; NFAT5 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CHEMISTRY; COMPUTER PROGRAM; GENETICS; HUMAN; METABOLISM; MOLECULAR DYNAMICS; MUTATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

BINDING SITES; DNA; HUMANS; MOLECULAR DYNAMICS SIMULATION; MUTATION; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SOFTWARE; TRANSCRIPTION FACTORS;

EID: 84885180170     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp403310a     Document Type: Article

References (40)

1. Burg, M. B.; Ferraris, J. D.; Dmitrieva, N. I. Cellular Response to Hyperosmotic Stresses Physiol. Rev. 2007, 87, 1441-1474
2. Chen, M.; Sinha, M.; Luxon, B. A.; Bresnick, A. R.; O'Connor, K. L. Integrin Alpha6beta4 Controls the Expression of Genes Associated with Cell Motility, Invasion, and Metastasis, Including S100a4/Metastasin J. Biol. Chem. 2009, 284, 1484-1494
3. Halterman, J. A.; Kwon, H. M.; Zargham, R.; Bortz, P. D.; Wamhoff, B. R. Nuclear Factor of Activated T Cells 5 Regulates Vascular Smooth Muscle Cell Phenotypic Modulation Arterioscler., Thromb., Vasc. Biol. 2011, 31, 2287-2296
4. Lopez-Rodriguez, C.; Aramburu, J.; Jin, L.; Rakeman, A. S.; Michino, M.; Rao, A. Bridging the Nfat and Nf-Kappab Families: Nfat5 Dimerization Regulates Cytokine Gene Transcription in Response to Osmotic Stress Immunity 2001, 15, 47-58
5. Stroud, J. C.; Lopez-Rodriguez, C.; Rao, A.; Chen, L. Structure of a Tonebp-DNA Complex Reveals DNA Encircled by a Transcription Factor Nat. Struct. Biol. 2002, 9, 90-94
6. Marchler-Bauer, A.; Lu, S.; Anderson, J. B.; Chitsaz, F.; Derbyshire, M. K.; DeWeese-Scott, C.; Fong, J. H.; Geer, L. Y.; Geer, R. C.; Gonzales, N. R. Cdd: A Conserved Domain Database for the Functional Annotation of Proteins Nucleic Acids Res. 2011, 39, D225-229
7. Tong, E. H.; Guo, J. J.; Huang, A. L.; Liu, H.; Hu, C. D.; Chung, S. S.; Ko, B. C. Regulation of Nucleocytoplasmic Trafficking of Transcription Factor Orebp/Tonebp/Nfat5 J. Biol. Chem. 2006, 281, 23870-23879
8. Izumi, Y.; Li, J.; Villers, C.; Hashimoto, K.; Burg, M. B.; Ferraris, J. D. Mutations That Reduce Its Specific DNA Binding Inhibit High Nacl-Induced Nuclear Localization of the Osmoprotective Transcription Factor Nfat5 Am. J. Physiol.: Cell Physiol. 2012, 303, C1061-1069
9. Humphrey, W.; Dalke, A.; Schulten, K. Vmd: Visual Molecular Dynamics J. Mol. Graphics 1996, 14 (33-38) 27-38
10. Bertonati, C.; Honig, B.; Alexov, E. Poisson-Boltzmann Calculations of Nonspecific Salt Effects on Protein-Protein Binding Free Energies Biophys. J. 2007, 92, 1891-1899
11. Martyna, G. J.; Hughes, A.; Tuckerman, M. E. Molecular Dynamics Algorithms for Path Integrals at Constant Pressure J. Chem. Phys. 1999, 110, 3275-3291
12. Deserno, M.; Holm, C. How to Mesh up Ewald Sums. I. A Theoretical and Numerical Comparison of Various Particle Mesh Routines J. Chem. Phys. 1998, 109, 7678-7694
13. Hoover, W. G. Canonical Dynamics: Equilibrium Phase-Space Distributions Phys. Rev. A 1985, 31, 1695-1697
14. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. Scalable Molecular Dynamics with Namd J. Comput. Chem. 2005, 26, 1781-1802
15. MacKerrell, A. D. J.; Bashford, D.; Dunbrack, R. L. J.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D. All-Atom Empirical Potential for Molecular Modeling and Dynamics Studies of Proteins J. Phys. Chem. B 1998, 102, 3586-3616
16. Foloppe, N.; MacKerell, A. D. J. All-Atom Empirical Force Field for Nucleic Acids: I. Parameter Optimization Based on Small Molecule and Condensed Phase Macromolecular Target Data J. Comput. Chem. 2000, 21, 86-104
17. Amadei, A.; Linssen, A. B.; Berendsen, H. J. Essential Dynamics of Proteins Proteins 1993, 17, 412-425
18. Li, M. H.; Luo, Q.; Li, Z. S. Molecular Dynamics Study on the Interactions of Porphyrin with Two Antiparallel Human Telomeric Quadruplexes J. Phys. Chem. B 2010, 114, 6216-6224
19. Russell, S. T.; Warshel, A. Calculations of Electrostatic Energies in Proteins. The Energetics of Ionized Groups in Bovine Pancreatic Trypsin Inhibitor J. Mol. Biol. 1985, 185, 389-404
20. Jo, S.; Vargyas, M.; Vasko-Szedlar, J.; Roux, B.; Im, W. Pbeq-Solver for Online Visualization of Electrostatic Potential of Biomolecules Nucleic Acids Res. 2008, 36, W270-275
21. Massova, I.; P.A., K. Combined Molecular Mechanical and Continuum Solvent Approach (Mm-Pbsa/Gbsa) to Predict Ligand Binding Perspect. Drug Discovery Des. 2000, 18, 113-135
22. Spassov, V. Z.; Yan, L. Ph-Selective Mutagenesis of Protein-Protein Interfaces: In Silico Design of Therapeutic Antibodies with Prolonged Half-Life Proteins 2013, 81, 704-714
23. Olson, M. A.; Reinke, L. T. Modeling Implicit Reorganization in Continuum Descriptions of Protein-Protein Interactions Proteins 2000, 38, 115-119
24. Li, M.; Zheng, W. Probing the Structural and Energetic Basis of Kinesin-Microtubule Binding Using Computational Alanine-Scanning Mutagenesis Biochemistry 2011, 50, 8645-8655
25. Nina, M.; Beglov, D.; Roux, B. Atomic Radii for Continuum Electrostatics Calculations Based on Molecular Dynamics Free Energy Simulations J. Phys. Chem. B 1997, 101, 5239-5248
26. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. Charmm: A Program for Macromolecular Energy, Minimization, and Dynamics Calculations J. Comput. Chem. 1983, 4, 187-217
27. Guerois, R.; Nielsen, J. E.; Serrano, L. Predicting Changes in the Stability of Proteins and Protein Complexes: A Study of More Than 1000 Mutations J. Mol. Biol. 2002, 320, 369-387
28. Shoemaker, B. A.; Zhang, D.; Tyagi, M.; Thangudu, R. R.; Fong, J. H.; Marchler-Bauer, A.; Bryant, S. H.; Madej, T.; Panchenko, A. R. Ibis (Inferred Biomolecular Interaction Server) Reports, Predicts and Integrates Multiple Types of Conserved Interactions for Proteins Nucleic Acids Res. 2012, 40, D834-840
29. Obenauer, J. C.; Cantley, L. C.; Yaffe, M. B. Scansite 2.0: Proteome-Wide Prediction of Cell Signaling Interactions Using Short Sequence Motifs Nucleic Acids Res. 2003, 31, 3635-3641
30. Wong, Y. H.; Lee, T. Y.; Liang, H. K.; Huang, C. M.; Wang, T. Y.; Yang, Y. H.; Chu, C. H.; Huang, H. D.; Ko, M. T.; Hwang, J. K. Kinasephos 2.0: A Web Server for Identifying Protein Kinase-Specific Phosphorylation Sites Based on Sequences and Coupling Patterns Nucleic Acids Res. 2007, 35, W588-594
31. Xue, Y.; Liu, Z.; Cao, J.; Ma, Q.; Gao, X.; Wang, Q.; Jin, C.; Zhou, Y.; Wen, L.; Ren, J. Gps 2.1: Enhanced Prediction of Kinase-Specific Phosphorylation Sites with an Algorithm of Motif Length Selection Protein Eng., Des. Sel. 2011, 24, 255-260
32. Iakoucheva, L. M.; Radivojac, P.; Brown, C. J.; O'Connor, T. R.; Sikes, J. G.; Obradovic, Z.; Dunker, A. K. The Importance of Intrinsic Disorder for Protein Phosphorylation Nucleic Acids Res. 2004, 32, 1037-1049
33. Rohs, R.; West, S. M.; Sosinsky, A.; Liu, P.; Mann, R. S.; Honig, B. The Role of DNA Shape in Protein-DNA Recognition Nature 2009, 461, 1248-1253
34. Chirgadze, Y. N.; Sivozhelezov, V. S.; Polozov, R. V.; Stepanenko, V. A.; Ivanov, V. V. Recognition Rules for Binding of Homeodomains to Operator DNA J. Biomol. Struct. Dyn. 2012, 29, 715-731
35. Kalodimos, C. G.; Biris, N.; Bonvin, A. M.; Levandoski, M. M.; Guennuegues, M.; Boelens, R.; Kaptein, R. Structure and Flexibility Adaptation in Nonspecific and Specific Protein-DNA Complexes Science 2004, 305, 386-389
36. Bryngelson, J. D.; Onuchic, J. N.; Socci, N. D.; Wolynes, P. G. Funnels, Pathways, and the Energy Landscape of Protein Folding: A Synthesis Proteins 1995, 21, 167-195
37. Levy, Y.; Onuchic, J. N.; Wolynes, P. G. Fly-Casting in Protein-DNA Binding: Frustration between Protein Folding and Electrostatics Facilitates Target Recognition J. Am. Chem. Soc. 2007, 129, 738-739
38. Shoemaker, B. A.; Portman, J. J.; Wolynes, P. G. Speeding Molecular Recognition by Using the Folding Funnel: The Fly-Casting Mechanism Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 8868-8873
39. Shen, T.; Zong, C.; Hamelberg, D.; McCammon, J. A.; Wolynes, P. G. The Folding Energy Landscape and Phosphorylation: Modeling the Conformational Switch of the Nfat Regulatory Domain FASEB J. 2005, 19, 1389-1395
40. Kwon, M. S.; Lee, S. D.; Kim, J. A.; Colla, E.; Choi, Y. J.; Suh, P. G.; Kwon, H. M. Novel Nuclear Localization Signal Regulated by Ambient Tonicity in Vertebrates J. Biol. Chem. 2008, 283, 22400-22409