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Structural analysis of WW domains and design of a WW prototype.

Macias MJ, Gervais V, Civera C, Oschkinat H
Nat Struct Biol 7 375-9 (2000)
Related entries: 1e0l, 1e0n

Cited: 144 times
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Abstract

Two new NMR structures of WW domains, the mouse formin binding protein and a putative 84.5 kDa protein from Saccharomyces cerevisiae, show that this domain, only 35 amino acids in length, defines the smallest monomeric triple-stranded antiparallel beta-sheet protein domain that is stable in the absence of disulfide bonds, tightly bound ions or ligands. The structural roles of conserved residues have been studied using site-directed mutagenesis of both wild type domains. Crucial interactions responsible for the stability of the WW structure have been identified. Based on a network of highly conserved long range interactions across the beta-sheet structure that supports the WW fold and on a systematic analysis of conserved residues in the WW family, we have designed a folded prototype WW sequence.

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  1. The OPEP protein model: from single molecules, amyloid formation, crowding and hydrodynamics to DNA/RNA systems. Sterpone F, Melchionna S, Tuffery P, Pasquali S, Mousseau N, Cragnolini T, Chebaro Y, St-Pierre JF, Kalimeri M, Barducci A, Laurin Y, Tek A, Baaden M, Nguyen PH, Derreumaux P. Chem Soc Rev 43 4871-4893 (2014)
  2. General lack of structural characterization of chemically synthesized long peptides. Boutin JA, Tartar AL, van Dorsselaer A, Vaudry H. Protein Sci 28 857-867 (2019)

Articles - 1e0m mentioned but not cited (5)

  1. Factors involved in the stability of isolated beta-sheets: Turn sequence, beta-sheet twisting, and hydrophobic surface burial. Santiveri CM, Santoro J, Rico M, Jiménez MA. Protein Sci. 13 1134-1147 (2004)
  2. Crystal structure of Streptococcus pyogenes EndoS, an immunomodulatory endoglycosidase specific for human IgG antibodies. Trastoy B, Lomino JV, Pierce BG, Carter LG, Günther S, Giddens JP, Snyder GA, Weiss TM, Weng Z, Wang LX, Sundberg EJ. Proc. Natl. Acad. Sci. U.S.A. 111 6714-6719 (2014)
  3. MALISAM: a database of structurally analogous motifs in proteins. Cheng H, Kim BH, Grishin NV. Nucleic Acids Res. 36 D211-7 (2008)
  4. Constraint Logic Programming approach to protein structure prediction. Dal Palù A, Dovier A, Fogolari F. BMC Bioinformatics 5 186 (2004)
  5. Learning protein constitutive motifs from sequence data. Tubiana J, Cocco S, Monasson R. Elife 8 (2019)


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  1. The ankyrin repeat as molecular architecture for protein recognition. Mosavi LK, Cammett TJ, Desrosiers DC, Peng ZY. Protein Sci. 13 1435-1448 (2004)
  2. WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. Macias MJ, Wiesner S, Sudol M. FEBS Lett. 513 30-37 (2002)
  3. Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Reinhardt HC, Yaffe MB. Nat. Rev. Mol. Cell Biol. 14 563-580 (2013)
  4. The WW domain: linking cell signalling to the membrane cytoskeleton. Ilsley JL, Sudol M, Winder SJ. Cell. Signal. 14 183-189 (2002)
  5. Adaptable hydrogel networks with reversible linkages for tissue engineering. Wang H, Heilshorn SC. Adv. Mater. Weinheim 27 3717-3736 (2015)
  6. Smart self-assembled hybrid hydrogel biomaterials. Kopeček J, Yang J. Angew. Chem. Int. Ed. Engl. 51 7396-7417 (2012)
  7. The use of in vitro peptide-library screens in the analysis of phosphoserine/threonine-binding domain structure and function. Yaffe MB, Smerdon SJ. Annu Rev Biophys Biomol Struct 33 225-244 (2004)
  8. Consensus design of repeat proteins. Forrer P, Binz HK, Stumpp MT, Plückthun A. Chembiochem 5 183-189 (2004)
  9. Knowledge-based potential functions in protein design. Russ WP, Ranganathan R. Curr. Opin. Struct. Biol. 12 447-452 (2002)
  10. Combining experiment and simulation in protein folding: closing the gap for small model systems. Schaeffer RD, Fersht A, Daggett V. Curr. Opin. Struct. Biol. 18 4-9 (2008)
  11. Interactions between proteins and carbon-based nanoparticles: exploring the origin of nanotoxicity at the molecular level. Zuo G, Kang SG, Xiu P, Zhao Y, Zhou R. Small 9 1546-1556 (2013)
  12. Solid-state NMR spectroscopy of amyloid proteins. Heise H. Chembiochem 9 179-189 (2008)
  13. Designing ECM-mimetic materials using protein engineering. Cai L, Heilshorn SC. Acta Biomater 10 1751-1760 (2014)
  14. The depsipeptide method for solid-phase synthesis of difficult peptides. Coin I. J Pept Sci 16 223-230 (2010)
  15. Consensus protein design. Porebski BT, Buckle AM. Protein Eng. Des. Sel. 29 245-251 (2016)
  16. Protein folds and protein folding. Schaeffer RD, Daggett V. Protein Eng. Des. Sel. 24 11-19 (2011)
  17. Recombinant proteins as cross-linkers for hydrogelations. Wang H, Shi Y, Wang L, Yang Z. Chem Soc Rev 42 891-901 (2013)
  18. Tombusvirus-yeast interactions identify conserved cell-intrinsic viral restriction factors. Sasvari Z, Alatriste Gonzalez P, Nagy PD. Front Plant Sci 5 383 (2014)
  19. Hydrogels Constructed from Engineered Proteins. Li H, Kong N, Laver B, Liu J. Small 12 973-987 (2016)
  20. Multicomponent self-assembly as a tool to harness new properties from peptides and proteins in material design. Okesola BO, Mata A. Chem Soc Rev 47 3721-3736 (2018)
  21. Ready, SET, Go: Post-translational regulation of the histone lysine methylation network in budding yeast. Separovich RJ, Wilkins MR. J Biol Chem 297 100939 (2021)
  22. SMURF1, a promoter of tumor cell progression? Xia Q, Li Y, Han D, Dong L. Cancer Gene Ther 28 551-565 (2021)
  23. Protein-Based Hydrogels and Their Biomedical Applications. Lee KZ, Jeon J, Jiang B, Subramani SV, Li J, Zhang F. Molecules 28 4988 (2023)

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  1. The folding mechanism of a beta-sheet: the WW domain. Jäger M, Nguyen H, Crane JC, Kelly JW, Gruebele M. J. Mol. Biol. 311 373-393 (2001)
  2. Consensus-derived structural determinants of the ankyrin repeat motif. Mosavi LK, Minor DL, Peng ZY. Proc. Natl. Acad. Sci. U.S.A. 99 16029-16034 (2002)
  3. Solid-phase peptide synthesis: from standard procedures to the synthesis of difficult sequences. Coin I, Beyermann M, Bienert M. Nat Protoc 2 3247-3256 (2007)
  4. Design of stable alpha-helical arrays from an idealized TPR motif. Main ER, Xiong Y, Cocco MJ, D'Andrea L, Regan L. Structure 11 497-508 (2003)
  5. Ab initio simulations of protein-folding pathways by molecular dynamics with the united-residue model of polypeptide chains. Liwo A, Khalili M, Scheraga HA. Proc. Natl. Acad. Sci. U.S.A. 102 2362-2367 (2005)
  6. Structure-function-folding relationship in a WW domain. Jäger M, Zhang Y, Bieschke J, Nguyen H, Dendle M, Bowman ME, Noel JP, Gruebele M, Kelly JW. Proc. Natl. Acad. Sci. U.S.A. 103 10648-10653 (2006)
  7. Principal component analysis for protein folding dynamics. Maisuradze GG, Liwo A, Scheraga HA. J. Mol. Biol. 385 312-329 (2009)
  8. General structural motifs of amyloid protofilaments. Ferguson N, Becker J, Tidow H, Tremmel S, Sharpe TD, Krause G, Flinders J, Petrovich M, Berriman J, Oschkinat H, Fersht AR. Proc. Natl. Acad. Sci. U.S.A. 103 16248-16253 (2006)
  9. Modification and optimization of the united-residue (UNRES) potential energy function for canonical simulations. I. Temperature dependence of the effective energy function and tests of the optimization method with single training proteins. Liwo A, Khalili M, Czaplewski C, Kalinowski S, Ołdziej S, Wachucik K, Scheraga HA. J Phys Chem B 111 260-285 (2007)
  10. The transcription elongation factor CA150 interacts with RNA polymerase II and the pre-mRNA splicing factor SF1. Goldstrohm AC, Albrecht TR, Suñé C, Bedford MT, Garcia-Blanco MA. Mol. Cell. Biol. 21 7617-7628 (2001)
  11. Tuning the free-energy landscape of a WW domain by temperature, mutation, and truncation. Nguyen H, Jager M, Moretto A, Gruebele M, Kelly JW. Proc. Natl. Acad. Sci. U.S.A. 100 3948-3953 (2003)
  12. Two-component protein-engineered physical hydrogels for cell encapsulation. Wong Po Foo CT, Lee JS, Mulyasasmita W, Parisi-Amon A, Heilshorn SC. Proc. Natl. Acad. Sci. U.S.A. 106 22067-22072 (2009)
  13. Domains of the Rsp5 ubiquitin-protein ligase required for receptor-mediated and fluid-phase endocytosis. Dunn R, Hicke L. Mol. Biol. Cell 12 421-435 (2001)
  14. WW domain sequence activity relationships identified using ligand recognition propensities of 42 WW domains. Otte L, Wiedemann U, Schlegel B, Pires JR, Beyermann M, Schmieder P, Krause G, Volkmer-Engert R, Schneider-Mergener J, Oschkinat H. Protein Sci. 12 491-500 (2003)
  15. A coarse-grained protein force field for folding and structure prediction. Maupetit J, Tuffery P, Derreumaux P. Proteins 69 394-408 (2007)
  16. Ultrafast folding of WW domains without structured aromatic clusters in the denatured state. Ferguson N, Johnson CM, Macias M, Oschkinat H, Fersht A. Proc. Natl. Acad. Sci. U.S.A. 98 13002-13007 (2001)
  17. Phi-analysis at the experimental limits: mechanism of beta-hairpin formation. Petrovich M, Jonsson AL, Ferguson N, Daggett V, Fersht AR. J. Mol. Biol. 360 865-881 (2006)
  18. Characterizing Class I WW domains defines key specificity determinants and generates mutant domains with novel specificities. Kasanov J, Pirozzi G, Uveges AJ, Kay BK. Chem. Biol. 8 231-241 (2001)
  19. Using flexible loop mimetics to extend phi-value analysis to secondary structure interactions. Ferguson N, Pires JR, Toepert F, Johnson CM, Pan YP, Volkmer-Engert R, Schneider-Mergener J, Daggett V, Oschkinat H, Fersht A. Proc. Natl. Acad. Sci. U.S.A. 98 13008-13013 (2001)
  20. Demonstration of long-range interactions in a PDZ domain by NMR, kinetics, and protein engineering. Gianni S, Walma T, Arcovito A, Calosci N, Bellelli A, Engström A, Travaglini-Allocatelli C, Brunori M, Jemth P, Vuister GW. Structure 14 1801-1809 (2006)
  21. Solution structure and ligand recognition of the WW domain pair of the yeast splicing factor Prp40. Wiesner S, Stier G, Sattler M, Macias MJ. J. Mol. Biol. 324 807-822 (2002)
  22. Relation between free energy landscapes of proteins and dynamics. Maisuradze GG, Liwo A, Scheraga HA. J Chem Theory Comput 6 583-595 (2010)
  23. Multifunctional materials through modular protein engineering. DiMarco RL, Heilshorn SC. Adv. Mater. Weinheim 24 3923-3940 (2012)
  24. Rapid amyloid fiber formation from the fast-folding WW domain FBP28. Ferguson N, Berriman J, Petrovich M, Sharpe TD, Finch JT, Fersht AR. Proc. Natl. Acad. Sci. U.S.A. 100 9814-9819 (2003)
  25. Integrating folding kinetics and protein function: biphasic kinetics and dual binding specificity in a WW domain. Karanicolas J, Brooks CL. Proc. Natl. Acad. Sci. U.S.A. 101 3432-3437 (2004)
  26. Investigation of protein folding by coarse-grained molecular dynamics with the UNRES force field. Maisuradze GG, Senet P, Czaplewski C, Liwo A, Scheraga HA. J Phys Chem A 114 4471-4485 (2010)
  27. NMR solution structure of the isolated Apo Pin1 WW domain: comparison to the x-ray crystal structures of Pin1. Kowalski JA, Liu K, Kelly JW. Biopolymers 63 111-121 (2002)
  28. The tumour suppressor gene WWOX is mutated in autosomal recessive cerebellar ataxia with epilepsy and mental retardation. Mallaret M, Synofzik M, Lee J, Sagum CA, Mahajnah M, Sharkia R, Drouot N, Renaud M, Klein FA, Anheim M, Tranchant C, Mignot C, Mandel JL, Bedford M, Bauer P, Salih MA, Schüle R, Schöls L, Aldaz CM, Koenig M. Brain 137 411-419 (2014)
  29. Exploring the parameter space of the coarse-grained UNRES force field by random search: selecting a transferable medium-resolution force field. He Y, Xiao Y, Liwo A, Scheraga HA. J Comput Chem 30 2127-2135 (2009)
  30. SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Fleissner A, Glass NL. Eukaryotic Cell 6 84-94 (2007)
  31. Implicit solvent models for flexible protein-protein docking by molecular dynamics simulation. Wang T, Wade RC. Proteins 50 158-169 (2003)
  32. Y65C missense mutation in the WW domain of the Golabi-Ito-Hall syndrome protein PQBP1 affects its binding activity and deregulates pre-mRNA splicing. Tapia VE, Nicolaescu E, McDonald CB, Musi V, Oka T, Inayoshi Y, Satteson AC, Mazack V, Humbert J, Gaffney CJ, Beullens M, Schwartz CE, Landgraf C, Volkmer R, Pastore A, Farooq A, Bollen M, Sudol M. J. Biol. Chem. 285 19391-19401 (2010)
  33. A de novo redesign of the WW domain. Kraemer-Pecore CM, Lecomte JT, Desjarlais JR. Protein Sci. 12 2194-2205 (2003)
  34. Increasing protein stability using a rational approach combining sequence homology and structural alignment: Stabilizing the WW domain. Jiang X, Kowalski J, Kelly JW. Protein Sci. 10 1454-1465 (2001)
  35. How adequate are one- and two-dimensional free energy landscapes for protein folding dynamics? Maisuradze GG, Liwo A, Scheraga HA. Phys. Rev. Lett. 102 238102 (2009)
  36. Sequence determinants of thermodynamic stability in a WW domain--an all-beta-sheet protein. Jäger M, Dendle M, Kelly JW. Protein Sci. 18 1806-1813 (2009)
  37. The role of the turn in beta-hairpin formation during WW domain folding. Sharpe T, Jonsson AL, Rutherford TJ, Daggett V, Fersht AR. Protein Sci. 16 2233-2239 (2007)
  38. Evolution of binding affinity in a WW domain probed by phage display. Dalby PA, Hoess RH, DeGrado WF. Protein Sci. 9 2366-2376 (2000)
  39. Folding, misfolding, and amyloid protofibril formation of WW domain FBP28. Mu Y, Nordenskiöld L, Tam JP. Biophys. J. 90 3983-3992 (2006)
  40. Structure of the dimeric exonuclease TREX1 in complex with DNA displays a proline-rich binding site for WW Domains. Brucet M, Querol-Audí J, Serra M, Ramirez-Espain X, Bertlik K, Ruiz L, Lloberas J, Macias MJ, Fita I, Celada A. J Biol Chem 282 14547-14557 (2007)
  41. Replica Exchange and Multicanonical Algorithms with the coarse-grained UNRES force field. Nanias M, Czaplewski C, Scheraga HA. J Chem Theory Comput 2 513-528 (2006)
  42. NMR structures of 36 and 73-residue fragments of the calreticulin P-domain. Ellgaard L, Bettendorff P, Braun D, Herrmann T, Fiorito F, Jelesarov I, Güntert P, Helenius A, Wüthrich K. J. Mol. Biol. 322 773-784 (2002)
  43. Solution structure of an atypical WW domain in a novel beta-clam-like dimeric form. Ohnishi S, Güntert P, Koshiba S, Tomizawa T, Akasaka R, Tochio N, Sato M, Inoue M, Harada T, Watanabe S, Tanaka A, Shirouzu M, Kigawa T, Yokoyama S. FEBS Lett. 581 462-468 (2007)
  44. Synthesis of an Array Comprising 837 Variants of the hYAP WW Protein Domain This work was supported by the DFG (INK 16/B1-1), by the Fonds der Chemischen Industrie, and by the Universitätsklinikum Charité Berlin. Toepert F, Pires JR, Landgraf C, Oschkinat H, Schneider-Mergener J. Angew. Chem. Int. Ed. Engl. 40 897-900 (2001)
  45. A single WW domain is the predominant mediator of the interaction between the human ubiquitin-protein ligase Nedd4 and the human epithelial sodium channel. Lott JS, Coddington-Lawson SJ, Teesdale-Spittle PH, McDonald FJ. Biochem. J. 361 481-488 (2002)
  46. Computer simulations aimed at structure prediction of supersecondary motifs in proteins. Forcellino F, Derreumaux P. Proteins 45 159-166 (2001)
  47. Structure and function of the two tandem WW domains of the pre-mRNA splicing factor FBP21 (formin-binding protein 21). Huang X, Beullens M, Zhang J, Zhou Y, Nicolaescu E, Lesage B, Hu Q, Wu J, Bollen M, Shi Y. J. Biol. Chem. 284 25375-25387 (2009)
  48. Folding, stability, and secondary structure of a new dimeric cysteine proteinase inhibitor. Kidric M, Fabian H, Brzin J, Popovic T, Pain RH. Biochem. Biophys. Res. Commun. 297 962-967 (2002)
  49. Determination of side-chain-rotamer and side-chain and backbone virtual-bond-stretching potentials of mean force from AM1 energy surfaces of terminally-blocked amino-acid residues, for coarse-grained simulations of protein structure and folding. II. Results, comparison with statistical potentials, and implementation in the UNRES force field. Kozłowska U, Maisuradze GG, Liwo A, Scheraga HA. J Comput Chem 31 1154-1167 (2010)
  50. Influence of hPin1 WW N-terminal domain boundaries on function, protein stability, and folding. Jäger M, Nguyen H, Dendle M, Gruebele M, Kelly JW. Protein Sci. 16 1495-1501 (2007)
  51. Physics-based potentials for the coupling between backbone- and side-chain-local conformational states in the UNited RESidue (UNRES) force field for protein simulations. Sieradzan AK, Krupa P, Scheraga HA, Liwo A, Czaplewski C. J Chem Theory Comput 11 817-831 (2015)
  52. Structural basis for APPTPPPLPP peptide recognition by the FBP11WW1 domain. Pires JR, Parthier C, Aido-Machado Rd, Wiedemann U, Otte L, Böhm G, Rudolph R, Oschkinat H. J. Mol. Biol. 348 399-408 (2005)
  53. Temperature-dependent folding pathways of Pin1 WW domain: an all-atom molecular dynamics simulation of a Gō model. Luo Z, Ding J, Zhou Y. Biophys. J. 93 2152-2161 (2007)
  54. Engineering of beta-propeller protein scaffolds by multiple gene duplication and fusion of an idealized WD repeat. Nikkhah M, Jawad-Alami Z, Demydchuk M, Ribbons D, Paoli M. Biomol. Eng. 23 185-194 (2006)
  55. Identification of the PXW sequence as a structural gatekeeper of the headpiece C-terminal subdomain fold. Vermeulen W, Van Troys M, Bourry D, Dewitte D, Rossenu S, Goethals M, Borremans FA, Vandekerckhove J, Martins JC, Ampe C. J. Mol. Biol. 359 1277-1292 (2006)
  56. Protein structure prediction with the UNRES force-field using Replica-Exchange Monte Carlo-with-Minimization; Comparison with MCM, CSA, and CFMC. Nanias M, Chinchio M, Ołdziej S, Czaplewski C, Scheraga HA. J Comput Chem 26 1472-1486 (2005)
  57. Structure and dynamics of human Nedd4-1 WW3 in complex with the αENaC PY motif. Bobby R, Medini K, Neudecker P, Lee TV, Brimble MA, McDonald FJ, Lott JS, Dingley AJ. Biochim. Biophys. Acta 1834 1632-1641 (2013)
  58. Design and NMR conformational study of a beta-sheet peptide based on Betanova and WW domains. Fernández-Escamilla AM, Ventura S, Serrano L, Jiménez MA. Protein Sci. 15 2278-2289 (2006)
  59. WW domain folding complexity revealed by infrared spectroscopy. Davis CM, Dyer RB. Biochemistry 53 5476-5484 (2014)
  60. An inhibitory function of WW domain-containing host proteins in RNA virus replication. Qin J, Barajas D, Nagy PD. Virology 426 106-119 (2012)
  61. Extension of UNRES force field to treat polypeptide chains with D-amino-acid residues. Sieradzan AK, Hansmann UH, Scheraga HA, Liwo A. J Chem Theory Comput 8 4746-4757 (2012)
  62. Probing the ligand-binding specificity and analyzing the folding state of SPOT-synthesized FBP28 WW domain variants. Przezdziak J, Tremmel S, Kretzschmar I, Beyermann M, Bienert M, Volkmer-Engert R. Chembiochem 7 780-788 (2006)
  63. Transition states in protein folding kinetics: modeling phi-values of small beta-sheet proteins. Weikl TR. Biophys. J. 94 929-937 (2008)
  64. 13C-labeled tyrosine residues as local IR probes for monitoring conformational changes in peptides and proteins. Tremmel S, Beyermann M, Oschkinat H, Bienert M, Naumann D, Fabian H. Angew. Chem. Int. Ed. Engl. 44 4631-4635 (2005)
  65. Ionic self-complementarity induces amyloid-like fibril formation in an isolated domain of a plant copper metallochaperone protein. Mira H, Vilar M, Esteve V, Martinell M, Kogan MJ, Giralt E, Salom D, Mingarro I, Peñarrubia L, Pérez-Payá E. BMC Struct. Biol. 4 7 (2004)
  66. Binding of external ligands onto an engineered virus capsid. Schmidt U, Rudolph R, Böhm G. Protein Eng. 14 769-774 (2001)
  67. Effects of mutation, truncation, and temperature on the folding kinetics of a WW domain. Maisuradze GG, Zhou R, Liwo A, Xiao Y, Scheraga HA. J. Mol. Biol. 420 350-365 (2012)
  68. Folding kinetics of WW domains with the united residue force field for bridging microscopic motions and experimental measurements. Zhou R, Maisuradze GG, Suñol D, Todorovski T, Macias MJ, Xiao Y, Scheraga HA, Czaplewski C, Liwo A. Proc. Natl. Acad. Sci. U.S.A. 111 18243-18248 (2014)
  69. Improvement of the treatment of loop structures in the UNRES force field by inclusion of coupling between backbone- and side-chain-local conformational states. Krupa P, Sieradzan AK, Rackovsky S, Baranowski M, Ołldziej S, Scheraga HA, Liwo A, Czaplewski C. J Chem Theory Comput 9 (2013)
  70. Dynamics of an ultrafast folding subdomain in the context of a larger protein fold. Davis CM, Dyer RB. J. Am. Chem. Soc. 135 19260-19267 (2013)
  71. Comment Folding by consensus. Tripp KW, Barrick D. Structure 11 486-487 (2003)
  72. Local vs global motions in protein folding. Maisuradze GG, Liwo A, Senet P, Scheraga HA. J Chem Theory Comput 9 2907-2921 (2013)
  73. Native atomic burials, supplemented by physically motivated hydrogen bond constraints, contain sufficient information to determine the tertiary structure of small globular proteins. Pereira de Araújo AF, Gomes AL, Bursztyn AA, Shakhnovich EI. Proteins 70 971-983 (2008)
  74. Solution structure and binding specificity of FBP11/HYPA WW domain as Group-II/III. Kato Y, Hino Y, Nagata K, Tanokura M. Proteins 63 227-234 (2006)
  75. Structural characterization of a new binding motif and a novel binding mode in group 2 WW domains. Ramirez-Espain X, Ruiz L, Martin-Malpartida P, Oschkinat H, Macias MJ. J. Mol. Biol. 373 1255-1268 (2007)
  76. The ensemble folding kinetics of the FBP28 WW domain revealed by an all-atom Monte Carlo simulation in a knowledge-based potential. Xu J, Huang L, Shakhnovich EI. Proteins 79 1704-1714 (2011)
  77. The Role of Electrostatic Interactions in Folding of β-Proteins. Davis CM, Dyer RB. J. Am. Chem. Soc. 138 1456-1464 (2016)
  78. Calorimetric dissection of thermal unfolding of OspA, a predominantly beta-sheet protein containing a single-layer beta-sheet. Nakagawa T, Shimizu H, Link K, Koide A, Koide S, Tamura A. J. Mol. Biol. 323 751-762 (2002)
  79. Preventing fibril formation of a protein by selective mutation. Maisuradze GG, Medina J, Kachlishvili K, Krupa P, Mozolewska MA, Martin-Malpartida P, Maisuradze L, Macias MJ, Scheraga HA. Proc. Natl. Acad. Sci. U.S.A. 112 13549-13554 (2015)
  80. Sequence-based modeling of Abeta42 soluble oligomers. Dulin F, Callebaut I, Colloc'h N, Mornon JP. Biopolymers 85 422-437 (2007)
  81. (Un)Folding mechanisms of the FBP28 WW domain in explicit solvent revealed by multiple rare event simulation methods. Juraszek J, Bolhuis PG. Biophys. J. 98 646-656 (2010)
  82. A sequential assignment procedure for proteins that have intermediate line widths in MAS NMR spectra: amyloid fibrils of human CA150.WW2. Becker J, Ferguson N, Flinders J, van Rossum BJ, Fersht AR, Oschkinat H. Chembiochem 9 1946-1952 (2008)
  83. Coupling between conformation and proton binding in proteins. Vila JA, Ripoll DR, Arnautova YA, Vorobjev YN, Scheraga HA. Proteins 61 56-68 (2005)
  84. Nuclear Magnetic Resonance Structure of a Novel Globular Domain in RBM10 Containing OCRE, the Octamer Repeat Sequence Motif. Martin BT, Serrano P, Geralt M, Wüthrich K. Structure 24 158-164 (2016)
  85. A polarizable coarse-grained protein model for dissipative particle dynamics. Peter EK, Lykov K, Pivkin IV. Phys Chem Chem Phys 17 24452-24461 (2015)
  86. A study of the influence of charged residues on β-hairpin formation by nuclear magnetic resonance and molecular dynamics. Makowska J, Zmudzińska W, Uber D, Chmurzyński L. Protein J. 33 525-535 (2014)
  87. Correlation analysis for protein evolutionary family based on amino acid position mutations and application in PDZ domain. Du QS, Wang CH, Liao SM, Huang RB. PLoS ONE 5 e13207 (2010)
  88. Nanopore-Based Sensors for Detecting Toxicity of a Carbon Nanotube to Proteins. Luan B, Zhou R. J Phys Chem Lett 2012 2337-2341 (2012)
  89. Novel mechanism of regulation of tomato bushy stunt virus replication by cellular WW-domain proteins. Barajas D, Kovalev N, Qin J, Nagy PD. J. Virol. 89 2064-2079 (2015)
  90. Probing the free energy landscape of the FBP28WW domain using multiple techniques. Periole X, Allen LR, Tamiola K, Mark AE, Paci E. J Comput Chem 30 1059-1068 (2009)
  91. Probing the nanosecond dynamics of a designed three-stranded beta-sheet with a massively parallel molecular dynamics simulation. Voelz VA, Luttmann E, Bowman GR, Pande VS. Int J Mol Sci 10 1013-1030 (2009)
  92. Redesign of a WW domain peptide for selective recognition of single-stranded DNA. Stewart AL, Park JH, Waters ML. Biochemistry 50 2575-2584 (2011)
  93. Theory and Practice of Coarse-Grained Molecular Dynamics of Biologically Important Systems. Liwo A, Czaplewski C, Sieradzan AK, Lipska AG, Samsonov SA, Murarka RK. Biomolecules 11 1347 (2021)
  94. A general method for the derivation of the functional forms of the effective energy terms in coarse-grained energy functions of polymers. III. Determination of scale-consistent backbone-local and correlation potentials in the UNRES force field and force-field calibration and validation. Liwo A, Sieradzan AK, Lipska AG, Czaplewski C, Joung I, Żmudzińska W, Hałabis A, Ołdziej S. J Chem Phys 150 155104 (2019)
  95. Changes in the folding landscape of the WW domain provide a molecular mechanism for an inherited genetic syndrome. Pucheta-Martinez E, D'Amelio N, Lelli M, Martinez-Torrecuadrada JL, Sudol M, Saladino G, Gervasio FL. Sci Rep 6 30293 (2016)
  96. Implementation of a Serial Replica Exchange Method in a Physics-Based United-Residue (UNRES) Force Field. Shen H, Czaplewski C, Liwo A, Scheraga HA. J Chem Theory Comput 4 1386-1400 (2008)
  97. Structural and cellular mechanisms of peptidyl-prolyl isomerase Pin1-mediated enhancement of Tissue Factor gene expression, protein half-life, and pro-coagulant activity. Kurakula K, Koenis DS, Herzik MA, Liu Y, Craft JW, van Loenen PB, Vos M, Tran MK, Versteeg HH, Goumans MTH, Ruf W, de Vries CJM, Şen M. Haematologica 103 1073-1082 (2018)
  98. Structures of single-layer β-sheet proteins evolved from β-hairpin repeats. Xu Q, Biancalana M, Grant JC, Chiu HJ, Jaroszewski L, Knuth MW, Lesley SA, Godzik A, Elsliger MA, Deacon AM, Wilson IA. Protein Sci 28 1676-1689 (2019)
  99. Characterization of substrate binding of the WW domains in human WWP2 protein. Jiang J, Wang N, Jiang Y, Tan H, Zheng J, Chen G, Jia Z. FEBS Lett. 589 1935-1942 (2015)
  100. Common folding processes of mini-proteins: Partial formations of secondary structures initiate the immediate protein folding. Harada R, Takano Y, Shigeta Y. J Comput Chem 38 790-797 (2017)
  101. Funneled energy landscape unifies principles of protein binding and evolution. Yan Z, Wang J. Proc Natl Acad Sci U S A 117 27218-27223 (2020)
  102. In situ data analytics and indexing of protein trajectories. Johnston T, Zhang B, Liwo A, Crivelli S, Taufer M. J Comput Chem 38 1419-1430 (2017)
  103. Linking time-series of single-molecule experiments with molecular dynamics simulations by machine learning. Matsunaga Y, Sugita Y. Elife 7 (2018)
  104. Molecular dynamics of protein A and a WW domain with a united-residue model including hydrodynamic interaction. Lipska AG, Seidman SR, Sieradzan AK, Giełdoń A, Liwo A, Scheraga HA. J Chem Phys 144 184110 (2016)
  105. New Insights into Folding, Misfolding, and Nonfolding Dynamics of a WW Domain. Kachlishvili K, Korneev A, Maisuradze L, Liu J, Scheraga HA, Molochkov A, Senet P, Niemi AJ, Maisuradze GG. J Phys Chem B 124 3855-3872 (2020)
  106. A quantitative connection of experimental and simulated folding landscapes by vibrational spectroscopy. Davis CM, Zanetti-Polzi L, Gruebele M, Amadei A, Dyer RB, Daidone I. Chem Sci 9 9002-9011 (2018)
  107. Cooperative binding of the tandem WW domains of PLEKHA7 to PDZD11 promotes conformation-dependent interaction with tetraspanin 33. Rouaud F, Tessaro F, Aimaretti L, Scapozza L, Citi S. J Biol Chem 295 9299-9312 (2020)
  108. How Useful can the Voigt Profile be in Protein Folding Processes? Maisuradze L, Maisuradze GG. Protein J (2021)
  109. Identification of novel functional mini-receptors by combinatorial screening of split-WW domains. Neitz H, Paul NB, Häge FR, Lindner C, Graebner R, Kovermann M, Thomas F. Chem Sci 13 9079-9090 (2022)
  110. Letter Multiple WW domains of Nedd4-1 undergo conformational exchange that is quenched upon peptide binding. Panwalkar V, Neudecker P, Willbold D, Dingley AJ. FEBS Lett. 591 1573-1583 (2017)
  111. Superfunneled Energy Landscape of Protein Evolution Unifies the Principles of Protein Evolution, Folding, and Design. Yan Z, Wang J. Phys. Rev. Lett. 122 018103 (2019)
  112. The WW domain of IQGAP1 binds directly to the p110α catalytic subunit of PI 3-kinase. Bardwell AJ, Paul M, Yoneda KC, Andrade-Ludeña MD, Nguyen OT, Fruman D, Bardwell L. Biochem J BCJ20220493 (2023)
  113. The effect of context on the folding of β-hairpins. Jonsson AL, Daggett V. J. Struct. Biol. 176 143-150 (2011)
  114. Tunable Protein Hydrogels: Present State and Emerging Development. Nie J, Zhang X, Wang W, Ren J, Zeng AP. Adv Biochem Eng Biotechnol 178 63-97 (2021)


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