Interactions of Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 with membranes at cold and ambient temperatures - Surface morphology and single-molecule force measurements show phase separation, and reveal tertiary and quaternary associations

Biochimica et Biophysica Acta - Biomembranes

Volumn 1828, Issue 3, 2013, Pages 967-980

  Rahman, Luna N ^a   McKay, Fraser ^a   Giuliani, Maximiliano ^a   Quirk, Amanda ^a   Moffatt, Barbara A ^b   Harauz, George ^a   Dutcher, John R ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Atomic force microscopy; Cold and drought tolerance; Dehydrin; Intrinsically disordered protein; Langmuir Blodgett monolayers; Supported lipid bilayer

Indexed keywords

DEHYDRIN 1; DEHYDRIN 2; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BRASSICA; COLD STRESS; CONTROLLED STUDY; ELLIPSOMETRY; ENVIRONMENTAL TEMPERATURE; LANGMUIR BLODGETT FILM; LIPID BILAYER; LIPID COMPOSITION; LIPID MONOLAYER; MITOCHONDRION; MOLECULAR INTERACTION; NONHUMAN; PHASE SEPARATION; PHASE TRANSITION; PLANT DEFENSE; PLANT STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY; TEMPERATURE DEPENDENCE; THELLUNGIELLA SALSUGINEA;

AMINO ACID SEQUENCE; BIOPHYSICS; BRASSICACEAE; CELL MEMBRANE; COLD TEMPERATURE; DIMERIZATION; LIPIDS; MICROSCOPY, ATOMIC FORCE; MODELS, STATISTICAL; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SURFACE PROPERTIES; TEMPERATURE;

THELLUNGIELLA SALSUGINEA;

EID: 84872100193     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.11.031     Document Type: Article

References (106)

1. A. Tunnacliffe, and M.J. Wise The continuing conundrum of the LEA proteins Naturwissenschaften 94 2007 791 812
2. M. Battaglia, Y. Olvera-Carrillo, A. Garciarrubio, F. Campos, and A.A. Covarrubias The enigmatic LEA proteins and other hydrophilins Plant Physiol. 148 2008 6 24
3. T.J. Close Dehydrins: a commonality in the response of plants to dehydration and low temperature Physiol. Plant. 100 1997 291 296
4. C. Allagulova, F.R. Gimalov, F.M. Shakirova, and V.A. Vakhitov The plant dehydrins: structure and putative functions Biochem. Mosc. 68 2003 945 951
5. K. Kosova, P. Vitamvas, and I.T. Prasil The role of dehydrins in plant response to cold Biol. Plant. 51 2007 601 617
6. S.K. Eriksson, and P. Harryson Dehydrins: molecular biology, structure, and function U. Lüttge, Plant Desiccation Tolerance, Ecological Studies 2011 Springer-Verlag Berlin, Heidelberg 289 304
7. M. Hanin, F. Brini, C. Ebel, Y. Toda, S. Takeda, and K. Masmoudi Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms Plant Signal. Behav. 6 2011 1503 1509
8. C. Zhang, Z. Ding, X. Xu, Q. Wang, G. Qin, and S. Tian Crucial roles of membrane stability and its related proteins in the tolerance of peach fruit to chilling injury Amino Acids 39 2010 181 194
9. B. Li, C. Zhang, B. Cao, G. Qin, W. Wang, and S. Tian Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids Amino Acids 43 2012 2469 2480
10. E.H. Beck, S. Fettig, C. Knake, K. Hartig, and T. Bhattarai Specific and unspecific responses of plants to cold and drought stress J. Biosci. 32 2007 501 510
11. L.N. Rahman, L. Chen, S. Nazim, V.V. Bamm, M.W. Yaish, B.A. Moffatt, J.R. Dutcher, and G. Harauz Interactions of intrinsically disordered Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 with membranes - synergistic effects of lipid composition and temperature on secondary structure Biochem. Cell Biol. 88 2010 791 807
12. L.N. Rahman, V.V. Bamm, J.A.M. Voyer, G.S. Smith, L. Chen, M.W. Yaish, B.A. Moffatt, J.R. Dutcher, and G. Harauz Zinc induces disorder-to-order transitions in free and membrane-associated Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2: a solution CD and solid-state ATR-FTIR study Amino Acids 40 2011 1485 1502
13. C. Ruibal, I.P. Salamo, V. Carballo, A. Castro, M. Bentancor, O. Borsani, L. Szabados, and S. Vidal Differential contribution of individual dehydrin genes from Physcomitrella patens to salt and osmotic stress tolerance Plant Sci. 190 2012 89 102
14. S. Haaning, S. Radutoiu, S.V. Hoffmann, J. Dittmer, L. Giehm, D.E. Otzen, and J. Stougaard An unusual intrinsically disordered protein from the model legume Lotus japonicus stabilizes proteins in vitro J. Biol. Chem. 283 2008 31142 31152
15. D. Kovacs, E. Kalmar, Z. Torok, and P. Tompa Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins Plant Physiol. 147 2008 381 390
16. S. Hughes, and S.P. Graether Cryoprotective mechanism of a small intrinsically disordered dehydrin protein Protein Sci. 20 2011 42 50
17. M. Drira, W. Saibi, F. Brini, A. Gargouri, K. Masmoudi, and M. Hanin The K-segments of the wheat dehydrin DHN-5 are essential for the protection of lactate dehydrogenase and beta-glucosidase activities in vitro Mol. Biotechnol. 2012 10.1007/s12033†012†9606â€8
18. M. Hundertmark, R. Dimova, J. Lengefeld, R. Seckler, and D.K. Hincha The intrinsically disordered late embryogenesis abundant protein LEA18 from Arabidopsis thaliana modulates membrane stability through binding and folding Biochim. Biophys. Acta 1808 2011 446 453
19. S.K. Eriksson, M. Kutzer, J. Procek, G. Grobner, and P. Harryson Tunable membrane binding of the intrinsically disordered dehydrin lti30, a cold-induced plant stress protein Plant Cell 23 2011 2391 2404
20. M. Abu-Abied, L. Golomb, E. Belausov, S. Huang, B. Geiger, Z. Kam, C.J. Staiger, and E. Sadot Identification of plant cytoskeleton-interacting proteins by screening for actin stress fiber association in mammalian fibroblasts Plant J. 48 2006 367 379
21. L.N. Rahman, G.S.T. Smith, V.V. Bamm, J.A. Voyer-Grant, B.A. Moffatt, J.R. Dutcher, and G. Harauz Phosphorylation of Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 facilitates cation-induced conformational changes and actin assembly Biochemistry 50 2011 9587 9604
22. J.M. Mouillon, S.K. Eriksson, and P. Harryson Mimicking the plant-cell interior under water stress by macromolecular crowding: disordered dehydrin proteins are highly resistant to structural collapse Plant Physiol. 148 2008 1925 1937
23. P. Tompa, and D. Kovacs Intrinsically disordered chaperones in plants and animals Biochem. Cell Biol. 88 2010 167 174
24. M.C. Koag, R.D. Fenton, S. Wilkens, and T.J. Close The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity Plant Physiol. 131 2003 309 316
25. M.C. Koag, S. Wilkens, R.D. Fenton, J. Resnik, E. Vo, and T.J. Close The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes Plant Physiol. 150 2009 1503 1514
26. J.L. Soulages, K. Kim, C. Walters, and J.C. Cushman Temperature-induced extended helix/random coil transitions in a group 1 late embryogenesis-abundant protein from soybean Plant Physiol. 128 2002 822 832
27. J.L. Soulages, K. Kim, E.L. Arrese, C. Walters, and J.C. Cushman Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly (l-proline)-type II structure Plant Physiol. 131 2003 963 975
28. P. Tompa, P. Banki, M. Bokor, P. Kamasa, D. Kovacs, G. Lasanda, and K. Tompa Protein-water and protein-buffer interactions in the aqueous solution of an intrinsically unstructured plant dehydrin: NMR intensity and DSC aspects Biophys. J. 91 2006 2243 2249
29. E.E. Findlater, and S.P. Graether NMR assignments of the intrinsically disordered K2 and YSK2 dehydrins Biomol. NMR Assign. 3 2009 273 275
30. C.E. Wong, Y. Li, B.R. Whitty, C. Diaz-Camino, S.R. Akhter, J.E. Brandle, G.B. Golding, E.A. Weretilnyk, B.A. Moffatt, and M. Griffith Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap Plant Mol. Biol. 58 2005 561 574
31. M. Griffith, M. Timonin, A.C. Wong, G.R. Gray, S.R. Akhter, M. Saldanha, M.A. Rogers, E.A. Weretilnyk, and B. Moffatt Thellungiella: an Arabidopsis-related model plant adapted to cold temperatures Plant Cell Environ. 30 2007 529 538
32. K. Lin, V.A. Simossis, W.R. Taylor, and J. Heringa A simple and fast secondary structure prediction method using hidden neural networks Bioinformatics 21 2005 152 159
33. M.C. Petty Langmuir-Blodgett Films - An Introduction 1996 Cambridge University Press Cambridge (UK)
34. I. Langmuir, and D.F. Waugh The adsorption of proteins at oil-water interfaces and artificial protein-lipoid membranes J. Gen. Physiol. 21 1938 745 755
35. T.J. Senden, and C.J. Drummond Surface-chemistry and tip sample interactions in atomic-force microscopy Colloids Surf., A Physicochem. Eng. Asp. 94 1995 29 51
36. J.W. Eaton, D. Bateman, and S. Hauberg GNU Octave Manual Version 3 2008 Network Theory Ltd. Bristol, UK
37. M. Rief, M. Gautel, F. Oesterhelt, J.M. Fernandez, and H.E. Gaub Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276 1997 1109 1112
38. C. Bouchiat, M.D. Wang, J. Allemand, T. Strick, S.M. Block, and V. Croquette Estimating the persistence length of a worm-like chain molecule from force-extension measurements Biophys. J. 76 1999 409 413
39. V.V. Bamm, M. De Avila, G.S.T. Smith, M.A. Ahmed, and G. Harauz Structured functional domains of myelin basic protein: cross talk between actin polymerization and Ca(2 +)-dependent calmodulin interaction Biophys. J. 101 2011 1248 1256
40. M.A.M. Ahmed, A.M. De, E. Polverini, K. Bessonov, V.V. Bamm, and G. Harauz Solution NMR structure and molecular dynamics simulations of murine 18.5-kDa myelin basic protein segment (S72-S107) in association with dodecylphosphocholine micelles Biochemistry 51 2012 7475 7487
41. S. Suresh, C. Wang, R. Nanekar, P. Kursula, and J.M. Edwardson Myelin basic protein and myelin protein 2 act synergistically to cause stacking of lipid bilayers Biochemistry 49 2010 3456 3463
42. Y. Min, T.F. Alig, D.W. Lee, J.M. Boggs, J.N. Israelachvili, and J.A. Zasadzinski Critical and off-critical miscibility transitions in model extracellular and cytoplasmic myelin lipid monolayers Biophys. J. 100 2011 1490 1498
43. R.G. Oliveira, and B. Maggio Compositional domain immiscibility in whole myelin monolayers at the air-water interface and Langmuir-Blodgett films Biochim. Biophys. Acta 1561 2002 238 250
44. H. Haas, R. Steitz, A. Fasano, G.M. Liuzzi, E. Polverini, P. Cavatorta, and P. Riccio Laminar order within Langmuir-Blodgett multilayers from phospholipid and myelin basic protein: a neutron reflectivity study Langmuir 23 2007 8491 8496
45. C.M. Rosetti, B. Maggio, and R.G. Oliveira The self-organization of lipids and proteins of myelin at the membrane interface. Molecular factors underlying the microheterogeneity of domain segregation Biochim. Biophys. Acta Biomembr. 1778 2008 1665 1675
46. A.J. Verkleij, B. de Kruyff, P.H. Ververgaert, J.F. Tocanne, and L.L. van Deenen The influence of pH, Ca2 + and protein on the thermotropic behaviour of the negatively charged phospholipid, phosphatidylglycerol Biochim. Biophys. Acta 339 1974 432 437
47. J.M. Boggs, M.A. Moscarello, and D. Papahadjopoulos Phase separation of acidic and neutral phospholipids induced by human myelin basic protein Biochemistry 16 1977 5420 5426
48. J.M. Boggs, D.D. Wood, and M.A. Moscarello Hydrophobic and electrostatic interactions of myelin basic proteins with lipid. Participation of N-terminal and C-terminal portions Biochemistry 20 1981 1065 1073
49. J.M. Boggs, M.A. Moscarello, and D. Papahadjopoulos Structural organization of myelin: role of lipid-protein interactions determined in model systems P.C. Jost, O.H. Griffith, Lipid-Protein Interactions vol. 2 1982 Wiley-Interscience New York 1 51
50. J.M. Boggs, P.M. Yip, G. Rangaraj, and E. Jo Effect of posttranslational modifications to myelin basic protein on its ability to aggregate acidic lipid vesicles Biochemistry 36 1997 5065 5071
51. J. Kim, T. Shishido, X. Jiang, A. Aderem, and S. McLaughlin Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles J. Biol. Chem. 269 1994 28214 28219
52. J. Kim, P.J. Blackshear, J.D. Johnson, and S. McLaughlin Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin Biophys. J. 67 1994 227 237
53. A.J. Verkleij Lipid phase transitions and micro-domains in biomembranes and their possible relevance for biological processes H. Plattner, Electron Microscopy of Subcellular Dynamics 1989 CRC Press Boca Raton 75 93
54. R.C. Dougherty Temperature and pressure dependence of hydrogen bond strength: a perturbation molecular orbital approach J. Chem. Phys. 109 1998 7372 7378
55. S.V. Mac Millan, N. Ishiyama, G.F. White, N. Palaniyar, F.R. Hallett, and G. Harauz Myelin basic protein component C1 in increasing concentrations can elicit fusion, aggregation, and fragmentation of myelin-like membranes Eur. J. Cell Biol. 79 2000 327 335
56. D.R. Kattnig, T. Bund, J.M. Boggs, G. Harauz, and D. Hinderberger Lateral self-assembly of 18.5-kDa myelin basic protein (MBP) charge component-C1 on membranes Biochim. Biophys. Acta 1818 2012 2636 2647
57. P.E. Milhiet, M.C. Giocondi, and G.C. Le AFM imaging of lipid domains in model membranes Sci. World J. 3 2003 59 74
58. M.C. Giocondi, and G.C. Le Temperature dependence of the surface topography in dimyristoylphosphatidylcholine/distearoylphosphatidylcholine multibilayers Biophys. J. 86 2004 2218 2230
59. L. Opilik, T. Bauer, T. Schmid, J. Stadler, and R. Zenobi Nanoscale chemical imaging of segregated lipid domains using tip-enhanced Raman spectroscopy Phys. Chem. Chem. Phys. 13 2011 9978 9981
60. P.A. Janmey, and P.K. Kinnunen Biophysical properties of lipids and dynamic membranes Trends Cell Biol. 16 2006 538 546
61. J.F. Tocanne, L. Cezanne, A. Lopez, B. Piknova, V. Schram, J.F. Tournier, and M. Welby Lipid domains and lipid/protein interactions in biological membranes Chem. Phys. Lipids 73 1994 139 158
62. J.F. Tocanne, L. Dupou-Cezanne, and A. Lopez Lateral diffusion of lipids in model and natural membranes Prog. Lipid Res. 33 1994 203 237
63. R. Welti, and M. Glaser Lipid domains in model and biological membranes Chem. Phys. Lipids 73 1994 121 137
64. A. Wisniewska, J. Draus, and W.K. Subczynski Is a fluid-mosaic model of biological membranes fully relevant? Studies on lipid organization in model and biological membranes Cell. Mol. Biol. Lett. 8 2003 147 159
65. M.C. Mansilla, L.E. Cybulski, D. Albanesi, and D. de Mendoza Control of membrane lipid fluidity by molecular thermosensors J. Bacteriol. 186 2004 6681 6688
66. P.F. Almeida, A. Pokorny, and A. Hinderliter Thermodynamics of membrane domains Biochim. Biophys. Acta 1720 2005 1 13
67. D.A. Redfern, and A. Gericke pH-dependent domain formation in phosphatidylinositol polyphosphate/phosphatidylcholine mixed vesicles J. Lipid Res. 46 2005 504 515
68. V. Kiessling, C. Wan, and L.K. Tamm Domain coupling in asymmetric lipid bilayers Biochim. Biophys. Acta 1788 2009 64 71
69. H.M. Seeger, C.A. Di, A. Alessandrini, and P. Facci Supported lipid bilayers on mica and silicon oxide: comparison of the main phase transition behavior J. Phys. Chem. B 114 2010 8926 8933
70. J.N. Israelachvili, and D.J. Mitchell A model for the packing of lipids in bilayer membranes Biochim. Biophys. Acta 389 1975 13 19
71. D.A. Brown, and E. London Structure and origin of ordered lipid domains in biological membranes J. Membr. Biol. 164 1998 103 114
72. P.W. Van Dijck, K.B. De, L.L. van Deenen, G.J. De, and R.A. Demel The preference of cholesterol for phosphatidylcholine in mixed phosphatidylcholine- phosphatidylethanolamine bilayers Biochim. Biophys. Acta 455 1976 576 587
73. D. Chapman, R.M. Williams, and B.D. Ladbrooke Physical studies of phospholipids. VI. Thermotropic and lyotropic mesomorphism of some 1,2-diacyl-phosphatidylcholines (lecithins) Chem. Phys. Lipids 1 1967 445 475
74. E.M. Puchner, and H.E. Gaub Single-molecule mechanoenzymatics Annu. Rev. Biophys. 41 2012 497 518
75. T. Hoffmann, and L. Dougan Single molecule force spectroscopy using polyproteins Chem. Soc. Rev. 41 2012 4781 4796
76. A. Janshoff, M. Neitzert, Y. Oberdörfer, and H. Fuchs Force spectroscopy of molecular systems - single molecule spectroscopy of polymers and biomolecules Angew. Chem. Int. Ed. Engl. 39 2000 3212 3237
77. A. Kedrov, M. Krieg, C. Ziegler, W. Kühlbrandt, and D.J. Muller Locating ligand binding and activation of a single antiporter EMBO Rep. 6 2005 668 674
78. M. Brucale, I. Tessari, L. Bubacco, and B. Samori Single-molecule force spectroscopy of chimeric polyprotein constructs containing intrinsically disordered domains Methods Mol. Biol. 896 2012 47 56
79. J. Oroz, R. Hervas, A. Valbuena, and M. Carrion-Vazquez Unequivocal single-molecule force spectroscopy of intrinsically disordered proteins Methods Mol. Biol. 896 2012 71 87
80. A. Touhami, and J.R. Dutcher pH-induced changes in adsorbed beta-lactoglobulin molecules measured using atomic force microscopy Soft Matter 5 2009 220 227
81. A. Touhami, M. Alexander, M. Kurylowicz, C. Gram, M. Corredig, and J.R. Dutcher Probing protein conformations at the oil droplet-water interface using single-molecule force spectroscopy Soft Matter 7 2011 10274 10284
82. M. Rief, M. Gautel, and H.E. Gaub Unfolding forces of titin and fibronectin domains directly measured by AFM Adv. Exp. Med. Biol. 481 2000 129 136
83. M. Rief, and H. Grubmuller Force spectroscopy of single biomolecules ChemPhysChem 3 2002 255 261
84. M.S. Kellermayer, C. Bustamante, and H.L. Granzier Mechanics and structure of titin oligomers explored with atomic force microscopy Biochim. Biophys. Acta 1604 2003 105 114
85. B.H. Kim, N.Y. Palermo, S. Lovas, T. Zaikova, J.F. Keana, and Y.L. Lyubchenko Single-molecule atomic force microscopy force spectroscopy study of Abeta-40 interactions Biochemistry 50 2011 5154 5162
86. C. McAllister, M.A. Karymov, Y. Kawano, A.Y. Lushnikov, A. Mikheikin, V.N. Uversky, and Y.L. Lyubchenko Protein interactions and misfolding analyzed by AFM force spectroscopy J. Mol. Biol. 354 2005 1028 1042
87. J. Yu, S. Malkova, and Y.L. Lyubchenko alpha-Synuclein misfolding: single molecule AFM force spectroscopy study J. Mol. Biol. 384 2008 992 1001
88. A.F. Oberhauser, P.E. Marszalek, H.P. Erickson, and J.M. Fernandez The molecular elasticity of the extracellular matrix protein tenascin Nature 393 1998 181 185
89. M. Carrion-Vazquez, A.F. Oberhauser, S.B. Fowler, P.E. Marszalek, S.E. Broedel, J. Clarke, and J.M. Fernandez Mechanical and chemical unfolding of a single protein: a comparison Proc. Natl. Acad. Sci. U. S. A. 96 1999 3694 3699
90. M. Rief, J. Pascual, M. Saraste, and H.E. Gaub Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles J. Mol. Biol. 286 1999 553 561
91. J.I. Sulkowska, and M. Cieplak Stretching to understand proteins - a survey of the protein data bank Biophys. J. 94 2008 6 13
92. K. Sweers, K. van der Werf, M. Bennink, and V. Subramaniam Nanomechanical properties of alpha-synuclein amyloid fibrils: a comparative study by nanoindentation, harmonic force microscopy, and Peakforce QNM Nanoscale Res. Lett. 6 2011 270
93. J. Yu, and Y.L. Lyubchenko Early stages for Parkinson's development: alpha-synuclein misfolding and aggregation J. Neuroimmune Pharmacol. 4 2009 10 16
94. J.M. Mouillon, P. Gustafsson, and P. Harryson Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments Plant Physiol. 141 2006 638 650
95. M. Sunde, L.C. Serpell, M. Bartlam, P.E. Fraser, M.B. Pepys, and C.C. Blake Common core structure of amyloid fibrils by synchrotron X-ray diffraction J. Mol. Biol. 273 1997 729 739
96. C.M. Dobson Protein misfolding, evolution and disease Trends Biochem. Sci. 24 1999 329 332
97. D. Thirumalai, D.K. Klimov, and R.I. Dima Emerging ideas on the molecular basis of protein and peptide aggregation Curr. Opin. Struct. Biol. 13 2003 146 159
98. L.M. Iakoucheva, P. Radivojac, C.J. Brown, T.R. O'Connor, J.G. Sikes, Z. Obradovic, and A.K. Dunker The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 32 2004 1037 1049
99. P. Tompa, C. Szasz, and L. Buday Structural disorder throws new light on moonlighting Trends Biochem. Sci. 30 2005 484 489
100. V. Vacic, C.J. Oldfield, A. Mohan, P. Radivojac, M.S. Cortese, V.N. Uversky, and A.K. Dunker Characterization of molecular recognition features, MoRFs, and their binding partners J. Proteome Res. 6 2007 2351 2366
101. P. Tompa, and M. Fuxreiter Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions Trends Biochem. Sci. 33 2008 2 8
102. V.N. Uversky What does it mean to be natively unfolded? Eur. J. Biochem. 269 2002 2 12
103. V.N. Uversky Intrinsically disordered proteins and their environment: effects of strong denaturants, temperature, pH, counter ions, membranes, binding partners, osmolytes, and macromolecular crowding Protein J. 28 2009 305 325
104. A.B. Szalaine, D. Kovacs, P. Tompa, and A. Perczel Full backbone assignment and dynamics of the intrinsically disordered dehydrin ERD14 Biomol. NMR Assign. 5 2011 189 193
105. H. Wang, Z. Wu, Y. Chen, C. Yang, and D. Shi Effects of salt and alkali stresses on growth and ion balance in rice (Oryza sativa L.) Plant Soil Environ. 57 2011 286 294
106. M. Kurylowicz, M. Giuliani, J.R. Dutcher. Using nanoscale substrate curvature to control the dimerization of a surface-bound protein. ACS Nano, in press online, http://dx.doi.org/10.1021.nn302948d.