Intrinsically Disordered Proteins

NMR of Biomolecules: Towards Mechanistic Systems Biology

Volumn , Issue , 2012, Pages 136-152

  Felli, Isabella C ^a   Pierattelli, Roberta ^a   Tompa, Peter ^b,c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c INSTITUTE OF ENZYMOLOGY   (Hungary)

Author keywords

Bioinformatics; Intrinsically disordered protein; NMR; Regulatory protein; Signaling protein; Structural biology; Three dimensional structure

Indexed keywords

EID: 84885489725     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527644506.ch7     Document Type: Chapter

References (170)

1. Uversky, V.N., Gillespie, J.R., and Fink, A.L. (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Protein Sci., 41, 415-427.
2. Dunker,A.K., Lawson, J.D., Brown, C.J.,Romero, P., Oh, J.S. et al. (2001) Intrinsically disordered protein. J. Mol. Graph. Model., 19, 26-59.
3. Dyson, H.J. and Wright, P.E. (2005) Intrinsically unstructured proteins and their functions. Nat. Rev. Mol. Cell Biol., 6, 197-208.
4. Bermel, W., Bertini, I., Felli, I.C., Lee, Y.-M., Luchinat, C., and Pierattelli, R. (2006)Protonless NMR experiments for sequencespecific assignment of backbone nuclei in unfolded proteins. J. Am. Chem. Soc., 128, 3918-3919.
5. Bermel,W., Bertini, I., Felli, I.C., Piccioli,M., and Pierattelli, R. (2006) 13C-detected protonless NMRspectroscopy ofproteins insolution. Prog. Nucl. Magn. Reson. Spectrosc., 48, 25-45.
6. Mittag, T. and Forman-Kay, J. (2007) Atomic-level characterization of disordered protein ensembles. Curr. Opin. Struct. Biol., 17, 3-14.
7. Bermel, W., Bertini, I., Csizmok, V., Felli, I.C., Pierattelli, R., and Tompa, P. (2009) H-start for exclusively heteronuclear NMR spectroscopy: the case of intrinsically disordered proteins. J. Magn. Reson., 198, 275-281.
8. Eliezer, D. (2009) Biophysical characterization of intrinsically disordered proteins. Curr. Opin. Struct. Biol., 19, 23-30.
9. Ringkjobing Jensen, M., Markwick, P.R.L., Meier, S., Griesinger, C., Zweckstetter, M., Grzesiek, S., Bernadó, P., and Blackledge, M. (2009) Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings. Structure, 17, 1169-1185.
10. Tompa, P. (2009) Structure and Function of Intrinsically Disordered Proteins, Taylor & Francis, Boca Raton, FL.
11. McMeekin, T.L. (1952) J. Food Protect., 15, 57.
12. Holt, C. and Sawyer, L. (1993) J. Chem. Soc. Faraday Trans., 89, 2683.
13. Schweers, O., Schonbrunn-Hanebeck, E., Marx, A., and Mandelkow, E. (1994) J. Biol. Chem., 269, 24290.
14. Gast, K. et al. (1995) Biochemistry, 34, 13211.
15. Lynch, W.P., Riseman, V.M., and Bretscher, A. (1987) J. Biol. Chem., 262, 7429.
16. Penkett, C.J. et al. (1997) J. Mol. Biol., 274, 152.
17. Kriwacki, R.W., Hengst, L., Tennant, L., Reed, S.I., and Wright, P.E. (1996) Proc. Natl. Acad. Sci. USA, 93, 11504.
18. Hope, I.A.,Mahadevan, S., and Struhl, K. (1988) Nature, 333, 635.
19. Hernandez, M.A., Avila, J., and Andreu, J.M. (1986) Eur. J. Biochem., 154, 41.
20. Sigler, P.B. (1988) Nature, 333, 210.
21. Dobson, C.M. (1993) Curr. Biol., 3, 530.
22. Garner, E., Cannon, P., Romero, P., Obradovic, Z., and Dunker, A.K. (1998) Genome Informat., 9, 201.
23. Romero, P. et al. (1998) Pac. Symp. Biocomput., 3, 437.
24. Wright, P.E. and Dyson, H.J. (1999) J. Mol. Biol., 293, 321.
25. Dunker, A.K. et al. (2001) J. Mol. Graph. Model, 19, 26.
26. Uversky, V.N., Gillespie, J.R., and Fink, A.L. (2000) Proteins, 41, 415.
27. Tompa, P. (2002) Trends Biochem. Sci., 27, 527.
28. Dunker, A.K., Brown, C.J., Lawson, J.D., Iakoucheva, L.M., and Obradovic, Z. (2002) Biochemistry, 41, 6573.
29. Sickmeier, M. et al. (2007) Nucleic Acids Res., 35, D786.
30. Dunker, A.K., Obradovic, Z., Romero, P., Garner, E.C., and Brown, C.J. (2000) Genome Informat., 11, 161.
31. Tompa, P., Dosztányi, S., and Simon, I. (2006) J. Proteome Res., 5, 1996.
32. Dyson, H.J. and Wright, P.E. (2005) Nat. Rev. Mol. Cell Biol., 6, 197.
33. Peng, K., Radivojac, P., Vucetic, S., Dunker, A.K., and Obradovic, Z. (2006) BMC Bioinformatics, 7, 201.
34. Fuxreiter, M., Simon, I., Friedrich, P., and Tompa, P. (2004) J. Mol. Biol., 338, 1015.
35. Fuxreiter, M., Tompa, P., and Simon, I. (2007) Bioinformatics, 23, 950.
36. Diella, F. et al. (2008) Front Biosci., 13, 6580.
37. Vacic, V. et al. (2007) Proteomics, 6, 2351.
38. Tompa, P. et al. (2009) Bioessays, 31, 328.
39. Tompa, P. (2005) FEBS Lett., 579, 3346.
40. Tompa, P. (2009) Structure and Function of Intrinsically Disordered Proteins, CRC Press, Boca Raton, FL.
41. Pometun, M.S., Chekmenev, E.Y., and Wittebort, R.J. (2004) J. Biol. Chem., 279, 7982.
42. Patel, S.S., Belmont, B.J., Sante, J.M., and Rexach, M.F. (2007) Cell, 129, 83.
43. van Leeuwen, H.C., Strating, M.J., Rensen, M., de Laat, W., and van der Vliet, P.C. (1997) EMBO J., 16, 2043.
44. Bhattacharyya, R.P. et al. (2006) Science, 311, 822.
45. Collins, M.O., Yu, L., Campuzano, I., Grant, S.G., and Choudhary, J.S. (2008) Mol. Cell, 7, 1331.
46. Radivojac, P. et al. (2010) Proteins, 78, 365.
47. Khan, A.N. and Lewis, P.N. (2005) J. Biol. Chem., 280, 36073.
48. Tompa, P. and Csermely, P. (2004) FASEB J., 18, 1169.
49. Machida, K., Kono-Okada, A., Hongo, K., Mizobata, T., and Kawata, Y. (2008) J. Biol. Chem., 283, 6886.
50. Kovacs, D., Kalmar, E., Toroc, Zs., and Tompa, P. (2008) Plant Physiol., 147, 381.
51. Kiss, R., Kovacs, D., Tompa, P., and Perczel, A. (2008) Biochemistry, 47, 6936.
52. Marsh, J.A. et al. (2010) Structure, 18, 1094.
53. Tompa, P., Szasz, C., and Buday, L. (2005) Trends Biochem. Sci., 30, 484.
54. Dosztanyi, Z., Chen, J., Dunker, A.K., Simon, I., and Tompa, P. (2006) J. Proteome Res., 5, 2985.
55. Ekman, D., Light, S., Bjorklund, A.K., and Elofsson, A. (2006) Genome Biol., 7, R45.
56. Haynes, C. et al. (2006) PLoS Comput. Biol., 2, e100-1.
57. Hegyi, H., Schad, E., and Tompa, P. (2007) BMC Struct. Biol., 7, 65.
58. Buday, L. and Tompa, P. (2010) FEBS J., 277, 4348.
59. Cortese, M.S., Uversky, V.N., and Dunker, A.K. (2008) Prog. Biophys. Mol. Biol., 98, 85.
60. He, Z., Dunker, A.K., Wesson, C.R., and Trumble,W.R. (1993) J. Biol. Chem., 268, 24635.
61. Pierce, M.M., Baxa, U., Steven, A.C., Bax, A., and Wickner, R.B. (2005) Biochemistry, 44, 321.
62. Fowler, D.M., Koulov, A.V., Balch, W.E., and Kelly, J.W. (2007) Trends Biochem. Sci., 32, 217.
63. Zhang, H., Neal, S., and Wishart, D.S. (2003) J. Biomol. NMR, 25, 173.
64. Braun, D., Wider, G., and Wüthrich, K. (1994) J. Am. Chem. Soc., 116, 8466.
65. Zhang, O., Forman-Kay, J.D., Shortle, D., and Kay, L.E. (1997) J. Biomol. NMR, 9, 181.
66. Bermel,W., Bertini, I., Felli, I.C., Piccioli, M., and Pierattelli, R. (2006) Prog. Nucl. Magn. Reson. Spectrosc., 48, 25.
67. Bermel,W. et al. (2006) J. Am. Chem. Soc., 128, 3918.
68. Schwarzinger, S. et al. (2001) J. Am. Chem. Soc., 123, 2970.
69. Dyson, H.J. and Wright, P.E. (2001) Methods Enzymol., 339, 258.
70. Grzesiek, S. and Bax, A. (1993) J. Biomol. NMR, 3, 185.
71. Liu, A. et al. (2000) J. Biomol. NMR, 16, 127.
72. Kay, L.E., Ikura, M., Tschudin, R., and Bax, A. (1990) J. Magn. Reson., 89, 496.
73. Grzesiek, S. and Bax, A. (1992) J. Magn. Reson., 99, 201.
74. Weisemann, R., Rüterjans, H., and Bermel,W. (1993) J. Biomol.NMR, 3, 113.
75. Sattler, M., Schleucher, J., and Griesinger, C. (1999) Prog. Nucl. Magn. Reson. Spectrosc., 34, 93.
76. Lohr, F. et al. (2000) J. Biomol. NMR, 18, 337.
77. Panchal, S.C., Bhavesh, N.S., and Hosur, R.V. (2001) J. Biomol. NMR, 20, 135.
78. Bermel, W., Bertini, I., Felli, I.C., Pierattelli, R., and Vasos, P.R. (2005) J. Magn. Reson., 172, 324.
79. Bermel, W., Bertini, I., Felli, I.C., Kümmerle, R., and Pierattelli, R. (2006) J. Magn. Reson., 178, 56.
80. Bermel, W. et al. (2009) J. Magn. Reson., 198, 275.
81. Bermel, W., Bertini, I., Felli, I.C., Peruzzini, R., and Pierattelli, R. (2010) Chem. Phys. Chem., 11, 689.
82. Csizmok, V., Felli, I.C., Tompa, P., Banci, L., and Bertini, I. (2008) J. Am. Chem. Soc., 130, 16873.
83. Narayanan, R.L. et al. (2010) J. Am. Chem. Soc., 132, 11906.
84. Mittag, T. and Forman-Kay, J. (2007) Curr. Opin. Struct. Biol., 17, 3.
85. Cavalli, A., Salvatella, X., Dobson, C.M., and Vendruscolo, M. (2009) Proc. Natl. Acad. Sci. USA, 104, 9615.
86. Shen, Y. et al. (2008) Proc. Natl. Acad. Sci. USA, 105, 4685.
87. Spera, S. and Bax, A. (1991) J. Am. Chem. Soc., 113, 5490.
88. Marsh, J.A., Singh, V.K., Jia, Z., and Forman-Kay, J.D. (2006) Protein Sci., 15, 2795.
89. Bax, A. and Wang, A.C. (1995) J. Am. Chem. Soc., 117, 1810.
90. Griesinger, C. et al. (1999) in Modern Techniques in ProteinNMR(eds.R. Krishna and L.J. Berliner), PlenumPress, London.
91. Smith, L.J. et al. (1996) J. Mol. Biol., 255, 494.
92. Weisemann, R. et al. (1994) J. Biomol. NMR, 4, 231.
93. Hennig, M. et al. (1999) J. Mol. Biol., 288, 705.
94. Grzesiek, S. and Bax, A. (1997) J. Biomol. NMR, 9, 207.
95. Cordier, F. and Grzesiek, S. (1999) J. Am. Chem. Soc., 121, 1601.
96. Tolman, J.R., Flanagan, J.M., Kennedy, M.A., and Prestegard, J.H. (1995) Proc. Natl. Acad. Sci. USA, 92, 9279.
97. Tjandra, N. and Bax, A. (1997) Science, 278, 1111.
98. Louhivouri, M. et al. (2003) J. Am. Chem. Soc., 125, 15647.
99. Bernadó, P., Bertoncini, C., Griesinger, C., Zweckstetter, M., and Blackledge, M. (2005) J. Am. Chem. Soc., 127, 17968.
100. Mukrasch, M.D. et al. (2007) J. Am. Chem. Soc., 129, 5235.
101. Ringkjobing Jensen, M. et al. (2009) Structure, 17, 1169.
102. Marsh, J.A., Baker, J.M.R., Tollinger, M., and Forman-Kay, J. (2008) J. Am. Chem. Soc., 130, 7804.
103. Meier, S., Grzesiek, S., and Blackledge, M. (2007) J. Am. Chem. Soc., 129, 9799.
104. Hwang, T.L., Van Zijl, P.C.M., and Mori, S. (1998) J. Biomol. NMR, 11, 221.
105. Hwang, T.L., Mori, S., Shaka, A.J., and Van Zijl, P.C.M. (1998) J. Am. Chem. Soc., 119, 6203.
106. Chevelkov, V., Xue, Y., Rao, D.K., Forman-Kay, J., and Skrynnikov, N.R. (2010) J. Biomol. NMR, 46, 227.
107. Bertini, I. et al. (2006) J. Biomol. NMR, 36, 111.
108. Hsu, S.T., Bertoncini, C.W., and Dobson, C.M. (2009) J. Am. Chem. Soc., 131, 7222.
109. Skora, L., Becker, S., and Zweckstetter,M. (2010) J. Am. Chem. Soc., 132, 9223.
110. Peng, J.W. and Wagner,G. (1994)Methods Enzymol., 239, 563.
111. Kay, L.E., Torchia, D.A., and Bax, A. (1989) Biochemistry, 28, 8972.
112. Bertini, I., Luchinat, C., and Parigi, G. (2001) Solution NMR of Paramagnetic Molecules, Elsevier, Amsterdam.
113. Teilum, K., Kragelund, B.B., and Poulsen, F.M. (2002) J. Mol. Biol., 324, 349.
114. Dedmon, M.M., Lindorff-Larsen, K., Christodoulou, J., Vendruscolo, M., and Dobson, C.M. (2005) J. Am. Chem. Soc., 127, 476.
115. Bertoncini, C.W. et al. (2005) Proc. Natl. Acad. Sci. USA, 102, 1430.
116. Allison, J.R., Varnai, P., Dobson, C.M., and Vendruscolo,M. (2009) J. Am. Chem. Soc., 131, 18314.
117. Lindorff-Larsen, K. et al. (2004) J. Am. Chem. Soc., 126, 3291.
118. Mal, T.K., Matthews, S.J., Kovacs, H., Campbell, I.D., and Boyd, J. (1998) J. Biomol. NMR, 12, 259.
119. Crowhurst, K.A. and Forman-Kay, J. (2003) Biochem., 42, 8687.
120. Ellis, R.J. (2001) Trends Biochem. Sci., 26, 597.
121. Reckel, S., Hänsel, R., Löhr, F., and Dötsch,V. (2007) Prog. Nucl. Magn. Reson. Spectrosc., 51, 91.
122. Ito, Y. and Selenko, P. (2010) Curr. Opin. Struct. Biol., 20, 640.
123. Sakakibara, D. et al. (2009) Nature, 458, 102.
124. Bertini, I., Felli, I.C., Gonnelli, L., Vasantha Kumar, M.V., and Pierattelli, R. (2011) Angew. Chem. Int. Ed., 50, 1.
125. Serber,Z. et al. (2006) Nat. Protoc., 1, 2701.
126. Bodart, J.F. et al. (2008) J. Magn. Reson., 192, 252.
127. Inomata, K. et al. (2009) Nature, 458, 106.
128. Ferron, F., Longin, S., Canard, B., and Karlin, K. (2006) Bioinformatics, 65, 1.
129. Dosztanyi, Z. and Tompa, P. (2008) Methods Mol. Biol., 426, 103.
130. He, B. et al. (2009) Cell Res., 19, 929.
131. Prilusky, J. et al. (2005) Bioinformatics, 21, 3435.
132. Ward, J.J., Sodhi, J.S., McGuffin, L.J., Buxton, B.F., and Jones, D.T. (2004) J. Mol. Biol., 337, 635.
133. Dosztanyi, Z., Csizmok, V., Tompa, P., and Simon, I. (2005) Bioinformatics, 21, 3433.
134. Dosztanyi, Z., Csizmok, V., Tompa, P., and Simon, I. (2005) J. Mol. Biol., 347, 827.
135. Schlessinger, A., Punta, M., and Rost, B. (2007) Bioinformatics, 23, 2376.
136. Xue, B., Dunbrack, R.L. Jr., Williams, R.W., Dunker, A.K., and Uversky, V. (2010) Biochim. Biophys. Acta, 1804, 996.
137. Schlessinger, A., Punta, M., Yachdav, G., Kajan, L., and Rost, B. (2009) PLoS ONE, 4, e4433.
138. Ishida, T. and Kinoshita, K. (2008) Bioinformatics, 24, 1344.
139. Mészaros, B., Simon, I., and Dosztanyi, Z. (2009) PloS Comput. Biol., 5, e1000376.
140. Vendruscolo, M. (2007) Curr. Opin. Struct. Biol., 17, 15.
141. Wells, M. et al. (2008) Proc. Natl. Acad. Sci. USA, 105, 5762.
142. Jensen, M.R. et al. (2009) Structure, 17, 1169.
143. Nodet, L. et al. (2009) J. Am. Chem. Soc., 131, 17908.
144. Dosztanyi, Zs., Sandor, M., Tompa, P., and Simon, I. (2007) Curr. Protein Pept. Sci., 8, 161.
145. Joerger, A.C. and Fersht, A.R. (2008) Annu. Rev. Biochem., 77, 557.
146. Banci, L. et al. (2010) Proc. Natl. Acad. Sci. USA, 107, 20190.
147. Sugase, K., Dyson, H.J., and Wright, P.E. (2007) Nature, 447, 1021.
148. Luheshi, L.M., Crowther, D.C., and Dobson, C.M. (2008) Curr. Opin. Chem. Biol., 12, 25.
149. Dobson, C.M. (2003) Nature, 426, 884.
150. Lippens, G., Landrieu, I., and Hanoulle, X. (2008) Chem. Biol., 15, 311.
151. Bentrop, D., Beyermann, M., Wissmann, R., and Fakler, B. (2001) J. Biol. Chem., 276, 42116.
152. Mukrasch, M.D. et al. (2009) PLoS Biol., 7, e34.
153. Olson, K.E. et al. (2005) J. Biomol. Struct. Dyn., 23, 113.
154. Radhakrishnan, I., Perez-Alvaredo, G.C., Dyson, H.J., and Wright, P.E. (1998) FEBS Lett., 430, 317.
155. Vise, P.D., Baral, B., Latos, A.J., and Daughdrill,G.W. (2005)NucleicAcid Res., 33, 2061.
156. Vise, P.D., Baral, B., Stancik, A., Lowry, D.F., and Daughdrill, G.W. (2007) Proteins, 67, 526.
157. Bertoncini, C.W. et al. (2007) J. Mol. Biol., 372, 708.
158. Sivakolundu, S.G., Bashford, D., and Kriwacki, R.W. (2005) J. Mol. Biol., 353, 1118.
159. Daughdrill, G.W., Hanely, L.J., and Dahlquist, F.W. (1998) Biochemistry, 37, 1076.
160. Green, T.B. et al. (2004) Biochem, 43, 4071.
161. Radhakrishnan, I. et al. (1997) Cell, 91, 741.
162. Huq, N.L.,Cross, K.J., and Reynolds, E.C. (2004) J. Dairy Res., 71, 28.
163. Shewmaker, F., Wickner, R.B., and Tycko, R. (2006) Proc. Natl. Acad. Sci. USA, 103, 19754.
164. Linding, R., Russel, R.B., Neduva, V., and Gibson, T.J. (2003) Nucleic Acids Res., 31, 3701.
165. Liu, J. and Rost, B. (2003) Nucleic Acid Res., 31, 3833.
166. Yang, Z.R., Thomson, R., McNeil, P., and Esnouf, R. (2005) Bioinoformatics, 21, 3369.
167. Vullo, A., Bortolami, O., Pollastri, G., and Tosatto, S.C. (2006) Nucleic Acid Res., 34, W164.
168. Ishida, T. and Kinoshita, K. (2007)Nucleic Acid Res., 35, W460.
169. Galzitskaya, O.V., Garbuzynskiy, S.O., and Lobanov, M.Y. (2006) Bioinformatics, 22, 2948.
170. Lieutaud, P., Canard, B., and Longhi, S. (2008) BMC Genomics, 9, S25.