The Protein Journal

, Volume 28, Issue 7–8, pp 305–325 | Cite as

Intrinsically Disordered Proteins and Their Environment: Effects of Strong Denaturants, Temperature, pH, Counter Ions, Membranes, Binding Partners, Osmolytes, and Macromolecular Crowding

Article

Abstract

Intrinsically disordered proteins (IDPs) differ from “normal” ordered proteins at several levels, structural, functional and conformational. Amino acid biases characteristic for IDPs determine their structural variability and lack of rigid well-folded structure. This structural plasticity is necessary for the unique functional repertoire of IDPs, which is complementary to the catalytic activities of ordered proteins. Amino acid biases also drive atypical responses of IDPs to changes in their environment. The conformational behavior of IDPs is characterized by the low cooperativity (or the complete lack thereof) of the denaturant-induced unfolding, lack of the measurable excess heat absorption peak(s) characteristic for the melting of ordered proteins, “turned out” response to heat and changes in pH, the ability to gain structure in the presence of various counter ions, osmolytes, membranes and binding partners, and by the unique response to macromolecular crowding. This review describes some of the most characteristic features of the IDP conformational behavior and the unique response of IDPs to changes in their environment.

Keywords

Intrinsically disordered protein Intrinsic disorder Conformational behavior Partially folded conformation Macromolecular crowding Protein–protein interaction Protein unfolding Osmolyte 

Abbreviations

ANS

8-Anilinonaphthalene-1-sulfonate

CD

Circular dichroism

GdmCl

Guanidinium chloride

ID

Intrinsic disorder

IDP

Intrinsically disordered protein

IDR

Intrinsically disordered region

LUV

Large unilamellar vesicle

PA

1,2-Dipalmitoyl-sn-glycero-3-phosphate

PC

1,2-Dipalmitoyl-sn-glycero-3-phosphocholine

PG

1,2-Dipalmitoyl-sn-glycero-3-phospho-RAC-(1-glycerol

SUV

Small unilamellar vesicle

TMAO

Trimethylamine-N-oxide

Notes

Acknowledgments

I am grateful to Prof. Keith A. Dunker for numerous valuable discussions and constant support. Many thanks to all of my colleagues and collaborators around the globe for their invaluable contributions to the IDP field. This work was supported in part by the Program of the Russian Academy of Sciences for the “Molecular and cellular biology”, and by grants R01 LM007688-01A1 and GM071714-01A2 from the National Institutes of Health. I gratefully acknowledge the support of the IUPUI Signature Centers Initiative.

References

  1. 1.
    Alexandrescu AT, Ng YL, Dobson CM (1994) J Mol Biol 235:587–599CrossRefGoogle Scholar
  2. 2.
    Anderson CW, Appella E (2004) In: Bradshaw RA, Dennis EA (eds) Handbook of cell signaling. Academic Press, New York, pp 237–247Google Scholar
  3. 3.
    Anfinsen CB, Haber E, Sela M, White FH Jr (1961) Proc Natl Acad Sci USA 47:1309–1314CrossRefGoogle Scholar
  4. 4.
    Anson ML, Mirsky AE (1932) J Gen Physiol 15:341–350CrossRefGoogle Scholar
  5. 5.
    Arakawa T, Goddette D (1985) Arch Biochem Biophys 240:21–32CrossRefGoogle Scholar
  6. 6.
    Avalos JL, Celic I, Muhammad S, Cosgrove MS, Boeke JD, Wolberger C (2002) Mol Cell 10:523–535CrossRefGoogle Scholar
  7. 7.
    Baskakov I, Bolen DW (1998) J Biol Chem 273:4831–4834CrossRefGoogle Scholar
  8. 8.
    Baskakov I, Wang A, Bolen DW (1998) Biophys J 74:2666–2673CrossRefGoogle Scholar
  9. 9.
    Baskakov IV, Kumar R, Srinivasan G, Ji YS, Bolen DW, Thompson EB (1999) J Biol Chem 274:10693–10696CrossRefGoogle Scholar
  10. 10.
    Baum J, Dobson CM, Evans PA, Hanley C (1989) Biochemistry 28:7–13CrossRefGoogle Scholar
  11. 11.
    Bienkiewicz EA, Adkins JN, Lumb KJ (2002) Biochemistry 41:752–759CrossRefGoogle Scholar
  12. 12.
    Bismuto E, Irace G (2001) FEBS Lett 509:476–480CrossRefGoogle Scholar
  13. 13.
    Bismuto E, Martelli PL, De Maio A, Mita DG, Irace G, Casadio R (2002) Biopolymers 67:85–95CrossRefGoogle Scholar
  14. 14.
    Bolen DW (2001) Methods Mol Biol 168:17–36Google Scholar
  15. 15.
    Bolen DW, Baskakov IV (2001) J Mol Biol 310:955–963CrossRefGoogle Scholar
  16. 16.
    Bose HS, Whittal RM, Baldwin MA, Miller WL (1999) Proc Natl Acad Sci USA 96:7250–7255CrossRefGoogle Scholar
  17. 17.
    Bracken C (2001) J Mol Graph Model 19:3–12CrossRefGoogle Scholar
  18. 18.
    Brennan JD (1999) Appl Spec 53:106A–121ACrossRefGoogle Scholar
  19. 19.
    Buck M, Radford SE, Dobson CM (1993) Biochemistry 32:669–678CrossRefGoogle Scholar
  20. 20.
    Burg MB (1995) Am J Physiol 268:F983–F996Google Scholar
  21. 21.
    Bushnell GW, Louie GV, Brayer GD (1990) J Mol Biol 214:585–595CrossRefGoogle Scholar
  22. 22.
    Bussell R Jr, Ramlall TF, Eliezer D (2005) Protein Sci 14:862–872CrossRefGoogle Scholar
  23. 23.
    Bychkova VE, Dujsekina AE, Klenin SI, Tiktopulo EI, Uversky VN, Ptitsyn OB (1996) Biochemistry 35:6058–6063CrossRefGoogle Scholar
  24. 24.
    Campbell KM, Terrell AR, Laybourn PJ, Lumb KJ (2000) Biochemistry 39:2708–2713CrossRefGoogle Scholar
  25. 25.
    Christensen H, Pain RH (1991) Eur Biophys J 19:221–229CrossRefGoogle Scholar
  26. 26.
    Chyan CL, Wormald C, Dobson CM, Evans PA, Baum J (1993) Biochemistry 32:5681–5691CrossRefGoogle Scholar
  27. 27.
    Cortese MS, Uversky VN, Dunker AK (2008) Prog Biophys Mol Biol 98:85–106CrossRefGoogle Scholar
  28. 28.
    Dajani R, Fraser E, Roe SM, Yeo M, Good VM, Thompson V, Dale TC, Pearl LH (2003) EMBO J 22:494–501CrossRefGoogle Scholar
  29. 29.
    Daughdrill GW, Hanely LJ, Dahlquist FW (1998) Biochemistry 37:1076–1082CrossRefGoogle Scholar
  30. 30.
    Daughdrill GW, Chadsey MS, Karlinsey JE, Hughes KT, Dahlquist FW (1997) Nat Struct Biol 4:285–291CrossRefGoogle Scholar
  31. 31.
    Daughdrill GW, Pielak GJ, Uversky VN, Cortese MS, Dunker AK (2005) In: Buchner J, Kiefhaber T (eds) Handbook of protein folding. Wiley-VCH, Verlag GmbH & Co., Weinheim, p 271Google Scholar
  32. 32.
    Dave BC, Dunn B, Valentine JS, Zink JI (1994) Anal Chem 66:1120–1127CrossRefGoogle Scholar
  33. 33.
    Davidson WS, Jonas A, Clayton DF, George JM (1998) J Biol Chem 273:9443–9449CrossRefGoogle Scholar
  34. 34.
    de Laureto PP, Tosatto L, Frare E, Marin O, Uversky VN, Fontana A (2006) Biochemistry 45:11523–11531CrossRefGoogle Scholar
  35. 35.
    Dedmon MM, Patel CN, Young GB, Pielak GJ (2002) Proc Natl Acad Sci USA 99:12681–12684CrossRefGoogle Scholar
  36. 36.
    Diaz MD, Berger S (2001) Magn Res Chem 39:369–373CrossRefGoogle Scholar
  37. 37.
    Diaz MD, Fioroni M, Burger K, Berger S (2002) Chemistry 8:1663–1669CrossRefGoogle Scholar
  38. 38.
    Dufour E, Bertrand-Harb C, Haertle T (1993) Biopolymers 33:589–598CrossRefGoogle Scholar
  39. 39.
    Dufour E, Robert P, Bertrand D, Haertle T (1994) J Protein Chem 13:143–149CrossRefGoogle Scholar
  40. 40.
    Dunker AK, Obradovic Z (2001) Nat Biotechnol 19:805–806CrossRefGoogle Scholar
  41. 41.
    Dunker AK, Brown CJ, Obradovic Z (2002) Adv Protein Chem 62:25–49CrossRefGoogle Scholar
  42. 42.
    Dunker AK, Silman I, Uversky VN, Sussman JL (2008) Curr Opin Struct Biol 18:756–764CrossRefGoogle Scholar
  43. 43.
    Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Biochemistry 41:6573–6582CrossRefGoogle Scholar
  44. 44.
    Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN (2005) FEBS J 272:5129–5148CrossRefGoogle Scholar
  45. 45.
    Dunker AK, Oldfield CJ, Meng J, Romero P, Yang JY, Chen JW, Vacic V, Obradovic Z, Uversky VN (2008) BMC Genomics 9(Suppl 2):S1CrossRefGoogle Scholar
  46. 46.
    Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z (2001) J Mol Graph Model 19:26–59CrossRefGoogle Scholar
  47. 47.
    Dyson HJ, Wright PE (2002) Curr Opin Struct Biol 12:54–60CrossRefGoogle Scholar
  48. 48.
    Dyson HJ, Wright PE (2005) Nat Rev Mol Cell Biol 6:197–208CrossRefGoogle Scholar
  49. 49.
    Eggers DK, Valentine JS (2001) Protein Sci 10:250–261CrossRefGoogle Scholar
  50. 50.
    Eggers DK, Valentine JS (2001) J Mol Biol 314:911–922CrossRefGoogle Scholar
  51. 51.
    Eliezer D, Yao J, Dyson HJ, Wright PE (1998) Nat Struct Biol 5:148–155CrossRefGoogle Scholar
  52. 52.
    Eliezer D, Kutluay E, Bussell R Jr, Browne G (2001) J Mol Biol 307:1061–1073CrossRefGoogle Scholar
  53. 53.
    Eliezer D, Chiba K, Tsuruta H, Doniach S, Hodgson KO, Kihara H (1993) Biophys J 65:912–917CrossRefGoogle Scholar
  54. 54.
    Ellis RJ (2001) Trends Biochem Sci 26:597–604CrossRefGoogle Scholar
  55. 55.
    Endo T, Schatz G (1988) EMBO J 7:1153–1158Google Scholar
  56. 56.
    Fan P, Bracken C, Baum J (1993) Biochemistry 32:1573–1582CrossRefGoogle Scholar
  57. 57.
    Fink AL, Calciano LJ, Goto Y, Kurotsu T, Palleros DR (1994) Biochemistry 33:12504–12511CrossRefGoogle Scholar
  58. 58.
    Fioroni M, Diaz MD, Burger K, Berger S (2002) J Am Chem Soc 124:7737–7744CrossRefGoogle Scholar
  59. 59.
    Flaugh SL, Lumb KJ (2001) Biomacromolecules 2:538–540CrossRefGoogle Scholar
  60. 60.
    Fontana A, Polverino de Laureto P, De Philipps V (1993) In: van den Tweel W, Harder A, Buitelear M (eds) Protein stability and stabilization. Elsevier, Amsterdam, pp 101–110Google Scholar
  61. 61.
    Fulton AB (1982) Cell 30:345–347CrossRefGoogle Scholar
  62. 62.
    Furukawa K, Matsuzaki-Kobayashi M, Hasegawa T, Kikuchi A, Sugeno N, Itoyama Y, Wang Y, Yao PJ, Bushlin I, Takeda A (2006) J Neurochem 97:1071–1077CrossRefGoogle Scholar
  63. 63.
    Gast K, Siemer A, Zirwer D, Damaschun G (2001) Eur Biophys J 30:273–283CrossRefGoogle Scholar
  64. 64.
    Georgieva ER, Ramlall TF, Borbat PP, Freed JH, Eliezer D (2008) J Am Chem Soc 130:12856–12857CrossRefGoogle Scholar
  65. 65.
    Gill I, Ballestros A (2000) Trends Biotechnol 18:282–296CrossRefGoogle Scholar
  66. 66.
    Goto Y, Fink AL (1990) J Mol Biol 214:803–805CrossRefGoogle Scholar
  67. 67.
    Goto Y, Calciano LJ, Fink AL (1990) Proc Natl Acad Sci USA 87:573–577CrossRefGoogle Scholar
  68. 68.
    Goto Y, Takahashi N, Fink AL (1990) Biochemistry 29:3480–3488CrossRefGoogle Scholar
  69. 69.
    Gottfried DS, Kagan A, Hoffman BM, Friedman JM (1999) J Phys Chem B 103:2803–2807CrossRefGoogle Scholar
  70. 70.
    Grosberg AY, Khokhlov AR (1989) Nauka, MoscowGoogle Scholar
  71. 71.
    Haaning S, Radutoiu S, Hoffmann SV, Dittmer J, Giehm L, Otzen DE, Stougaard J (2008) J Biol Chem 283:31142–31152CrossRefGoogle Scholar
  72. 72.
    Hackel M, Hinz HJ, Hedwig GR (1999) J Mol Biol 291:197–213CrossRefGoogle Scholar
  73. 73.
    Hamada D, Kuroda Y, Tanaka T, Goto Y (1995) J Mol Biol 254:737–746CrossRefGoogle Scholar
  74. 74.
    Hatters DM, Minton AP, Howlett GJ (2002) J Biol Chem 277:7824–7830CrossRefGoogle Scholar
  75. 75.
    Hill TL (1963) Wiley, New YorkGoogle Scholar
  76. 76.
    Hollstein M, Sidransky D, Vogelstein B, Harris CC (1991) Science 253:49–53CrossRefGoogle Scholar
  77. 77.
    Jackson M, Mantsch HH (1992) Biochim Biophys Acta 1118:139–143Google Scholar
  78. 78.
    Jao CC, Der-Sarkissian A, Chen J, Langen R (2004) Proc Natl Acad Sci USA 101:8331–8336CrossRefGoogle Scholar
  79. 79.
    Jao CC, Hegde BG, Chen J, Haworth IS, Langen R (2008) Proc Natl Acad Sci USA 105:19666–19671CrossRefGoogle Scholar
  80. 80.
    Jeng MF, Englander SW, Elove GA, Wand AJ, Roder H (1990) Biochemistry 29:10433–10437CrossRefGoogle Scholar
  81. 81.
    Jo E, McLaurin J, Yip CM, St George-Hyslop P, Fraser PE (2000) J Biol Chem 275:34328–34334CrossRefGoogle Scholar
  82. 82.
    Jo E, Fuller N, Rand RP, St George-Hyslop P, Fraser PE (2002) J Mol Biol 315:799–807CrossRefGoogle Scholar
  83. 83.
    Johansson J, Gudmundsson GH, Rottenberg ME, Berndt KD, Agerberth B (1998) J Biol Chem 273:3718–3724CrossRefGoogle Scholar
  84. 84.
    Kataoka M, Hagihara Y, Mihara K, Goto Y (1993) J Mol Biol 229:591–596CrossRefGoogle Scholar
  85. 85.
    Kataoka M, Kuwajima K, Tokunaga F, Goto Y (1997) Protein Sci 6:422–430CrossRefGoogle Scholar
  86. 86.
    Kim TD, Ryu HJ, Cho HI, Yang CH, Kim J (2000) Biochemistry 39:14839–14846CrossRefGoogle Scholar
  87. 87.
    Konno T, Tanaka N, Kataoka M, Takano E, Maki M (1997) Biochim Biophys Acta 1342:73–82Google Scholar
  88. 88.
    Kumar R, Lee JC, Bolen DW, Thompson EB (2001) J Biol Chem 276:18146–18152CrossRefGoogle Scholar
  89. 89.
    Kumar R, Serrette JM, Khan SH, Miller AL, Thompson EB (2007) Arch Biochem Biophys 465:452–460CrossRefGoogle Scholar
  90. 90.
    Kuwajima K (1989) Proteins 6:87–103CrossRefGoogle Scholar
  91. 91.
    LaLonde JM, Levenson MA, Roe JJ, Bernlohr DA, Banaszak LJ (1994) J Biol Chem 269:25339–25347Google Scholar
  92. 92.
    Lan EH, Dave BC, Fukuto JM, Dunn B, Zink JI, Valentine JS (1999) J Mater Chem 9:45–53CrossRefGoogle Scholar
  93. 93.
    Lee BM, Xu J, Clarkson BK, Martinez-Yamout MA, Dyson HJ, Case DA, Gottesfeld JM, Wright PE (2006) J Mol Biol 357:275–291CrossRefGoogle Scholar
  94. 94.
    Lee HJ, Choi C, Lee SJ (2002) J Biol Chem 277:671–678CrossRefGoogle Scholar
  95. 95.
    Libich DS, Harauz G (2008) Eur Biophys J 37:1015–1029CrossRefGoogle Scholar
  96. 96.
    Lowe ED, Tews I, Cheng KY, Brown NR, Gul S, Noble ME, Gamblin SJ, Johnson LN (2002) Biochemistry 41:15625–15634CrossRefGoogle Scholar
  97. 97.
    Lynn A, Chandra S, Malhotra P, Chauhan VS (1999) FEBS Lett 459:267–271CrossRefGoogle Scholar
  98. 98.
    Madine J, Doig AJ, Middleton DA (2004) Biochem Soc Trans 32:1127–1129CrossRefGoogle Scholar
  99. 99.
    Manning-Bog AB, McCormack AL, Li J, Uversky VN, Fink AL, Di Monte DA (2002) J Biol Chem 277:1641–1644CrossRefGoogle Scholar
  100. 100.
    McLean PJ, Kawamata H, Ribich S, Hyman BT (2000) J Biol Chem 275:8812–8816CrossRefGoogle Scholar
  101. 101.
    McNulty BC, Young GB, Pielak GJ (2006) J Mol Biol 355:893–897CrossRefGoogle Scholar
  102. 102.
    Merrill AR, Cohen FS, Cramer WA (1990) Biochemistry 29:5829–5836CrossRefGoogle Scholar
  103. 103.
    Mihajlovic M, Lazaridis T (2008) Proteins 70:761–778CrossRefGoogle Scholar
  104. 104.
    Minton AP (1997) Curr Opin Biotechnol 8:65–69CrossRefGoogle Scholar
  105. 105.
    Minton AP (2000) Curr Opin Struct Biol 10:34–39CrossRefGoogle Scholar
  106. 106.
    Minton AP (2000) Curr Biol 10:R97–R99CrossRefGoogle Scholar
  107. 107.
    Minton AP (2001) J Biol Chem 276:10577–10580CrossRefGoogle Scholar
  108. 108.
    Mirsky AE, Pauling L (1936) Proc Natl Acad Sci USA 22:439–447CrossRefGoogle Scholar
  109. 109.
    Morar AS, Olteanu A, Young GB, Pielak GJ (2001) Protein Sci 10:2195–2199CrossRefGoogle Scholar
  110. 110.
    Mujtaba S, He Y, Zeng L, Yan S, Plotnikova O, Sachchidanand S, Sanchez R, Zeleznik-Le NJ, Ronai Z, Zhou MM (2004) Mol Cell 13:251–263CrossRefGoogle Scholar
  111. 111.
    Munishkina LA, Phelan C, Uversky VN, Fink AL (2003) Biochemistry 42:2720–2730CrossRefGoogle Scholar
  112. 112.
    Munishkina LA, Cooper EM, Uversky VN, Fink AL (2004) J Mol Recognit 17:456–464CrossRefGoogle Scholar
  113. 113.
    Narizhneva NV, Uversky VN (1997) Prot Pept Lett 4:243–249Google Scholar
  114. 114.
    Neurath H, Greenstein JP, Putnam FW, Erickson JO (1944) Chem Rew 34:157–265CrossRefGoogle Scholar
  115. 115.
    Neyroz P, Zambelli B, Ciurli S (2006) Biochemistry 45:8918–8930CrossRefGoogle Scholar
  116. 116.
    Nuscher B, Kamp F, Mehnert T, Odoy S, Haass C, Kahle PJ, Beyer K (2004) J Biol Chem 279:21966–21975CrossRefGoogle Scholar
  117. 117.
    Oldfield CJ, Meng J, Yang JY, Yang MQ, Uversky VN, Dunker AK (2008) BMC Genomics 9(Suppl 1):S1CrossRefGoogle Scholar
  118. 118.
    Pace CN (1986) Methods Enzymol 131:266–280CrossRefGoogle Scholar
  119. 119.
    Permyakov SE, Millett IS, Doniach S, Permyakov EA, Uversky VN (2003) Proteins 53:855–862CrossRefGoogle Scholar
  120. 120.
    Permyakov SE, Bakunts AG, Denesyuk AI, Knyazeva EL, Uversky VN, Permyakov EA (2008) Proteins 72:822–836CrossRefGoogle Scholar
  121. 121.
    Perrin RJ, Woods WS, Clayton DF, George JM (2000) J Biol Chem 275:34393–34398CrossRefGoogle Scholar
  122. 122.
    Perrin RJ, Woods WS, Clayton DF, George JM (2001) J Biol Chem 276:41958–41962CrossRefGoogle Scholar
  123. 123.
    Plaxco KW, Gross M (1997) Nature 386:657–659CrossRefGoogle Scholar
  124. 124.
    Pontius BW (1993) Trends Biochem Sci 18:181–186CrossRefGoogle Scholar
  125. 125.
    Popovic M, De Biasio A, Pintar A, Pongor S (2007) FEBS J 274:5325–5336CrossRefGoogle Scholar
  126. 126.
    Privalov PL (1979) Adv Protein Chem 33:167–241CrossRefGoogle Scholar
  127. 127.
    Privalov PL, Dragan AI (2007) Biophys Chem 126:16–24CrossRefGoogle Scholar
  128. 128.
    Ptitsyn OB (1987) J Prot Chem 6:273–293CrossRefGoogle Scholar
  129. 129.
    Ptitsyn OB (1995) Adv Protein Chem 47:83–229CrossRefGoogle Scholar
  130. 130.
    Ptitsyn OB (1995) Curr Opin Struct Biol 5:74–78CrossRefGoogle Scholar
  131. 131.
    Ptitsyn OB, Uversky VN (1994) FEBS Lett 341:15–18CrossRefGoogle Scholar
  132. 132.
    Ptitsyn OB, Bychkova VE, Uversky VN (1995) Philos Trans R Soc B-Biol Sci 348:35–41CrossRefGoogle Scholar
  133. 133.
    Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK (2007) Biophys J 92:1439–1456CrossRefGoogle Scholar
  134. 134.
    Rhoades E, Ramlall TF, Webb WW, Eliezer D (2006) Biophys J 90:4692–4700CrossRefGoogle Scholar
  135. 135.
    Roccatano D, Colombo G, Fioroni M, Mark AE (2002) Proc Natl Acad Sci USA 99:12179–12184CrossRefGoogle Scholar
  136. 136.
    Rodionova NA, Semisotnov GV, Kutyshenko VP, Uverskii VN, Bolotina IA (1989) Mol Biol (Mosk) 23:683–692Google Scholar
  137. 137.
    Romero P, Obradovic Z, Li X, Garner EC, Brown CJ, Dunker AK (2001) Proteins 42:38–48CrossRefGoogle Scholar
  138. 138.
    Rosenfeld R, Vajda S, DeLisi C (1995) Annu Rev Biophys Biomol Struct 24:677–700CrossRefGoogle Scholar
  139. 139.
    Schulz GE (1979) In: Balaban M (ed) Molecular mechanism of biological recognition. Elsevier/North-Holland Biomedical, New York, pp 79–94Google Scholar
  140. 140.
    Semisotnov GV, Rodionova NA, Razgulyaev OI, Uversky VN, Gripas AF, Gilmanshin RI (1991) Biopolymers 31:119–128CrossRefGoogle Scholar
  141. 141.
    Semisotnov GV, Kihara H, Kotova NV, Kimura K, Amemiya Y, Wakabayashi K, Serdyuk IN, Timchenko AA, Chiba K, Nikaido K, Ikura T, Kuwajima K (1996) J Mol Biol 262:559–574CrossRefGoogle Scholar
  142. 142.
    Shtilerman MD, Ding TT, Lansbury PT Jr (2002) Biochemistry 41:3855–3860CrossRefGoogle Scholar
  143. 143.
    Sickmeier M, Hamilton JA, LeGall T, Vacic V, Cortese MS, Tantos A, Szabo B, Tompa P, Chen J, Uversky VN, Obradovic Z, Dunker AK (2007) Nucleic Acids Res 35:D786–D793CrossRefGoogle Scholar
  144. 144.
    Spolar RS, Record MT Jr (1994) Science 263:777–784CrossRefGoogle Scholar
  145. 145.
    Sugase K, Dyson HJ, Wright PE (2007) Nature 447:1021–1025CrossRefGoogle Scholar
  146. 146.
    Sung YH, Eliezer D (2006) Protein Sci 15:1162–1174CrossRefGoogle Scholar
  147. 147.
    Sweede M, Ankem G, Chutvirasakul B, Azurmendi HF, Chbeir S, Watkins J, Helm RF, Finkielstein CV, Capelluto DG (2008) Biochemistry 47:13524–13536CrossRefGoogle Scholar
  148. 148.
    Tamamizu-Kato S, Kosaraju MG, Kato H, Raussens V, Ruysschaert JM, Narayanaswami V (2006) Biochemistry 45:10947–10956CrossRefGoogle Scholar
  149. 149.
    Tanford C (1968) Adv Protein Chem 23:121–282CrossRefGoogle Scholar
  150. 150.
    Tcherkasskaya O, Uversky VN (2001) Proteins 44:244–254CrossRefGoogle Scholar
  151. 151.
    Thomas PD, Dill KA (1993) Protein Sci 2:2050–2065CrossRefGoogle Scholar
  152. 152.
    Timm DE, Vissavajjhala P, Ross AH, Neet KE (1992) Protein Sci 1:1023–1031CrossRefGoogle Scholar
  153. 153.
    Tompa P (2002) Trends Biochem Sci 27:527–533CrossRefGoogle Scholar
  154. 154.
    Ulmer TS, Bax A (2005) J Biol Chem 280:43179–43187CrossRefGoogle Scholar
  155. 155.
    Ulmer TS, Bax A, Cole NB, Nussbaum RL (2005) J Biol Chem 280:9595–9603CrossRefGoogle Scholar
  156. 156.
    Uversky VN (1993) Biochemistry 32:13288–13298CrossRefGoogle Scholar
  157. 157.
    Uversky VN (1999) Biochemistry (Mosc) 64:250–266Google Scholar
  158. 158.
    Uversky VN (2002) Eur J Biochem 269:2–12CrossRefGoogle Scholar
  159. 159.
    Uversky VN (2002) Protein Sci 11:739–756CrossRefGoogle Scholar
  160. 160.
    Uversky VN (2003) In: Pandalai SG (ed) Recent research developments in biophysics & biochemistry. Transworld Research Network, Kerala, pp 711–745Google Scholar
  161. 161.
    Uversky VN (2003) Cell Mol Life Sci 60:1852–1871CrossRefGoogle Scholar
  162. 162.
    Uversky VN, Ptitsyn OB (1994) Biochemistry 33:2782–2791CrossRefGoogle Scholar
  163. 163.
    Uversky VN, Ptitsyn OB (1996) Fold Des 1:117–122CrossRefGoogle Scholar
  164. 164.
    Uversky VN, Ptitsyn OB (1996) J Mol Biol 255:215–228CrossRefGoogle Scholar
  165. 165.
    Uversky VN, Fink AL (1999) Biochemistry (Mosc) 64:552–555Google Scholar
  166. 166.
    Uversky VN, Winter S, Lober G (1996) Biophys Chem 60:79–88CrossRefGoogle Scholar
  167. 167.
    Uversky VN, Gillespie JR, Fink AL (2000) Proteins 41:415–427CrossRefGoogle Scholar
  168. 168.
    Uversky VN, Li J, Fink AL (2001) J Biol Chem 276:44284–44296CrossRefGoogle Scholar
  169. 169.
    Uversky VN, Li J, Fink AL (2001) FEBS Lett 509:31–35CrossRefGoogle Scholar
  170. 170.
    Uversky VN, Li J, Fink AL (2001) J Biol Chem 276:10737–10744CrossRefGoogle Scholar
  171. 171.
    Uversky VN, Li J, Fink AL (2001) FEBS Lett 500:105–108CrossRefGoogle Scholar
  172. 172.
    Uversky VN, Oldfield CJ, Dunker AK (2005) J Mol Recognit 18:343–384CrossRefGoogle Scholar
  173. 173.
    Uversky VN, Segel DJ, Doniach S, Fink AL (1998) Proc Natl Acad Sci USA 95:5480–5483CrossRefGoogle Scholar
  174. 174.
    Uversky VN, Li J, Bower K, Fink AL (2002) Neurotoxicology 23:527–536CrossRefGoogle Scholar
  175. 175.
    Uversky VN, Narizhneva NV, Kirschstein SO, Winter S, Lober G (1997) Fold Des 2:163–172CrossRefGoogle Scholar
  176. 176.
    Uversky VN, Cooper EM, Bower KS, Li J, Fink AL (2002) FEBS Lett 515:99–103CrossRefGoogle Scholar
  177. 177.
    Uversky VN, Karnoup AS, Segel DJ, Seshadri S, Doniach S, Fink AL (1998) J Mol Biol 278:879–894CrossRefGoogle Scholar
  178. 178.
    Uversky VN, Karnoup AS, Khurana R, Segel DJ, Doniach S, Fink AL (1999) Protein Sci 8:161–173Google Scholar
  179. 179.
    Uversky VN, Permyakov SE, Zagranichny VE, Rodionov IL, Fink AL, Cherskaya AM, Wasserman LA, Permyakov EA (2002) J Proteome Res 1:149–159CrossRefGoogle Scholar
  180. 180.
    Uversky VN, Gillespie JR, Millett IS, Khodyakova AV, Vasiliev AM, Chernovskaya TV, Vasilenko RN, Kozlovskaya GD, Dolgikh DA, Fink AL, Doniach S, Abramov VM (1999) Biochemistry 38:15009–15016CrossRefGoogle Scholar
  181. 181.
    Uversky VN, Gillespie JR, Millett IS, Khodyakova AV, Vasilenko RN, Vasiliev AM, Rodionov IL, Kozlovskaya GD, Dolgikh DA, Fink AL, Doniach S, Permyakov EA, Abramov VM (2000) Biochem Biophys Res Commun 267:663–668CrossRefGoogle Scholar
  182. 182.
    Vacic V, Uversky VN, Dunker AK, Lonardi S (2007) BMC Bioinformatics 8:211CrossRefGoogle Scholar
  183. 183.
    van Rooijen BD, Claessens MM, Subramaniam V (2008) FEBS Lett 582:3788–3792CrossRefGoogle Scholar
  184. 184.
    Volles MJ, Lee SJ, Rochet JC, Shtilerman MD, Ding TT, Kessler JC, Lansbury PT Jr (2001) Biochemistry 40:7812–7819CrossRefGoogle Scholar
  185. 185.
    Weinreb PH, Zhen W, Poon AW, Conway KA, Lansbury PT Jr (1996) Biochemistry 35:13709–13715CrossRefGoogle Scholar
  186. 186.
    Wilkinson KD, Mayer AN (1986) Arch Biochem Biophys 250:390–399CrossRefGoogle Scholar
  187. 187.
    Williams RM, Obradovi Z, Mathura V, Braun W, Garner EC, Young J, Takayama S, Brown CJ, Dunker AK (2001) Pac Symp Biocomput, pp 89–100Google Scholar
  188. 188.
    Wright PE, Dyson HJ (1999) J Mol Biol 293:321–331CrossRefGoogle Scholar
  189. 189.
    Wu H, Maciejewski MW, Marintchev A, Benashski SE, Mullen GP, King SM (2000) Nat Struct Biol 7:575–579CrossRefGoogle Scholar
  190. 190.
    Wu LC, Laub PB, Elove GA, Carey J, Roder H (1993) Biochemistry 32:10271–10276CrossRefGoogle Scholar
  191. 191.
    Yancey PH, Clark ME, Hand SC, Bowlus RD, Somero GN (1982) Science 217:1214–1222CrossRefGoogle Scholar
  192. 192.
    Zhao R, Gish K, Murphy M, Yin Y, Notterman D, Hoffman WH, Tom E, Mack DH, Levine AJ (2000) Genes Dev 14:981–993CrossRefGoogle Scholar
  193. 193.
    Zhu M, Fink AL (2003) J Biol Chem 278:16873–16877CrossRefGoogle Scholar
  194. 194.
    Zhu M, Li J, Fink AL (2003) J Biol Chem 278:40186–40197CrossRefGoogle Scholar
  195. 195.
    Zimmerman SB, Trach SO (1991) J Mol Biol 222:599–620CrossRefGoogle Scholar
  196. 196.
    Zimmerman SB, Minton AP (1993) Annu Rev Biophys Biomol Struct 22:27–65CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Institute for Intrinsically Disordered Protein Research, The Center for Computational Biology and Bioinformatics, and The Department of Biochemistry and Molecular BiologyIndiana University School of MedicineIndianapolisUSA
  2. 2.Institute for Biological InstrumentationRussian Academy of SciencesPushchino, Moscow RegionRussia

Personalised recommendations