Temperature and solvent dependence of the dynamical landscape of tau protein conformations

Journal of Biological Physics

Volumn 38, Issue 1, 2012, Pages 169-179

  Bianconi, Antonio ^a   Ciasca, Gabriele ^a   Tenenbaum, Alexander ^a   Battisti, Anna ^b   Campi, Gaetano ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF TRENTO   (Italy)

^c CNR   (Italy)

Author keywords

Intrinsic disordered proteins; Protein conformations; Temperature effects in protein fluctuations; Water effect in conformational landscape

Indexed keywords

TAU PROTEIN;

ARTICLE; COMPUTER SIMULATION; CONTROLLED STUDY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; SOLVENT EFFECT; SYNCHROTRON RADIATION; TEMPERATURE DEPENDENCE; X RAY CRYSTALLOGRAPHY;

EID: 84857654901     PISSN: 00920606     EISSN: 15730689     Source Type: Journal    
DOI: 10.1007/s10867-011-9244-6     Document Type: Article

References (55)

1. G Careri P Fasella E Gratton 1975 Statistical time events in enzymes: a physical assessment CRC Crit. Rev. Biochem. 3 141 164 10.3109/10409237509102555
2. Careri, G.: Order and Disorder in Matter. Benjamin/Cummings Pub. Co., Advanced Book Program. ISBN: 9780805317251 (1984)
3. H Frauenfelder F Parak RD Young 1988 Conformational sub-states in proteins Ann. Rev. Biophys. Biophys. Chem. 17 451 479 10.1146/annurev.bb.17. 060188.002315
4. Bianconi, A., Oesh, B., Alemà, S., Castellani, L., Davoli, I., Fasella, P., Mobilio S.: Structure of the calcium binding sites in troponin-C and calmodulin studied by EXAFS. In: Siegel, F.L., et al. (eds.) Calcium Binding Proteins: Structure and Function, p. 297. Elsevier North Holland, Amsterdam (1980)
5. A Bianconi A Giovannelli L Castellani S Alemà P Fasella B Oesch S Mobilio 1983 XANES determination of calcium sites of troponin-C and parvalbumin J. Mol. Biol. 165 125 138 10.1016/S0022-2836(83)80246-0 http://view.ncbi.nlm. nih.gov/pubmed/6842603
6. A Bianconi S Doniach D Lublin 1978 X-ray Ca K edge of calcium adenosine triphosphate system and of simple Ca compounds Chem. Phys. Lett. 59 121 124 1978CPL....59..121B 10.1016/0009-2614(78)85629-2
7. S Della Longa A Soldatov M Pompa A Bianconi 1995 Atomic and electronic structure probed by X-ray absorption spectroscopy: Full multiple scattering analysis with the G4XANES package Comput. Mater. Sci. 4 199 210 10.1016/0927-0256(95)00027-N
8. RH Kretsinger 1980 Structure and evolution of calcium modulated proteins CRC Crit. Rev. Biochem. 8 119 174 10.3109/10409238009105467
9. 2∈+∈-calmodulin reveals flexible hand-like properties of its domains Nat. Struct. Mol. Biol. 8 990 997 10.1038/nsb1101-990 (Pubitemid 33032370)
10. SE Permyakov AG Bakunts AI Denesyuk EL Knyazeva VN Uversky EA Permyakov 2008 Apo-parvalbumin as an intrinsically disordered protein Proteins 72 822 836 10.1002/prot.21974 (Pubitemid 352000861)
11. V Motáčková J Nováček A Zawadzka-Kazimierczuk K Kazimierczuk L Zídek H Sanderová L Krásný W Koźmiński V Sklenář 2010 Strategy for complete NMR assignment of disordered proteins with highly repetitive sequences based on resolution-enhanced 5D experiments J. Biomol. NMR 48 169 177 10.1007/s10858-010-9447-3
12. I Bertini P Kursula C Luchinat G Parigi J Vahokoski M Willmans J Yuan 2009 Accurate solution structures of proteins from X-ray data and minimal set of NMR data: calmodulin peptide complexes as examples J. Am. Chem. Soc. 131 5134 5144 10.1021/ja8080764
13. G Chen PW Fenimore H Frauenfelder F Mezei J Swenson RD Young 2008 Protein fluctuations explored by inelastic neutron scattering and dielectric relaxation spectroscopy Phil. Mag. 88 3877 3883 2008PMag...88.3877C 10.1080/ 14786430802585117
14. G Careri A Giansanti JA Rupley 1986 Proton percolation on hydrated lysozyme powders Proc. Nat. Acad. Sci. USA 83 6810 6814 1986PNAS...83.6810C 10.1073/pnas.83.18.6810
15. HJ Dyson PE Wright 2005 Intrinsically unstructured proteins and their functions Nat. Rev. Mol. Cell Biol. 6 197 208 10.1038/nrm1589 (Pubitemid 40314921)
16. T Chouard 2011 Structural biology: breaking the protein rules Nature 471 151 153 10.1038/471151 2011Natur.471..151C 10.1038/471151a
17. MY Lobanov EI Furletova NS Bogatyreva MA Roytberg OV Galzitskaya 2010 Library of disordered patterns in 3D protein structures PLoS Comput. Biol. 6 e1000958+ 10.1371/journal.pcbi.1000958 (The data bank DisProt (www.disprot.org) lists about 650 intrinsically disordered proteins)
18. A-L Barabási ZN Oltvai 2004 Network biology: understanding the cell's functional organization Nat. Rev. Genet. 5 101 113 10.1038/nrg1272 (Pubitemid 38160277)
19. G Bianconi 2005 Emergence of weight-topology correlations in complex scale-free networks Europhys. Lett. 71 1029 1035 2005EL.....71.1029B 10.1209/epl/i2005-10167-2 (Pubitemid 41352692)
20. S Bradde F Caccioli L Dall'Asta G Bianconi 2010 Critical fluctuations in spatial complex networks Phys. Rev. Lett. 104 218701 2010PhRvL.104u8701B 10.1103/PhysRevLett.104.218701
21. K Sugase HJ Dyson PE Wright 2007 Mechanism of coupled folding and binding of an intrinsically disordered protein Nature 447 1021 1025 2007Natur.447.1021S 10.1038/nature05858 (Pubitemid 46975749)
22. CJ Oldfield J Meng JY Yang MQ Yang VN Uversky AK Dunker 2008 Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners BMC Genomics 9 Suppl 1 S1 10.1186/1471-2164-9-S1-S1 (Pubitemid 351833876)
23. S Brocca L Testa F Sobott M Šamalikova A Natalello E Papaleo M Lotti L De Gioia SM Doglia L Alberghina R Grandori 2011 Compaction properties of an intrinsically disordered protein: Sic1 and its kinase inhibitor domain Biophys. J. 100 2243 2252 2011BpJ...100.2243B 10.1016/j.bpj.2011.02.055
24. T Mittag S Orlicky W-Y Choy X Tang H Lin F Sicheri LE Kay M Tyers JD Forman-Kay 2008 Dynamic equilibrium engagement of a polyvalent ligand with a single-site receptor Proc. Nat. Acad. Sci. USA 105 17772 17777 2008PNAS..10517772M 10.1073/pnas.0809222105
25. LC Wang YX Pang T Holder JR Brender AV Kurochkin 2001 Functional dynamics in the active site of the ribonuclease binase Proc. Natl. Acad. Sci. USA 98 7684 7689 2001PNAS...98.7684W 10.1073/pnas.121069998 (Pubitemid 32642621)
26. EZ Eisenmesser DA Bosco M Akke D Kern 2002 Enzyme dynamics during catalysis Science 295 1520 1523 2002Sci...295.1520E 10.1126/science.1066176 (Pubitemid 34174006)
27. K Lindorff-Larsen RB Best MA DePristo CM Dobson M Vendruscolo 2005 Simultaneous determination of protein structure and dynamics Nature 433 128 132 2005Natur.433..128L 10.1038/nature03199
28. A Bianconi A Congiu-Castellano PJ Durham SS Hasnain S Phillips 1985 The CO bond angle of carboxymyoglobin determined by angular-resolved XANES spectroscopy Nature 318 685 687 10.1038/318685a0 1985Natur.318..685B 10.1038/318685a0 (Pubitemid 16172424)
29. A Ansari J Berendzen D Braunstein BR Cowen H Frauenfelder MK Hong IET Iben Johnson P Ormos TB Sauke 1987 Rebinding and relaxation in the myoglobin pocket Biophys. Chem. 26 337 355 10.1016/0301-4622(87)80034-0 (Pubitemid 17121463)
30. H Frauenfelder SG Sligar PG Wolynes 1991 The energy landscapes and motions of proteins Science 254 1598 1603 1991Sci...254.1598F 10.1126/science.1749933 (Pubitemid 21917496)
31. H Frauenfelder 2005 Energy landscape and dynamics of biomolecules J. Biol. Phys. 31 413 416 10.1007/s10867-005-0696-4 (Pubitemid 41758696)
32. A Bianconi F Natali ML Alosi S Grande A Lanzara NL Saini M Brunelli TDXAS 1999 study of the conformational landscape of MbCO J. Synchrotron Radiat. 6 389 391 10.1107/S0909049598017063
33. PW Fenimore H Frauenfelder BH McMahon FG Parak 2002 Slaving: Solvent fluctuations dominate protein dynamics and functions Proc. Nat. Acad. Sci. USA 99 16047 16051 2002PNAS...9916047F 10.1073/pnas.212637899 (Pubitemid 35462746)
34. P Fenimore H Frauenfelder B McMahon R Young 2005 Proteins are paradigms of stochastic complexity Phys. A: Stat. Mech. Appl. 351 1 13 10.1016/j.physa.2004.12.004 (Pubitemid 40391102)
35. H Frauenfelder PW Fenimore G Chen BH McMahon 2006 Protein folding is slaved to solvent motions Proc. Nat. Acad. Sci. USA 103 15469 15472 2006PNAS..10315469F 10.1073/pnas.0607168103 (Pubitemid 44625615)
36. KJ Rosenberg JL Ross HE Feinstein SC Feinstein J Israelachvili 2008 Complementary dimerization of microtubule-associated tau protein: implications for microtubule bundling and tau-mediated pathogenesis Proc. Natl. Acad. Sci. USA 105 7445 7450 2008PNAS..105.7445R 10.1073/pnas.0802036105 (Pubitemid 351830037)
37. J Avila JJ Lucas M Pérez F Hernández 2004 Role of tau protein in both physiological and pathological conditions Physiol. Rev. 84 361 384 10.1152/physrev.00024.2003 (Pubitemid 38365487)
38. TL Spires-Jones WH Stoothoff A de Calignon J Alix B Phillip BT Hyman 2008 Tau pathophysiology in neurodegeneration: a tangled issue Trends Neurosci. 32 150 159 10.1016/j.tins.2008.11.007
39. Tompa, P.: Intrinsically disordered proteins. In: Sussman, J., Silman, I. (eds.) Structural Proteomics and its Impact on the Life Sciences. World Scientific (2008)
40. V Uversky 2009 Intrinsically disordered proteins and their environment: effects of strong denaturants, temperature, pH, counter ions, membranes, binding partners, osmolytes, and macromolecular crowding The Protein J. 28 305 325 10.1007/s10930-009-9201-4
41. D Nettels S Müller-Späth F Küster H Hofmann D Haenni S Rüegger L Reymond A Hoffmann J Kubelka B Heinz K Gast RB Best B Schuler 2009 Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins Proc. Natl. Acad. Sci. USA 106 20740 20745 2009PNAS..10620740N 10.1073/pnas.0900622106
42. JE Kohn IS Millett J Jacob B Zagrovic TM Dillon N Cingel RS Dothager S Seifert P Thiyagarajan TR Sosnick MZ Hasan VS Pande I Ruczinski S Doniach KW Plaxco 2004 Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 101 12491 12496 2004PNAS..10112491K 10.1073/pnas.0403643101 (Pubitemid 39122051)
43. O Schweers E Schonbrunn-Hanebeck A Marx E Mandelkow 1994 Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure J. Biol. Chem. 269 24290 24297
44. Glatter, O., Kratky, O.: Small-angle X-ray Scattering. Academic Press (1982)
45. G Beaucage 1996 Small-angle scattering from polymeric mass fractals of arbitrary mass-fractal dimension J. Appl. Crystallogr. 29 134 146 10.1107/S0021889895011605 (Pubitemid 126466797)
46. P Pernot P Theveneau T Giraud R Nogueira Fernandes D Nurizzo D Spruce J Surr S McSweeney A Round F Felisaz L Foedinger A Gobbo J Huet C Villard F Cipriani 2010 New beamline dedicated to solution scattering from biological macromolecules at the ESRF J. Phys.: Conf. Ser. 247 012009 012028 2010JPhCS.247a2009P 10.1088/1742-6596/247/1/012009
47. A Battisti A Tenenbaum 2011 Molecular dynamics simulation of intrinsically disordered proteins Mol. Simulat. 10.1080/08927022.2011.608671
48. W Humphrey A Dalke K Schulten 1996 VMD - Visual Molecular Dynamics J. Mol. Graphics 14 33 38 10.1016/0263-7855(96)00018-5 (Pubitemid 26152973)
49. GROMACS release 4.5.3. www.gromacs.org
50. E Mylonas A Hascher P Bernado M Blackledge E Mandelkow DI Svergun 2008 Domain conformation of tau protein studied by solution small-angle X-ray scattering Biochemistry 47 10345 10353 10.1021/bi800900d
51. JW Caldwell PA Kollman 1995 Structure and properties of neat liquids using nonadditive molecular-dynamics - water, methanol, and N-methylacetamide J. Phys. Chem. 99 6208 6219 10.1021/j100016a067
52. 4∈+∈y Nature 466 841 844 2010Natur.466..841F 10.1038/nature09260
53. N Poccia M Fratini A Ricci G Campi L Barba A Vittorini-Orgeas G Bianconi G Aeppli A Bianconi 2011 Evolution and control of oxygen order in a cuprate superconductor Nat. Mater. 10 733 736 10.1038/nmat3088 2011NatMa..10..733P 10.1038/nmat3088
54. N Poccia A Ricci D Innocenti A Bianconi 2009 A possible mechanism for evading temperature quantum decoherence in living matter by Feshbach resonance Int. J. Mol. Sci. 10 2084 2106 10.3390/ijms10052084 10.3390/ijms10052084
55. N Poccia A Bianconi 2011 The physics of life and quantum complex matter: a case of cross-fertilization Life 1 3 6 10.3390/life1010003 10.3390/life1010003