Continuous thermal collapse of the intrinsically disordered protein tau is driven by its entropic flexible domain

Langmuir

Volumn 28, Issue 37, 2012, Pages 13405-13410

  Ciasca, Gabriele ^a   Campi, Gaetano ^b   Battisti, Anna ^c   Rea, Giuseppina ^b   Rodio, Marina ^a   Papi, Massimiliano ^d   Pernot, Petra ^e   Tenenbaum, Alexander ^a   Bianconi, Antonio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF TRENTO   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; BINDING DOMAIN; BIOLOGICAL STUDIES; DISORDERED PROTEINS; FOLDED STRUCTURES; MICROTUBULES; MOLECULAR DYNAMICS SIMULATIONS; MOLECULAR MECHANISM; N-TERMINAL DOMAINS; NATIVE STATE; OPTIMIZATION METHOD; PAIRED HELICAL FILAMENTS; PHYSIOLOGICAL STATE; PROJECTION DOMAIN; PROLINE-RICH DOMAINS; REPULSIVE FORCES; SMALL ANGLE X-RAY SCATTERING; STRUCTURAL INFORMATION; TAU PROTEINS; TEMPERATURE VARIATION; TWO DOMAINS;

AMINO ACIDS; MOLECULAR DYNAMICS;

NEURONS;

TAU PROTEIN;

ADSORPTION; ARTICLE; CHEMISTRY; ENTROPY; HUMAN; MOLECULAR DYNAMICS; SURFACE PROPERTY; TEMPERATURE;

ADSORPTION; ENTROPY; HUMANS; MOLECULAR DYNAMICS SIMULATION; SURFACE PROPERTIES; TAU PROTEINS; TEMPERATURE;

EID: 84866423020     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la302628y     Document Type: Article

References (32)

1. Tompa, P. Structure and Function of Intrinsically Disorderd Proteins; Taylor Francis Group: Boca Raton, FL, 2010.
2. Nettels, D; Mueller-Spaeth, S.; Kuester, F.; Hofmann, H; Haenni, D.; Rueegger, S; Reymond, L; Hofmann, A; Kubelka, J; Heinz, B; Gast, K; Best, R.-B.; Schuler, B. Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 20740-20745
3. Uversky, V. Intrinsically Disordered Proteins and Their Environment: Effects of Strong Denaturants, Temperature, pH, Counter Ions, Membranes, Binding Partners, Osmolytes, and Macromolecular Crowding Protein J. 2009, 28, 305-325
4. Shkumatov, A.-V.; Chinnathambi, S.; Mandelkow, E.; Svergun, D.-I. Structural memory of natively unfolded tau protein detected by small-angle X-ray scattering Proteins: Struct., Funct., Bioinf. 2011, 79, 2122-2131
5. Sadqi, M.; Lapidus, L.-J.; Muoz, V. How fast is protein hydrophobic collapse? Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 12117-12122
6. Noppert, A.; Gast, K.; Marlies, M.-F.; Zirwer, D.; Damaschun, G. Reduced-denatured ribonuclease A is not in a compact state FEBS Lett. 1996, 380, 179-182
7. Gast, K.; Zirwer, D.; Damaschun, H.; Hahn, U.; Marlies, M.-F.; Wirth, M.; Damaschun, G. Ribonuclease T1 has different dimensions in the thermally and chemically denatured states: a dynamic light scattering study FEBS Lett. 1997, 403, 245-248
8. Tompa, P. Intrinsically unstructured protein Trends Biochem. Sci. 2002, 27, 527-533
9. Goedert, M.; Spillantini, M.-G.; Potier, M.-C.; Ulrich, J.; Crowther, R.-A. Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain EMBO J. 1989, 8, 393-399
10. Rosenberg, K.-J.; Kenneth, J.; Ross, J.-L.; Feinstein, H.-E.; Feinstein, S.-C.; Israelachvili, J. Complementary dimerization of microtubule-associated tau protein: Implications for microtubule bundling and tau-mediated pathogenesis Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 7445-7450
11. Avila, J.; Lucas, J.-J.; Prez, M.; Hernández, F. Role of Tau Protein in Both Physiological and Pathological Conditions Physiol. Rev. 2004, 84, 361-384
12. von Bergen, M.; Barghorn, S.; Biernat, J.; Mandelkow, E.-M.; Mandelkow, E. Tau aggregation is driven by a transition from random coil to beta sheet structure Biochim. Biophys. Acta, Mol. Basis Dis. 2005, 1739, 158-166
13. 311) forming β structure Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 5129-5134
14. Mukrasch, M.-D.; Bibow, S.; Korukottu, J.; Jeganathan, J.; Sadasivam, J.; Biernat, J.; Griesinger, C.; Mandelkow, E.; Zweckstetter, M. Structural Polymorphism of 441-Residue Tau at Single Residue Resolution PLoS Biol. 2009, 7 (e1000034) 0399-0414
15. Spires-Jones, T.-L; Stoothoff, W.-H.; de Calignon, A.; Jones, P.-B.; Hyman, B.-T. Tau pathophysiology in neurodegeneration: a tangled issue Trends Neurosci. 2009, 32, 150-159
16. Svergun, D.; Koch, M. Small-angle scattering studies of biological macromolecules in solution Rep. Prog. Phys. 2003, 66, 1735-1782
17. Ciasca, G.; Papi, M.; Chiarpotto, M.; Rodio, M.; Campi, G.; Rossi, C.; De Sole, P.; Bianconi, A. Transient state kinetic investigation of ferritin iron release Appl. Phys. Lett. 2012, 100 (073703) 1-3
18. De Spirito, M; Arcovito, G.; Papi, M.; Rocco, M.; Ferri, F. Small- and wide-angle elastic light scattering study of fibrin structure J. Appl. Crystallogr. 2003, 36, 636-641
19. Caracciolo, G.; Pozzi, D.; Caminiti, R.; Amenitsch, H. Lipid mixing upon deoxyribonucleic acid-induced liposomes fusion investigated by small-angle x-ray scattering Appl. Phys. Lett. 2005, 87, 133901
20. Campi, G.; Ricci, A.; Guagliardi, A.; Giannini, C.; Lagomarsino, S.; Cancedda, R.; Mastrogiacomo, M.; Cedola, A. Early stage mineralization in tissue engineering mapped by high resolution X-ray microdiffraction Acta Biomater. 2012, 8, 3411-3418
21. Mylonas, E.; Hascher, A.; Bernadó, P.; Blackledge, M.; Mandelkow, E.; Svergun, D.-I. Domain Conformation of Tau Protein Studied by Solution Small-Angle X-ray Scattering Biochemistry 2008, 47, 10345-10353
22. Schweers, O.; Schoenbrunn-Hanebeck, E.; Marx, A.; Mandelkow, E. Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure J. Biol. Chem. 1994, 269, 24290-24297
23. Bernadó, P.; Mylonas, E.; Petoukhov, M.-V.; Blackledge, M.; Svergun, D.-I. Structural Characterization of Flexible Proteins Using Small-Angle X-ray Scattering J. Am. Chem. Soc. 2007, 129, 5656-5664
24. Laemmli, U.-K. Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 Nature 1970, 227, 680-685
25. Pernot, P.; Theveneau, P.; Giraud, T.; Nogueira, R.-F.; Nurizzo, D.; Spruce, D.; Surr, J.; McSweeney, S.; Round, A.; Felisaz, F.; Foedinger, L.; Gobbo, A.; Huet, J.; Villard, C.; Cipriani, F. New beamline dedicated to solution scattering from biological macromolecules at the ESRF J. Phys.: Conf. Ser. 2010, 247, 012009
26. EOM manual, http://www.embl-hamburg.de/biosaxs/eom.html.
27. 3; G53a6 force field; time step 2 fs; modified Berendsen thermostat, Parrinello-Rahman pressure coupling.
28. Battisti, A.; Tenenbaum, A. Molecular Dynamics simulation of intrinsically disordered proteins Mol. Simul. 2012, 38, 139-143
29. Battisti, A.; Ciasca, G.; Grottesi, A.; Bianconi, A.; Tenenbaum, A. Temporary secondary structures in tau, an intrinsically disordered protein Mol. Simul. 2012, 38, 525-533
30. Kohn, J.-E.; Millett, I.-S.; Jacob, J.; Zagrovic, B.; Dillon, T.-M.; Cingel, N.; Dothager, R.-S.; Seifert, S.; Thiyagarajan, P.; Tobin, R.; Sosnick, T.-R.; Hasan, M.-Z.; Pande, V.-S.; Ruczinski, S.; Doniach, S.; Plaxco, K.-V. Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 12491-12496
31. Papi, M.; Arcovito, G.; De Spirito, M; Amiconi, G.; Bellelli, A.; Boumis, G. Simultaneous static and dynamic light scattering approach to the characterization of the different fibrin gel structures occurring by changing chloride concentration Appl. Phys. Lett. 2005, 86 (183901) 1-3
32. De Spirito, M.; Brunelli, R.; Mei, G.; Bertani, F.-R.; Ciasca, G.; Greco, G.; Papi, M.; Arcovito, G.; Ursini, F.; Parasassi, T. Low Density Lipoprotein Aged in Plasma Forms Clusters Resembling Subendothelial Droplets: Aggregation via Surface Sites Biophys. J. 2006, 90, 4239-4247