p25α is flexible but natively folded and binds tubulin with oligomeric stoichiometry

Protein Science

Volumn 14, Issue 6, 2005, Pages 1396-1409

  Otzen, Daniel E ^a   Lundvig, Ditte M S ^b   Wimmer, Reinhard ^a   Nielsen, Lotte H ^b   Pedersen, Jakob R ^a   Jensen, Poul H ^b  

^a AALBORG UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

Binding stoichiometry; Flexibility; Folding kinetics; Natively unfolded protein; Stability; Tubulin

Indexed keywords

ALIPHATIC COMPOUND; AMIDE; PROTEIN P25; PROTON; TUBULIN; UREA; NERVE PROTEIN; P25 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; DELETION MUTANT; GEL FILTRATION; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SOLVENT EFFECT; STOICHIOMETRY; CHEMISTRY; HUMAN; METABOLISM; MICROTUBULE;

HUMANS; MICROTUBULES; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN FOLDING; TUBULIN;

EID: 22444431956     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.041285605     Document Type: Article

References (53)

1. Andrade, M.A., Chacón, P., Merelo, J.J., and Morán, F. 1993. Evaluation of secondary structure of proteins from UV circular dichroism using an unsupervised learning neural network. Protein Eng. 6: 383-390.
2. Baldwin, R. 1996. On-pathway versus off-pathway folding intermediates. Fold. Des. 1: R1-R8.
3. Buck, M., Radford, S.E., and Dobson, C.M. 1993. A partially folded state of hen egg white lysozyme in trifluoroethanol: Structural characterization and implications for protein folding. Biochemistry 32: 669-678.
4. Capaldi, A.P., Shastry, M.C., Kleanthous, C., Roder, H., and Radford, S.E. 2001. Ultrarapid mixing experiments reveal that Im7 folds via an on-pathway intermediate. Nat. Struct. Biol. 8: 68-72.
5. Chiti, F., Taddei, N., Bucciantini, M., White, P., Ramponi, G., and Dobson, C.M. 2000. Mutational analysis of the propensity for amyloid formation by a globular protein. EMBO J. 19: 1441-1449.
6. Clarke, J. and Fersht, A.R. 1993. Engineered disulfide bonds as probes of the folding pathway of barnase: Increasing the stability of proteins against the rate of denaturation. Biochemistry 32: 4322-4329.
7. De Prat Gay, G., Ruiz-Sanz, J., Neira, J.L., Corrales, F.J., Otzen, D.E., Ladurner, A.G., and Fersht, A.R. 1995. Conformational pathway of the polypeptide chain of CI2 growing from its N-terminus in vitro. Parallels with the protein folding pathway. J. Mol. Biol. 254: 968-979.
8. Dunker, A.K., Lawson, J.D., Brown, C.J., Williams, R.M., Romero, P., Oh, J.S., Oldfield, C.J., Campen, A.M., Ratliff, C.M., and Hipps, K.W., et al. 2001. Intrinsically disordered protein. J. Mol. Graph. Model. 19: 26-59.
9. Dunker, A.K., Brown, C.J., Lawson, J.D., Iakoucheva, L.M., and Obradovic, Z. 2002a. Intrinsic disorder and protein function. Biochemistry 41: 6573-6580.
10. Dunker, A.K., Brown, C.J., and Obradovic, Z. 2002b. Identification and functions of usefully disordered proteins. Adv. Prot. Chem. 62: 25-49.
11. Dyson, H.J. and Wright, P.E. 2002. Coupling of folding and binding for unstructured protein. Curr. Opin. Struct. Biol. 12: 54-60.
12. Fersht, A.R. 1999. Structure and mechanism in protein science. A guide to enzyme catalysis and protein folding. Freeman & Co. New York.
13. Gill, S.C. and von Hippel, P.H. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182: 319-326.
14. Goto, Y. and Fink, A.L. 1989. Conformational states of β-lactamase molten-globule states at acidic and alkaline pH with high salt. Biochemistry 28: 945-952.
15. Hamill, S.J., Meekhof, A.E., and Clarke, J. 1998. The effect of boundary selection on the stability and folding of the third fibronectin type III domain from human tenascin. Biochemistry 37: 8071-8079.
16. Hlavanda, E., Kovacs, J., Olah, J., Orosz, F., Medzihradszky, K.F., and Ovadi, J. 2002. Brain-specific p25 protein binds to tubulin and microtubules and induces aberrant microtubule assemblies at substoichiometric concentrations. Biochemistry 41: 8657-8664.
17. Jackson, S.E. and Fersht, A.R. 1991. Folding of chymotrypsin inhibitor 2. 1: Evidence for a two-state transition. Biochemistry 30: 10428-10435.
18. Jackson, S.E., Moracci, M., elMasry, N., Johnson, C.M., and Fersht, A.R. 1993. Effect of cavity-creating mutations in the hydrophobic core of chymotrypsin inhibitor 2. Biochemistry 32: 11259-11269.
19. Kovacs, G.G., Laszlo, L., Kovacs, J., Jensen, P.H., Lindersson, E., Boton, G., Molnar, T., Perczel, A., Hudecz, F., and Mezö, G. et al. 2004. Natively unfolded tubulin polymerization promoting protein TPPP/p25 is a common marker of α-synucleinopathies. Neurobiol. Dis. 17: 155-162.
20. Kumar, Y., Tayyab, S., and Muzammil, S. 2004. Molten-globule like partially folded states of human serum albumin induced by fluoro and alkyl alcohols at low pH. Arch. Biochem. Biophys. 426: 3-10.
21. Lacy, E.R., Filippov, I., Lewis, W.S., Otieno, S., Xiao, L., Weiss, S., Hengst, L., and Kriwacki, R.W. 2004. p27 binds cyclin-CDK complexes through a sequential mechanism involving binding-induced protein folding. Nat. Struct. Mol. Biol. 11: 358-364.
22. Lakowicz, J.R. 1999. Principles of fluorescence spectroscopy, 2nd ed. Kluwer Academic/Plenum Publishers, New York.
23. Lee, L.K., Stollar, E., Chang, J.G., Grossman, R., O'Brien, J., Ladbury, B., Carpenter, S., Roberts, S., and Luisi, B. 2001. Expression of the Oct-1 transcription factor and characterization of its interactions with the Bob1 coactivator. Biochemistry 40: 6580-6588.
24. Lindersson, E., Lundvig, D., Petersen, C., Madsen, P., Højrup, P., Moos, T., Otzen, D.E., Gai, W.-P., and Jensen, P.H. 2005. P25a is coexpressed with α-synuclein in α-synucleinopathies and stimulates its aggregation. J. Biol. Chem. 280: 5703-5715.
25. Martin, C.P., Vazquez, J., Avila, J., and Moreno, F.J. 2002. P24, a glycogen synthase kinase 3 (GSK 3) inhibitor. Biochim. Biophys. Acta 1586: 113-122.
26. Matouschek, A., Kellis, J.T., Serrano, L., Bycroft, M., and Fersht, A.R. 1990. Transient folding intermediates characterized by protein engineering. Nature 346: 440-445.
27. Matouschek, A., Serrano, L., and Fersht, A.R. 1992. The folding of an enzyme IV. Structure of the intermediate in the refolding of barnase analysed by a protein engineering procedure. J. Mol. Biol. 224: 819-835.
28. Mogensen, J.E., Ibsen, H., Lund, J., and Otzen, D.E. 2004. Elimination of an off-pathway folding intermediate by a single point mutation. Biochemistry 43: 3357-3367.
29. Muro-Pastor, M.I., Barrera, F.N., Reyes, J.C., Florencio, F.J., and Neira, J.L. 2003. The inactivating factor of glutamine synthetase, IF7, is a "natively unfolded" protein. Protein Sci. 12: 1443-1454.
30. Nölting, B., Golbik, R., Neira, J.L., Soler-Gonzalez, A.S., Schreiber, G., and Fersht, A.R. 1997. The folding pathway of a protein at high resolution from microseconds to seconds. Proc. Natl. Acad. Sci. 94: 826-830.
31. Orosz, F., Kovacs, G.G., Lehotzky, A., Olah, J., Vincze, O., and Ovadi, J. 2004. TPPP/p25: From unfolded protein to misfolding disease: Prediction and experiments. Biol. Cell 96: 701-711.
32. Otzen, D.E. and Oliveberg, M. 1999. Salt-induced detour through compact regions of the protein folding landscape. Proc. Nat. Acad. Sci. 96: 11746-11751.
33. Pace, C.N. 1986. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131: 266-279.
34. _. 1990. Conformational stability of globular proteins. Trends Biochem. Sci. 15: 14-17.
35. Parker, M.J., Spencer, J., and Clarke, A.R. 1995. An integrated kinetic analysis of intermediates and transition states in protein folding reactions. J. Mol. Biol. 253: 771-786.
36. Parker, M.J., Dempsey, C.E., Hosszu, L.L.P., Waltho, J.P., and Clarke, A.R. 1998. Topology, sequence evolution and folding dynamics of an immunoglobulin domain. Nat. Struct. Biol. 5: 194-198.
37. Seki, N., Hattori, N., Sugano, S., Suzuki, Y., Nakagawara, A., Muramatsu, M., Hori, T., and Saito, T. 1999. A novel human gene whose product shares significant homology with the bovine brain-specific protein p25 on chromosome 5p15.3. J. Hum. Genet. 44: 121-122.
38. Semisotnov, G.V., Rodinova, N.A., Razgulyaev, O.I., Uversky, V.N., Gripas, A.F., and Gilmanshin, R.I. 1991. Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 31: 119-128.
39. Shiratsuchi, A., Sato, S., Oomori, A., Ishiguro, K., Uchida, T., and Imahori, K. 1995. cDNA cloning of a novel brain-specific protein p25. Biochim. Biophys. Acta 1251: 66-68.
40. Shoemaker, B.A., Portman, J.J., and Wolynes, P.G. 2000. Speeding molecular recognition by using the folding funnel: The fly-casting mechanism. Proc. Natl. Acad. Sci. 97: 8868-8873.
41. Takahashi, M., Tomizawa, K., Ishiguro, K., Sato, K., Omori, A., Sato, S., Shiratsuchi, A., Uchida, T., and Imahori, K. 1991. A novel brain-specific 25 kDa protein (p25) is phosphorylated by a Ser-Thr-Pro kinase (Tpk-Ii) from tau protein-kinase fractions. FEBS Lett. 289: 37-43.
42. Tanford, C. 1970. Protein denaturation. Part C. Theoretical models for the mechanism of denaturation. Adv. Prot. Chem. 24: 1-95.
43. Timasheff, S. 2002. Protein hydration, thermodynamic binding, and preferential hydration. Biochemistry 41: 13473-13482.
44. Tirian, L., Hlavanda, E., Olah, J., Horvath, I., Orosz, F., Szabo, B., Kovacs, J., Szabad, J., and Ovadi, J. 2003. TPPP/p25 promotes tubulin assemblies and blocks mitotic spindle formation. Proc. Natl. Acad. Sci. 100: 13976-13981.
45. Tompa, P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27: 527-533.
46. Tsai, C.-J., De Laureto, P.P., Fontana, A., and Nussinov, R. 2002. Comparison of protein fragments identified by limited proteolysis and by computational cutting of proteins. Protein Sci. 11: 1753-1770.
47. Uversky, V.N. 2003. A protein-chameleon: Conformational plasticity of a-synuclein, a disordered protein involved in neurodegenerative disorders. J. Biomol. Struct. Dyn. 21: 211-234.
48. Uversky, V.N. and Narizhneva, N.V. 1998. Effect of natural ligands on the structural properties and conformational stability of proteins. Biochemistry (Moscow) 63: 420-433.
49. Uversky, V.N., Abdullaev, Z.K., Arseniev, A.S., Bocharov, E.V., Dolgikh, D.A., Latypov, R.F., Melnik, T.N., Vassilenko, K.S., and Kirpichnikov, M.P. 1999. Structure and stability of recombinant protein depend on the extra N-terminal methionine residue: S6 permutein from direct and fusion expression systems. Biochim. Biophys. Acta 1432: 324-332.
50. Uversky, V.N., Gillespie, J.R., and Fink, A.L. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41: 415-427.
51. Wolff, J. 1998. Promotion of microtubule assembly by oligocations: Cooperativity between charged groups. Biochemistry 37: 10722-10729.
52. Yokozeki, T., Homma, K., Kuroda, S., Kikkawa, U., Ohno, S., Takahashi, M., Imahori, K., and Kanaho, Y. 1998. Phosphatidic acid-dependent phosphorylation of a 29-kDa protein by protein kinase C α in bovine brain cytosol. J. Neurochem. 71: 410-417.
53. Zhang, Z., Wu, C.C., Huang, W.-N., Wang, S., Zhao, E., Huang, Q., Xie, Y., and Mao, Y. 2002. A novel human gene whose product shares homology with bovine brain-specific protein p25 is expressed in fetal brain but not in adult brain. J. Hum. Genet. 47: 266-268.