Biophysical characterization of the free IκBα ankyrin repeat domain in solution

Protein Science

Volumn 13, Issue 7, 2004, Pages 1767-1777

  Croy, Carrie Hughes ^a   Bergqvist, Simon ^a   Huxford, Tom ^a   Ghosh, Gourisankar ^a   Komives, Elizabeth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amide H 2H exchange; Ankyrin repeat domain; Functionally disordered proteins; I B ; MALDI TOF; Protein folding

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ANKYRIN; DEUTERIUM; HYDROGEN; I KAPPA B ALPHA; SOLVENT; TRANSCRIPTION FACTOR;

ARTICLE; BIOPHYSICS; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; DIFFERENTIAL SCANNING CALORIMETRY; MOLECULAR STABILITY; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; SPECTROSCOPY;

AMIDES; AMINO ACID MOTIFS; ANIMALS; ANKYRIN REPEAT; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; DEUTERIUM; HUMANS; HYDROGEN; I-KAPPA B PROTEINS; NF-KAPPA B; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSCRIPTION FACTOR RELA;

EID: 3042628330     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.04731004     Document Type: Article

References (49)

1. Baeuerle, P.A. and Baltimore, D. 1988. I κ B: A specific inhibitor of the NF-κ B transcription factor. Science 242: 540-546.
2. Bai, Y., Milne, J.S., Mayne, L., and Englander, S.W. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins 17: 75-86.
3. Baldwin, A.S. 1996. The NF-κ-B and I-κ-B proteins: New discoveries and insights. Annu. Rev. Immunol. 87: 13-20.
4. Baumgartner, R., Fernandez-Catalan, C., Winoto, A., Huber, R., Engh, R.A., and Holak, T.A. 1998. Structure of human cyclin-dependent kinase inhibitor p19INK4d: Comparison to known ankyrin-repeat-containing structures and implications for the dysfunction of tumor suppressor p16INK4a. Structure 6: 1279-1290.
5. Boice, J.A. and Fairman, R. 1996. Structural characterization of the tumor suppressor p16, an ankyrin-like repeat protein. Protein Sci. 5: 1776-1784.
6. Bork, P. 1993. Hundreds of ankyrin-like repeats in functionally diverse proteins: Mobile modules that cross phyla horizontally? Proteins 17: 363-374.
7. Breeden, L. and Nasmyth, K. 1987. Similarity of cell-cycle genes of budding yeast and fission yeast and the Notch gene in Drosophila. Nature 395: 651-654.
8. Byeon, I.J., Li, J., Ericson, K., Selby, T.L., Tevelev, A., Kim, H.J., O'Maille, P., and Tsai, M.D. 1998. Tumor suppressor p16INK4A: Determination of solution structure and analyses of its interaction with cyclin-dependent kinase 4. Mol. Cell 1: 421-431.
9. Chen, Z., Hagler, J., Palombella, V.J., Melandri, F., Scherer, D., Ballard, D., and Maniatis, T. 1995. Signal-induced site-specific phosphorylation targets I κ B α to the ubiquitin-proteasome pathway. Genes & Dev. 9: 1586-1597.
10. Foord, R., Taylor, I.A., Sedgwick, S.G., and Smerdon, S.J. 1999. X-ray structural analysis of the yeast cell cycle regulator Swi6 reveals variations of the ankyrin fold and has implications for Swi6 function. Nat. Struct. Biol. 6. 157-165.
11. Forrer, P., Stumpp, M.T., Binz, H.K., and Pluckthun, A. 2003. A novel strategy to design binding molecules harnessing the modular nature of repeat proteins. FEBS Lett. 539: 2-6.
12. Ghosh, G., van Duyne, G., Ghosh, S., and Sigler, P.B. 1995. Links structure of NF-λ B p50 homodimer bound to a κ B site. Nature 373: 303-310.
13. Ghosh, S., May, M.J., and Kopp, E.B. 1998. NF-κ B and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260.
14. Groves, M.R. and Barford, D. 1999. Topological characteristics of helical repeat proteins. Curr. Opin. Struct. Biol. 9: 383-389.
15. Hoffmann, A., Levchenko, A., Scott, M.L., and Baltimore. D. 2002. The IκB-NF-κB signaling module: Temporal control and selective gene activation. Science 298: 1241-1245.
16. Huang, D.B., Huxford, T., Chen, Y.Q., and Ghosh, G. 1997. The role of DNA in the mechanism of NFκB dimer formation: Crystal structures of the dimerization domains of the p50 and p65 subunits. Structure 15: 1427-1436.
17. Hughes, C.A., Mandell, J.G., Anand, G.S., Stock, A.M., and Komives, E.A. 2001. Phosphorylation causes subtle changes in solvent accessibility at the interdomain interface of methylesterase CheB. J. Mol. Biol. 307: 967-976.
18. Huxford, T., Huang, D.B., Malek, S., and Ghosh, G. 1998. The crystal structure of the IκBα/NF-κB complex reveals mechanisms of NF-κB inactivation. Cell 95: 759-770.
19. Jacobs, M.D. and Harrison, S.C. 1998. Structure of an IκBα/NF-κB complex. Cell 95: 749-758.
20. Kalus, W., Baumgartner, R., Renner, C., Noegel, A., Chan, F.K., Winoto, A., and Holak, T.A. 1997. NMR structural characterization of the CDK inhibitor p19INK4d. FEBS Lett. 401: 127-132.
21. Kohl, A., Binz, H.K., Forrer, P., Stumpp, M.T., Pluckthun, A., and Grutter, M.G. 2003. Designed to be stable: Crystal structure of a consensus ankyrin repeat protein. Proc. Nat. Acad. Sci. 100: 1700-1705.
22. Kriwacki, R.W., Hengst, L., Tennant, L., Reed, S.I., and Wright, P.E. 1996. Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: Conformational disorder mediates binding diversity. Proc. Natl. Acad. Sci. 93: 11504-11509.
23. Li, J., Byeon, I.J., Ericson, K., Poi, M.J., O'Maille, P., Selby, T., and Tsai, M.D. 1999. Tumor suppressor INK4: Determination of the solution structure of p18INK4C and demonstration of the functional significance of loops in p18INK4C and p16INK4A. Biochemistry 38: 2930-2940.
24. Luh, F.Y., Archer, S.J., Domaille, P.J., Smith, B.O., Owen, D., Brotherton, D.H., Raine, A.R., Xu, X., Brizuela, L., Brenner, S.L., et al. 1997. Structure of the cyclin-dependent kinase inhibitor p19Ink4d. Nature 389: 999-1003.
25. Mandell, J.G., Falick, A.M., and Komives, E.A. 1998a. Identification of protein-protein interfaces by decreased amide proton solvent accessibility. Proc. Natl. Acad. Sci. 95: 14705-14710.
26. -. 1998b. Measurement of amide hydrogen exchange by MALDI-TOF mass spectrometry. Anal. Chem. 70: 3987-3995.
27. Mandell, J.G., Baerga-Ortiz, A., Akashi, S., Takio, K., and Komives, E.A. 2001. Solvent accessibility of the thrombin-thrombomodulin interface. J. Mol. Biol. 306: 575-589.
28. Michaely, P. and Bennett, V. 1993. The membrane-binding domain of ankyrin contains four independently folded subdomains, each comprised of six ankyrin repeats. J. Biol. Chem. 268: 22703-22709.
29. Michel, F., Soler-Lopez, M., Petosa, C., Cramer, P., Siebenlist, U., and Muller, C.W. 2001. Crystal structure of the ankyrin repeat domain of Bcl-3: A unique member of the IκB protein family. EMBO J. 20: 6180-6190.
30. Mosavi, L.K., Minor Jr., D.L., and Peng, Z.Y. 2002a. Consensus-derived structural determinants of the ankyrin repeat motif. Proc. Natl. Acad. Sci. 99: 16029-16034.
31. Mosavi, L.K., Williams, S., and Peng, Z.Y. 2002b. Equilibrium folding and stability of myotrophin: A model ankyrin repeat protein. J. Mol. Biol. 320: 165-170.
32. Muller, C.W., Rey, F.A., Sodeoka, M., Verdine, G.L., and Harrison, S.C. 1995. Structure of the NF-κ B p50 homodimer bound to DNA. Nature 373: 311-317.
33. Pando, M.P. and Verma, I.M. 2000. Signal-dependent and -independent degradation of free and NF-κ B bound IκBα. J. Biol. Chem. 275: 21278-21286.
34. Phelps, C.B., Sengchanthalangsy, L.L., Huxford, T., and Ghosh, G. 2000. Mechanism of IκBα Binding to NF-κB dimers. J. Biol. Chem. 275: 29840-29846.
35. Ramboarina, S. and Redfield, C. 2003. Structural characterisation of the human α-lactalbumin molten globule at high temperature. J. Mol. Biol. 330: 1177-1188.
36. Semisotnov, G.V., Rodionova, 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.
37. 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.
38. Simeonidis, S., Liang, S., Chen, G., and Thanos, D. 1997. Cloning and functional characterization of mouse IκBε. Proe. Natl. Acad. Sci. 94: 14372-14377.
39. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185: 60-89.
40. Tang, K.S., Guralnick, B.J., Wang, W.K., Fersht, A.R., and Itzhaki, L.S. 1999. Stability and folding of the tumour suppressor protein p16. J. Mol. Biol. 285: 1869-1886.
41. INK4a: Structural characterization of wild-type and mutant proteins by NMR and circular dichroism. Biochemistry 35: 9475-9487.
42. Tran, K., Merika, M., and Thanos. D. 1997. Distinct functional properties of IκB α and IκB β. Mol. Cell Biol. 17: 5386-5399.
43. Venkataramani, R., Swaminathan, K., and Marmorstein, R. 1998. Crystal structure of the CDK4/6 inhibitory protein p18INK4c provides insights into ankyrin-like repeat structure/function and tumor-derived p16INK4 mutations. Nat. Struct. Biol. 5: 74-81.
44. Yang, Y., Nanduri, S., Sen, S., and Qin, J. 1998. The structural basis of ankyrin-like repeat function as revealed by the solution structure of myotrophin. Structure 6: 619-626.
45. Yuan, C., Li, J., Selby, T.L., Byeon, I.J., and Tsai, M.D. 1999. Tumor suppressor INK4: Comparisons of conformational properties between p16(INK4A) and p18(INK4C). J. Mol. Biol. 294: 201-211.
46. Zeeb, M., Rosner, H., Zeslawski, W., Canet, D., Holak, T.A., and Balbach, J. 2002. Protein folding and stability of human CDK inhibitor p19(INK4d). J. Mol. Biol. 315: 447-457.
47. Zhang, B. and Peng, Z. 1996. Defective folding of mutant p16(INK4) proteins encoded by tumor-derived alleles. J. Biol. Chem. 271: 28734-28737.
48. -. 2000. A minimum folding unit in the ankyrin repeat protein p16(INK4). J. Mol. Biol. 299: 1121-1132.
49. Zweifel, M.E. and Barrick, D. 2001. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 2. Solution stability and cooperativity of unfolding. Biochemistry 40: 14357-14367.