Contributions of conserved TPLH tetrapeptides to the conformational stability of ankyrin repeat proteins

Journal of Molecular Biology

Volumn 399, Issue 1, 2010, Pages 168-181

  Guo, Yi ^a   Yuan, Chunhua ^a   Tian, Feng ^b   Huang, Kun ^a   Weghorst, Christopher M ^a,c   Tsai, Ming Daw ^a,d   Li, Junan ^a,c  

^a OHIO STATE UNIVERSITY   (United States)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c OHIO STATE UNIVERSITY   (United States)

^d INSTITUTE OF BIOLOGICAL CHEMISTRY   (Taiwan)

Author keywords

Ankyrin repeat; Gankyrin; P16; Stability; TPLH motif

Indexed keywords

ALANINE; ANKYRIN; ANKYRIN REPEAT PROTEIN; CYCLIN DEPENDENT KINASE 4; GANKYRIN; HISTIDINE; ONCOPROTEIN; PROTEIN P16; TETRAPEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS;

EID: 77953081931     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.04.010     Document Type: Article

References (37)

1. Li J., Mahajan A., Tsai M.-D. Ankyrin repeat: a unique motif mediating protein-protein interactions. Biochemistry 2006, 45:15168-15178.
2. Mosavi L.K., Cammett T.J., Desrosiers D.C., Peng Z.-Y. The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 2004, 13:1435-1448.
3. Dawson S., Higashitsuji H., Wilkinson A.J., Fujita J., Mayer R.J. Gankyrin: a new oncoprotein and regulator of pRb and p53. Trends Cell Biol. 2006, 16:229-233.
4. Lozano G., Zambetti G.P. Gankyrin: an intriguing name fore a novel regulator of p53 and RB. Cancer Cell 2005, 8:3-4.
5. Higashitsuji H., Higashitsuji H., Itoh K., Sakurai T., Nagao T., Sumitomo H., et al. The oncoprotein gankyrin binds to MDM2/HDM2, enhancing ubiquitylation and degradation of p53. Cancer Cell 2005, 8:75-97.
6. Ortega S., Malumbres M., Barbacid M. Cyclin D-dependent kinases, INK4 inhibitors and cancer. Biochim. Biophys. Acta 2002, 1602:73-89.
7. Li J., Tsai M.-D. Novel insights into the INK4-CDK4/6-Rb pathway: counter action of gankyrin against INK4 proteins regulates the CDK4-mediated phosphorylation of Rb. Biochemistry 2002, 41:3977-3983.
8. Sedgwick S.G., Smerdon S.J. The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem. Sci. 1999, 24:311-316.
9. Kohl A., Binz H.K., Forrer P, Stumpp M.T., Plückthun A., Grütter M.G. Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc. Natl Acad. Sci. USA 2003, 100:1700-1705.
10. Yuan C., Li J., Mahajan A., Poi M.J., Byeon I.J., Tsai M.-D. Solution structure of the human oncogenic protein gankyrin containing seven ankyrin repeats and analysis of its structure-function relationship. Biochemistry 2004, 43:12152-12161.
11. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 1986, 131:266-280.
12. Pace C.N., Scholtz J.M. Measuring the conformational stability of a protein. Protein Structure: A Practical Approach 1997, 197-319. IRL Press, Oxford, UK. T.E. Creighton (Ed.).
13. Hondal R.J., Riddle S.R., Kravchuk A.V., Zhao Z., Liao H., Bruzik K.S., Tsai M.-D. Phosphatidylinositol-specific phospholipase C: kinetic and stereochemical evidence for an interaction between arginine-69 and the phosphate group of phosphatidylinositol. Biochemistry 1997, 36:6633-6642.
14. Tevelev A., Byeon I.J., Selby T., Ericson K., Kim H.J., Kraynov V., Tsai M.-D. Tumor suppressor p16INK4A: structural characterization of wild-type and mutant proteins by NMR and circular dichroism. Biochemistry 1996, 35:9475-9487.
15. Mahajan A., Guo Y., Yuan C., Weghorst C.M., Tsai M.-D., Li J. Dissection of protein-protein interaction and CDK4 inhibition in the oncogenic versus tumor suppressing functions of gankyrin and p16. J. Mol. Biol. 2007, 373:990-1005.
16. Devi V.S., Binz H.K., Stumpp M.T., Plückthun A., Bosshard H.R., Jelesarov I. Folding of a designed simple ankyrin repeat protein. Protein Sci. 2004, 13:2864-2870.
17. Byeon I.L., Li J., Ericson K., Selby T., Tevelev A., Kim H.J., et al. Tumor suppressor p16INK4A: determination of solution structure and analyses of its interaction with cyclin-dependent kinase 4. Mol. Cell 1998, 1:421-431.
18. Cammett T.J., Luo L., Peng Z.Y. Design and characterization of a hyperstable p16INK4a that restores Cdk4 binding activity when combined with oncogenic mutations. J. Mol. Biol. 2003, 327:285-297.
19. Guo Y., Mahajan A., Yuan C., Joo S.H., Weghorst C.M., Tsai M.-D., Li J. Comparisons of the conformational stability of cyclin-dependent kinase (CDK) 4-interacting ankyrin repeat (AR) proteins. Biochemistry 2009, 48:4050-4062.
20. Yuan C., Li J., Selby T.L., Byeon I.J., Tsai M.-D. Tumor suppressor INK4: comparisons of conformational properties between p16(INK4A) and p18(INK4C). J. Mol. Biol. 1999, 294:201-211.
21. Manjasetty B.A., Quedenau C., Sievert V., Bussow K., Niessen F., Delbruck H., Heinemann U. X-ray structure of human gankyrin, the product of a gene linked to hepatocellular carcinoma. Proteins 2004, 55:214-217.
22. Matthews B.W. Structural and genetic analysis of protein stability. Annu. Rev. Biochem. 1993, 62:139-160.
23. Tan Y., Luo R. Structural and functional implications of p53 missense cancer mutations. PMC Biophys. 2009, 2:5-14.
24. Doig A.J., Baldwin R.L. N- and C-capping preferences for all 20 amino acids in alpha-helical peptides. Protein Sci. 1995, 4:1325-1336.
25. Iqbalsyah T., Doig A.J. Effect of the N3 residue on the stability of the alpha-helix. Protein Sci. 2004, 13:32-39.
26. Richardson J.S., Richardson D.C. Amino acid preferences for specific locations at the ends of alpha helices. Science 1988, 240:1648-1652.
27. Ferreiro D.U., Cervantes C.F., Truhlar S.M., Cho S.S., Wolynes P.G., Komives E.A. Stabilizing IκBα by "consensus" design. J. Mol. Biol. 2007, 365:1201-1216.
28. Forrer P., Binz H.K., Stumpp M.T., Plückthun A. Consensus design of repeat proteins. ChemBioChem 2004, 5:183-189.
29. Tripp K.W., Barrick D. Enhancing the stability and folding rate of a repeat protein through the addition of consensus repeats. J. Mol. Biol. 2007, 375:1187-1200.
30. Tripp K.W., Barrick D. Rerouting the folding pathway of the Notch ankyrin repeat domain by reshaping the energy landscape. J. Am. Chem. Sci. 2008, 130:5681-5688.
31. Binz H.K., Amstutz P., Kohl A., Stumpp M.T., Briand C., Forrer P., Plückthun A. High-affinity binders selected from designed ankyrin repeat protein libraries. Nat. Biotechnol. 2004, 22:575-582.
32. Amstutz P., Binz H.K., Parizek P., Stumpp M.T., Kohl A., Grutter M.G., Plückthun A. Intracellular kinase inhibitors selected from combinatorial libraries of designed ankyrin repeat proteins. J. Biol. Chem. 2005, 280:24715-24722.
33. Kohl A., Amstutz P., Parizek P., Binz H.K., Briand C., Capitani G., Plückthun A. Allosteric inhibition of aminoglycoside phosphotransferase by a designed ankyrin repeat protein. Structure 2005, 13:1131-1141.
34. Wetzel S.K., Settanni G., Kenig M., Binz H.K., Plückthun A. Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J. Mol. Biol. 2008, 376:241-257.
35. Binz H.K., Stumpp M.T., Forrer P., Amstutz P., Plückthun A. Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J. Mol. Biol. 2003, 332:489-503.
36. Li J., Byeon I.L., Ericson K., Poi M.J., O'Maille P., Selby T., Tsai M.-D. Tumor suppressor INK4: determination of the solution structure of p18INK4C and demonstration of the functional significance of loops in p18INK4C and p16INK4A. Biochemistry 1999, 38:2930-2940.
37. Li J., Joo S.H., Tsai M.-D. An NF-κB-specific inhibitor, IκBα, binds to and inhibits cyclin-dependent kinase 4. Biochemistry 2003, 42:13476-13483.