Conformational switch upon phosphorylation: Human CDK inhibitor p19 INK4d between the native and partially folded state

ACS Chemical Biology

Volumn 4, Issue 1, 2009, Pages 53-63

  Löw, Christian ^a   Homeyer, Nadine ^b   Weininger, Ulrich ^a   Sticht, Heinrich ^b   Balbach, Jochen ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 2D; CDK4 PROTEIN, HUMAN; CDK6 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; MUTANT PROTEIN; UREA;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; BODY TEMPERATURE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; MOLECULAR DYNAMICS; MOLECULAR MIMICRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTON NUCLEAR MAGNETIC RESONANCE; UBIQUITINATION; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; GENETICS; HUMAN; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PHOSPHORYLATION; PROTEIN DENATURATION; SPECTROFLUOROMETRY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; ANKYRIN REPEAT; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; CYCLIN-DEPENDENT KINASE 4; CYCLIN-DEPENDENT KINASE 6; CYCLIN-DEPENDENT KINASE INHIBITOR P19; HUMANS; MODELS, MOLECULAR; MUTANT PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; UBIQUITINATION; UREA;

EID: 60749093946     PISSN: 15548929     EISSN: None     Source Type: Journal    
DOI: 10.1021/cb800219m     Document Type: Article

References (53)

1. Pines, J. (1996) Cell cycle: reaching for a role for the Cks proteins, Curr. Biol. 6, 1399-1402.
2. Morgan, D. O. (1995) Principles of CDK regulation, Nature 374, 131-134.
3. Bartek, J., Bartkova, J., and Lukas, J. (1996) The retinoblastoma protein pathway and the restriction point, Curr. Opin. Cell Biol. 8, 805-814.
4. Sherr, C.J. (1996) Cancer cell cycles, Science 274, 1672-1677.
5. Lees, E. (1995) Cyclin dependent kinase regulation, Curr. Opin. Cell Biol. 7, 773-780.
6. Sherr, C. J., and Roberts, J. M. (1999) CDK inhibitors: positive and negative regulators of G1-phase progression, Genes Dev. 13, 1501-1512.
7. Harper, J. W., and Elledge, S. J. (1996) CDK inhibitors in development and cancer, Curr. Opin. Genet. Dev. 6, 56-64.
8. Bartek, J., Bartkova, J., and Lukas, J. (1997) The retinoblastoma protein pathway in cell cycle control and cancer, Exp. Cell Res. 237, 1-6.
9. 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.
10. 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., and Laue, E. D. (1997) Structure of the cyclin-dependent kinase inhibitor p19Ink4d, Nature 389, 999-1003.
11. 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.
12. 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.
13. Yuan, C., Selby, T. L., Li, J., Byeon, I. J., and Tsai, M. D. (2000) Tumor suppressor INK4: refinement of p16INK4A structure and determination of p15INK4B structure by comparative modeling and NMR data, Protein Sci. 9, 1120-1128.
14. Serrano, M. (1997) The tumor suppressor protein p16INK4a, Exp. Cell Res. 237, 7-13.
15. Ruas, M., and Peters, G. (1998) The p16INK4a/CDKN2A tumor suppressor and its relatives, Biochim. Biophys. Acta 1378, F115-177.
16. Drexler, H. G. (1998) Review of alterations ot the cyclin-dependent kinase inhibitor INK4 family genes p15, p16, p18 and p19 in human leukemia-lymphoma cells, Leukemia 12, 845-859.
17. Bartkova, J., Thullberg, M., Rajpert-De Meyts, E., Skakkebaek, N. E., and Bartek, J. (2000) Lack of p19INK4d in human testicular germ cell tumours contrasts with high expression during normal spermatogenesis, Oncogene 19, 4146-4150.
18. Thullberg, M., Bartek, J., and Lukas, J. (2000) Ubiquitin/proteasome- mediated degradation of p191NK4d determines its periodic expression during the cell cycle, Oncogene 19, 2870-2876.
19. Thullberg, M., Bartkova, J., Khan, S., Hansen, K., Ronnstrand, L., Lukas, J., Strauss, M., and Bartek, J. (2000) Distinct versus redundant properties among members of the INK4 family of cyclin-dependent kinase inhibitors, FEBS Lett. 470, 161-166.
20. Scassa, M. E., Marazita, M. C., Ceruti, J. M., Carcagno, A. L., Sirkin, P. F., Gonzzalez-Cid, M., Pignataro, O. P., and Canepa, E. T. (2007) Cell cycle inhibitor, p19INK4d, promotes cell survival and decreasese chromosomal aberrations after genotoxic insult due to enhanced DNA repair, DNA Repair 6, 626-638.
21. Ceruti, J. M., Scassa, M. E., Flo, J. M., Varone, C. L., and Canepa, E. T. (2005) Induction of p19INK4d in response to ultraviolet light improves DNA repair and confers resistance to apoptosis in neuroblastoma cells, Oncogene 24, 4065-4080.
22. Löw, C., Weininger, U., Zeeb, M., Zhang, W., Laue, E. D., Schmid, F. X., and Balbach, J. (2007) Folding mechanism ot an ankyrin repeat protein: scaffold and active site formation of human CDK inhibitor p19(INK4d), J. Mol. Biol. 373, 219-231.
23. Zeeb, M., Rösner, H., Zeslawski, W., Canet, D., Holak, T. A., and Balbach, J. (2002) Protein folding and stability of human CDK inhibitor p19INK4d, J. Mol. Biol. 315, 447-457.
24. Tang, K. S., Fersht, A. R., and Itzhaki, L. S. (2003) Sequential unfolding of ankyrin repeats in tumor: suppressor p16, Structure 11, 67- 73.
25. 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.
26. 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.
27. Hunter, T. (2000) Signaling 2000 and beyond, Cell 100, 113-127.
28. Johnson, L. N., and Barford, D. (1993) The effects of phosphorylation on the structure and function of proteins, Annu. Rev. Biophys. Biomol. Struct. 22, 199-232.
29. Kreegipuu, A., Blom, N., and Brunak, S. (1999) PhosphoBase, a database of phosphorylation sites: release 2.0, Nucleic Acids Res. 27, 237-239.
30. Steen, H., Jebanathirajah, J. A., Springer, M., and Kirschner, M. W. (2005) Stable isotope-free relative and absolute quantitation of protein phosphorylation stoichiometry by MS, Proc. Natl. Acad. Sci. U.S.A. 102, 3948-3953.
31. Hupp, T. R., and Lane, D. P. (1995) Two distinct signaling pathways activate the latent DNA binding function of p53 in a casein kinase II-independent manner, J. Biol. Chem. 270, 18165-18174.
32. Li, M., Stukenberg, P. T., and Brautigan, D. L. (2008) Binding of phosphatase inhibitor-2 to prolyl isomerase Pin1 modifies specificity for mitotic phosphoproteins, Biochemistry 47, 292-300.
33. Park, K. S., Mohapatra, D. P., Misonou, H., and Trimmer, J. S. (2006) Graded regulation of the Kv2.1 potassium channel by variable phosphorylation, Science 313, 976-979.
34. Löw, C., Weininger, U., Neumann, P., Klepsch, M., Lilie, H., Stubbs, M. T., and Balbach, J. (2008) Structural insights into an equilibrium folding intermediate of an archaeal ankyrin repeat protein, Proc. Natl. Acad. Sci. U.S.A. 105, 3779-3784.
35. Mello, C. C., Bradley, C. M., Tripp, K. W., and Barrick, D. (2005) Experimental characterization of the folding kinetics of the notch ankyrin domain, J. Mol. Biol. 352, 266-281.
36. Feldman, R. M., Correll, C. C., Kaplan, K. B., and Deshaies, R. J. (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p, Cell 91, 221-230.
37. Koepp, D. M., Schaefer, L. K., Ye, X., Keyomarsi, K., Chu, C., Harper, J. W., and Elledge, S. J. (2001) Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase, Science 294, 173-7.
38. Hao, B., Oehlmann, S., Sowa, M. E., Harper, J. W., and Pavletich, N. P. (2007) Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases, Mol. Cell 26, 131-143.
39. 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.
40. Hecky, J., and Müller, K. M. (2005) Structural perturbation and compensation by directed evolution at physiological temperature leads to thermostabilization of β-lactamase, Biochemistry 44, 12640-12654.
41. Ikai, A., and Tanford, C. (1973) Kinetics of unfolding and refolding of proteins. I. Mathematical analysis, J. Mol. Biol. 73, 145-163.
42. Bachmann, A., and Kiefhaber, T. (2005) Kinetic mechanisms in protein folding, in Protein Folding Handbook (Buchner, J., and Kiefhaber, T., Eds.) pp 379-406, Wiley-VCH, Weinheim.
43. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes, J. Biomol. NMR 6, 277-293.
44. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for visualization and analysis of NMR data, J. Biomol. NMR 4, 603-614.
45. Case, D. A., Pearlman, D. A., Caldwell, J. W., Cheatham, T. E., III, Wang, J., Ross, W. S., Simmerling, C. L., Darden, T. A., Merz, K. M., Stanton, R. V., Cheng, A. L., Vincent, J. J., Crowley, M., Tsui, V., Gohlke, H., Radmer, R. J., Duan, Y., Pitera, J., Massova, I., Seibel, G. L., Singh, U. C., Weiner, P. K., and Kollman, P. A. (2002) AMBER 7, University of California, San Francisco, CA.
46. Homeyer, N., Essigke, T., Meiselbach, H., Ullmann, G. M., and Sticht, H. (2007) Effect of HPr phosphorylation on structure, dynamics, and interactions in the course of transcriptional control, J. Mol. Modell. 13, 431-444.
47. Case, D. A., Darden, T. A., Cheatham, T. E., III, Simmerling, C. L., Wang, J., Duke, R. E., Luo, R., Merz, K. M., Pearlman, D. A., Crowley, M., Walker, R. C., Zhang, W., Wang, B., Hayik, S., Roitberg, A., Seabra, G., Wong, K. F., Paesani, F., Wu, X., Brozell, S., Tsui, V., Gohlke, H., Yang, L., Tan, C., Mongan, J., Homak, V., Cui, G., Beroza, P., Mathews, D. H., Schafmeister, C., Ross, W. S., and Kollman, P. A. (2006) AMBER 9, University of California, San Francisco, CA.
48. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
49. Cheatham, T. E., 3rd, Cieplak, P., and Kollman, P. A. (1999) A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat, J. Biomol. Struct. Dyn. 16, 845-862.
50. Homeyer, N., Horn, A. H. C., Lanig, H., and Sticht, H. (2006) AMBER force-field parameters for phosphorylated amino acids in different protonafion states: phosphoserine, phosphothreonine, phosphotyrosine, and phosphohistidine, J. Mol. Modell. 12, 281-289.
51. Simonson, T., and Brunger, A. T. (1992) Thermodynamics of protein-peptide interactions in the ribonuclease-S system studied by molecular dynamics and free energy calculations, Biochemistry 31, 8661-8674.
52. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics, J. Mol. Graphics 14, 33-38.
53. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics. 14, 51-55.