Tumor suppressor p16(INK4A): Structural characterization of wild-type and mutant proteins by NMR and circular dichroism

Biochemistry

Volumn 35, Issue 29, 1996, Pages 9475-9487

  Tevelev, Anton ^a   Byeon, In L ^a   Selby, Thomas ^a   Ericson, Karen ^a   Kim, Hee Jung ^a   Kraynov, Vadim ^a   Tsai, Ming Daw ^b  

^a OHIO STATE UNIVERSITY   (United States)

^b Biophysics Program   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CALCULATION; CIRCULAR DICHROISM; DATA ANALYSIS; GEL ELECTROPHORESIS; GENE MUTATION; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; TUMOR SUPPRESSOR GENE; AMINO ACID SEQUENCE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

ESCHERICHIA COLI;

CARRIER PROTEIN; PRIMER DNA; PROTEIN P16INK4A; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; BASE SEQUENCE; CARRIER PROTEINS; CIRCULAR DICHROISM; CLONING, MOLECULAR; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; GENE EXPRESSION; GENES, TUMOR SUPPRESSOR; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; REPETITIVE SEQUENCES, NUCLEIC ACID; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 0029665942     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi960211+     Document Type: Article

References (69)

1. Aves, S. J., Durkacz, B. W., Carr, A., & Nurse, P. (1985) EMBO J. 4, 457-463.
2. Bates, S., Bonetta, L., MacAllan, D., Parry, D., Holder, A., Dickson, C., & Peters, G. (1994) CDK6 (PLSTIRE) and CDK4 (PSK-J3) Are a Distinct Subset of the Cyclin-Dependent Kinases That Associate with Cyclin D1. Oncogene 9, 71-79.
3. Bax, A., & Davis, D. G. (1985) J. Magn. Reson. 65, 355-360.
4. Bax, A., & Icura, M. (1991) J. Biomol. NMR 1, 99-104.
5. Bax, A., & Pochapsky, S. (1992) J. Magn. Reson. 99, 638-643.
6. Bax, A., Ikura, M., Kay, L. E., Torchia, D. A., & Tschudin, R. (1990a) J. Magn. Reson. 86, 304-318.
7. Bax, A., Clore, G. M., & Gronenborn, A. M. (1990b) J. Magn. Reson. 88, 425-431.
8. Bodenhausen, G., & Ruben, D. J. (1980) Chem. Phys. Lett. 69, 185-189.
9. Cairns, P., Mao, L., Merlo, A., Lee, D. J., Schwab, D., Eby, Y., Tokino, K., van der Riet, P., Blaugrund, J. E., & Sidransky, D. (1994) Rates of p 16 (MTS1) Mutations in Primary Tumors with 9p Loss, Science 265, 415-416.
10. Caldas, C., Hahn, S. A., de Costa, L. T., Redston, M. S., Schutte, M., Seymour, A. B., Weinstein, C. L., Hruban, R. H., Yeo, C. J., & Kern, S. E. (1994) Frequent Somatic Mutations and Homozygous Deletions of the p16 (MTS1) Gene in Pancreatic Adenocarcinoma, Nature Genet. 8, 27-32.
11. Cantor, C. R., & Schimmel, P. R. Biophysical Chemistry, Part II, W. H. Freeman, & Co., San Francisco.
12. INK4A, Mol. Cell Biol. 15, 2682-2688.
13. Cordon-Cardo, C. (1995) Mutation of Cell Cycle Regulators. Biological and Clinical Implications for Human Neoplasia, Am. J. Pathol. 147, 545-560.
14. Doherty, A. J., Ashford, S. R., Brannigan, J. A., & Wigley, D. B. (1995) A Superior Host Strain for the Over-Expression of Cloned Genes Using T7 Promoter Based Vectors, Nucleic Acids Res. 23, 2074-2075.
15. Dyson, N. (1994) pRb, p107 and the Regulation of the E2F Transcription Factor, J. Cell Sci. Suppl. 18, 81-87.
16. Gillard, S., Spehner, D., Drillien, R., & Kirn, A. (1986) Proc. Natl. Acad. Sci. U.S.A. 83, 5573-5577.
17. Greenwald, I., & Rubin, G. M. (1992) Making a Difference: The Role of Cell-Cell Interactions in Establishing Separate Identities for Equivalent Cells, Cell 68, 271-281.
18. Grzesiek, S., & Bax, A. (1992a) J. Magn. Reson. 96, 432-440.
19. Grzesiek, S., & Bax, A. (1992b) J. Am. Chem. Soc. 114, 6291-6293.
20. INK4B/MTS2-Related CDK6 Inhibitor, Correlates with Wild-Type pRb Function, Genes and Dev. 8, 2939-2952.
21. INK4B Is a Potential Effector of TGF-b-Induced Cell Cycle Arrest, Nature 371, 257-261.
22. Hartwell, L. H., & Kastan, M. B. (1994) Cell Cycle Control and Cancer, Science 266, 1821-1828.
23. Helps, N. R., Barker, H. M., Elledge, S. J., & Cohen, P. T. (1995) Protein Phosphatase 1 Interacts with p53BP2, a Protein Which Binds to the Tumour Suppressor p53, FEBS Lett. 377, 295-300.
24. Hirai, H., Roussel, M. F., Kato, J.-Y., Ashmun, R. A., & Sherr, C. J. (1995) Novel INK4 Proteins, p19 and p18, Are Specific Inhibitors of the Cyclin D-Dependent Kinases CDK4 and CDK6, Mol. Cell. Biol. 15, 2672-2681.
25. Hopkin, K. (1994) p16/MTS-1: All-Star Tumor Suppressor or Team Player, J. NIH Res. 6, 32-36.
26. INK4A Gene Mediated by an Adenovirus Vector, Cancer Res. 55, 3250-3253.
27. Kamb, A., Gruis, N. A., Weaver-Feldhaus, J., Liu, Q., Harshman, K., Tavtigian, S. V., Stockert, E., Day III, R. S., Johnston, B. E., & Skolnik, M. H. (1994) A Cell Cycle Regulator Potentially Involved in Genesis of Many Tumor Types, Science 264, 436-440.
28. Kao, L.-R., Peterson, J., Ji, R., Bender, L., & Bender, A. (1996) Interactions between the Ankyrin Repeat-Containing Protein Akr1p and the Pheromone Response Pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 168-178.
29. Kato, J.-Y., Matsuoka, M., Strom, D. K., & Sherr, C. J. (1994) Regulation of Cyclin D-Dependent Kinase 4 (Cdk4) by Cdk4-Activating Kinase, Mol. Cell. Biol. 14, 2713-2721.
30. Kay, L. E., Keifer, P., & Saarinen, T. (1992) J. Am. Chem. Soc. 114, 10663-10665.
31. Kay, L. E., Xu, G.-Y., Singer, A. U., Muhandiram, D. R., & Forman-Kay, J. D. (1993) J. Magn. Reson. B 101, 333-337.
32. Koh, J., Enders, G. H., Dynlacht, B. D., & Harlow, E. (1995) Tumour-Derived p16 Alleles Encoding Proteins Defective in Cell-Cycle Inhibition, Nature 375, 506-510.
33. Kouzarides, T. (1995) Transcriptional Control by the Retinoblastoma Protein, Semin. Cancer Biol. 6, 91-98.
34. Kunkel, T. A. (1985) Rapid and Efficient Site-Specific Mutagenesis without Phenotypic Selection, Proc. Natl. Acad. Sci. U.S.A. 82, 488-492.
35. Lee, K. M., Androphy, E. J., & Baleja, J. D. (1995) A Novel Method for Selective Isotope Labeling of Bacterially Expressed Proteins, J. Biomol. NMR 5, 93-96.
36. Lux, S. E., John, K. M., & Bennett, V. (1990) Analysis of cDNA for Human Erythrocyte Ankyrin Indicates a Repeated Structure with Homology to Tissue-Differentiation and Cell-Cycle Control Proteins, Nature 344, 36-42.
37. Matsuno, K., Diedrich, R. J., Go, M. J., Blaumueller, C. M., & Artavanis-Tsakonas, S. (1995) Deltex Acts as a Positive Regulator of Notch Signaling through Interactions with the Notch Ankyrin Repeats, Development 121, 2633-2644.
38. PSK-J3/cdk4) for Mammalian D Type G1 Cyclins, Cell 71, 323-334.
39. Meyerson, M., & Harlow, E. (1994) Identification of G1 Kinase Activity for Cdk6, a Novel Cyclin D Partner, Mol. Cell. Biol. 14, 2077-2086.
40. Muchmore, D. C., McIntosh, L. P., Russell, C. B., Anderson, D. E., & Dahlquist, F. W. (1989) Expression and Nitrogen-15 Labeling of Proteins for Proton and Nitrogen-15 Nuclear Magnetic Resonance, Methods Enzymol. 177, 44-73.
41. Muhandiran, D. R., & Kay, L. E. (1994) J. Magn. Reson. B 103, 203-216.
42. Muhandiran, D. R., Xu, G.-Y., & Kay, L. E. (1993) J. Biomol. NMR 3, 463-70.
43. Müller, R. (1995) Transcriptional Regulation during the Mammalian Cell Cycle, Trends Genet. 11, 173-178.
44. Ohta, M., Nagai, H., Shimizu, M., Rasio, D., Berd, D., Mastrangelo, M., Singh, A. D., Shields, J. A., Shields, C. L., Croce, C. M., & Huebner, K. (1994) Rarity of Somatic and Germline Mutations of the Cyclin-Dependent Kinase 4 Inhibitor Gene, CDK41, in Melanoma, Cancer Res. 54, 5269-5272.
45. INK4 in Human Cancer, Proc. Natl. Acad. Sci. U.S.A. 91, 11045-11049.
46. Pace, C. N. (1986) Determination and Analysis of Urea and Guanidine Hydrochloride Denaturation Curves, Methods Enzymol. 131, 266-280.
47. Piotto, M., Saudek, V., & Sklenár, V. (1992) J. Biomol. NMR 2, 661-666.
48. INK4B Genes, Oncogene 11, 635-645.
49. INK4 Function, Nature Genet. 10, 114-116.
50. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Schägger, H., & von Jagow, G. (1987) Tricine-Sodium Dodecyl Sulfate - Polyacrylamide Gel Electrophoresis for the Separation of Proteins in the Range from 1 to 100 kDa, Anal. Biochem. 166, 368-379.
52. INK4A, Science 267, 249-252.
53. Serrano, M., Hannon, G. J., & Beach, D. (1993) A New Regulatory Motif in Cell-Cycle Control Causing Specific Inhibition of Cyclin D/Cdk4, Nature 366, 704-707.
54. Serrano, M., Lee, H.-W., Chin, L., Cordon-Cardo, C., Beach, D., & DePinho, R. A. (1996) Cell 85, 27-37.
55. Shaka, A. J., Lee, C. J., & Pines, A. (1988) J. Magn. Reson. 77, 274-293.
56. Shpaer, E. G. (1986) J. Mol. Biol. 188, 555-564.
57. Sklenar, V., Piotto, M., Leppik, R., & Saudek, V. (1993) J. Magn. Reson., 241-245.
58. Spera, S., & Bax, A. (1991) J. Am. Chem. Soc. 113, 5490-5492.
59. Srinvasan, P. R., & Lichter, R. L. (1977) J. Magn. Reson. 28, 227-234.
60. Suzuki-Takahashi, I., Kitagawa, M., Saijo, M., Higashi, H., Ogino, H., Matsumoto, H., Taya, Y., Nishimura, S., & Okuyama, A. (1995) The Interactions of E2F with pRb and with p107 Are Regulated via the Phosphorylation of pRb and p107 by a Cyclin-Dependent Kinase, Oncogene 10, 1691-1698.
61. Tsai, M.-D., & Yan, H. (1991) Biochemistry 30, 6806-6818.
62. Vuister, G. W., Clore, G. M., Gronenborn, A. M., Powers, R., Garrett, D. S., Tshudin, R., & Bax, A. (1993) J. Magn. Reson. B 101, 210-213.
63. Weinberg, R. A. (1995) The Retinoblastoma Protein and Cell Cycle Control, Cell 81, 323-330.
64. Whyte, P. (1995) The Retinoblastoma Protein and Its Relatives, Semin. Cancer Biol. 6, 83-90.
65. Wishart, D. S., Sykes, B. D., & Richards, F. M. (1991) FEBS Lett. 193, 72-80.
66. Wishart, D. S., Bigam, C. G., Holm, A., Hodges, R. S., & Sykes, B. D. (1995) J. Biomol. NMR 5, 67-81.
67. Wittekind, M., & Mueller, L. (1993) J. Magn. Reson. B 101, 201-205.
68. Wüthrich, K. (1986) Familial Melanoma and p16 - a Hung Jury, NMR of Proteins and Nucleic Acids, John Wiley & Sons, Inc., New York.
69. INK4A Tumor Suppressor Protein, Cancer Res. 55, 2503-2506.