Probing cAMP-Dependent Protein Kinase Holoenzyme Complexes Iα and IIβ by FT-IR and Chemical Protein Footprinting

Biochemistry

Volumn 43, Issue 7, 2004, Pages 1908-1920

  Yu, Shaoning ^a   Mei, Fang C ^a   Lee, J Ching ^a   Cheng, Xiaodong ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; ENZYME KINETICS; ENZYMES; FOURIER TRANSFORM INFRARED SPECTROSCOPY; MOLECULAR STRUCTURE;

CHEMICAL CLEAVAGE PATTERNS; CHEMICAL PROTEIN FOOTPRINTING;

BIOCHEMISTRY;

AMIDE; CYCLIC AMP; DEUTERIUM; HOLOENZYME; HYDROGEN; PROTEIN KINASE; PROTEIN KINASE 1ALPHA; PROTEIN KINASE 2BETA; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BETA SHEET; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; INFRARED SPECTROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOOTPRINTING; RAT;

ANIMALS; CATALYTIC DOMAIN; CATTLE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DEUTERIUM EXCHANGE MEASUREMENT; HOLOENZYMES; LIGANDS; MICE; PROTEIN CONFORMATION; PROTEIN FOOTPRINTING; PROTEIN SUBUNITS; RATS; RECOMBINANT PROTEINS; SOLUTIONS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; WATER;

EID: 1242330291     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0354435     Document Type: Article

References (62)

1. Hanks, S. K., Quinn, A. M., and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains, Science 241, 42-52.
2. Taylor, S. S., Buechler, J. A., and Yonemoto, W. (1990) cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes, Annu. Rev. Biochem. 59, 971-1005.
3. Zetterqvist, Ö. Z., Ragnarsson, U., and Engstrom, L. (1990) in Peptides and protein phosphorylation (Kemp, B. E., Ed.) pp 1-41, CRC Press, Boca Raton, FL.
4. Knighton, D. R., Zheng, J. H., Ten Eyck, L. F., Ashford, V. A., Xuong, N. H., Taylor, S. S., and Sowadski, J. M. (1991) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase, Science 253, 407-414.
5. Su, Y., Dostmann, W. R., Herberg, F. W., Durick, K., Xuong, N. H., Ten Eyck, L., Taylor, S. S., and Varughese, K. I. (1995) Regulatory subunit of protein kinase A: structure of deletion mutant with cAMP binding domains, Science 269, 807-813.
6. Zheng, J., Knighton, D. R., Ten Eyck, L. F., Karlsson, R., Xuong, N., Taylor, S. S., and Sowadski, J. M. (1993) Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MgATP and peptide inhibitor, Biochemistry 32, 2154-2161.
7. Diller, T. C., Madhusudan, Xuong, N. H., and Taylor, S. S. (2001) Molecular basis for regulatory subunit diversity in cAMP-dependent protein kinase: crystal structure of the type II beta regulatory subunit, Structure 9, 73-82.
8. Beebe, S. J., and Corbin, J. D. (1986) in The Enzymes (Boyer, P. D., and Krebs, E. G., Eds.) pp 43-111, Academic Press, New York.
9. Lee, D. C., Carmichael, D. F., Krebs, E. G., and McKnight, G. S. (1983) Isolation of a cDNA clone for the type I regulatory subunit of bovine cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 80, 3608-3612.
10. Clegg, C. H., Cadd, G. G., and McKnight, G. S. (1988) Genetic characterization of a brain-specific form of the type I regulatory subunit of cAMP-dependent protein kinase, Proc. Natl. Acad. Sci. U.S.A. 85, 3703-3707.
11. Scott, J. D., Glaccum, M. B., Zoller, M. J., Uhler, M. D., Helfman, D. M., McKnight, G. S., and Krebs, E. G. (1987) The molecular cloning of a type II regulatory subunit of the cAMP-dependent protein kinase from rat skeletal muscle and mouse brain, Proc. Natl. Acad. Sci. U.S.A. 84, 5192-5196.
12. Jahnsen, T., Hedin, L., Kidd, V. J., Beattie, W. G., Lohmann, S. M., Walter, U., Durica, J., Schulz, T. Z., Schiltz, E., and Browner, M. (1986) Molecular cloning, cDNA structure, and regulation of the regulatory subunit of type II cAMP-dependent protein kinase from rat ovarian granulosa cells, J. Biol. Chem. 261, 12352-12361.
13. Doskeland, S. O., Maronde, E., and Gjertsen, B. T. (1993) The genetic subtypes of cAMP-dependent protein kinase: functionally different or redundant? Biochim. Biophys. Acta 1178, 249-258.
14. Beebe, S. J., Oyen, O., Sandberg, M., Froysa, A., Hansson, V., and Jahnsen, T. (1990) Molecular cloning of a tissue-specific protein kinase (C gamma) from human testis: representing a third isoform for the catalytic subunit of cAMP-dependent protein kinase, Mol. Endocrinol. 4, 465-475.
15. Hofmann, F., Bechtel, P. J., and Krebs, E. G. (1977) Concentrations of cyclic AMP-dependent protein kinase subunits in various tissues, J. Biol. Chem. 252, 1441-1447.
16. Sugden, P. H., and Corbin, J. D. (1976) Adenosine 3′:5′ -cyclic monophosphate-binding proteins in bovine and rat tissues, Biochem. J. 159, 423-427.
17. Lohmann, S. M., and Walter, U. (1984) Regulation of the cellular and subcellular concentrations and distribution of cyclic nucleotide-dependent protein kinases, Adv. Cyclic Nucleotide Protein Phosphorylation Res. 18, 63-117.
18. Cho-Chung, Y. S. (1990) Role of cyclic AMP receptor proteins in growth, differentiation, and suppression of malignancy: new approaches to therapy, Cancer Res. 50, 7093-7100.
19. Cho-Chung, Y. S., and Clair, T. (1993) The regulatory subunit of cAMP-dependent protein kinase as a target for chemotherapy of cancer and other cellular dysfunctional-related diseases, Pharmacol. Ther. 60, 265-288.
20. Tortora, G., Pepe, S., Bianco, C., Baldassarre, G., Budillon, A., Clair, T., Cho-Chung, Y. S., Bianco, A. R., and Ciardiello, F. (1994) The RI alpha subunit of protein kinase A controls serum dependency and entry into cell cycle of human mammary epithelial cells, Oncogene 9, 3233-3240.
21. Ciardiello, F., Pepe, S., Bianco, C., Baldassarre, G., Ruggiero, A., Bianco, C., Selvam, M. P., Bianco, A. R., and Tortora, G. (1993) Down-regulation of RI alpha subunit of cAMP-dependent protein kinase induces growth inhibition of human mammary epithelial cells transformed by c-Ha-ras and c-erbB-2 protooncogenes, Int. J. Cancer 53, 438-443.
22. Ciardiello, F., Tortora, G., Kim, N., Clair, T., Ally, S., Salomon, D. S., and Cho-Chung, Y. S. (1990) 8-Chloro-cAMP inhibits transforming growth factor alpha transformation of mammary epithelial cells by restoration of the normal mRNA patterns for cAMP-dependent protein kinase regulatory subunit isoforms which show disruption upon transformation, J. Biol. Chem. 265, 1016-1020.
23. Tortora, G., Damiano, V., Bianco, C., Baldassarre, G., Bianco, A. R., Lanfrancone, L., Pelicci, P. G., and Ciardiello, F. (1997) The RIalpha subunit of protein kinase A (PKA) binds to Grb2 and allows PKA interaction with the activated EGF-receptor, Oncogene 14, 923-928.
24. Boshart, M., Weih, F., Nichols, M., and Schutz, G. (1991) The tissue-specific extinguisher locus TSE1 encodes a regulatory subunit of cAMP-dependent protein kinase, Cell 66, 849-859.
25. Gordge, P. C., Hulme, M. J., Clegg, R. A., and Miller, W. R. (1996) Elevation of protein kinase A and protein kinase C activities in malignant as compared with normal human breast tissue, Eur. J. Cancer 32A, 2120-2126.
26. Bartlett, J. M., Hulme, M. J., and Miller, W. R. (1996) Analysis of cAMP RI alpha mRNA expression in breast cancer: evaluation of quantitative polymerase chain reaction for routine use, Br. J. Cancer 73, 1538-1544.
27. Bradbury, A. W., Carter, D. C., Miller, W. R., Cho-Chung, Y. S., and Clair, T. (1994) Protein kinase A (PK-A) regulatory subunit expression in colorectal cancer and related mucosa, Br. J. Cancer 69, 738-742.
28. McDaid, H. M., Cairns, M. T., Atkinson, R. J., McAleer, S., Harkin, D. P., Gilmore, P., and Johnston, P. G. (1999) Increased expression of the RIalpha subunit of the cAMP-dependent protein kinase A is associated with advanced stage ovarian cancer, Br. J. Cancer 79, 933-939.
29. Beebe, S. J., Salomonsky, P., Holroyd, C., and Becker, D. (1993) Differential expression of cyclic AMP-dependent protein kinase isozymes in normal human melanocytes and malignant melanomas, Cell Growth Differ. 4, 1005-1012.
30. Skalhegg, B. S., Johansen, A. K., Levy, F. O., Andersson, K. B., Aandahl, E. M., Blomhoff, H. K., Hansson, V., and Tasken, K. (1998) Isozymes of cyclic AMP-dependent protein kinases (PKA) in human lymphoid cell lines: levels of endogenous cAMP influence levels of PKA subunits and growth in lymphoid cell lines, J. Cell. Physiol. 177, 85-93.
31. Tortora, G., Clair, T., and Cho-Chung, Y. S. (1990) An antisense oligodeoxynucleotide targeted against the type II beta regulatory subunit mRNA of protein kinase inhibits cAMP-induced differentiation in HL-60 leukemia cells without affecting phorbol ester effects, Proc. Natl. Acad. Sci. U.S.A. 87, 705-708.
32. Rohlff, C., Clair, T., and Cho-Chung, Y. S. (1993) 8-Cl-cAMP induces truncation and down-regulation of the RI alpha subunit and up-regulation of the RII beta subunit of cAMP-dependent protein kinase leading to type II holoenzyme-dependent growth inhibition and differentiation of HL-60 leukemia cells, J. Biol. Chem. 268, 5774-5782.
33. Tortora, G., Budillon, A., Yokozaki, H., Clair, T., Pepe, S., Merlo, G., Rohlff, C., and Cho-Chung, Y. S. (1994) Retroviral vector-mediated overexpression of the RII beta subunit of the cAMP-dependent protein kinase induces differentiation in human leukemia cells and reverts the transformed phenotype of mouse fibroblasts, Cell Growth Differ. 5, 753-759.
34. Cummings, D. E., Brandon, E. P., Planas, J. V., Motamed, K., Idzerda, R. L., and McKnight, G. S. (1996) Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A, Nature 382, 622-626.
35. Michel, J. J., and Scott, J. D. (2002) AKAP mediated signal transduction, Annu. Rev. Pharmacol. Toxicol. 42, 235-257.
36. Cheng, X., Phelps, C., and Taylor, S. S. (2001) Differential binding of cAMP-dependent protein kinase regulatory subunit isoforms Ialpha and IIbeta to the catalytic subunit, J. Biol. Chem. 276, 4102-4108.
37. Herberg, F. W., Bell, S. M., and Taylor, S. S. (1993) Expression of the catalytic subunit of cAMP-dependent protein kinase in Escherichia coli: multiple isozymes reflect different phosphorylation states, Protein Eng. 6, 771-777.
38. Gibson, R. M., Ji-Buechler, Y., and Taylor, S. S. (1997) Interaction of the regulatory and catalytic subunits of cAMP-dependent protein kinase. Electrostatic sites on the type Ialpha regulatory subunit, J. Biol. Chem. 272, 16343-16350.
39. Hemmer, W., McGlone, M., and Taylor, S. S. (1997) Recombinant strategies for rapid purification of catalytic subunits of cAMP-dependent protein kinase, Anal. Biochem. 245, 115-122.
40. Buechler, Y. J., Herberg, F. W., and Taylor, S. S. (1993) Regulation-defective mutants of type I cAMP-dependent protein kinase. Consequences of replacing arginine 94 and arginine 95, J. Biol. Chem. 268, 16495-16503.
41. Dong, A., and Caughey, W. S. (1994) Infrared methods for study of hemoglobin reactions and structures, Methods Enzymol. 232, 139-175.
42. Dong, A., Malecki, J. M., Lee, L., Carpenter, J. F., and Lee, J. C. (2002) Ligand-induced conformational and structural dynamics changes in Escherichia coli cyclic AMP receptor protein, Biochemistry 41, 6660-6667.
43. Jung, C. (2000) Insight into protein structure and protein-ligand recognition by Fourier transform infrared spectroscopy, J. Mol. Recognit. 13, 325-351.
44. Susi, H., and Byler, D. M. (1986) Resolution-enhanced Fourier transform infrared spectroscopy of enzymes, Methods Enzymol. 130, 290-311.
45. Dong, A., Huang, P., and Caughey, W. S. (1990) Protein secondary structures in water from second-derivative amide I infrared spectra, Biochemistry 29, 3303-3308.
46. Barksdale, A. D., and Rosenberg, A. (1982) Acquisition and interpretation of hydrogen exchange data from peptides, polymers, and proteins, Methods Biochem. Anal. 28, 1-113.
47. Cheng, X., Shaltiel, S., and Taylor, S. S. (1998) Mapping substrate-induced conformational changes in cAMP-dependent protein kinase by protein footprinting, Biochemistry 37, 14005-14013.
48. Blout, E. R., de Lozé, C., and Asadourian, A. (1961) The Deuterium Exchange of Water-soluble Polypeptides and Proteins as Measured by Infrared Spectroscopy, J. Am. Chem. Soc. 83, 1895-1900.
49. Kim, K. S., Fuchs, J. A., and Woodward, C. K. (1993) Hydrogen exchange identifies native-state motional domains important in protein folding, Biochemistry 32, 9600-9608.
50. de Jongh, H. H., Goormaghtigh, E., and Ruysschaert, J. M. (1995) Tertiary stability of native and methionine-80 modified cytochrome c detected by proton-deuterium exchange using on-line Fourier transform infrared spectroscopy, Biochemistry 34, 172-179.
51. Li, J., Cheng, X., and Lee, J. C. (2002) Structure and dynamics of the modular halves of Escherichia coli cyclic AMP receptor protein, Biochemistry 41, 14771-14778.
52. Brenowitz, M., Senear, D. F., Shea, M. A., and Ackers, G. K. (1986) Quantitative DNase footprint titration: a method for studying protein-DNA interactions, Methods Enzymol. 130, 132-181.
53. Levin, L. R., Kuret, J., Johnson, K. E., Powers, S., Cameron, S., Michaeli, T., Wigler, M., and Zoller, M. J. (1988) A mutation in the catalytic subunit of cAMP-dependent protein kinase that disrupts regulation, Science 240, 68-70.
54. Levin, L. R., and Zoller, M. J. (1990) Association of catalytic and regulatory subunits of cyclic AMP-dependent protein kinase requires a negatively charged side group at a conserved threonine, Mol. Cell. Biol. 10, 1066-1075.
55. Orellana, S. A., and McKnight, G. S. (1992) Mutations in the catalytic subunit of cAMP-dependent protein kinase result in unregulated biological activity, Proc. Natl. Acad. Sci. U.S.A. 89, 4726-4730.
56. Orellana, S. A., Amieux, P. S., Zhao, X., and McKnight, G. S. (1993) Mutations in the catalytic subunit of the cAMP-dependent protein kinase interfere with holoenzyme formation without disrupting inhibition by protein kinase inhibitor, J. Biol. Chem. 268, 6843-6846.
57. Francis, S. H., and Corbin, J. D. (1994) Structure and function of cyclic nucleotide-dependent protein kinases, Annu. Rev. Physiol. 56, 237-272.
58. Krimm, S., and Bandekar, J. (1986) Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins, Adv. Protein Chem. 38, 181-364.
59. 2H exchange reveals communication between the cAMP and catalytic subunit-binding sites in the R(I)alpha subunit of protein kinase A, J. Mol. Biol. 323, 377-386.
60. 2H exchange mass spectrometry (DXMS), J. Mol. Biol. 327, 1065-1076.
61. 2H exchange and protein docking, Proc. Natl. Acad. Sci. U.S.A. 100, 13264-13269.
62. Yang, S., Fletcher, W. H., and Johnson, D. A. (1995) Regulation of cAMP-dependent protein kinase: enzyme activation without dissociation, Biochemistry 34, 6267-6271.