Overexpresson of RIIβ regulatory subunit of protein kinase a in human colon carcinoma cell induces growth arrest and phenotypic changes that are abolished by site-directed mutation of RIIβ

European Journal of Biochemistry

Volumn 235, Issue 3, 1996, Pages 486-494

  Nesterova, Maria ^a   Yokozaki, Hiroshi ^a   McDuffie, Elwood ^a   Cho Chung, Yoon S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Gene transfer; Growth inhibition; Human cancer cells; Protein kinase A; Site directed mutation

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOENZYME; MESSENGER RNA; VIRUS VECTOR;

ARTICLE; CELL GROWTH; COLON CANCER; CONTROLLED STUDY; GENE EXPRESSION; GENE TRANSFER; HUMAN; HUMAN CELL; IN VITRO STUDY; PHENOTYPE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; TUMOR CELL;

ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; CELL DIVISION; COLONIC NEOPLASMS; CULTURE MEDIA, SERUM-FREE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOENZYMES; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OLIGONUCLEOTIDES, ANTISENSE; PHENOTYPE; THYMIDINE; TUMOR CELLS, CULTURED;

EID: 0029671412     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.00486.x     Document Type: Article

References (48)

1. Krebs, E. G. (1972) Protein kinase, Curr. Top. Cell. Regul. 5, 99-133.
2. Krebs, E. G. & Beavo, J. A. (1979) Phosphorylation-dephosphorylation of enzymes, Annu. Rev. Biochem. 48, 923-939.
3. Beebe, S. J. & Corbin, J. D. (1986) Cyclic nucleotide-dependent protein kinases, in The enzymes: control by phosphorylation (Boyer, P. D. & Kerbes, E. G., eds) part A, vol. 17, pp. 43-111, Academic Press, New York.
4. McKnight, G. S., Clegg, C. H., Uhler, M. D., Chrivia, J. C., Cadd, G. G., Correll, L. A. & Otten, A. D. (1988) Analysis of the cAMP-dependent protein kinase system using molecular genetic approaches, Recent Prog. Horm. Res. 44, 307-335.
5. Levy, F. O., Øyen, O., Sandberg, M., Taskén, K., Eskild, W., Hansson, V. & Jahnsen, T. (1988) Molecular cloning, complementary deoxyribonucleic acid structure and predicted full-length amino acid sequence of the hormone-inducible regulatory subunit of 3′,5′-cyclic adenosine monophosphate-dependent protein kinase from human testis, Mol. Endocrinol. 2, 1364-1373.
6. Uhler, M. D., Carmichael, D. R. Lee, D. C., Chrivia, J. C., Krebs, E. G. & McKnight, G. S. (1986) Isolation of cDNA clones coding for the catalytic subunit of mouse cAMP-dependent protein kinase, Proc. Natl Acad. Sci. USA 83, 1300-1304.
7. Uhler, M. D., Chrivia, J. C. & McKnight, G. S. (1986) Evidence for a second isoform of the catalytic subunit of cAMP-dependent protein kinase, J Biol. Chem. 261, 15360-15363.
8. Showers, M. O. & Maurer, R. A. (1986) A cloned bovine cDNA encodes an alternate form of the catalytic subunit of cAMP-dependent protein kinase, J. Biol. Chem. 261, 16288-16291.
9. Beebe, S. J., Øyen, O., Sandberg, M., Froysa, A., Hansson, V. & Jahnsen, T. (1990) Molecular cloning of a unique tissue-specific protein kinase (C.) from human testis - representing a third isoform for the catalytic subunit of the cAMP-dependent protein kinase, Mol. Endocrinol. 4, 465-475.
10. Øyen, O., Scott, J. D., Cadd, G. G., McKnight, G. S., Krebs, E. G., Hansson, V. & Jahnsen, T. (1988) A unique mRNA species for a regulatory subunit of cAMP-dependent protein kinase is specifi-cally induced in haploid germ cells, FEBS Lett. 229, 391-394.
11. Cadd, G. & McKnight, G. S.(1989) Distinct patterns of cAMP-dependent protein kinase gene expression in mouse brain, Neuron 3, 71-79.
12. Cadd, G. G., Uhler, M. D. & McKnight, G. S. (1990) Holoenzymes of cAMP-dependent protein kinase containing the neural form of type I regulatory subunit have an increased sensitivity to cyclic nucleotides, J. Biol. Chem. 265, 19502-19506.
13. Lehmann, S. M. & Walter, U. (1984) Regulation of the cellular and subcellular concentrations and distribution of cyclic nucleotide-dependent protein kinases, Adv. Cyclic Nudeotide Protein Phosphoarylation Res. 18, 63-117.
14. Cho-Chung, Y. S. (1990) Perspectives in cancer research: role of cyclic AMP receptor proteins in growth, differentiation, and suppression of malignancy: new approaches to therapy, Cancer Res. 50, 7093-7100.
15. Schwartz, D. A. & Rubin, C. S. (1985) Identification and differential expression of two forms of regulatory subunits (RII) of cAMP-dependent protein kinase II in Friend erythroleukemic cells, J. Biol. Chem. 260, 6296-6303.
16. Ally, S., Tortora, G., Clair, T., Grieco, D., Merlo, G., Katsaros, D., Ogreid, D., Døskeland, S. O., Jahnsen, T. & Cho-Chung, Y. S. (1988) Selective modulation of protein kinase isozyme by the site-selective analog 8-chloroadenosine 3′,5′ monophosphate provides a biological means for control of human colon cancer cell growth, Proc. Natl Acad. Sci. USA 85, 6319-6322.
17. Ally, S., Clair, T., Katsaros, D., Tortora, G., Yokozaki, H., Finch, R. A., Avery, T. L. & Cho-Chung, Y. S. (1989) Inhibition of growth and modulation of gene expression in human lung carcinoma in athymic mice by site-selective 8-Cl-cAMP, Cancer Res. 49, 5650-5655.
18. Tortora, G., Yokozaki, H., Pepe, S., Clair, T. & Cho-Chung, Y. S. (1991) Differentiation of HL-60 leukemia by type I regulatory subunit antisense oligodeoxynucleotide of cAMP-dependent protein kinase, Proc. Natl Acad. Sci. USA 88, 2011-2015.
19. Yokozaki, H., Budillon, A., Tortora, G., Meissner, S., Beaucage, S., Miki, K. & Cho-Chung, Y. S. (1993) An antisense oligodeoxynucleotide that depletes RIβ subunit of cAMP-dependent protein kinase induces growth inhibition in human cancer cells, Cancer Res. 53, 868-872.
20. Tortora, G. & Cho-Chung, Y. S. (1990) Type II regulatory subunit of protein kinase restores cAMP-dependent transcription in a cAMP-unresponsive cell line, J. Biol. Chem. 265, 18067-18070.
21. Radhakrishnan, P. I., Egan, W., Regan, J. B. & Beaucage, S. L. (1990) 3H-1,2-benzodithiole-3-one 1,1-dioxide as an improved sulfurizing reagent in the solid-phase synthesis of oligodeoxyribonucleoside phosphorothioates, J. Am. Chem. Soc. 112, 1253-1254.
22. Tortora, G., Clair, T. & Cho-Chung, Y. S. (1990) An antisense oligodeoxynucleotide targeted against the type IIβ regulatory subunit mRNA of protein kinase inhibits cAMP-induced differentiation in HL-60 leukemia cells without affecting phorbol ester effects, Proc. Natl Acad. Sci. USA 87, 705-708.
23. Sandberg, M., Tasken, K., Oyen, O., Hansson, V. & Jahnsen, T. (1987) Molecular cloning, cDNA structure and deduced amino acid sequence for a type I regulatory subunit of cDNA-dependent protein kinase from human testis, Biochem. Biophys. Re.s. Commun. 149, 939-945.
24. α of cAMP-dependent protein kinase encodes an alternate amino-terminal region, FEBS Lett. 246, 57-64.
25. α, Nucleic Acids Res. 16, 8189-8190.
26. McGeady, M. L., Kerby, S., Shankar, V., Ciardiello, F., Solomon, D. S. & Seidman, M. (1989) Infection with a TGFα retroviral vector transforms normal mouse mammary epithelial cells but not normal rat fibroblasts, Oncogene 4, 1375-1382.
27. Ciardiello, F., Gottardis, M., Basolo, F., Pepe, S., Normanno, N., Dickson, R. B., Bianco, A. R. & Salomon, D. S. (1993) Additive effects of c-erbB-2,c-Ha-ras, and transforming growth factor-α genes on in vitro transformation of human mammary epithelial cells, Mol. Carcinog. 6, 43-52.
28. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
29. Bhattacharya, B., Prasad, G. L., Valverius, E. M., Solomon, D. S. & Cooper, H. (1990) Tropomyosins of human mammary epithelial cells: consistent defects of expression in mammary carcinoma cell lines, Cancer Res. 50, 2105-2112.
30. β 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.
31. β on sodium dodecyl sulfate-polyacrylamide gel electrophoresis compared with rat and bovine RIIs, J. Biol. Chem. 267, 5374-5379.
32. β subunits of the cAMP-dependent protein kinase, J. Biol. Chem. 266, 23074-23082.
33. Tortora, G., Pepe, S., Cirafici, A. M., Ciardiello, F., Porcellini, A., Clair, T., Colletta, G., Cho-Chung, Y. S. & Bianco, A. R. (1993) Thyroid-stimulating hormone-regulated growth and cell cycle distribution of thyroid cells involve type I isozyme of cyclic AMP-dependent protein kinase, Cell Growth & Differ. 4, 359-365.
34. Cobb, C. E., Beth, A. H. & Corbin, J. D. (1987) Purification and characterization of an inactive form of cAMP-dependent protein kinase containing bound cAMP, J. Biol. Chem. 262, 16566-16574.
35. Otten, A. D. & McKnight, G. S. (1989) Overexpression of the type II regulatory subunit of the cAMP-dependent protein kinase eliminates the type I holoenzyme in mouse cells, J. Biol. Chem. 264, 20255-20260.
36. Tortora, G., Tagliaferri, P., Clair, T., Colamonici, O., Neckers, L. M., Robins, R. & Cho-Chung, Y. S. (1988) Site-selective cAMP analogs at micromolar concentrations induce growth arrest and differentiation of acute promyelocytic, chronic myelocytic, and acute lymphocytic human leukemia cell lines, Blood 71, 230 -233.
37. Tortora, G., Clair, T., Katsaros, D., Ally, S., Colamonici, O., Neckers, L. M., Tagliaferri, P., Jahnsen, T., Robins, R. K. & Cho-Chung, Y. S. (1989) Induction of megakaryocytic differentiation and modulation of protein kinase gene expression by site-selective cAMP analogs in K-562 human leukemic cells, Proc. Natl Acad. Sci. USA 86, 2849-2852.
38. Hofmann, F. (1980) Apparent constants for the interaction of regulatory and catalytic subunit of cAMP-dependent protein kinase I and II, J. Biol. Chem. 255, 1559-1564.
39. Corbin, J. D., Keely, S. L. & Park, C. R. (1975) The distribution and dissociation of cyclic adenosine 3′,5′-monophosphate-dependent protein kinases in adipose, cardiac, and other tissues, J. Biol. Chem. 250, 218-225.
40. Corbin, J. D., Keely, S. L., Soderling, T. R. & Park, C. R. (1975) Hormonal regulation of adenosine 3′,5′-monophosphate-dependent protein kinase, Adv. Cyclic Nucleotide Res. 5, 265-279.
41. Hofmann, F., Beavo, J. A., Bechtel, P. J. & Krebs, E. G. (1975) Comparison of adenosine 3′,5′-monophosphate-dependent protein kinase from rabbit skeletal and bovine heart muscle, J. Biol. Chem. 250, 7795-7801.
42. Rangel-Aldao, R. & Rosen, O. M. (1976) Mechanism of self-phosphorylation of adenosine 3′,5′-monophosphate-dependent protein kinase from bovine cardiac muscle, J. Biol. Chem. 251, 3375-3380.
43. Durgerian, S. & Taylor, S. S. (1989) The consequences of introducing an autophosphorylation site into the type I regulatory subunit of cAMP-dependent protein kinase, J. Biol. Chem. 264, 9807-9813.
44. Kuret, J., Johnson, K. K., Nicolette, C. & Zoller, M. J. (1988) Mutagenesis of the regulatory subunit of yeast cAMP-dependent protein kinase. Isolation of site-directed mutants with altered binding affinity for catalytic subunit, J. Biol. Chem. 263, 9149-9154.
45. Lange-Carter, C. A., Fossli, T., Jahnsen, T. & Malkinson, A. M. (1990) Decreased expression of the type I isozyme of cAMP-dependent protein kinase in tumor cell lines of lung epithelial origin, J. Biol. Chem. 265, 7814-7818.
46. Kapoor, L., Grantham, F. & Cho-Chung, Y. S. (1984) Nucleolar accumulation of cyclic adenosine-3′:5′-monophosphate receptor proteins during regression of MCF-7 human breast tumors, Cancer Res. 44, 3554-3560.
47. Meinkoth, J. L., Ying, J., Taylor, S. S. & Feramisco, J. R. (1990) Dynamics of the distribution of cAMP-dependent protein kinase in living cells, Proc. Natl Acad. Sci. USA 87, 9595-9599.
48. β 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.