Abstract
The effect of sodium butyrate (NaBut) on cell growth was studied in normal rat kidney (NRK) fibroblasts, and in NRK cells stably transfected with either the adenoviral gene E1A (wild-type), or mutated E1A (E1Amut; with a deletion in the CR1 domain), or with the transforming Ha-ras (EJ) gene. The growth of all these cell lines was inhibited by milimolar concentrations of sodium butyrate (NaBut). However, whereas the NRK cells as well as the NRK-E1Amut and NRK-ras cells were arrested in the G1 phase of the cell cycle, the NRK-E1A cells progressively accumulated in the G2 phase, suggesting that the E1A gene expression caused a “leaky” inhibition of G1 phase progression. The expression of late cell cycle-related genes cdc2 and PCNA (proliferating cell nuclear antigen) was not affected by NaBut in the NRK-E1A cells while it was totally suppressed in the other NRK-derived cell lines.
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Prasad, K. N. (1980) Butyric acid: a small fatty acid with diverse biological functions.Life Sci. 27:1351–1358.
Kruh, J. (1982) Effects of sodium butyrate, a new pharmacological agent, on cells in culture.Mol. Cell. Biochem. 42:65–82.
Yamada, K., Ohtsu, M., Sugano, M. and Kimura, G. (1992) Effects of butyrate on cell cycle progression and polyploidization of various types of mammalian cells.Biosci. Biotech. Biochem. 56:1261–1265.
Fagot, D., Buquet-Fagot, C, Lallemand, F. and Mester, J. (1994) Antiproliferative effects of sodium butyrate in human multidrug-resistant cancer cell lines (in preparation).
Charollais, R. H., Buquet, C. and Mester, J. (1990) Butyrate blocks the accumulation of cdc2 mRNA in late G1 phase but inhibits both the early and late G1 progression in chemically transformed mouse fibroblasts BP-A31.J. Cell. Physiol. 145:46–52.
Dalton, S. (1992) Cell cycle regulation of the human cdc2 gene.EMBO J. 11:1797–1804.
Bagchi, S., Raychaudhuri, P. and Nevins, J. R. (1990) Adenovirus E1A proteins can dissociate heteromeric complexes involving the E2F transcription factor: a novel mechanism for E1A transactivation.Cell 62:656–669.
Bagchi, S., Weinmann, R. and Raydhauchuri, P. (1991) The retinoblastoma protein copurifies with E2F-I, and E1A-regulated inhibitor of the transcription factor E2F.Cell 65:1063–1072.
Bandara, L. R. and La Thangue, N. B. (1991) Adenovirus E1A prevents the retinoblastoma gene product from complexing with a cellular transcription factor.Nature 352:249–251.
Dyson, N., Buchkovich, K., Whyte, P. and Harlow, E. (1989) The cellular 107 K protein that binds to adenovirus E1A also associates with the large T antigens of SV40 and JC virus.Cell 58:249–255.
Buchou, T., Kranenburg, O., van Dam, H., Roelen, D., Zantema, A., Hall, F. L. and van der Eb, A. (1993) Increased cyclin A and decreased cyclin D levels in adenovirus E1A-transformed rodent cell lines.Oncogene 8:1765–1773.
Forgue-Lafitte, M. E., Coudray, A. M., Fagot, D. and Mester, J. (1992) Effects of ketoconazole on the proliferation and cell cycle of human cancer cell lines.Cancer Res. 52:6827–6831.
Maniatis, T., Fritch, E. F. and Sambrook, J. (1989)Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y., U.S.A.
Cisek, L. J. and Corden, J. L. (1989) Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2.Nature 339:679–684.
Jaskulski, D., Gatti, G., Travali, S., Calabretta, B. and Baserga, R. (1988). Regulation of the proliferating cell nuclear antigen cyclin and thymidine kinase mRNA levels by growth factors.J. Biol. Chem. 263:10175–10179.
Hickok, N. J., Seppänen, P. J., Kontula, K. K., Jänne, P. A., Bardin, C. W. and Jänne, O. A. (1986) Two ornithine decarboxylase mRNA species in mouse kidney arise from size heterogeneity at their 3′ termini.Proc. Natl. Acad. Sci. USA 83:594–528.
Lemishka, I., Farmer, S., Racaniello, V. R. and Sharp, P. A. (1980) Nucleotide sequence and evolution of a mammalian α-tubulin messenger RNA.J. Mol. Biol. 151:101–120.
Souleimani, A. and Asselin, C. (1993) Regulation of c-myc expression by sodium butyrate in the colon carcinoma cell line Caco-2.FEBS Letters 326:45–50.
Toscani, A., Robert-Soprano, D. and Soprano, K. J. (1988) Molecular analysis of sodium butyrate-induced growth arrest.Oncogene Res. 3:223–238.
Herold, K. M. and Rothberg, P. G. (1988) Evidence for a labile intermediate in the butyrate induced reduction of the level of c-myc mRNA in SW837 rectal carcinoma cells.Oncogene 3:423–428.
Prelich, G. and Stillman, B. (1988) Coordinated leading and lagging strand synthesis during SV40 replication in vitro requires PCNA.Cell 53:117–126.
Xiong, Y., Zhang, H. and Beach, D. (1992) D-type cyclins associate with multiple protein kinases and DNA replication and repair factor PCNA.Cell 71:505–514.
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Joensuu, T., Mester, J. Inhibition of cell cycle progression by sodium butyrate in normal rat kidney fibroblasts is altered by expression of the adenovirus 5 early 1A gene. Biosci Rep 14, 291–300 (1994). https://doi.org/10.1007/BF01199053
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DOI: https://doi.org/10.1007/BF01199053