Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1988 Nov;85(21):8072–8075. doi: 10.1073/pnas.85.21.8072

Sodium butyrate increases glucose transporter expression in LLC-PK1 cells.

M Takano 1, D B Rhoads 1, K J Isselbacher 1
PMCID: PMC282356  PMID: 3186708

Abstract

The effect of sodium butyrate on the expression of the facilitated glucose transporter (GT) was investigated in the pig kidney cell line LLC-PK1. When cells were treated with butyrate, GT mRNA expression was remarkably enhanced with a maximal effect at 5 mM. Levels of GT mRNA were increased at 1 day after butyrate treatment and continued to increase for at least 4 days; however, acetate and propionate did not affect GT mRNA levels significantly. The induction of GT mRNA by butyrate was accompanied by an increase in GT function. The expression of GT mRNA decreased in HepG2, HT-29, and COS cells by treatment with butyrate for 1 day. Interestingly, glucose deprivation of LLC-PK1 cells reduced the induction of GT mRNA by butyrate, although starvation itself slightly enhanced steady-state GT mRNA levels. Therefore, expression of GT in LLC-PK1 cells is strongly induced by butyrate by a pathway that apparently depends on the presence of glucose in culture medium.

Full text

PDF
8072

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson J. W., Bridges S. R. Short-chain fatty acid fermentation products of plant fiber affect glucose metabolism of isolated rat hepatocytes. Proc Soc Exp Biol Med. 1984 Nov;177(2):372–376. doi: 10.3181/00379727-177-41958. [DOI] [PubMed] [Google Scholar]
  2. Birnbaum M. J., Haspel H. C., Rosen O. M. Cloning and characterization of a cDNA encoding the rat brain glucose-transporter protein. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5784–5788. doi: 10.1073/pnas.83.16.5784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Birnbaum M. J., Haspel H. C., Rosen O. M. Transformation of rat fibroblasts by FSV rapidly increases glucose transporter gene transcription. Science. 1987 Mar 20;235(4795):1495–1498. doi: 10.1126/science.3029870. [DOI] [PubMed] [Google Scholar]
  4. Birren B. W., Herschman H. R. Regulation of the rat metallothionein-I gene by sodium butyrate. Nucleic Acids Res. 1986 Jan 24;14(2):853–867. doi: 10.1093/nar/14.2.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Byrd J. C., Lichti U. Two types of transglutaminase in the PC12 pheochromocytoma cell line. Stimulation by sodium butyrate. J Biol Chem. 1987 Aug 25;262(24):11699–11705. [PubMed] [Google Scholar]
  6. Cox G. S., McClure D. S., Cosgrove D. E. Dual effects of 2-deoxyglucose on synthesis of the glycoprotein hormone common alpha-subunit in butyrate-treated HeLa cells. Mol Cell Biol. 1987 May;7(5):1592–1601. doi: 10.1128/mcb.7.5.1592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Darnell R. B. Independent regulation by sodium butyrate of gonadotropin alpha gene expression and cell cycle progression in HeLa cells. Mol Cell Biol. 1984 May;4(5):829–839. doi: 10.1128/mcb.4.5.829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dobson M. E., Ingram V. M. In vitro transcription of chromatin containing histones hyperacetylated in vivo. Nucleic Acids Res. 1980 Sep 25;8(18):4201–4219. doi: 10.1093/nar/8.18.4201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Flier J. S., Mueckler M. M., Usher P., Lodish H. F. Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science. 1987 Mar 20;235(4795):1492–1495. doi: 10.1126/science.3103217. [DOI] [PubMed] [Google Scholar]
  10. Flier J. S., Mueckler M., McCall A. L., Lodish H. F. Distribution of glucose transporter messenger RNA transcripts in tissues of rat and man. J Clin Invest. 1987 Feb;79(2):657–661. doi: 10.1172/JCI112864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gattoni-Celli S., Kirsch K., Kalled S., Isselbacher K. J. Expression of type C-related endogenous retroviral sequences in human colon tumors and colon cancer cell lines. Proc Natl Acad Sci U S A. 1986 Aug;83(16):6127–6131. doi: 10.1073/pnas.83.16.6127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gluzman Y. SV40-transformed simian cells support the replication of early SV40 mutants. Cell. 1981 Jan;23(1):175–182. doi: 10.1016/0092-8674(81)90282-8. [DOI] [PubMed] [Google Scholar]
  13. Handler J. S. Use of cultured epithelia to study transport and its regulation. J Exp Biol. 1983 Sep;106:55–69. doi: 10.1242/jeb.106.1.55. [DOI] [PubMed] [Google Scholar]
  14. Haspel H. C., Wilk E. W., Birnbaum M. J., Cushman S. W., Rosen O. M. Glucose deprivation and hexose transporter polypeptides of murine fibroblasts. J Biol Chem. 1986 May 25;261(15):6778–6789. [PubMed] [Google Scholar]
  15. Hediger M. A., Coady M. J., Ikeda T. S., Wright E. M. Expression cloning and cDNA sequencing of the Na+/glucose co-transporter. 1987 Nov 26-Dec 2Nature. 330(6146):379–381. doi: 10.1038/330379a0. [DOI] [PubMed] [Google Scholar]
  16. Hull R. N., Cherry W. R., Weaver G. W. The origin and characteristics of a pig kidney cell strain, LLC-PK. In Vitro. 1976 Oct;12(10):670–677. doi: 10.1007/BF02797469. [DOI] [PubMed] [Google Scholar]
  17. Inui K. I., Tillotson L. G., Isselbacher K. J. Hexose and amino acid transport by chicken embryo fibroblasts infected with temperature-sensitive mutant of Rous sarcoma virus. Comparison of transport properties of whole cells and membrane vesicles. Biochim Biophys Acta. 1980 Jun 6;598(3):616–627. doi: 10.1016/0005-2736(80)90041-3. [DOI] [PubMed] [Google Scholar]
  18. Kasahara M., Inui K., Takano M., Hori R. Distinction of three types of D-glucose transport systems in animal cells. Biochem Biophys Res Commun. 1985 Oct 30;132(2):490–496. doi: 10.1016/0006-291x(85)91160-x. [DOI] [PubMed] [Google Scholar]
  19. Kletzien R. F., Perdue J. F. Induction of sugar transport in chick embryo fibroblasts by hexose starvation. Evidence for transcriptional regulation of transport. J Biol Chem. 1975 Jan 25;250(2):593–600. [PubMed] [Google Scholar]
  20. Knowles B. B., Howe C. C., Aden D. P. Human hepatocellular carcinoma cell lines secrete the major plasma proteins and hepatitis B surface antigen. Science. 1980 Jul 25;209(4455):497–499. doi: 10.1126/science.6248960. [DOI] [PubMed] [Google Scholar]
  21. McClure D. S., Cox G. S. Glucose requirement for induction by sodium butyrate of the glycoprotein hormone alpha subunit in HeLa cells. Arch Biochem Biophys. 1984 Aug 15;233(1):93–105. doi: 10.1016/0003-9861(84)90605-2. [DOI] [PubMed] [Google Scholar]
  22. McKnight G. S., Hager L., Palmiter R. D. Butyrate and related inhibitors of histone deacetylation block the induction of egg white genes by steroid hormones. Cell. 1980 Nov;22(2 Pt 2):469–477. doi: 10.1016/0092-8674(80)90357-8. [DOI] [PubMed] [Google Scholar]
  23. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Misfeldt D. S., Sanders M. J. Transepithelial transport in cell culture: D-glucose transport by a pig kidney cell line (LLC-PK1). J Membr Biol. 1981 Mar 15;59(1):13–18. doi: 10.1007/BF01870816. [DOI] [PubMed] [Google Scholar]
  25. Mueckler M., Caruso C., Baldwin S. A., Panico M., Blench I., Morris H. R., Allard W. J., Lienhard G. E., Lodish H. F. Sequence and structure of a human glucose transporter. Science. 1985 Sep 6;229(4717):941–945. doi: 10.1126/science.3839598. [DOI] [PubMed] [Google Scholar]
  26. O'Brien T. G. Hexose transport in undifferentiated and differentiated BALB/c 3T3 preadipose cells: effects 12-O-tetradecanoylphorbol-13-acetate and insulin. J Cell Physiol. 1982 Jan;110(1):63–71. doi: 10.1002/jcp.1041100111. [DOI] [PubMed] [Google Scholar]
  27. Pessin J. E., Tillotson L. G., Yamada K., Gitomer W., Carter-Su C., Mora R., Isselbacher K. J., Czech M. P. Identification of the stereospecific hexose transporter from starved and fed chicken embryo fibroblasts. Proc Natl Acad Sci U S A. 1982 Apr;79(7):2286–2290. doi: 10.1073/pnas.79.7.2286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Prasad K. N., Sinha P. K. Effect of sodium butyrate on mammalian cells in culture: a review. In Vitro. 1976 Feb;12(2):125–132. doi: 10.1007/BF02796360. [DOI] [PubMed] [Google Scholar]
  29. Rabito C. A., Ausiello D. A. Na+-dependent sugar transport in a cultured epithelial cell line from pig kidney. J Membr Biol. 1980;54(1):31–38. doi: 10.1007/BF01875374. [DOI] [PubMed] [Google Scholar]
  30. Reeves R. Transcriptionally active chromatin. Biochim Biophys Acta. 1984 Sep 10;782(4):343–393. doi: 10.1016/0167-4781(84)90044-7. [DOI] [PubMed] [Google Scholar]
  31. Rouault T. A., Hentze M. W., Dancis A., Caughman W., Harford J. B., Klausner R. D. Influence of altered transcription on the translational control of human ferritin expression. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6335–6339. doi: 10.1073/pnas.84.18.6335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sealy L., Chalkley R. The effect of sodium butyrate on histone modification. Cell. 1978 May;14(1):115–121. doi: 10.1016/0092-8674(78)90306-9. [DOI] [PubMed] [Google Scholar]
  33. Silverman M. Glucose transport in the kidney. Biochim Biophys Acta. 1976 Dec 14;457(3-4):303–351. doi: 10.1016/0304-4157(76)90003-4. [DOI] [PubMed] [Google Scholar]
  34. Simpson I. A., Cushman S. W. Hormonal regulation of mammalian glucose transport. Annu Rev Biochem. 1986;55:1059–1089. doi: 10.1146/annurev.bi.55.070186.005211. [DOI] [PubMed] [Google Scholar]
  35. Toyoda N., Robinson F. W., Smith M. M., Flanagan J. E., Kono T. Apparent translocation of glucose transport activity in rat epididymal adipocytes by insulin-like effects of high pH or hyperosmolarity. J Biol Chem. 1986 Feb 15;261(5):2117–2122. [PubMed] [Google Scholar]
  36. White M. K., Weber M. J. Transformation by the src oncogene alters glucose transport into rat and chicken cells by different mechanisms. Mol Cell Biol. 1988 Jan;8(1):138–144. doi: 10.1128/mcb.8.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yamada K., Tillotson L. G., Isselbacher K. J. Regulation of hexose carriers in chicken embryo fibroblasts. Effect of glucose starvation and role of protein synthesis. J Biol Chem. 1983 Aug 25;258(16):9786–9792. [PubMed] [Google Scholar]
  38. Yamada K., Tillotson L. G., Isselbacher K. J. Regulation of hexose transporters in chicken embryo fibroblasts: stimulation by the phorbol ester TPA leads to increased numbers of functioning transporters. J Cell Physiol. 1986 May;127(2):211–215. doi: 10.1002/jcp.1041270204. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES