Skip to main content
PMC home page
Biochemical Journal logoLink to Biochemical Journal
. 1995 Oct 15;311(Pt 2):567–573. doi: 10.1042/bj3110567

Differential modulation of expression of the two acylphosphatase isoenzymes by thyroid hormone.

P Chiarugi 1, G Raugei 1, R Marzocchini 1, T Fiaschi 1, C Ciccarelli 1, A Berti 1, G Ramponi 1
PMCID: PMC1136037  PMID: 7487897

Abstract

The modulation of expression of the skeletal muscle and erythrocyte acylphosphatase isoenzymes by thyroid hormone has been investigated. Our results indicate a differential regulation of the two enzymic isoforms by tri-iodothyronine (T3) in K562 cells in culture: an increase in the specific mRNA during T3-stimulation is shown only for the skeletal muscle isoenzyme. A fast and transient T3 induction of the accumulation of the specific mRNA can be observed, reaching a maximum 8 h after hormone treatment and then rapidly decreasing almost to the steady-state level after 24 h. A nuclear run-on assay was performed to explore the mechanisms of this regulation. These studies indicate that T3 induction of skeletal muscle acylphosphatase mRNA is due, at least in part, to a fast and transient increase in the rate of gene transcription, within 4 h after hormone administration. A very rapid decrease is then observed within a further 2 h. T3-dependent accumulation of the mRNA for the skeletal muscle acylphosphatase requires ongoing protein synthesis, as confirmed by inhibition with cycloheximide or puromycin. These findings indicate that the transcriptional regulation of the gene may be indirect.

Full text

PDF
567

Images in this article

570Figure 2
on p.570

Selected References

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

  1. Arumanayagam M., Swaminathan R. Stimulation of the Na+,K(+)-ATPase activity of K562 human erythroleukemia cells by triiodothyronine. Life Sci. 1992;51(25):1913–1920. doi: 10.1016/0024-3205(92)90107-z. [DOI] [PubMed] [Google Scholar]
  2. BACCARI V., GUERRITORE A., RAMPONI G., SABATELLI M. P. [Action of acyl phosphatases on glycolysis]. Boll Soc Ital Biol Sper. 1960 Apr 30;36:360–362. [PubMed] [Google Scholar]
  3. Berti A., Degl'Innocenti D., Stefani M., Ramponi G. Expression and turnover of acylphosphatase (muscular isoenzyme) in L6 myoblasts during myogenesis. Arch Biochem Biophys. 1992 Apr;294(1):261–264. doi: 10.1016/0003-9861(92)90166-t. [DOI] [PubMed] [Google Scholar]
  4. Berti A., Stefani M., Degl'Innocenti D., Ruggiero M., Chiarugi V., Ramponi G. Effect of exogenously added acylphosphatases on inositol lipid metabolism in human platelets. FEBS Lett. 1988 Aug 1;235(1-2):229–232. doi: 10.1016/0014-5793(88)81268-7. [DOI] [PubMed] [Google Scholar]
  5. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  6. Cleveland D. W., Lopata M. A., MacDonald R. J., Cowan N. J., Rutter W. J., Kirschner M. W. Number and evolutionary conservation of alpha- and beta-tubulin and cytoplasmic beta- and gamma-actin genes using specific cloned cDNA probes. Cell. 1980 May;20(1):95–105. doi: 10.1016/0092-8674(80)90238-x. [DOI] [PubMed] [Google Scholar]
  7. Elgin S. C. The formation and function of DNase I hypersensitive sites in the process of gene activation. J Biol Chem. 1988 Dec 25;263(36):19259–19262. [PubMed] [Google Scholar]
  8. Fan H., Penman S. Regulation of protein synthesis in mammalian cells. II. Inhibition of protein synthesis at the level of initiation during mitosis. J Mol Biol. 1970 Jun 28;50(3):655–670. doi: 10.1016/0022-2836(70)90091-4. [DOI] [PubMed] [Google Scholar]
  9. Groudine M., Casimir C. Post-transcriptional regulation of the chicken thymidine kinase gene. Nucleic Acids Res. 1984 Feb 10;12(3):1427–1446. doi: 10.1093/nar/12.3.1427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Groudine M., Peretz M., Weintraub H. Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol. 1981 Mar;1(3):281–288. doi: 10.1128/mcb.1.3.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. HARARY I. The hydrolysis of 1,3-diphosphoglyceric acid by acyl phosphatase. Biochim Biophys Acta. 1957 Nov;26(2):434–436. doi: 10.1016/0006-3002(57)90032-x. [DOI] [PubMed] [Google Scholar]
  12. Hokin L. E., Sastry P. S., Galsworthy P. R., Yoda A. Evidence that a phosphorylated intermediate in a brain transport adenosine triphosphatase is an acyl phosphate. Proc Natl Acad Sci U S A. 1965 Jul;54(1):177–184. doi: 10.1073/pnas.54.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jacoby D. B., Engle J. A., Towle H. C. Induction of a rapidly responsive hepatic gene product by thyroid hormone requires ongoing protein synthesis. Mol Cell Biol. 1987 Apr;7(4):1352–1357. doi: 10.1128/mcb.7.4.1352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  15. Liguri G., Camici G., Manao G., Cappugi G., Nassi P., Modesti A., Ramponi G. A new acylphosphatase isoenzyme from human erythrocytes: purification, characterization, and primary structure. Biochemistry. 1986 Dec 2;25(24):8089–8094. doi: 10.1021/bi00372a044. [DOI] [PubMed] [Google Scholar]
  16. MOKRASCH L. C. Acylphosphatase and adenosinetriphosphatase of hibernating hamsters. Am J Physiol. 1960 Nov;199:950–954. doi: 10.1152/ajplegacy.1960.199.5.950. [DOI] [PubMed] [Google Scholar]
  17. Manao G., Camici G., Cappugi G., Stefani M., Liguri G., Berti A., Ramponi G. Rabbit skeletal muscle acylphosphatase: the amino acid sequence of form Ra1. Arch Biochem Biophys. 1985 Sep;241(2):418–424. doi: 10.1016/0003-9861(85)90565-x. [DOI] [PubMed] [Google Scholar]
  18. Nassi P., Liguri G., Nediani C., Taddei N., Piccinni P., Degl'Innocenti D., Gheri R. G., Ramponi G. Increased acylphosphatase levels in erythrocytes from hyperthyroid patients. Clin Chim Acta. 1989 Aug 31;183(3):351–358. doi: 10.1016/0009-8981(89)90370-7. [DOI] [PubMed] [Google Scholar]
  19. Nassi P., Liguri G., Nediani C., Taddei N., Ramponi G. Increased acylphosphatase levels in erythrocytes, muscle and liver of tri-iodothyronine treated rabbits. Horm Metab Res. 1990 Jan;22(1):33–37. doi: 10.1055/s-2007-1004843. [DOI] [PubMed] [Google Scholar]
  20. Nassi P., Nediani C., Liguri G., Taddei N., Ramponi G. Effects of acylphosphatase on the activity of erythrocyte membrane Ca2+ pump. J Biol Chem. 1991 Jun 15;266(17):10867–10871. [PubMed] [Google Scholar]
  21. Piechaczyk M., Blanchard J. M., Marty L., Dani C., Panabieres F., El Sabouty S., Fort P., Jeanteur P. Post-transcriptional regulation of glyceraldehyde-3-phosphate-dehydrogenase gene expression in rat tissues. Nucleic Acids Res. 1984 Sep 25;12(18):6951–6963. doi: 10.1093/nar/12.18.6951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ramponi G. 1, 3-diphosphoglycerate phosphatase. Methods Enzymol. 1975;42:409–426. doi: 10.1016/0076-6879(75)42147-4. [DOI] [PubMed] [Google Scholar]
  23. Ramponi G., Liguri G., Nediani C., Stefani M., Taddei N., Nassi P. Acylphosphatase increases the rate of ethanol production from glucose in cell-free extracts of Saccharomyces cerevisiae. Biotechnol Appl Biochem. 1988 Oct;10(5):408–413. [PubMed] [Google Scholar]
  24. Salati L. M., Ma X. J., McCormick C. C., Stapleton S. R., Goodridge A. G. Triiodothyronine stimulates and cyclic AMP inhibits transcription of the gene for malic enzyme in chick embryo hepatocytes in culture. J Biol Chem. 1991 Feb 25;266(6):4010–4016. [PubMed] [Google Scholar]
  25. Samuels H. H., Forman B. M., Horowitz Z. D., Ye Z. S. Regulation of gene expression by thyroid hormone. Annu Rev Physiol. 1989;51:623–639. doi: 10.1146/annurev.ph.51.030189.003203. [DOI] [PubMed] [Google Scholar]
  26. Samuels H. H., Stanley F., Casanova J. Depletion of L-3,5,3'-triiodothyronine and L-thyroxine in euthyroid calf serum for use in cell culture studies of the action of thyroid hormone. Endocrinology. 1979 Jul;105(1):80–85. doi: 10.1210/endo-105-1-80. [DOI] [PubMed] [Google Scholar]
  27. Song M. K., Dozin B., Grieco D., Rall J. E., Nikodem V. M. Transcriptional activation and stabilization of malic enzyme mRNA precursor by thyroid hormone. J Biol Chem. 1988 Dec 5;263(34):17970–17974. [PubMed] [Google Scholar]
  28. Stefani M., Liguri G., Berti A., Nassi P., Ramponi G. Hydrolysis by horse muscle acylphosphatase of (Ca2+ + Mg2+)-ATPase phosphorylated intermediate. Arch Biochem Biophys. 1981 Apr 15;208(1):37–41. doi: 10.1016/0003-9861(81)90120-x. [DOI] [PubMed] [Google Scholar]
  29. TRAUT R. R., MONRO R. E. THE PUROMYCIN REACTION AND ITS RELATION TO PROTEIN SYNTHESIS. J Mol Biol. 1964 Oct;10:63–72. doi: 10.1016/s0022-2836(64)80028-0. [DOI] [PubMed] [Google Scholar]
  30. Tabilio A., Pelicci P. G., Vinci G., Mannoni P., Civin C. I., Vainchenker W., Testa U., Lipinski M., Rochant H., Breton-Gorius J. Myeloid and megakaryocytic properties of K-562 cell lines. Cancer Res. 1983 Oct;43(10):4569–4574. [PubMed] [Google Scholar]
  31. Ucker D. S., Yamamoto K. R. Early events in the stimulation of mammary tumor virus RNA synthesis by glucocorticoids. Novel assays of transcription rates. J Biol Chem. 1984 Jun 25;259(12):7416–7420. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES