GLUT1 glucose transporter gene transcription is repressed by Sp3. Evidence for a regulatory role of Sp3 during myogenesis

Journal of Molecular Biology

Volumn 294, Issue 1, 1999, Pages 103-119

  Fandos, César ^a   Sánchez Feutrie, Manuela ^a   Santalucía, Tomàs ^a   Viñals, Francesc ^a   Cadefau, Joan ^a   Gumà, Anna ^a   Cussó, Roser ^a   Kaliman, Perla ^a   Canicio, Judith ^a   Palacín, Manuel ^a   Zorzano, Antonio ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Gene expression; Glucose transporters; Muscle cells; Sp1; Sp3

Indexed keywords

CELL EXTRACT; GLUCOSE TRANSPORTER; MYOD PROTEIN; REPRESSOR PROTEIN; SOMATOMEDIN BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP3; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; COMPETITIVE INHIBITION; CONTROLLED STUDY; DOWN REGULATION; FETUS HEART; GENE EXPRESSION; HUMAN; HUMAN CELL; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; RAT; TRANSCRIPTION REGULATION; TRANSLATION INITIATION;

ANIMALIA;

EID: 0344614690     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3216     Document Type: Article

References (49)

1. Apt D., Watts R. M., Suske G., Bernard H. U. High Sp1/Sp3 ratios in epithelial cells during epithelial differentiation and cellular transformation correlate with the activation of the HPV-16 promoter. Virology. 224:1996;281-291.
2. Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Smith J. A., Seidman J. G., Struhl K. Edited by Current Protocols in Molecular Biology. 1987;Wiley Interscience, New York.
3. Baldwin S. A. Mammalian passive glucose transporters: members of an ubiquitous family of active and passive transport proteins. Biochim. Biophys. Acta. 1154:1993;17-49.
4. Bessereau J. L., Laudenbach V., Le Poupon C., Changeux J. P. Nonmyogenic factors bind nicotinic acetylcholine receptor promoter elements required for response to denervation. J. Biol. Chem. 273:1998;12786-12793.
5. Bigger C. B., Melnikova I. N., Gardner P. D. Sp1 and Sp3 regulate expression of the neuronal nicotinic acetylcholine receptor beta4 subunit gene. J. Biol. Chem. 272:1997;25976-25982.
6. Block N. E., Menick D. R., Robinson K. A., Buse M. G. Effect of denervation on the expression of two glucose transporter isoforms in rat hindlimb muscle. J. Clin. Invest. 88:1991;1546-1552.
7. Boheler K., Chassagne C., Martin X., Wisnewsky C., Schwartz K. Cardiac expressions of alpha- and beta-myosin heavy chains and sarcomeric alpha-actins are regulated through transcriptional mechanisms. Results from nuclear run-on assays in isolated rat cardiac nuclei. J. Biol. Chem. 267:1992;12979-12985.
8. Camps M., Castelló A., Muñoz P., Monfar M., Testar X., Palacín M., Zorzano A. Effect of diabetes and fasting on GLUT-4 (muscle/fat) glucose-transporter expression in insulin-sensitive tissues. Heterogeneous response in heart, red and white muscle. Biochem. J. 282:1992;765-772.
9. Camps M., Vilaró S., Testar X., Palacín M., Zorzano A. High and polarized expression of GLUT1 glucose transporters in epithelial cells from mammary gland: acute down-regulation of GLUT1 carriers by weaning. Endocrinology. 134:1994;924-934.
10. Canicio J., Gallardo E., Illa I., Testar X., Palacín M., Zorzano A., Kaliman P. p70 S6 kinase activation is not required for insulin-like growth factor-induced differentiation of rat, mouse, or human skeletal muscle cells. Endocrinology. 139:1998;5042-5049.
11. Castelló A., Cadefau J., Cussó R., Testar X., Hesketh J. E., Palacín M., Zorzano A. GLUT-4 and GLUT-1 glucose transporter expression is differentially regulated by contractile activity in skeletal muscle. J. Biol. Chem. 268:1993;14998-15003.
12. Castelló A., Rodriguez-Manzaneque J. C., Camps M., Perez-Castillo A., Testar X., Palacin M., Santos A., Zorzano A. Perinatal hypothyroidism impairs the normal transition of GLUT4 and GLUT1 glucose transporters from fetal to neonatal levels in heart and brown adipose tissue. Evidence for tissue-specific regulation of GLUT4 expression by thyroid hormone. J. Biol. Chem. 269:1994;5905-5912.
13. Cherrington J. M., Mocarski E. S. Human cytomegalovirus ie1 transactivates the alpha promoter-enhancer via an 18-base-pair repeat element. J. Virol. 63:1989;1435-1440.
14. Clark C. M. Jr. Carbohydrate metabolism in the isolated fetal rat heart. Am. J. Physiol. 220:1971;583-588.
15. Coderre L., Monfar M., Chen K. S., Heydrick S. J., Kurowski T. G., Ruderman N. B., Pilch P. F. Alteration in the expression of GLUT-1 and GLUT-4 protein and messenger RNA levels in denervated rat muscles. Endocrinology. 131:1992;1821-1825.
16. De Luca P., Majello B., Lania L. Sp3 represses transcription when tethered to promoter DNA or targeted to promoter proximal RNA. J. Biol. Chem. 271:1996;8533-8536.
17. Dennig J., Beato M., Suske G. An inhibitor domain in Sp3 regulates its glutamine-rich activation domains. EMBO J. 15:1996;5659-5667.
18. De Vivo D. C., Trifiletti R. R., Jacobson R. I., Ronen G. M., Behmand R. A., Harik S. I. Defective glucose transport across the blood-brain barrier as a cause of persistent hypoglycorrhachia, seizures, and developmental delay. New Engl. J. Med. 325:1991;703-709.
19. Estévez R., Camps M., Testar X., Hediger M., Zorzano A., Palacín M. The amino acid transport system y+L/4F2hc is a heteromultimeric complex. FASEB J. 12:1998;1319-1329.
20. 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. 235:1987;1492-1495.
21. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1982;1044-1051.
22. Hagen G., Muller S., Beato M., Suske G. Cloning by recognition site screening of two novel GT box binding proteins: a family of Sp1 related genes. Nucl. Acids Res. 20:1992;5519-5525.
23. Hagen G., Müller S., Beato M., Suske G. Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13:1994;3843-3851.
24. Hagen G., Dennig J., Preiss A., Beato M., Suske G. Functional analyses of the transcription factor Sp4 reveal properties distinct from Sp1 and Sp3. J. Biol. Chem. 270:1995;24989-24994.
25. Henriksen E. J., Rodnick K. J., Mondon C. E., James D. E., Holloszy J. O. Effect of denervation or unweighting on GLUT-4 protein in rat soleus muscle. J. Appl. Physiol. 70:1991;2322-2327.
26. Hiraki Y., Rosen O. M., Birnbaum M. J. Growth factors rapidly induce expression of the glucose transporter gene. J. Biol. Chem. 263:1988;13655-13662.
27. Ihn H., Le Roy E. C., Trojanowska M. Oncostatin M stimulates transcription of the human alpha2(I) collagen gene via the Sp1/Sp3-binding site. J. Biol. Chem. 272:1997;24666-24672.
28. Imataka H., Sogawa K., Yasumoto K., Kikuchi Y., Sasano K., Kobayashi A., Hayami M., Fujii-Kuriyama Y. Two regulatory proteins that bind to the basic transcription element (BTE), a GC box sequence in the promoter region of the rat P-4501A1 gene. EMBO J. 11:1992;3663-3671.
29. Kaliman P., Viñals F., Testar X., Palacín M., Zorzano A. Phosphatidylinositol 3-kinase inhibitors block differentiation of skeletal muscle cells. J. Biol. Chem. 271:1996;19146-19151.
30. Kaliman P., Canicio J., Shepherd P. R., Beeton C. A., Testar X., Palacín M., Zorzano A. Insulin-like growth factors require phosphatidylinositol 3-kinase to signal myogenesis: dominant negative p85 expression blocks differentiation of L6E9 muscle cells. Mol. Endocrinol. 12:1998;66-77.
31. Kennett S. B., Udvadia A. J., Horowitz J. M. Sp3 encodes multiple proteins that differ in their capacity to stimulate or repress transcription. Nucl. Acids Res. 25:1997;3110-3117.
32. Kingsley C., Winoto A. Cloning of GT box-binding proteins: a novel Sp1 multigene family regulating T-cell receptor gene expression. Mol. Cell. Biol. 12:1992;4251-4261.
33. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
34. Liang Y., Robinson D. F., Dennig J., Suske G., Fahl W. E. Transcriptional regulation of the SIS/PDGF-B gene in human osteosarcoma cells by the Sp family of transcription factors. J. Biol. Chem. 271:1996;11792-11797.
35. Majello B., De Luca P., Hagen G., Suske G., Lania L. Different members of the Sp1 multigene family exert opposite transcriptional regulation of the long terminal repeat of HIV-1. Nucl. Acids Res. 22:1994;4914-4921.
36. Majello B., De Luca P., Suske G., Lania L. Differential transcriptional regulation of c-myc promoter through the same DNA binding sites targeted by Sp1-like proteins. Oncogene. 10:1995;1841-1848.
37. Majello B., De Luca P., Lania L. Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains. J. Biol. Chem. 272:1997;4021-4026.
38. Muñoz P., Mora S., Sevilla L., Kaliman P., Tomàs E., Gumà A., Testar X., Palacín M., Zorzano A. Expression and insulin-regulated distribution of caveolin in skeletal muscle. Caveolin does not colocalize with GLUT4 in intracellular membranes. J. Biol. Chem. 271:1996;8133-8139.
39. Netzker R., Weigert C., Brand K. Role of the stimulatory proteins Sp1 and Sp3 in the regulation of transcription of the rat pyruvate kinase M gene. Eur. J. Biochem. 245:1997;174-181.
40. Noti J. D. Sp3 mediates transcriptional activation of the leukocyte integrin genes CD11C and CD11B and cooperates with c-Jun to activate CD11C. J. Biol. Chem. 272:1997;24038-24045.
41. Rajakumar R. A., Thamotharan S., Menon R. K., Devaskar S. U. Sp1 and Sp3 regulate transcriptional activity of the facilitative glucose transporter isoform-3 gene in mammalian neuroblasts and trophoblasts. J. Biol. Chem. 273:1998;27474-27483.
42. Sack M. N., Disch D. L., Rockman H. A., Kelly D. P. A role for Sp and nuclear receptor transcription factors in a cardiac hypertrophic growth program. Proc. Natl Acad. Sci. USA. 94:1997;6438-6443.
43. Sambrook J., Fritsch E. F., Maniatis T. Molecular Cloning. A Laboratory Manual. 1989;. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
44. Santalucía T., Camps M., Castelló A., Muñoz P., Nuel A., Testar X., Palacín M., Zorzano A. Developmental regulation of GLUT-1 (erythroid/Hep G2) and GLUT-4 (muscle/fat) glucose transporter expression in rat heart, skeletal muscle, and brown adipose tissue. Endocrinology. 130:1992;837-846.
45. Santalucía T., Boheler K. R., Brand N. J., Sahye U., Fandos C., Viñals F., Ferré J., Testar X., Palacín M., Zorzano A. Factors involved in GLUT1 glucose transporter gene transcription in cardiac muscle. J. Biol. Chem. 274:1999;17626-17634.
46. Seidner G., García-Alvarez M., Yeh J. I., O'Driscoll K. R., Klepper J., Stump T. S., Wang D., Spinner N. B., Birnbaum M. J., De Vivo D. C. GLUT-1 deficiency syndrome caused by haploinsufficiency of the blood- brain barrier hexose carrier. Nature Genetics. 18:1998;188-191.
47. Sogawa K., Imataka H., Yamasaki Y., Kusume H., Abe H., Fujii-Kuriyama Y. cDNA cloning and transcriptional properties of a novel GC box-binding protein, BTEB2. Nucl. Acids Res. 21:1993;1527-1532.
48. Udvadia A. J., Templeton D. J., Horowitz J. M. Functional interactions between the retinoblastoma (Rb) protein and Sp- family members: superactivation by Rb requires amino acids necessary for growth suppression. Proc. Natl Acad. Sci. USA. 92:1995;3953-3957.
49. Viñals F., Fandos C., Santalucia T., Ferre J., Testar X., Palacin M., Zorzano A. Myogenesis and MyoD down-regulate Sp1. A mechanism for the repression of GLUT1 during muscle cell differentiation. J. Biol. Chem. 272:1997;12913-12921.