Site-specific methylation of the rat prolactin and growth hormone promoters correlates with gene expression

Molecular and Cellular Biology

Volumn 16, Issue 7, 1996, Pages 3245-3254

  Ngo V ^a,b   Gourdji, D ^a,c   Laverriere J N ^a,b  

^a l'alimentation et l'Environnement   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c CENTRE PAUL BROCA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE; PROLACTIN; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; DNA METHYLATION; GENE EXPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GROWTH HORMONE BLOOD LEVEL; HORMONE DETERMINATION; NONHUMAN; PRIORITY JOURNAL; PROLACTIN BLOOD LEVEL; PROMOTER REGION; RAT;

EID: 0029940384     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.16.7.3245     Document Type: Article

References (72)

1. Bach, I., S. J. Rhodes, R. V. Pearse II, T. Heinzel, B. Gloss, K. M. Scully, P. E. Sawchenko, and M. G. Rosenfeld. 1995. P-Lim, a LIM homeodomain factor, is expressed during pituitary organ and cell commitment and synergizes with Pit-1. Proc. Natl. Acad. Sci. USA 92:2720-2724.
2. Bodner, M., J.-L. Castrillo, L. E. Theill, T. Deerinck, M. Ellisman, and M. Karin. 1988. The pituitary-specific transcription factor GHF-1 is a homeobox-containing protein. Cell 55:505-518.
3. Borrelli, E., R. A. Heyman, C. Arias, P. E. Sawchenko, and R. M. Evans. 1989. Transgenic mice with inducible dwarfism. Nature (London) 339:538-541.
4. Boyes, J., and A. Bird. 1991. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64:1123-1134.
5. Boyes, J., and A. Bird. 1992. Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein. EMBO J. 11:327-333.
6. Bradford, A. P., K. E. Conrad, C. Wasylyk, B. Wasylyk, and A. Gutierrez-Hartmann. 1995. Functional interaction of c-Ets-1 and GHF1/Pit-1 mediates Ras activation of pituitary-specific gene expression: mapping of the essential c-Ets-1 domain. Mol. Cell. Biol. 15:2849-2857.
7. Brandeis, M., D. Frank, I. Keshet, Z. Siegfried, M. Mendelsohn, A. A. Nemes, V. Temper, A. Razin, and H. Cedar. 1994. Sp1 elements protect a CpG island from de novo melhylation. Nature (London) 371:435-438.
8. Brunet, N., D. Gourdji, M. F. Moreau, D. Grouselle, F. Bournaud, and A. Tixier-Vidal. 1977. Effect of 17-β-estradiol on prolactin secretion and thyroliherin responsiveness in two rat prolactin continuous cell lines. Definition of an experimental model. Ann. Biol. Anim. Biochim. Biophys. 17:413-424.
9. Bryans, M., S. Kass, C. Seivwright, and R. L. P. Adams. 1992. Vector methylation inhibits transcription from the SV40 early promoter. FEBS Lett. 309:97-102.
10. Cherington, P. V., and A. H. Tashjian, Jr. 1983. Clonal analysis of 5-azacytidine-induccd specific increase in growth hormone production by rat pituitary cells. Endocrinology 113:418.
11. Choi, Y.-C., and C.-B. Chae. 1991. DNA hypomethylation and germ cell-specific expression of lestis-specific H2B histone gene. J. Biol. Chem. 266:20504-20511.
12. Clark, S. J., J. Harrison, C. L. Paul, and M. Frommer. 1994. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 22:2990-2997.
13. Day, R. N., S. Koike, M. Sakai, M. Muramatsu, and R. A. Maurer. 1990. Both Pit-1 and the estrogen receptor are required for estrogen responsiveness of the rat prolactin gene. Mol. Endocrinol. 4:1964-1971.
14. Eden, S., and H. Cedar. 1994. Role of DNA methylation in the regulation of transcription. Curr. Opin. Genet. Dev. 4:255-259.
15. Ehrlich, M., and K. C. Ehrlieh. 1993. Effect of DNA methylation on the binding of vertebrate and plant proteins to DNA, p. 145-168. In J. P. Jost and H. P. Saluz (ed.), DNA methylation: molecular biology and biological significance. Birkhäuser Verlag, Basel.
16. Elsholtz, H. P., V. R. Albert, M. N. Treacy, and M. G. Rosenfeld. 1990. A two-base change in a POU factor-binding site switches pituitary-specific to lymphoid-specific gene expression. Genes Dev. 4:43-51.
17. Feil, R., J. Charlton, A. P. Bird, J. Walter, and W. Reik. 1994. Methylation analysis on individual chromosomes: improved protocol for bisulphite genomic sequencing. Nucleic Acids Res. 22:695-696.
18. Frommer, M., L. E. MacDonald, D. S. Millar, C. M. Collis, F. Watt, G. W. Grigg, P. L. Mollin, and C. L. Paul. 1992. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. USA 80:1827-1831.
19. Class, C. K., R. Franco, C. Weinberger, V. R. Albert, R. M. Evans, and M. G. Rosenfeld. 1987. A c-erb-A binding site in rat growth hormone gene mediates trans-activation by thyroid hormone. Nature (London) 329:738-741.
20. Gourdji, D., and J.-N. Laverrière. 1994. The rat prolactin gene: a target for tissue-specific and hormone-dependent transcription factors. Mol. Cell. Endocrinol. 100:133-142.
21. Gourdji, D., C. Tougard, and A. Tixier-Vidal. 1982. Clonal prolactin strains as a tool in neuroendocrinology. Front. Neuroendocrinol. 7:317-357.
22. Gutierrez-Hartmann, A. 1994. Insight: Pit-l/GHF-1: a pituitary-specific transcription factor linking general signaling pathways to cell-specific gene expression. Mol. Endocrinol, 8:1447-1449.
23. 3 pituitary cell-free extracts. Proc. Natl. Acad. Sci. USA 84:5211-5215.
24. Holliday, R. 1993. Epigenetic inheritance based on DNA methylation. p. 452-468. In J. P. Jost and H. P. Saluz (ed.), DNA methylation: molecular biology and biological significance. Birkhäuser Verlag, Basel.
25. Hornsby, P. J., L. Yang, S. G. Raju, and C. Y. Cheng. 1991. Changes in gene expression and DNA methylation in adrenocortical cells in culture. Mutat. Res. 256:105-113.
26. Hornstra, I. K., and T. P. Yang. 1994. High-resolution methylation analysis of the human hypoxanthine phosphoribosyltransferase gene 5′ region on the active and inactive X chromosomes: correlation with binding sites for transcription factors. Mol. Cell. Biol. 14:1419-1430.
27. Hsieh, C.-L. 1994. Dependence of transcriptional repression on CpG methylation density. Mol. Cell. Biol. 14:5487-5494.
28. Ivarie, R. D., B. S. Schacter, and P. O'Farrell. 1983. The level of expression of the rat growth hormone gene in liver tumor cells is at least eight orders of magnitude less than that in anterior pituitary cells. Mol. Cell. Biol. 3:1460-1467.
29. Jackson, S. M., C. A. Keech, D. J. Williamson, and A. Gulierrez-Hartmann. 1992. Interaction of basal positive and negative transcription elements controls repression of the proximal rat prolactin promoter in nonpituitary cells. Mol. Cell. Biol. 12:2708-2719.
30. Johnson, C. A., J. P. Goddard, and R. L. P. Adams. 1995. The effect of histone III and DNA methylation on transcription. Biochem. J. 305:791-798.
31. Jost, J. P., H. P. Saluz, and A. Pawlak. 1991. Estradiol down-regulates the binding activity of an avian vitellogenin gene repressor MDBP-2 and triggers a gradual demethylation of the mCpG pair of its DNA binding site. Nucleic Acids Res. 19:5771-5775.
32. Kass, S. U., J. P. Goddard, and R. L. P. Adams. 1993. Inactive chromatin spreads from a focus of methylation. Mol. Cell. Biol. 13:7372-7379.
33. Komura, J.-I., T. Okada, and T. Ono. 1995. Repression of transient expression by DNA methylation in transcribed regions of reporter genes introduced into cultured human cells. Biochim. Biophys. Acta 1260:73-78.
34. Larsen, P. R., J. W. Harney, and D. D. Moore. 1986. Repression mediates cell-type specific expression of the rat growth hormone gene. Proc. Natl. Acad. Sci. USA 83:8283-8287.
35. Laverrière, J.-N., A. Morin, A. Tixier-Vidal, A. T. Truong, D. Gourdji, and J. A. Martial. 1983. Inverse control of prolactin and growth hormone gene expression: effect of thyroliberin on transcription and RNA stabilization. EMBO J. 2:1493-1499.
36. Laverrière, J.-N., M. Muller, N. Buisson, C. Tougard, A. Tixier-Vidal, J. A. Martial, and D. Gourdji. 1986. Differential implication of deoxyribonucleic acid methylation in rat prolactin and rat growth hormone gene expressions: a comparison between rat pituitary cells strains. Endocrinology 118:198-206.
37. 3 cells. Neuroendocrinology 50:693-701.
38. Levine, A., G. L. Cantoni, and A. Razin. 1992. Methylation in the preimtiation domain suppresses gene transcription by an indirect mechanism. Proc. Natl. Acad. Sci. USA 89:10119-10123.
39. Levine, A., A. Yievin, E. Ben-Asher, Y. Aloni, and A. Razin. 1993. Histone H1-mediated inhibition of transcription initiation of methylated template in vitro. J. Biol. Chem. 268:21754-21759.
40. Liang, J., K. E. Kim, W. E. Schoderbek, and R. A. Maurer. 1992. Characterization of a nontissue-specific. 3′, 5′-cyclic adenosinc monophosphate-responsive element in the proximal region of the rat prolactin gene. Mol. Endocrinol. 6:885-892.
41. Lipkin, S. M., A. M. Näär, K. A. Kalla, R. A. Sack, and M. G. Rosenfeld. 1993. Identification of a novel zinc finger protein binding a conserved element critical for Pit-1-dependent growth hormone gene expression. Genes Dev. 7:1674-1687.
42. Mangalam, H. J., V. R. Albert, H. A. Ingraham, M. Kapiloff, L. Wilson, C. Nelson, H. P. Elsholtz, and M. G. Rosenfeld. 1989. A pituitary POU domain protein, Pit-1, activates both growth hormone and prolactin promoters transcriptionally. Genes Dev. 3:946-958.
43. Meehan, R. R., J. D. Lewis, and A. P. Bird. 1992. Characterization of MeCP2, a vertebrate DNA binding protein with affinity for methylated DNA. Nucleic Acids Res. 20:5085-5092.
44. Meyer, P., I. Niedenhof, and M. ten Lohuis. 1994. Evidence for cytosine methylation of non-symmetrical sequences in transgenic Petunia hybrida. EMBO J. 13:2084-2088.
45. Nelson, C., V. R. Albert, H. P. Elsholtz, W. Lti Li, and M. G. Rosenfeld. 1988. Activation of cell-specific expression of rat growth hormone and prolactin genes by a common transcription factor. Science 239:1400-1405.
46. Ngô, V., J. N. Laverrière, and D. Gourdji. 1993. Binding capacity and cis-acting efficiency of DNA regulatory sequences can be distinguished in an in vivo competition assay. Nucleic Acids Res. 21:5795-5796.
47. 3 pituitary cell lines. Mol. Cell. Endocrinol. 108:95-105.
48. Okimura, Y., P. W. Howard, and R. A. Maurer. 1994. Pit-1 binding sites mediate transcriptional responses to cyclic adenosine 3′, 5′-monophosphate through a mechanism that does not require inducible phosphorylation of Pit-1. Mol. Endocrinol. 8:1559-1565.
49. Pan, W. T., Q. R. Liu, and C. Bancroft. 1990. Identification of a growth hormone gene promoter represser element and its cognate double- and single-stranded DNA binding proteins. J. Biol. Chem. 265:7022-7028.
50. Park, J.-G., and V. M. Chapman. 1994. CpG island promoter region methylation patterns of the inactive-X-chromosome hypoxanthine phosphoribosyl-transferase (Hprt) gene. Mol. Cell. Biol. 14:7975-7983.
51. Pfeifer, G. P., S. D. Steigerwald, R. S. Hansen, S. M. Gartler, and A. D. Riggs. 1990. Polymerase chain reaction-aided genomic sequencing of an X chromosome-linked CpG island: methylation patterns suggest clonal inheritance, CpG autonomy, and an explanation of activity state stability. Proc. Natl. Acad. Sci. USA 87:8252-8256.
52. Pichon, B., C. Christophe-Hobertus, G. Vassart, and D. Christophe. 1994. Unmethylaled thyroglobulin promoter may be repressed by methylation of flanking DNA sequences. Biochem. J. 298:537-541.
53. Rajnarayan, S., M. Chiono, L. M. Alexander, and A. Gutierrez-Hartmann. 1995. Reconstitution of protein kinase A regulation of the rat prolactin promoter in HeLa nonpituitary cells: identification of both GHF-1/Pit-1 dependent and -independent mechanisms. Mol. Endocrinol. 9:502-512.
54. Reddy, P. M. S., G. Stamatoyannopoulos, T. Papayannopoulou, and C.-K. J. Shen. 1994. Genomic footprinting and sequencing of human β-globin locus. J. Biol. Chem. 269:8287-8295.
55. Reis, R. J. S., and S. Goldstein. 1982. Variability of DNA methylation patterns during serial passage of human diploid fibroblasts. Proc. Natl. Acad. Sci. USA 79:3949-3953.
56. Rosenfeld, M. G. 1991. POU-domain transcription factors: pou-er-ful developmental regulators. Genes Dev. 5:897-907.
57. Roy, R. J., L. Vallières, S. Leclerc, and S. Guérin. 1994. The rat growth hormone proximal silencer contains a novel DNA-binding site for multiple nuclear proteins that represses basal promoter activity. Eur. J Biochem. 225:419-432.
58. Saluz, H. P., J. Jiricny, and J. P. Jost. 1986. Genomic sequencing reveals a positive correlation between the kinetics of strand-specific DNA demethylation of the overlapping estradiol/glucocorticoid-receptor binding sites and the rate of the avian vitellogenin mRNA synthesis. Proc. Natl. Acad. Sci. USA 83:7167-7171.
59. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
60. Santoro, R., M. D'Enne, S. Mastrantonio, A. Reale, S. Marenz, H.-P. Saluz, R. Strom, and P. Caiafa. 1995. Binding of historic H1e-c variants to CpG-rich DNA correlates with the inhibitory effect on enzymic DNA methylation. Biochem. J. 305:739-744.
61. Schaufele, F., J. A. Cassill, B. L. West, and T. Reudelhuber. 1990. Resolution by diagonal gel mobility shift assays of multisubunit complexes binding to a functionally important element of the rat growth hormone gene promoter. J. Biol. Chem. 265:14592-14598.
62. Seidah, N. G., J.-C. Barale, M. Marcinkitwicz, M.-G. Mattel, R. Day, and M. Chretien. 1994. The mouse homeoprotein mLIM-3 is expressed early in cells derived from the neuroepithelium and persists in adult pituitary. DNA Cell Biol. 13:1163-1180.
63. Silva, A. J., K. Ward, and R. White. 1993. Mosaic methylation in clonal tissue. Dev. Biol. 156:391-398.
64. Simmons, D. M., J. W. Voss, H. A. Ingraham, J. M. Holloway, R. S. Broide, M. G. Rosenfeld, and L. W. Swanson. 1990. Pituitary cell phenotype involves cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Genes Dev. 4:695-711.
65. Slatko, B. E., and L. M. Albright. 1994. Thermal cycle sequencing reactions using 5′ end-labeled primers. In F. M. Ausubet, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. Greene Publishing Associates and Wiley Interscience, New York.
66. Steel, R. G. D., and J. H. Tome. 1960. Principles and procedures of statistics with special reference to the biological sciences, p. 379-380. McGraw-Hill Book Co., Inc., New York.
67. Szyf, M., J. Rouleau, J. Theberge, and V. Bozovic. 1992. Induction of myogenic differentiation by an expression vector encoding the DNA methyltransferase cDNA sequence in the antisense orientation. J. Biol. Chem. 267:12831-12836.
68. Tate, P. H., and A. P. Bird. 1993. Effects of DNA methylation on DNA-binding proteins and gene expression. Curr. Opin. Genet. Dev. 3:226-231.
69. Theill, L. E., and M. Karin. 1993. Transcriptional control of GH expression and anterior pituitary development. Endocrine Rev. 14:670-689.
70. Toth, M., U. Lichtenberg, and W. Doerfler. 1989. Genomic sequencing reveals a 5-methylcytosine-free domain in active promoters and the spreading of preimposed methylation patterns. Proc. Natl. Acad. Sci. USA 86:3728-3732.
71. Voss, J. W., L. Wilson, and M. G. Rosenfeld. 1991. POU-domain proteins Pit-1 and Oct-1 interact to form a heterodimeric complex and can cooperate to induce expression of the prolactin promoter. Genes Dev. 5:1309-1320.
72. Zhang, Z. X., V. Kumar, R. T. Rivera, S. G. Pasion, J. Chilshom, and D. K. Biswas. 1989. Suppression of prolactin gene expression in GH cells correlates with site-specific DNA methylation. DNA 8:605-613.