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. 1993 Apr 25;21(8):1873–1879. doi: 10.1093/nar/21.8.1873

Transactivation of mouse insulin-like growth factor II (IGF-II) gene promoters by the AP-1 complex.

A Caricasole 1, A Ward 1
PMCID: PMC309427  PMID: 8493103

Abstract

The mouse insulin-like growth factor II gene (Igf2) is transcribed from three promoters (P1, P2 and P3), and is expressed in a tissue-specific and developmentally regulated fashion; however, little information is available on the transcription factors controlling Igf2 expression. The AP-1 complex is a transcription factor involved in the regulation of a variety of genes, including those encoding certain growth factors. We show that Igf2 P3 is transactivated by AP-1 in a transient expression assay, and that this effect is mediated through two non-consensus AP-1 binding sites characterised by DNA-protein interaction studies. Mutational analysis indicates these sites are required for AP-1 responsiveness and full promoter activity.

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  1. Andrews N. C., Faller D. V. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 1991 May 11;19(9):2499–2499. doi: 10.1093/nar/19.9.2499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Angel P., Hattori K., Smeal T., Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 1988 Dec 2;55(5):875–885. doi: 10.1016/0092-8674(88)90143-2. [DOI] [PubMed] [Google Scholar]
  3. Angel P., Imagawa M., Chiu R., Stein B., Imbra R. J., Rahmsdorf H. J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987 Jun 19;49(6):729–739. doi: 10.1016/0092-8674(87)90611-8. [DOI] [PubMed] [Google Scholar]
  4. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  5. Beddington R. S., Morgernstern J., Land H., Hogan A. An in situ transgenic enzyme marker for the midgestation mouse embryo and the visualization of inner cell mass clones during early organogenesis. Development. 1989 May;106(1):37–46. doi: 10.1242/dev.106.1.37. [DOI] [PubMed] [Google Scholar]
  6. Bishopric N. H., Jayasena V., Webster K. A. Positive regulation of the skeletal alpha-actin gene by Fos and Jun in cardiac myocytes. J Biol Chem. 1992 Dec 15;267(35):25535–25540. [PubMed] [Google Scholar]
  7. Bradley A., Evans M., Kaufman M. H., Robertson E. Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature. 1984 May 17;309(5965):255–256. doi: 10.1038/309255a0. [DOI] [PubMed] [Google Scholar]
  8. Caricasole A., Ward A. A luciferase-reporter vector with blue-white selection for rapid subcloning and mutational analysis of eukaryotic promoters. Gene. 1993 Feb 14;124(1):139–140. doi: 10.1016/0378-1119(93)90777-z. [DOI] [PubMed] [Google Scholar]
  9. Caubet J. F., Bernaudin J. F. Expression of the c-fos proto-oncogene in bone, cartilage and tooth forming tissues during mouse development. Biol Cell. 1988;64(1):101–104. doi: 10.1016/0248-4900(88)90100-1. [DOI] [PubMed] [Google Scholar]
  10. DeChiara T. M., Efstratiadis A., Robertson E. J. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature. 1990 May 3;345(6270):78–80. doi: 10.1038/345078a0. [DOI] [PubMed] [Google Scholar]
  11. DeChiara T. M., Robertson E. J., Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell. 1991 Feb 22;64(4):849–859. doi: 10.1016/0092-8674(91)90513-x. [DOI] [PubMed] [Google Scholar]
  12. Diamond M. I., Miner J. N., Yoshinaga S. K., Yamamoto K. R. Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science. 1990 Sep 14;249(4974):1266–1272. doi: 10.1126/science.2119054. [DOI] [PubMed] [Google Scholar]
  13. Drummond I. A., Madden S. L., Rohwer-Nutter P., Bell G. I., Sukhatme V. P., Rauscher F. J., 3rd Repression of the insulin-like growth factor II gene by the Wilms tumor suppressor WT1. Science. 1992 Jul 31;257(5070):674–678. doi: 10.1126/science.1323141. [DOI] [PubMed] [Google Scholar]
  14. Evans T., DeChiara T., Efstratiadis A. A promoter of the rat insulin-like growth factor II gene consists of minimal control elements. J Mol Biol. 1988 Jan 5;199(1):61–81. doi: 10.1016/0022-2836(88)90379-8. [DOI] [PubMed] [Google Scholar]
  15. Faisst S., Meyer S. Compilation of vertebrate-encoded transcription factors. Nucleic Acids Res. 1992 Jan 11;20(1):3–26. doi: 10.1093/nar/20.1.3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gaub M. P., Bellard M., Scheuer I., Chambon P., Sassone-Corsi P. Activation of the ovalbumin gene by the estrogen receptor involves the fos-jun complex. Cell. 1990 Dec 21;63(6):1267–1276. doi: 10.1016/0092-8674(90)90422-b. [DOI] [PubMed] [Google Scholar]
  17. Gutman A., Wasylyk B. The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites. EMBO J. 1990 Jul;9(7):2241–2246. doi: 10.1002/j.1460-2075.1990.tb07394.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Heine U., Munoz E. F., Flanders K. C., Ellingsworth L. R., Lam H. Y., Thompson N. L., Roberts A. B., Sporn M. B. Role of transforming growth factor-beta in the development of the mouse embryo. J Cell Biol. 1987 Dec;105(6 Pt 2):2861–2876. doi: 10.1083/jcb.105.6.2861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hornes E., Korsnes L. Magnetic DNA hybridization properties of oligonucleotide probes attached to superparamagnetic beads and their use in the isolation of poly(A) mRNA from eukaryotic cells. Genet Anal Tech Appl. 1990 Oct;7(6):145–150. doi: 10.1016/0735-0651(90)90028-e. [DOI] [PubMed] [Google Scholar]
  20. Imbra R. J., Karin M. Phorbol ester induces the transcriptional stimulatory activity of the SV40 enhancer. Nature. 1986 Oct 9;323(6088):555–558. doi: 10.1038/323555a0. [DOI] [PubMed] [Google Scholar]
  21. Kim S. J., Denhez F., Kim K. Y., Holt J. T., Sporn M. B., Roberts A. B. Activation of the second promoter of the transforming growth factor-beta 1 gene by transforming growth factor-beta 1 and phorbol ester occurs through the same target sequences. J Biol Chem. 1989 Nov 15;264(32):19373–19378. [PubMed] [Google Scholar]
  22. Kitabayashi I., Kawakami Z., Chiu R., Ozawa K., Matsuoka T., Toyoshima S., Umesono K., Evans R. M., Gachelin G., Yokoyama K. Transcriptional regulation of the c-jun gene by retinoic acid and E1A during differentiation of F9 cells. EMBO J. 1992 Jan;11(1):167–175. doi: 10.1002/j.1460-2075.1992.tb05039.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lee J. E., Pintar J., Efstratiadis A. Pattern of the insulin-like growth factor II gene expression during early mouse embryogenesis. Development. 1990 Sep;110(1):151–159. doi: 10.1242/dev.110.1.151. [DOI] [PubMed] [Google Scholar]
  24. Lee W., Haslinger A., Karin M., Tjian R. Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40. Nature. 1987 Jan 22;325(6102):368–372. doi: 10.1038/325368a0. [DOI] [PubMed] [Google Scholar]
  25. Matsuguchi T., Takahashi K., Ikejiri K., Ueno T., Endo H., Yamamoto M. Functional analysis of multiple promoters of the rat insulin-like factor II gene. Biochim Biophys Acta. 1990 Apr 6;1048(2-3):165–170. doi: 10.1016/0167-4781(90)90052-4. [DOI] [PubMed] [Google Scholar]
  26. Mummery C. L., van den Eijnden-van Raaij A. J. Growth factors and their receptors in differentiation and early murine development. Cell Differ Dev. 1990 Apr;30(1):1–18. doi: 10.1016/0922-3371(90)90069-9. [DOI] [PubMed] [Google Scholar]
  27. Nomura S., Wills A. J., Edwards D. R., Heath J. K., Hogan B. L. Developmental expression of 2ar (osteopontin) and SPARC (osteonectin) RNA as revealed by in situ hybridization. J Cell Biol. 1988 Feb;106(2):441–450. doi: 10.1083/jcb.106.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Owen T. A., Bortell R., Yocum S. A., Smock S. L., Zhang M., Abate C., Shalhoub V., Aronin N., Wright K. L., van Wijnen A. J. Coordinate occupancy of AP-1 sites in the vitamin D-responsive and CCAAT box elements by Fos-Jun in the osteocalcin gene: model for phenotype suppression of transcription. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9990–9994. doi: 10.1073/pnas.87.24.9990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Raizis A. M., Eccles M. R., Reeve A. E. Structural analysis of the human insulin-like growth factor-II P3 promoter. Biochem J. 1993 Jan 1;289(Pt 1):133–139. doi: 10.1042/bj2890133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Risse G., Jooss K., Neuberg M., Brüller H. J., Müller R. Asymmetrical recognition of the palindromic AP1 binding site (TRE) by Fos protein complexes. EMBO J. 1989 Dec 1;8(12):3825–3832. doi: 10.1002/j.1460-2075.1989.tb08560.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rotwein P., Hall L. J. Evolution of insulin-like growth factor II: characterization of the mouse IGF-II gene and identification of two pseudo-exons. DNA Cell Biol. 1990 Dec;9(10):725–735. doi: 10.1089/dna.1990.9.725. [DOI] [PubMed] [Google Scholar]
  32. Rotwein P. Structure, evolution, expression and regulation of insulin-like growth factors I and II. Growth Factors. 1991;5(1):3–18. doi: 10.3109/08977199109000267. [DOI] [PubMed] [Google Scholar]
  33. Smeal T., Binetruy B., Mercola D. A., Birrer M., Karin M. Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature. 1991 Dec 12;354(6353):494–496. doi: 10.1038/354494a0. [DOI] [PubMed] [Google Scholar]
  34. Smith A. G., Hooper M. L. Buffalo rat liver cells produce a diffusible activity which inhibits the differentiation of murine embryonal carcinoma and embryonic stem cells. Dev Biol. 1987 May;121(1):1–9. doi: 10.1016/0012-1606(87)90132-1. [DOI] [PubMed] [Google Scholar]
  35. Soares M. B., Turken A., Ishii D., Mills L., Episkopou V., Cotter S., Zeitlin S., Efstratiadis A. Rat insulin-like growth factor II gene. A single gene with two promoters expressing a multitranscript family. J Mol Biol. 1986 Dec 20;192(4):737–752. doi: 10.1016/0022-2836(86)90025-2. [DOI] [PubMed] [Google Scholar]
  36. Stempien M. M., Fong N. M., Rall L. B., Bell G. I. Sequence of a placental cDNA encoding the mouse insulin-like growth factor II precursor. DNA. 1986 Oct;5(5):357–361. doi: 10.1089/dna.1986.5.357. [DOI] [PubMed] [Google Scholar]
  37. Stylianopoulou F., Efstratiadis A., Herbert J., Pintar J. Pattern of the insulin-like growth factor II gene expression during rat embryogenesis. Development. 1988 Jul;103(3):497–506. doi: 10.1242/dev.103.3.497. [DOI] [PubMed] [Google Scholar]
  38. Sussenbach J. S. The gene structure of the insulin-like growth factor family. Prog Growth Factor Res. 1989;1(1):33–48. doi: 10.1016/0955-2235(89)90040-9. [DOI] [PubMed] [Google Scholar]
  39. Takimoto M., Quinn J. P., Farina A. R., Staudt L. M., Levens D. fos/jun and octamer-binding protein interact with a common site in a negative element of the human c-myc gene. J Biol Chem. 1989 May 25;264(15):8992–8999. [PubMed] [Google Scholar]
  40. Wilkinson D. G., Bhatt S., Ryseck R. P., Bravo R. Tissue-specific expression of c-jun and junB during organogenesis in the mouse. Development. 1989 Jul;106(3):465–471. doi: 10.1242/dev.106.3.465. [DOI] [PubMed] [Google Scholar]
  41. Zhang X. K., Dong J. M., Chiu J. F. Regulation of alpha-fetoprotein gene expression by antagonism between AP-1 and the glucocorticoid receptor at their overlapping binding site. J Biol Chem. 1991 May 5;266(13):8248–8254. [PubMed] [Google Scholar]
  42. de Groot R. P., Pals C., Kruijer W. Transcriptional control of c-jun by retinoic acid. Nucleic Acids Res. 1991 Apr 11;19(7):1585–1591. doi: 10.1093/nar/19.7.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. de Groot R. P., Schoorlemmer J., van Genesen S. T., Kruijer W. Differential expression of jun and fos genes during differentiation of mouse P19 embryonal carcinoma cells. Nucleic Acids Res. 1990 Jun 11;18(11):3195–3202. doi: 10.1093/nar/18.11.3195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. de Pagter-Holthuizen P., Jansen M., van der Kammen R. A., van Schaik F. M., Sussenbach J. S. Differential expression of the human insulin-like growth factor II gene. Characterization of the IGF-II mRNAs and an mRNA encoding a putative IGF-II-associated protein. Biochim Biophys Acta. 1988 Sep 7;950(3):282–295. doi: 10.1016/0167-4781(88)90124-8. [DOI] [PubMed] [Google Scholar]
  45. de Wet J. R., Wood K. V., DeLuca M., Helinski D. R., Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987 Feb;7(2):725–737. doi: 10.1128/mcb.7.2.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. van Dijk M. A., Holthuizen P. E., Sussenbach J. S. Elements required for activation of the major promoter of the human insulin-like growth factor II gene. Mol Cell Endocrinol. 1992 Oct;88(1-3):175–185. doi: 10.1016/0303-7207(92)90022-x. [DOI] [PubMed] [Google Scholar]
  47. van Dijk M. A., van Schaik F. M., Bootsma H. J., Holthuizen P., Sussenbach J. S. Initial characterization of the four promoters of the human insulin-like growth factor II gene. Mol Cell Endocrinol. 1991 Oct;81(1-3):81–94. doi: 10.1016/0303-7207(91)90207-9. [DOI] [PubMed] [Google Scholar]

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