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PMID: 8321221 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

An alternatively spliced mRNA from the AP-2 gene encodes a negative regulator of transcriptional activation by AP-2.

Molecular and cellular biology ·Vol. 13 ·No. 7 ·1993-07-00 ·Pages 4174-85

Buettner R, Kannan P, Imhof A, Bauer R, Yim SO, Glockshuber R, Van Dyke MW, Tainsky MA

Abstract

AP-2 is a retinoic acid-inducible and developmentally regulated activator of transcription. We have cloned an alternative AP-2 transcript (AP-2B) from the human teratocarcinoma cell line PA-1, which encodes a protein differing in the C terminus from the previously isolated AP-2 protein (AP-2A). This protein contains the activation domain of AP-2 and part of the DNA binding domain but lacks the dimerization domain which is necessary for DNA binding. Analysis of overlapping genomic clones spanning the entire AP-2 gene proves that AP-2A and AP-2B transcripts are alternatively spliced from the same gene. Both transient and stable transfection experiments show that AP-2B inhibits AP-2 transactivator function, as measured by an AP-2-responsive chloramphenicol acetyltransferase reporter plasmid. Furthermore, constitutive AP-2B expression in PA-1 cells causes a retinoic acid-resistant phenotype, anchorage-independent growth in soft agar, and tumorigenicity in nude mice, in a fashion similar to transformation of these cells by oncogenes. To determine the mechanism by which AP-2B exerts its inhibitory function, we purified bacterially expressed AP-2A and AP-2B proteins. While bacterial AP-2B does not bind an AP-2 consensus site, it strongly inhibits binding of the endogenous AP-2 present in PA-1 cell nuclear extracts. However, DNA sequence-specific binding of bacterially expressed AP-2A cannot be inhibited by bacterially expressed AP-2B. Therefore, inhibition of AP-2 activity by the protein AP-2B may require an additional factor or modification supplied by nuclear extracts.

Related Genes
MeSH Terms
Alternative Splicing Amino Acid Sequence Animals Base Sequence Cell Differentiation Cell Division Cloning, Molecular DNA/metabolism DNA-Binding Proteins/genetics,metabolism Drosophila Drosophila Proteins Female Humans Mice Mice, Nude Molecular Sequence Data Polymerase Chain Reaction Transcription Factor AP-2 Transcription Factors/genetics,metabolism Transcription, Genetic Transcriptional Activation Tretinoin/pharmacology Tumor Cells, Cultured
Chemicals
DNA-Binding Proteins Drosophila Proteins TfAP-2 protein, Drosophila Transcription Factor AP-2 Transcription Factors Tretinoin DNA
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Buettner R
Department of Tumor Biology, University of Texas M. D. Anderson Cancer Center, Houston 77030.
Kannan P
Imhof A
Bauer R
Yim S O
Glockshuber R
Van Dyke M W
Tainsky M A
References (58)
58 references, click to expand
  1. Transcription factor AP-2 mediates induction by two different signal-transduction pathways: protein kinase C and cAMP.
    Cell. 1987 Oct 23;51(2):251-60 PMID: 2822255
  2. Sequence discrimination by alternatively spliced isoforms of a DNA binding zinc finger domain.
    Science. 1992 Sep 25;257(5078):1951-5 PMID: 1290524
  3. Assembly of a functional immunoglobulin Fv fragment in Escherichia coli.
    Science. 1988 May 20;240(4855):1038-41 PMID: 3285470
  4. Human teratocarcinomas.
    Biochim Biophys Acta. 1988 Aug 3;948(1):17-36 PMID: 3293662
  5. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase.
    Gene. 1988 Jul 15;67(1):31-40 PMID: 3047011
  6. PA-1, a human cell model for multistage carcinogenesis: oncogenes and other factors.
    Anticancer Res. 1988 Sep-Oct;8(5A):899-913 PMID: 3052262
  7. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1.
    Cell. 1988 Dec 2;55(5):875-85 PMID: 3142689
  8. Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements.
    Genes Dev. 1988 Dec;2(12A):1557-69 PMID: 3063603
  9. Inhibition of thyroid hormone action by a non-hormone binding c-erbA protein generated by alternative mRNA splicing.
    Nature. 1989 Feb 16;337(6208):659-61 PMID: 2537467
  10. An AP-2 element acts synergistically with the cyclic AMP- and phorbol ester-inducible enhancer of the human proenkephalin gene.
    Mol Cell Biol. 1989 Jan;9(1):321-4 PMID: 2538722
  11. Novel Jun- and Fos-related proteins in Drosophila are functionally homologous to enhancer factor AP-1.
    EMBO J. 1988 Dec 20;7(13):4265-73 PMID: 3149584
  12. Retinoids and vertebrate limb pattern formation.
    Trends Genet. 1989 Aug;5(8):246-51 PMID: 2686112
  13. Regulation of transcription factor AP-2 by the morphogen retinoic acid and by second messengers.
    Genes Dev. 1989 Oct;3(10):1507-17 PMID: 2482225
  14. Interaction of cellular proteins with the human T-cell leukemia virus type I transcriptional control region. Purification of cellular proteins that bind the 21-base pair repeat elements.
    J Biol Chem. 1990 May 15;265(14):8230-6 PMID: 2335523
  15. Polarizing activity and retinoid synthesis in the floor plate of the neural tube.
    Nature. 1990 Jun 28;345(6278):819-22 PMID: 2359459
  16. A new technique for the assay of infectivity of human adenovirus 5 DNA.
    Virology. 1973 Apr;52(2):456-67 PMID: 4705382
  17. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  18. Characterization of a human ovarian teratocarcinoma-derived cell line.
    Int J Cancer. 1980 Jan 15;25(1):19-32 PMID: 6931103
  19. Teratocarcinomas and mammalian embryogenesis.
    Science. 1980 Aug 15;209(4458):768-76 PMID: 6250214
  20. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells.
    Mol Cell Biol. 1982 Sep;2(9):1044-51 PMID: 6960240
  21. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  22. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity.
    Anal Biochem. 1983 Jul 1;132(1):6-13 PMID: 6312838
  23. An activated rasN gene: detected in late but not early passage human PA1 teratocarcinoma cells.
    Science. 1984 Aug 10;225(4662):643-5 PMID: 6740333
  24. Upstream promoter element of the human metallothionein-IIA gene can act like an enhancer element.
    Proc Natl Acad Sci U S A. 1985 Dec;82(24):8572-6 PMID: 3866241
  25. Activation of transcription by two factors that bind promoter and enhancer sequences of the human metallothionein gene and SV40.
    Nature. 1987 Jan 22-28;325(6102):368-72 PMID: 3027570
  26. Causal role for an activated N-ras oncogene in the induction of tumorigenicity acquired by a human cell line.
    Cancer Res. 1987 Jun 15;47(12):3235-8 PMID: 3034405
  27. CAT constructions with multiple unique restriction sites for the functional analysis of eukaryotic promoters and regulatory elements.
    Nucleic Acids Res. 1987 Jul 10;15(13):5490 PMID: 3037497
  28. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  29. Positive and negative regulation of transcription in vitro: enhancer-binding protein AP-2 is inhibited by SV40 T antigen.
    Cell. 1987 Sep 11;50(6):847-61 PMID: 3040262
  30. Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells.
    Nature. 1990 Aug 23;346(6286):763-6 PMID: 1975088
  31. Structure and expression of the mouse Oct2a and Oct2b, two differentially spliced products of the same gene.
    Development. 1990 Jun;109(2):349-62 PMID: 1976089
  32. Transcription factor AP-2 is expressed in neural crest cell lineages during mouse embryogenesis.
    Genes Dev. 1991 Jan;5(1):105-19 PMID: 1989904
  33. CREM gene: use of alternative DNA-binding domains generates multiple antagonists of cAMP-induced transcription.
    Cell. 1991 Feb 22;64(4):739-49 PMID: 1847666
  34. A naturally occurring truncated form of FosB that inhibits Fos/Jun transcriptional activity.
    Cell. 1991 Feb 22;64(4):751-9 PMID: 1900040
  35. Characterization of a dimerization motif in AP-2 and its function in heterologous DNA-binding proteins.
    Science. 1991 Mar 1;251(4997):1067-71 PMID: 1998122
  36. Analysis of the DNA-binding and activation properties of the human transcription factor AP-2.
    Genes Dev. 1991 Apr;5(4):670-82 PMID: 2010091
  37. Multiple Oct2 isoforms are generated by alternative splicing.
    Nucleic Acids Res. 1991 Jan 11;19(1):43-51 PMID: 2011512
  38. I-POU: a POU-domain protein that inhibits neuron-specific gene activation.
    Nature. 1991 Apr 18;350(6319):577-84 PMID: 1673230
  39. Alteration of homeobox gene expression by N-ras transformation of PA-1 human teratocarcinoma cells.
    Mol Cell Biol. 1991 Jul;11(7):3573-83 PMID: 1675427
  40. Susceptibility to ras oncogene transformation is coregulated with signal transduction through growth factor receptors.
    Oncogene. 1991 May;6(5):713-20 PMID: 1646984
  41. Retinoid-mediated transcriptional regulation of keratin genes in human epidermal and squamous cell carcinoma cells.
    Proc Natl Acad Sci U S A. 1991 Jun 1;88(11):4582-6 PMID: 1711202
  42. An alternative spliced form of FosB is a negative regulator of transcriptional activation and transformation by Fos proteins.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5077-81 PMID: 1905017
  43. Alternative splicing of fosB transcripts results in differentially expressed mRNAs encoding functionally antagonistic proteins.
    Genes Dev. 1991 Jul;5(7):1212-23 PMID: 1648531
  44. Transcription factor AP2 and its role in epidermal-specific gene expression.
    Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):7948-52 PMID: 1716766
  45. Localization of the gene for the DNA-binding protein AP-2 to human chromosome 6p22.3-pter.
    Genomics. 1991 Aug;10(4):1100-2 PMID: 1916817
  46. Modulation of differentiation in PA-1 human teratocarcinoma cells after N-ras oncogene-induced tumorigenicity.
    Oncogene. 1991 Sep;6(9):1575-82 PMID: 1681491
  47. A dominant negative form of transcription activator mTFE3 created by differential splicing.
    Science. 1991 Oct 4;254(5028):94-7 PMID: 1840705
  48. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA.
    Cell. 1991 Nov 1;67(3):569-79 PMID: 1934061
  49. Retinoids and their receptors in differentiation, embryogenesis, and neoplasia.
    FASEB J. 1991 Nov;5(14):2924-33 PMID: 1661245
  50. Transcription factor AP-2 is tissue-specific in Xenopus and is closely related or identical to keratin transcription factor 1 (KTF-1).
    Development. 1991 Sep;113(1):283-93 PMID: 1722450
  51. Functional characterization of the NF-kappa B p65 transcriptional activator and an alternatively spliced derivative.
    Mol Cell Biol. 1992 Feb;12(2):444-54 PMID: 1732726
  52. More is better: activators and repressors from the same gene.
    Cell. 1992 Feb 7;68(3):411-4 PMID: 1739963
  53. In vitro squelching of activated transcription by serum response factor: evidence for a common coactivator used by multiple transcriptional activators.
    Nucleic Acids Res. 1992 Feb 11;20(3):513-20 PMID: 1531519
  54. Single-step purification of bacterially expressed polypeptides containing an oligo-histidine domain.
    Gene. 1992 Feb 1;111(1):99-104 PMID: 1547959
  55. The effect of retinoic acid on chemosensitivity of PA-1 human teratocarcinoma cells and its modulation by an activated N-ras oncogene.
    Int J Cancer. 1992 Jun 19;51(4):646-51 PMID: 1376303
  56. Modulation of DNA binding specificity by alternative splicing of the Wilms tumor wt1 gene transcript.
    Science. 1992 Jul 10;257(5067):235-7 PMID: 1321494
  57. Multiple zinc finger forms resulting from developmentally regulated alternative splicing of a transcription factor gene.
    Science. 1992 Sep 25;257(5078):1946-50 PMID: 1411512
  58. A versatile in vivo and in vitro eukaryotic expression vector for protein engineering.
    Nucleic Acids Res. 1988 Jan 11;16(1):369 PMID: 3340539
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1993-07-00
Pages
4174-85
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC359967
Subset
IM
Grants
PHS HHS · 16672 · United States
NCI NIH HHS · CA 42810 · United States
Databases
GENBANK
M61156
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