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PMID: 9811896 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

c-Myc target gene specificity is determined by a post-DNAbinding mechanism.

Boyd KE, Wells J, Gutman J, Bartley SM, Farnham PJ

Abstract

Uncertainty as to which member of a family of DNA-binding transcription factors regulates a specific promoter in intact cells is a problem common to many investigators. Determining target gene specificity requires both an analysis of protein binding to the endogenous promoter as well as a characterization of the functional consequences of transcription factor binding. By using a formaldehyde crosslinking procedure and Gal4 fusion proteins, we have analyzed the timing and functional consequences of binding of Myc and upstream stimulatory factor (USF)1 to endogenous cellular genes. We demonstrate that the endogenous cad promoter can be immunoprecipitated with antibodies against Myc and USF1. We further demonstrate that although both Myc and USF1 can bind to cad, the cad promoter can respond only to the Myc transactivation domain. We also show that the amount of Myc bound to the cad promoter fluctuates in a growth-dependent manner. Thus, our data analyzing both DNA binding and promoter activity in intact cells suggest that cad is a Myc target gene. In addition, we show that Myc binding can occur at many sites in vivo but that the position of the binding site determines the functional consequences of this binding. Our data indicate that a post-DNA-binding mechanism determines Myc target gene specificity. Importantly, we have demonstrated the feasibility of analyzing the binding of site-specific transcription factors in vivo to single copy mammalian genes.

MeSH Terms
3T3 Cells Animals Binding Sites DNA/genetics,metabolism DNA-Binding Proteins/genetics,metabolism Gene Targeting Genes, myc Mice Molecular Sequence Data Transcriptional Activation
Chemicals
DNA-Binding Proteins DNA
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Boyd K E
McArdle Laboratory for Cancer Research, University of Wisconsin Medical School, Madison, WI 53706, USA.
Wells J
Gutman J
Bartley S M
Farnham P J
References (31)
31 references, click to expand
  1. Mapping protein-DNA interactions in vivo with formaldehyde: evidence that histone H4 is retained on a highly transcribed gene.
    Cell. 1988 Jun 17;53(6):937-47 PMID: 2454748
  2. An embryonically expressed gene is a target for c-Myc regulation via the c-Myc-binding sequence.
    Genes Dev. 1992 Dec;6(12B):2513-23 PMID: 1340466
  3. c-Myc binds to 5' flanking sequence motifs of the dihydrofolate reductase gene in cellular extracts: role in proliferation.
    Nucleic Acids Res. 1994 Jun 25;22(12):2264-73 PMID: 8036154
  4. Base preferences for DNA binding by the bHLH-Zip protein USF: effects of MgCl2 on specificity and comparison with binding of Myc family members.
    Nucleic Acids Res. 1994 Jul 25;22(14):2801-10 PMID: 8052536
  5. Two homeo domain proteins bind with similar specificity to a wide range of DNA sites in Drosophila embryos.
    Genes Dev. 1994 Jul 15;8(14):1678-92 PMID: 7958848
  6. An E-box-mediated increase in cad transcription at the G1/S-phase boundary is suppressed by inhibitory c-Myc mutants.
    Mol Cell Biol. 1995 May;15(5):2527-35 PMID: 7739536
  7. Position and orientation independent transactivation by c-Myc.
    Cell Mol Biol Res. 1994;40(7-8):699-706 PMID: 7787888
  8. A link between increased transforming activity of lymphoma-derived MYC mutant alleles, their defective regulation by p107, and altered phosphorylation of the c-Myc transactivation domain.
    Mol Cell Biol. 1995 Aug;15(8):4031-42 PMID: 7623799
  9. c-Myc and Max transregulate the mouse ornithine decarboxylase promoter through interaction with two downstream CACGTG motifs.
    Oncogene. 1995 Nov 2;11(9):1721-7 PMID: 7478599
  10. Antiproliferative properties of the USF family of helix-loop-helix transcription factors.
    Proc Natl Acad Sci U S A. 1996 Feb 6;93(3):1308-13 PMID: 8577760
  11. Discrimination between different E-box-binding proteins at an endogenous target gene of c-myc.
    Genes Dev. 1996 Feb 15;10(4):447-60 PMID: 8600028
  12. Functional domains of the transcription factor USF2: atypical nuclear localization signals and context-dependent transcriptional activation domains.
    Mol Cell Biol. 1996 Apr;16(4):1367-75 PMID: 8657110
  13. Cdc25 cell-cycle phosphatase as a target of c-myc.
    Nature. 1996 Aug 8;382(6591):511-7 PMID: 8700224
  14. An essential E box in the promoter of the gene encoding the mRNA cap-binding protein (eukaryotic initiation factor 4E) is a target for activation by c-myc.
    Mol Cell Biol. 1996 Sep;16(9):4754-64 PMID: 8756633
  15. Myc-Max heterodimers activate a DEAD box gene and interact with multiple E box-related sites in vivo.
    EMBO J. 1996 Aug 15;15(16):4344-57 PMID: 8861962
  16. Mnt, a novel Max-interacting protein is coexpressed with Myc in proliferating cells and mediates repression at Myc binding sites.
    Genes Dev. 1997 Jan 1;11(1):44-58 PMID: 9000049
  17. Position-dependent transcriptional regulation of the murine dihydrofolate reductase promoter by the E2F transactivation domain.
    Mol Cell Biol. 1997 Apr;17(4):1966-76 PMID: 9121444
  18. Myc versus USF: discrimination at the cad gene is determined by core promoter elements.
    Mol Cell Biol. 1997 May;17(5):2529-37 PMID: 9111322
  19. Identification of substrates and regulators of the mitogen-activated protein kinase ERK5 using chimeric protein kinases.
    J Biol Chem. 1998 Feb 13;273(7):3854-60 PMID: 9461566
  20. TFE3: a helix-loop-helix protein that activates transcription through the immunoglobulin enhancer muE3 motif.
    Genes Dev. 1990 Feb;4(2):167-79 PMID: 2338243
  21. A helix-loop-helix protein related to the immunoglobulin E box-binding proteins.
    Mol Cell Biol. 1990 Aug;10(8):4384-8 PMID: 2115126
  22. The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer.
    Genes Dev. 1990 Oct;4(10):1730-40 PMID: 2249772
  23. Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc.
    Science. 1991 Mar 8;251(4998):1211-7 PMID: 2006410
  24. Characterization of the 5' end of the growth-regulated Syrian hamster CAD gene.
    Cell Growth Differ. 1990 Apr;1(4):179-89 PMID: 1982061
  25. Pro-Leu-Ser/Thr-Pro is a consensus primary sequence for substrate protein phosphorylation. Characterization of the phosphorylation of c-myc and c-jun proteins by an epidermal growth factor receptor threonine 669 protein kinase.
    J Biol Chem. 1991 Aug 15;266(23):15277-85 PMID: 1651323
  26. Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity.
    Cell. 1993 Jan 29;72(2):211-22 PMID: 8425218
  27. Mxi1, a protein that specifically interacts with Max to bind Myc-Max recognition sites.
    Cell. 1993 Jan 29;72(2):223-32 PMID: 8425219
  28. A protein synthesis-dependent increase in E2F1 mRNA correlates with growth regulation of the dihydrofolate reductase promoter.
    Mol Cell Biol. 1993 Mar;13(3):1610-8 PMID: 8441401
  29. Binding of myc proteins to canonical and noncanonical DNA sequences.
    Mol Cell Biol. 1993 Sep;13(9):5216-24 PMID: 8395000
  30. The ornithine decarboxylase gene is a transcriptional target of c-Myc.
    Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7804-8 PMID: 8356088
  31. Start site selection at the TATA-less carbamoyl-phosphate synthase (glutamine-hydrolyzing)/aspartate carbamoyltransferase/dihydroorotase promoter.
    J Biol Chem. 1994 Jan 21;269(3):2252-7 PMID: 7905000
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1998-11-10
Pages
13887-92
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC24949
Subset
IM
Grants
NCI NIH HHS · CA09135 · United States
NCI NIH HHS · CA07175 · United States
NCI NIH HHS · CA45240 · United States
NCI NIH HHS · T32 CA009135 · United States
NCI NIH HHS · T32 CA009681 · United States
NCI NIH HHS · R01 CA045240 · United States
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AF053338, AF053339
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