Home LiteratureArticle Details
PMID: 18818283 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Unique ERalpha cistromes control cell type-specific gene regulation.

Molecular endocrinology (Baltimore, Md.) ·Vol. 22 ·No. 11 ·2008-11-00 ·Pages 2393-406

Krum SA, Miranda-Carboni GA, Lupien M, Eeckhoute J, Carroll JS, Brown M

Abstract

Estrogens play an important role in normal physiology and in a variety of pathological states involving diverse tissues including breast and bone. The mechanism by which estrogens exert cell type- and disease-specific effects, however, remains to be explained. We have compared the gene expression profile of the MCF7 breast cancer cell line with that of the osteoblast-like cell line U2OS-ERalpha by expression microarrays. We find that fewer than 10% of the 17beta-estradiol (E2)-regulated genes are common to both cell types. We have validated this in primary calvarial osteoblasts. To dissect the mechanism underlying the cell type-specific E2 regulation of gene expression in MCF7 and U2OS-ERalpha cells, we compared the ERalpha binding sites on DNA in the two cell types by performing chromatin immunoprecipitation (ChIP) on genomic tiling arrays (ChIP-on-chip). Consistent with the distinct patterns of E2-regulated gene expression in these two cell lines, we find that the vast majority of ERalpha binding sites are also cell type specific and correlate both in position and number with cell type-specific gene regulation. Interestingly, although the forkhead factor FoxA1 plays a critical role in defining the ERalpha cistrome in MCF7 cells, it is not expressed in U2OS-ERalpha cells, and forkhead motifs are not enriched in the ERalpha cistrome in these cells. Finally, the ERalpha cistromes are correlated with cell type-specific epigenetic histone modifications. These results support a model for the cell type-specific action of E2 being driven primarily through specific ERalpha occupancy of epigenetically marked cis-regulatory regions of target genes.

MeSH Terms
Alkaline Phosphatase/genetics,metabolism Binding Sites/genetics Breast Neoplasms/genetics,metabolism Cell Line Cell Line, Tumor Chromatin/genetics,metabolism Chromatin Immunoprecipitation DNA/genetics,metabolism DNA, Neoplasm/genetics,metabolism Epigenesis, Genetic Estradiol/pharmacology Estrogen Receptor alpha/genetics,metabolism Female Gene Expression Profiling Genetic Complementation Test Hepatocyte Nuclear Factor 3-alpha/genetics,metabolism Humans Oligonucleotide Array Sequence Analysis Osteoblasts/metabolism Tissue Distribution Transcriptional Activation/drug effects
Chemicals
Chromatin DNA, Neoplasm Estrogen Receptor alpha FOXA1 protein, human Hepatocyte Nuclear Factor 3-alpha Estradiol DNA Alkaline Phosphatase
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Krum Susan A
Division of Molecular and Cellular Oncology, Department of Medical Oncology, Dana-Farber Cancer Institute, 44 Binney Street, D730, Boston, Massachusetts 02115, USA.
Miranda-Carboni Gustavo A
Lupien Mathieu
Eeckhoute Jerome
Carroll Jason S
Brown Myles
References (51)
51 references, click to expand
  1. Primer3 on the WWW for general users and for biologist programmers.
    Methods Mol Biol. 2000;132:365-86 PMID: 10547847
  2. Unraveling estrogen action in osteoporosis.
    Cell Cycle. 2008 May 15;7(10):1348-52 PMID: 18418063
  3. Characterisation of the temporal sequence of osteoblast gene expression during estrogen-induced osteogenesis in female mice.
    J Cell Biochem. 2001;82(4):683-91 PMID: 11500946
  4. Vitamin D control of osteoblast function and bone extracellular matrix mineralization.
    Crit Rev Eukaryot Gene Expr. 2001;11(1-3):199-226 PMID: 11693961
  5. Tissue-specific estrogen biosynthesis and metabolism.
    Ann N Y Acad Sci. 2001 Dec;949:58-67 PMID: 11795380
  6. Molecular determinants for the tissue specificity of SERMs.
    Science. 2002 Mar 29;295(5564):2465-8 PMID: 11923541
  7. Isoflavones regulate interleukin-6 and osteoprotegerin synthesis during osteoblast cell differentiation via an estrogen-receptor-dependent pathway.
    Biochem Biophys Res Commun. 2002 Jul 12;295(2):417-22 PMID: 12150965
  8. Estrogen enhances differentiation of osteoblasts in mouse bone marrow culture.
    Bone. 1998 Mar;22(3):201-9 PMID: 9514212
  9. Active genes are tri-methylated at K4 of histone H3.
    Nature. 2002 Sep 26;419(6905):407-11 PMID: 12353038
  10. Reversal of bone loss in mice by nongenotropic signaling of sex steroids.
    Science. 2002 Oct 25;298(5594):843-6 PMID: 12399595
  11. Estrogen receptor isoform-specific regulation of endogenous gene expression in human osteoblastic cell lines expressing either ERalpha or ERbeta.
    J Cell Biochem. 2003 Oct 1;90(2):315-26 PMID: 14505348
  12. The roles of annexins and alkaline phosphatase in mineralization process.
    Acta Biochim Pol. 2003;50(4):1019-38 PMID: 14739992
  13. Genome-wide identification of high-affinity estrogen response elements in human and mouse.
    Mol Endocrinol. 2004 Jun;18(6):1411-27 PMID: 15001666
  14. Genomic and non-genomic effects of estrogens on endothelial cells.
    Steroids. 2004 Aug;69(8-9):537-42 PMID: 15288766
  15. The estrogen-responsive element as an inducible enhancer: DNA sequence requirements and conversion to a glucocorticoid-responsive element.
    EMBO J. 1987 Dec 1;6(12):3719-27 PMID: 3480798
  16. Leukemia inhibitory factor binds with high affinity to preosteoblastic RCT-1 cells and potentiates the retinoic acid induction of alkaline phosphatase.
    Endocrinology. 1990 Oct;127(4):1602-8 PMID: 2119291
  17. Stimulatory effects of estrogen and progesterone on proliferation and differentiation of normal human osteoblast-like cells in vitro.
    Biochem Biophys Res Commun. 1992 Jul 15;186(1):54-60 PMID: 1632789
  18. Dysgenesis of cephalic neural crest derivatives in Pax7-/- mutant mice.
    Development. 1996 Mar;122(3):831-8 PMID: 8631261
  19. Two androgen response regions cooperate in steroid hormone regulated activity of the prostate-specific antigen promoter.
    J Biol Chem. 1996 Mar 15;271(11):6379-88 PMID: 8626436
  20. Estrogen inhibits interleukin-6 production and gene expression in a human osteoblastic cell line with high levels of estrogen receptors.
    J Bone Miner Res. 1996 Feb;11(2):193-9 PMID: 8822343
  21. SOX genes: architects of development.
    Mol Med. 1996 Jul;2(4):405-12 PMID: 8827711
  22. An androgen response element in a far upstream enhancer region is essential for high, androgen-regulated activity of the prostate-specific antigen promoter.
    Mol Endocrinol. 1997 Feb;11(2):148-61 PMID: 9013762
  23. Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts.
    J Exp Med. 1997 Aug 18;186(4):489-95 PMID: 9254647
  24. Bone morphogenetic protein-6 production in human osteoblastic cell lines. Selective regulation by estrogen.
    J Clin Invest. 1998 Jan 15;101(2):413-22 PMID: 9435314
  25. Estrogen receptor-alpha is developmentally regulated during osteoblast differentiation and contributes to selective responsiveness of gene expression.
    Endocrinology. 1998 Apr;139(4):2048-57 PMID: 9528993
  26. A Cbfa1-dependent genetic pathway controls bone formation beyond embryonic development.
    Genes Dev. 1999 Apr 15;13(8):1025-36 PMID: 10215629
  27. Genomic maps and comparative analysis of histone modifications in human and mouse.
    Cell. 2005 Jan 28;120(2):169-81 PMID: 15680324
  28. Mechanisms of sex steroid effects on bone.
    Biochem Biophys Res Commun. 2005 Mar 18;328(3):688-96 PMID: 15694402
  29. A transmembrane intracellular estrogen receptor mediates rapid cell signaling.
    Science. 2005 Mar 11;307(5715):1625-30 PMID: 15705806
  30. Estrogen receptor alpha and beta heterodimers exert unique effects on estrogen- and tamoxifen-dependent gene expression in human U2OS osteosarcoma cells.
    Mol Endocrinol. 2005 Jun;19(6):1555-68 PMID: 15802376
  31. Myt1 family recruits histone deacetylase to regulate neural transcription.
    J Neurochem. 2005 Jun;93(6):1444-53 PMID: 15935060
  32. Enzymatic DNA methylation is an epigenetic control for genetic functions of the cell.
    Biochemistry (Mosc). 2005 May;70(5):488-99 PMID: 15948703
  33. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1.
    Cell. 2005 Jul 15;122(1):33-43 PMID: 16009131
  34. NFAT and Osterix cooperatively regulate bone formation.
    Nat Med. 2005 Aug;11(8):880-5 PMID: 16041384
  35. The nuclear receptor liver receptor homolog-1 is an estrogen receptor target gene.
    Oncogene. 2005 Dec 8;24(55):8167-75 PMID: 16091743
  36. Estrogen carcinogenesis in breast cancer.
    N Engl J Med. 2006 Jan 19;354(3):270-82 PMID: 16421368
  37. Calcineurin/NFAT signaling in osteoblasts regulates bone mass.
    Dev Cell. 2006 Jun;10(6):771-82 PMID: 16740479
  38. Direct and indirect estrogen actions on osteoblasts and osteoclasts.
    Ann N Y Acad Sci. 2006 Apr;1068:173-9 PMID: 16831916
  39. CEAS: cis-regulatory element annotation system.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W551-4 PMID: 16845068
  40. Estrogen receptor target gene: an evolving concept.
    Mol Endocrinol. 2006 Aug;20(8):1707-14 PMID: 16396959
  41. Model-based analysis of tiling-arrays for ChIP-chip.
    Proc Natl Acad Sci U S A. 2006 Aug 15;103(33):12457-62 PMID: 16895995
  42. A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer.
    Genes Dev. 2006 Sep 15;20(18):2513-26 PMID: 16980581
  43. Genome-wide analysis of estrogen receptor binding sites.
    Nat Genet. 2006 Nov;38(11):1289-97 PMID: 17013392
  44. Induction of osteoblast differentiation by selective activation of kinase-mediated actions of the estrogen receptor.
    Mol Cell Biol. 2007 Feb;27(4):1516-30 PMID: 17158928
  45. Controlling the chromatin organization of vitamin D target genes by multiple vitamin D receptor binding sites.
    J Steroid Biochem Mol Biol. 2007 Mar;103(3-5):338-43 PMID: 17234401
  46. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  47. Dynamic FoxO transcription factors.
    J Cell Sci. 2007 Aug 1;120(Pt 15):2479-87 PMID: 17646672
  48. GPR30 estrogen receptor expression in the growth plate declines as puberty progresses.
    J Clin Endocrinol Metab. 2007 Dec;92(12):4873-7 PMID: 17878253
  49. Estrogen protects bone by inducing Fas ligand in osteoblasts to regulate osteoclast survival.
    EMBO J. 2008 Feb 6;27(3):535-45 PMID: 18219273
  50. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription.
    Cell. 2008 Mar 21;132(6):958-70 PMID: 18358809
  51. Estrogen regulation of cyclin D1 gene expression in ZR-75 breast cancer cells involves multiple enhancer elements.
    J Biol Chem. 2001 Aug 17;276(33):30853-61 PMID: 11410592
Article Info
Journal
Molecular endocrinology (Baltimore, Md.)
Abbr.
Mol Endocrinol
ISSN
0888-8809
Published
2008-11-00
Epub
2008-00-25
Pages
2393-406
Language
English
Region
United States
NLM ID
8801431
PMCID
PMC2582540
Subset
IM
Grants
NIDDK NIH HHS · R01 DK074967 · United States
NCI NIH HHS · P01 CA8011105 · United States
NIDDK NIH HHS · R01DK074967 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]