Ets target genes: past, present and future

Ets is a family of transcription factors present in species ranging from sponges to human. All family members contain an approximately 85 amino acid DNA binding domain, designated the Ets domain. Ets proteins bind to specific purine-rich DNA sequences with a core motif of GGAA/T, and transcriptionally regulate a number of viral and cellular genes. Thus, Ets proteins are an important family of transcription factors that control the expression of genes that are critical for several biological processes, including cellular proliferation, differentiation, development, transformation, and apoptosis. Here, we tabulate genes that are regulated by Ets factors and describe past, present and future strategies for the identification and validation of Ets target genes. Through definition of authentic target genes, we will begin to understand the mechanisms by which Ets factors control normal and abnormal cellular processes.

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[6]  J. Ware,et al.  Identification of Essential GATA and Ets Binding Motifs within the Promoter of the Platelet Glycoprotein Ibα Gene (*) , 1995, The Journal of Biological Chemistry.

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[12]  J. Otte,et al.  Ets transcription factor binding site is required for positive and TNF alpha-induced negative promoter regulation. , 1993, Nucleic acids research.

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[16]  V. Štolc,et al.  Characterization of a promoter within the first intron of the human CD4 gene. , 1997, European journal of biochemistry.

[17]  B. Graves,et al.  Specificity within the ets family of transcription factors. , 1998, Advances in cancer research.

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[27]  T. Libermann,et al.  Isolation and characterization of a novel epithelium-specific transcription factor, ESE-1, a member of the ets family , 1997, Molecular and cellular biology.

[28]  K. Klempnauer,et al.  Myb and Ets transcription factors cooperate at the myb-inducible promoter of the tom-1 gene. , 1999, Biochimica et biophysica acta.

[29]  Zhiyong Yang,et al.  NF-IL6 (C/EBPβ) Vigorously Activates il1b Gene Expression via a Spi-1 (PU.1) Protein-Protein Tether* , 2000, The Journal of Biological Chemistry.

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[33]  M. Krönke,et al.  Regulation of the Human TNF Promoter by the Transcription Factor Ets (*) , 1995, The Journal of Biological Chemistry.

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[38]  C. Backendorf,et al.  AP-1 and Ets Transcription Factors Regulate the Expression of the Human SPRR1A Keratinocyte Terminal Differentiation Marker* , 1998, The Journal of Biological Chemistry.

[39]  D. Markovitz,et al.  Differential regulation of the human immunodeficiency virus type 2 enhancer in monocytes at various stages of differentiation , 1993, Journal of virology.

[40]  Y. Yazaki,et al.  Transcription factor PU.1 mediates induction of c-fms in vascular smooth muscle cells: a mechanism for phenotypic change to phagocytic cells , 1996, Molecular and cellular biology.

[41]  Y. Okada,et al.  Ets-1 positively regulates expression of urokinase-type plasminogen activator (uPA) and invasiveness of astrocytic tumors. , 1999, Journal of neuropathology and experimental neurology.

[42]  U. Wirkner,et al.  Transcription Factors Ets1, NF-κB, and Sp1 Are Major Determinants of the Promoter Activity of the Human Protein Kinase CK2α Gene* , 2000, The Journal of Biological Chemistry.

[43]  G. Trinchieri,et al.  Synergistic Regulation of the Human Interleukin-12 p40 Promoter by NFκB and Ets Transcription Factors in Epstein-Barr Virus-transformed B Cells and Macrophages* , 1998, The Journal of Biological Chemistry.

[44]  C. Begley,et al.  Lineage-restricted regulation of the murine SCL/TAL-1 promoter. , 1995, Blood.

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[46]  K. Kinzler,et al.  p53 tagged sites from human genomic DNA. , 1994, Human molecular genetics.

[47]  J. D. Reid,et al.  Identification of a Cell Type-specific Enhancer in the Distal 5′-Region of the Platelet-derived Growth Factor A-chain Gene* , 1998, The Journal of Biological Chemistry.

[48]  J. Chambaz,et al.  Purification and characterization of nuclear factors binding to the negative regulatory element D of human apolipoprotein A-II promoter: a negative regulatory effect is reversed by GABP, an Ets-related protein. , 1994, Biochemistry.

[49]  R. Kobayashi,et al.  A DNA methylation site in the male-specific P450 (Cyp 2d-9) promoter and binding of the heteromeric transcription factor GABP , 1995, Molecular and cellular biology.

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[51]  W. Dang,et al.  A Three-protein-DNA Complex on a B Cell-specific Domain of the Immunoglobulin μ Heavy Chain Gene Enhancer* , 1997, The Journal of Biological Chemistry.

[52]  S. Mckercher,et al.  Defective trophoblast function in mice with a targeted mutation of Ets2. , 1998, Genes & development.

[53]  D. Tenen,et al.  PU.1 (Spi-1) and C/EBP alpha regulate expression of the granulocyte-macrophage colony-stimulating factor receptor alpha gene , 1995, Molecular and cellular biology.

[54]  J. Ghysdael,et al.  Characterization of a hepatoma mRNA transcribed from a third promoter of a 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-encoding gene and controlled by ets oncogene-related products. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Michael C. Ostrowski,et al.  Regulation of urokinase-type plasminogen activator gene transcription by macrophage colony-stimulating factor , 1995, Molecular and cellular biology.

[56]  R Taub,et al.  Transcriptional up-regulation of the delayed early gene HRS/SRp40 during liver regeneration. Interactions among YY1, GA-binding proteins, and mitogenic signals. , 1998, The Journal of biological chemistry.

[57]  M. Simon,et al.  The myeloid-cell-specific c-fes promoter is regulated by Sp1, PU.1, and a novel transcription factor , 1996, Molecular and cellular biology.

[58]  N. Bhat,et al.  Characterization of the human interleukin-2 receptor beta-chain gene promoter: regulation of promoter activity by ets gene products , 1993, Molecular and cellular biology.

[59]  PU.1 is a component of a multiprotein complex which binds an essential site in the murine immunoglobulin lambda 2-4 enhancer. , 1993, Molecular and cellular biology.

[60]  G. Evan,et al.  A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. , 1995, Nucleic acids research.

[61]  G. Pfeifer,et al.  In vivo structure of the human cdc2 promoter: release of a p130-E2F-4 complex from sequences immediately upstream of the transcription initiation site coincides with induction of cdc2 expression , 1995, Molecular and cellular biology.

[62]  G. Opdenakker,et al.  Structural and functional analysis of the promoter region of the human MCP-3 gene: transactivation of expression by novel recognition sequences adjacent to the transcription initiation site. , 1997, DNA and cell biology.

[63]  A. Albor,et al.  Regulation of the human poly(ADP-ribose) polymerase promoter by the ETS transcription factor , 1999, Oncogene.

[64]  A. Friedman,et al.  C/EBP, c-Myb, and PU.1 cooperate to regulate the neutrophil elastase promoter , 1996, Molecular and cellular biology.

[65]  N. Copeland,et al.  The murine interleukin-3 receptor alpha subunit gene: chromosomal localization, genomic structure, and promoter function. , 1995, Blood.

[66]  A. Malik,et al.  H2O2 and Tumor Necrosis Factor-α Activate Intercellular Adhesion Molecule 1 (ICAM-1) Gene Transcription through Distinct cis-Regulatory Elements within the ICAM-1 Promoter (*) , 1995, The Journal of Biological Chemistry.

[67]  D. Klatzmann,et al.  Characterization of the human CD4 gene promoter: transcription from the CD4 gene core promoter is tissue-specific and is activated by Ets proteins. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[68]  D. Markovitz,et al.  Activation of the human T-cell leukemia virus type I enhancer is mediated by binding sites for Elf-1 and the pets factor , 1993, Journal of virology.

[69]  R. Scarpulla,et al.  Transcriptional activation through ETS domain binding sites in the cytochrome c oxidase subunit IV gene , 1991, Molecular and cellular biology.

[70]  R. Maurer,et al.  A Composite Ets/Pit-1 Binding Site in the Prolactin Gene Can Mediate Transcriptional Responses to Multiple Signal Transduction Pathways (*) , 1995, The Journal of Biological Chemistry.

[71]  C. Murre,et al.  Ets proteins: new factors that regulate immunoglobulin heavy-chain gene expression , 1993, Molecular and cellular biology.

[72]  H. Handa,et al.  Synergistic Transcriptional Activation by hGABP and Select Members of the Activation Transcription Factor/cAMP Response Element-binding Protein Family* , 1999, The Journal of Biological Chemistry.

[73]  M. Fenton,et al.  NF beta A, a factor required for maximal interleukin-1 beta gene expression is identical to the ets family member PU.1. Evidence for structural alteration following LPS activation. , 1995, Molecular immunology.

[74]  Enhanced cell-free transcription of the ribosomal protein L32 gene by the polyoma virus enhancer PEA3 DNA-binding protein. , 1992, European journal of biochemistry.

[75]  J. Brady,et al.  Sequence-specific interaction of the Ets1 protein with the long terminal repeat of the human T-lymphotropic virus type I , 1991, Journal of virology.

[76]  M. Meisterernst,et al.  A conserved tissue-specific structure at a human T-cell receptor beta-chain core promoter , 1997, Molecular and cellular biology.

[77]  M. Hulander,et al.  The Kidney-expressed Winged Helix Transcription Factor FREAC-4 Is Regulated by Ets-1 , 1999, The Journal of Biological Chemistry.

[78]  M. Cole,et al.  c-myc null cells misregulate cad and gadd45 but not other proposed c-Myc targets. , 1998, Genes & development.

[79]  D. Goldman,et al.  Identification of a neuregulin and protein-tyrosine phosphatase response element in the nicotinic acetylcholine receptor epsilon subunit gene: regulatory role of an Rts transcription factor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[80]  J. Brady,et al.  Interaction of Human T-cell Lymphotropic Virus Type I Tax, Ets1, and Sp1 in Transactivation of the PTHrP P2 Promoter* , 1997, The Journal of Biological Chemistry.

[81]  H. Das,et al.  An Upstream Element Containing an ETS Binding Site Is Crucial for Transcription of the Human Presenilin-1 Gene* , 1999, The Journal of Biological Chemistry.

[82]  T. Graf,et al.  v-Myb of E26 leukemia virus up-regulates bcl-2 and suppresses apoptosis in myeloid cells. , 1996, Genes & development.

[83]  N. Sugg,et al.  The integrin alpha v gene: identification and characterization of the promoter region. , 1994, Biochimica et biophysica acta.

[84]  F. Moreau-Gachelin,et al.  Involvement of the transcription factor PU.1/Spi-1 in myeloid cell-restricted expression of an interferon-inducible gene encoding the human high-affinity Fc gamma receptor , 1994, Molecular and cellular biology.

[85]  P. Romeo,et al.  Analysis of the thrombopoietin receptor (MPL) promoter implicates GATA and Ets proteins in the coregulation of megakaryocyte-specific genes. , 1996, Blood.

[86]  A. Nordheim,et al.  The Spemann organizer‐expressed zinc finger gene Xegr‐1 responds to the MAP kinase/Ets‐SRF signal transduction pathway , 1998, The EMBO journal.

[87]  I. Imanaga,et al.  The Na+/Ca2+ Exchanger NCX1 Has Oppositely Oriented Reentrant Loop Domains That Contain Conserved Aspartic Acids Whose Mutation Alters Its Apparent Ca2+Affinity* , 2000, The Journal of Biological Chemistry.

[88]  T. Graf,et al.  Cooperative interaction of Ets‐1 with USF‐1 required for HIV‐1 enhancer activity in T cells , 1998, The EMBO journal.

[89]  K. Gaston,et al.  CpG methylation and the binding of YY1 and ETS proteins to the Surf-1/Surf-2 bidirectional promoter. , 1995, Gene.

[90]  T. Hirano,et al.  Identification of a novel interleukin-6 response element containing an Ets-binding site and a CRE-like site in the junB promoter , 1993, Molecular and cellular biology.

[91]  K. Gaston,et al.  CpG methylation has differential effects on the binding of YY1 and ETS proteins to the bi-directional promoter of the Surf-1 and Surf-2 genes. , 1995, Nucleic acids research.

[92]  J. Parrillo,et al.  Transcriptional Regulation of Fas Gene Expression by GA-binding Protein and AP-1 in T Cell Antigen Receptor·CD3 Complex-stimulated T Cells* , 1999, The Journal of Biological Chemistry.

[93]  D. Lillicrap,et al.  Binding of the Ets factor GA-binding protein to an upstream site in the factor IX promoter is a critical event in transactivation , 1996, Molecular and cellular biology.

[94]  C. Benz,et al.  A role for both Ets and C/EBP transcription factors and mRNA stabilization in the MAPK-dependent increase in p21 (Cip-1/WAF1/mda6) protein levels in primary hepatocytes. , 2000, Molecular biology of the cell.

[95]  Takahiro Ochi,et al.  Transcriptional regulation of osteopontin gene in vivo by PEBP2αA/CBFA1 and ETS1 in the skeletal tissues , 1998, Oncogene.

[96]  J. Brady,et al.  Transactivation of the P2 promoter of parathyroid hormone-related protein by human T-cell lymphotropic virus type I Tax1: evidence for the involvement of transcription factor Ets1 , 1993, Journal of virology.

[97]  D. Blair,et al.  Transactivation of erythroid transcription factor GATA-1 by a myb-ets-containing retrovirus , 1992, Journal of virology.

[98]  A. Aranda,et al.  Insulin-like growth factor-1 stimulates rat prolactin gene expression by a Ras, ETS and phosphatidylinositol 3- kinase dependent mechanism , 1998, Oncogene.

[99]  P. Hewett,et al.  Cloning and partial characterization of the human tie-2 receptor tyrosine kinase gene promoter. , 1998, Biochemical and biophysical research communications.

[100]  G. Fourel,et al.  Cellular and viral trans-acting factors modulate N-myc2 promoter activity in woodchuck liver tumors , 1997, Oncogene.

[101]  E. Sitnicka,et al.  The Tel-PDGFRβ fusion gene produces a chronic myeloproliferative syndrome in transgenic mice , 1999, Leukemia.

[102]  C. Chang,et al.  The murine L-plastin gene promoter: identification and comparison with the human L-plastin gene promoter. , 1997, DNA and cell biology.

[103]  G. Henkel,et al.  PU.1 and GATA: components of a mast cell-specific interleukin 4 intronic enhancer. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[104]  Y. Bernstein,et al.  Expression of the human acute myeloid leukemia gene AML1 is regulated by two promoter regions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[105]  G. Uzan,et al.  The tissue-specific transcriptional regulation of the megakaryocytic glycoprotein IIb gene is controlled by interactions between a repressor and positive cis-acting elements. , 1996, Blood.

[106]  D. Tenen,et al.  Function of PU.1 (Spi-1), C/EBP, and AML1 in early myelopoiesis: regulation of multiple myeloid CSF receptor promoters. , 1996, Current topics in microbiology and immunology.

[107]  Lufen Chang,et al.  Activity of the Distal Positive Element of the Peripherin Gene Is Dependent on Proteins Binding to an Ets-like Recognition Site and a Novel Inverted Repeat Site (*) , 1996, The Journal of Biological Chemistry.

[108]  S. Hirohashi,et al.  Cloning and Characterization of the Human β4-Integrin Gene Promoter and Enhancers* , 1998, The Journal of Biological Chemistry.

[109]  P. Gadue,et al.  Activation of the Megakaryocyte-specific Gene Platelet Basic Protein (PBP) by the Ets Family Factor PU.1* , 1997, The Journal of Biological Chemistry.

[110]  C. Albanese,et al.  Transforming p21ras Mutants and c-Ets-2 Activate the Cyclin D1 Promoter through Distinguishable Regions (*) , 1995, The Journal of Biological Chemistry.

[111]  P. Pennec,et al.  Characterization of the gene encoding the human LW blood group protein in LW+ and LW- phenotypes , 1996 .

[112]  M. Yaniv,et al.  Oncogenes as Transcriptional Regulators , 1997, Progress in Gene Expression.

[113]  A. A. Thompson,et al.  The promoter and 5' flanking sequences controlling human B29 gene expression. , 1996, Blood.

[114]  T. Hirano,et al.  Transcriptional activation of the IL-6 response element in the junB promoter is mediated by multiple Stat family proteins. , 1994, Biochemical and biophysical research communications.

[115]  T. Libermann,et al.  ELF-1 Interacts with and Transactivates the IgH Enhancer π Site* , 1996, The Journal of Biological Chemistry.

[116]  M Poncz,et al.  An Ets/Sp1 interaction in the 5'-flanking region of the megakaryocyte-specific alpha IIb gene appears to stabilize Sp1 binding and is essential for expression of this TATA-less gene. , 1996, Blood.

[117]  Andrew C. Li,et al.  The Macrosialin Promoter Directs High Levels of Transcriptional Activity in Macrophages Dependent on Combinatorial Interactions between PU.1 and c-Jun* , 1998, The Journal of Biological Chemistry.

[118]  R. Muschel,et al.  Transcriptional activation of the matrix metalloproteinase-9 gene in an H-ras and v-myc transformed rat embryo cell line , 1997, Oncogene.

[119]  R. Pankov,et al.  AP-1, ETS, and transcriptional silencers regulate retinoic acid-dependent induction of keratin 18 in embryonic cells , 1994, Molecular and cellular biology.

[120]  L. Garrett-Sinha,et al.  The Ets Factors PU.1 and Spi-B Regulate the Transcriptionin Vivo of P2Y10, a Lymphoid Restricted Heptahelical Receptor* , 1999, The Journal of Biological Chemistry.

[121]  A. Seth,et al.  ETS target genes: identification of egr1 as a target by RNA differential display and whole genome PCR techniques. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[122]  H. Fan,et al.  In Vivo Footprinting of the Enhancer Sequences in the Upstream Long Terminal Repeat of Moloney Murine Leukemia Virus: Differential Binding of Nuclear Factors in Different Cell Types , 1998, Journal of Virology.

[123]  A. Fischer,et al.  Tissue-specific Activity of the γc Chain Gene Promoter Depends upon an Ets Binding Site and Is Regulated by GA-binding Protein* , 1996, The Journal of Biological Chemistry.

[124]  N. Janel,et al.  Ets transcription factors bind and transactivate the core promoter of the  von Willebrand factor gene , 1997, Oncogene.

[125]  V. Shepherd,et al.  PU.1 and USF Are Required for Macrophage-specific Mannose Receptor Promoter Activity* , 1999, The Journal of Biological Chemistry.

[126]  F. Beier,et al.  The Raf-1/MEK/ERK Pathway Regulates the Expression of the p21Cip1/Waf1 Gene in Chondrocytes* , 1999, The Journal of Biological Chemistry.

[127]  I. Chiu,et al.  The Small GTPases Ras, Rac, and Cdc42 Transcriptionally Regulate Expression of Human Fibroblast Growth Factor 1* , 2000, The Journal of Biological Chemistry.

[128]  J. Ghysdael,et al.  Elf-1 Contributes to the Function of the Complex Interleukin (IL)-2–responsive Enhancer in the Mouse IL-2 Receptor α Gene , 1997, The Journal of experimental medicine.

[129]  M. Klagsbrun,et al.  Characterization of the promoter for the human antisense fibroblast growth factor‐2 gene; Regulation by Ets in Jurkat T cells , 1999, Journal of cellular biochemistry.

[130]  A. Friedman,et al.  An Enhancer Located between the Neutrophil Elastase and Proteinase 3 Promoters Is Activated by Sp1 and an Ets Factor* , 1999, The Journal of Biological Chemistry.

[131]  M. Klemsz,et al.  Methylation of an ETS site in the intron enhancer of the keratin 18 gene participates in tissue-specific repression , 1997, Molecular and cellular biology.

[132]  P. Steinert,et al.  Complex Interactions between Epidermal POU Domain and Activator Protein 1 Transcription Factors Regulate the Expression of the Profilaggrin Gene in Normal Human Epidermal Keratinocytes* , 2000, The Journal of Biological Chemistry.

[133]  E. Miyoshi,et al.  Transcriptional Regulation of the N-Acetylglucosaminyltransferase V Gene in Human Bile Duct Carcinoma Cells (HuCC-T1) Is Mediated by Ets-1* , 1996, The Journal of Biological Chemistry.

[134]  S. Smale,et al.  Both LyF-1 and an Ets protein interact with a critical promoter element in the murine terminal transferase gene , 1993, Molecular and cellular biology.

[135]  N. Bhat,et al.  Sequence-specific binding of human Ets-1 to the T cell receptor alpha gene enhancer. , 1990, Science.

[136]  R. Pictet,et al.  Participation of Ets transcription factors in the glucocorticoid response of the rat tyrosine aminotransferase gene , 1994, Molecular and cellular biology.

[137]  N. Kondoh,et al.  Enhanced expression of the urokinase-type plasminogen activator gene and reduced colony formation in soft agar by ectopic expression of PU.1 in HT1080 human fibrosarcoma cells. , 1998, British Journal of Cancer.

[138]  S. Mckercher,et al.  Use of RDA analysis of knockout mice to identify myeloid genes regulated in vivo by PU.1 and C/EBPalpha. , 1998, Nucleic acids research.

[139]  R. Sager,et al.  Expression of maspin in prostate cells is regulated by a positive ets element and a negative hormonal responsive element site recognized by androgen receptor. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[140]  M. Tymms,et al.  Down's syndrome-like skeletal abnormalities in Ets2 transgenic mice , 1996, Nature.

[141]  B. Erman,et al.  Regulation of lymphoid-specific immunoglobulin mu heavy chain gene enhancer by ETS-domain proteins. , 1993, Science.

[142]  H. Handa,et al.  GABP and PU.1 Compete for Binding, yet Cooperate to Increase CD18 (β2 Leukocyte Integrin) Transcription (*) , 1995, The Journal of Biological Chemistry.

[143]  R. Scheibe,et al.  Functional interference between retinoic acid or steroid hormone receptors and the oncoprotein Fli-1 , 1997, Oncogene.

[144]  Michael C. Ostrowski,et al.  Interaction between PU.1 and Another Ets Family Transcription Factor Promotes Macrophage-specific Basal Transcription Initiation* , 1998, The Journal of Biological Chemistry.

[145]  Y. Bang,et al.  A Novel ets-related Transcription Factor, ERT/ESX/ESE-1, Regulates Expression of the Transforming Growth Factor-β Type II Receptor* , 1998, The Journal of Biological Chemistry.

[146]  M. Montminy,et al.  Distinct roles for P-CREB and LEF-1 in TCR alpha enhancer assembly and activation on chromatin templates in vitro. , 1997, Genes & development.

[147]  A. Wellstein,et al.  Phorbol Ester-induced Transcription of a Fibroblast Growth Factor-binding Protein Is Modulated by a Complex Interplay of Positive and Negative Regulatory Promoter Elements* , 1998, The Journal of Biological Chemistry.

[148]  A. Cano,et al.  Regulation of E-cadherin gene expression during tumor progression: the role of a new Ets-binding site and the E-pal element. , 1999, Experimental cell research.

[149]  R. Krumlauf,et al.  Segmental regulation of Hoxb-3 by kreisler , 1997, Nature.

[150]  A. Yen,et al.  Regulation of MCL1 through a Serum Response Factor/Elk-1-mediated Mechanism Links Expression of a Viability-promoting Member of the BCL2 Family to the Induction of Hematopoietic Cell Differentiation* , 1999, The Journal of Biological Chemistry.

[151]  E. E. Max,et al.  Characterization of the human immunoglobulin kappa gene 3' enhancer: functional importance of three motifs that demonstrate B-cell-specific in vivo footprints. , 1992, Molecular and cellular biology.

[152]  C. Hauser,et al.  Oncogene activation of human keratin 18 transcription via the Ras signal transduction pathway. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[153]  T. Graf,et al.  Regulation of eosinophil‐specific gene expression by a C/EBP–Ets complex and GATA‐1 , 1998, The EMBO journal.

[154]  W. Vainchenker,et al.  Spi-1/PU.1 transgenic mice develop multistep erythroleukemias , 1996, Molecular and cellular biology.

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