Home LiteratureArticle Details
PMID: 20020479 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Does CTCF mediate between nuclear organization and gene expression?

BioEssays : news and reviews in molecular, cellular and developmental biology ·Vol. 32 ·No. 1 ·2010-01-00 ·Pages 37-50

Ohlsson R, Lobanenkov V, Klenova E

Abstract

The multifunctional zinc-finger protein CCCTC-binding factor (CTCF) is a very strong candidate for the role of coordinating the expression level of coding sequences with their three-dimensional position in the nucleus, apparently responding to a "code" in the DNA itself. Dynamic interactions between chromatin fibers in the context of nuclear architecture have been implicated in various aspects of genome functions. However, the molecular basis of these interactions still remains elusive and is a subject of intense debate. Here we discuss the nature of CTCF-DNA interactions, the CTCF-binding specificity to its binding sites and the relationship between CTCF and chromatin, and we examine data linking CTCF with gene regulation in the three-dimensional nuclear space. We discuss why these features render CTCF a very strong candidate for the role and propose a unifying model, the "CTCF code," explaining the mechanistic basis of how the information encrypted in DNA may be interpreted by CTCF into diverse nuclear functions.

MeSH Terms
Animals Base Sequence Binding Sites/genetics CCCTC-Binding Factor Cell Cycle Proteins/metabolism Cell Nucleus/genetics,metabolism Chromatin/genetics,metabolism Chromosomal Proteins, Non-Histone/metabolism DNA/genetics,metabolism DNA-Binding Proteins/chemistry,genetics,metabolism Epigenesis, Genetic Gene Expression Humans Mice Models, Biological Models, Genetic Nucleosomes/genetics,metabolism Protein Interaction Domains and Motifs Repressor Proteins/chemistry,genetics,metabolism
Chemicals
CCCTC-Binding Factor CTCF protein, human CTCFL protein, human Cell Cycle Proteins Chromatin Chromosomal Proteins, Non-Histone Ctcf protein, mouse Ctcfl protein, mouse DNA-Binding Proteins Nucleosomes Repressor Proteins cohesins DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Ohlsson Rolf
Department of Microbiology, Tumor and Cell Biology, Karolinska Institute, Stockholm, Sweden. Rolf.Ohlsson@ki.se
Lobanenkov Victor
Klenova Elena
References (125)
125 references, click to expand
  1. The binding sites for the chromatin insulator protein CTCF map to DNA methylation-free domains genome-wide.
    Genome Res. 2004 Aug;14(8):1594-602 PMID: 15256511
  2. Evidence that homologous X-chromosome pairing requires transcription and Ctcf protein.
    Nat Genet. 2007 Nov;39(11):1390-6 PMID: 17952071
  3. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer.
    Semin Cancer Biol. 2002 Oct;12(5):399-414 PMID: 12191639
  4. Cutting edge: developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development.
    J Immunol. 2009 Jan 1;182(1):44-8 PMID: 19109133
  5. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus.
    Nature. 2009 Jul 16;460(7253):410-3 PMID: 19458616
  6. Hierarchical hidden Markov model with application to joint analysis of ChIP-chip and ChIP-seq data.
    Bioinformatics. 2009 Jul 15;25(14):1715-21 PMID: 19447789
  7. Cohesins functionally associate with CTCF on mammalian chromosome arms.
    Cell. 2008 Feb 8;132(3):422-33 PMID: 18237772
  8. CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species.
    Mol Cell. 2004 Jan 30;13(2):291-8 PMID: 14759373
  9. CCCTC-binding factor meets poly(ADP-ribose) polymerase-1.
    J Cell Physiol. 2009 May;219(2):265-70 PMID: 19170077
  10. Analysis of the H19ICR insulator.
    Mol Cell Biol. 2007 May;27(9):3499-510 PMID: 17339341
  11. High-resolution circular chromosome conformation capture assay.
    Nat Protoc. 2008;3(2):303-13 PMID: 18274532
  12. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive.
    Curr Biol. 2000 Jul 13;10(14):853-6 PMID: 10899010
  13. A transcriptional insulator at the imprinted H19/Igf2 locus.
    Genes Dev. 2000 Aug 1;14(15):1908-19 PMID: 10921905
  14. CTCF: master weaver of the genome.
    Cell. 2009 Jun 26;137(7):1194-211 PMID: 19563753
  15. Identification of a perinuclear positioning element in human subtelomeres that requires A-type lamins and CTCF.
    EMBO J. 2009 Aug 19;28(16):2428-36 PMID: 19644448
  16. Multiple nucleosome positioning sites regulate the CTCF-mediated insulator function of the H19 imprinting control region.
    Mol Cell Biol. 2002 May;22(10):3339-44 PMID: 11971967
  17. Reciprocal binding of CTCF and BORIS to the NY-ESO-1 promoter coincides with derepression of this cancer-testis gene in lung cancer cells.
    Cancer Res. 2005 Sep 1;65(17):7763-74 PMID: 16140944
  18. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C).
    Nat Genet. 2006 Nov;38(11):1348-54 PMID: 17033623
  19. Familial cases of point mutations in the XIST promoter reveal a correlation between CTCF binding and pre-emptive choices of X chromosome inactivation.
    Hum Mol Genet. 2005 Apr 1;14(7):953-65 PMID: 15731119
  20. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1.
    Science. 2006 Apr 14;312(5771):269-72 PMID: 16614224
  21. Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary.
    Mol Cell. 2009 May 15;34(3):271-84 PMID: 19450526
  22. Functional phosphorylation sites in the C-terminal region of the multivalent multifunctional transcriptional factor CTCF.
    Mol Cell Biol. 2001 Mar;21(6):2221-34 PMID: 11238955
  23. The CTCF insulator protein is posttranslationally modified by SUMO.
    Mol Cell Biol. 2009 Feb;29(3):714-25 PMID: 19029252
  24. Thyroid hormone-regulated enhancer blocking: cooperation of CTCF and thyroid hormone receptor.
    EMBO J. 2003 Apr 1;22(7):1579-87 PMID: 12660164
  25. CTCF binds the proximal exonic region of hTERT and inhibits its transcription.
    Nucleic Acids Res. 2005 Dec 02;33(21):6850-60 PMID: 16326864
  26. We gather together: insulators and genome organization.
    Curr Opin Genet Dev. 2007 Oct;17(5):400-7 PMID: 17913488
  27. The chicken beta-globin insulator element conveys chromatin boundary activity but not imprinting at the mouse Igf2/H19 domain.
    Development. 2002 Feb;129(4):897-904 PMID: 11861473
  28. CTCF maintains differential methylation at the Igf2/H19 locus.
    Nat Genet. 2003 Jan;33(1):66-9 PMID: 12461525
  29. A novel sequence-specific DNA binding protein which interacts with three regularly spaced direct repeats of the CCCTC-motif in the 5'-flanking sequence of the chicken c-myc gene.
    Oncogene. 1990 Dec;5(12):1743-53 PMID: 2284094
  30. De novo formation of a subnuclear body.
    Science. 2008 Dec 12;322(5908):1713-7 PMID: 18948503
  31. Critical role for the transcription regulator CCCTC-binding factor in the control of Th2 cytokine expression.
    J Immunol. 2009 Jan 15;182(2):999-1010 PMID: 19124743
  32. The insulator factor CTCF controls MHC class II gene expression and is required for the formation of long-distance chromatin interactions.
    J Exp Med. 2008 Apr 14;205(4):785-98 PMID: 18347100
  33. Genome-wide identification of in vivo protein-DNA binding sites from ChIP-Seq data.
    Nucleic Acids Res. 2008 Sep;36(16):5221-31 PMID: 18684996
  34. Expression of the CTCF-paralogous cancer-testis gene, brother of the regulator of imprinted sites (BORIS), is regulated by three alternative promoters modulated by CpG methylation and by CTCF and p53 transcription factors.
    Nucleic Acids Res. 2007;35(21):7372-88 PMID: 17962299
  35. Decreased poly(ADP-ribosyl)ation of CTCF, a transcription factor, is associated with breast cancer phenotype and cell proliferation.
    Clin Cancer Res. 2009 Sep 15;15(18):5762-71 PMID: 19737964
  36. Looping and interaction between hypersensitive sites in the active beta-globin locus.
    Mol Cell. 2002 Dec;10(6):1453-65 PMID: 12504019
  37. Making contacts on a nucleic acid polymer.
    Trends Biochem Sci. 2001 Dec;26(12):733-40 PMID: 11738597
  38. Purification of proteins associated with specific genomic Loci.
    Cell. 2009 Jan 9;136(1):175-86 PMID: 19135898
  39. Epigenetic control of CTCFL/BORIS and OCT4 expression in urogenital malignancies.
    Biochem Pharmacol. 2006 Nov 30;72(11):1577-88 PMID: 16854382
  40. A complex deoxyribonucleic acid looping configuration associated with the silencing of the maternal Igf2 allele.
    Mol Endocrinol. 2008 Jun;22(6):1476-88 PMID: 18356289
  41. Mutation of a single CTCF target site within the H19 imprinting control region leads to loss of Igf2 imprinting and complex patterns of de novo methylation upon maternal inheritance.
    Mol Cell Biol. 2004 Apr;24(8):3497-504 PMID: 15060168
  42. Three-dimensional genome organization in interphase and its relation to genome function.
    Semin Cell Dev Biol. 2007 Oct;18(5):707-14 PMID: 17905616
  43. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene.
    Nature. 2000 May 25;405(6785):482-5 PMID: 10839546
  44. Three-dimensional conformation at the H19/Igf2 locus supports a model of enhancer tracking.
    Hum Mol Genet. 2008 Oct 1;17(19):3021-9 PMID: 18617529
  45. CTCF regulates allelic expression of Igf2 by orchestrating a promoter-polycomb repressive complex 2 intrachromosomal loop.
    Mol Cell Biol. 2008 Oct;28(20):6473-82 PMID: 18662993
  46. CTCF is conserved from Drosophila to humans and confers enhancer blocking of the Fab-8 insulator.
    EMBO Rep. 2005 Feb;6(2):165-70 PMID: 15678159
  47. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions.
    Nature. 2008 Jun 12;453(7197):948-51 PMID: 18463634
  48. Replication timing and epigenetic reprogramming of gene expression: a two-way relationship?
    Nat Rev Genet. 2009 Apr;10(4):269-76 PMID: 19274048
  49. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes.
    Mol Cell Biol. 1996 Jun;16(6):2802-13 PMID: 8649389
  50. CTCF, a candidate trans-acting factor for X-inactivation choice.
    Science. 2002 Jan 11;295(5553):345-7 PMID: 11743158
  51. CTCF-dependent chromatin insulator is linked to epigenetic remodeling.
    Mol Cell. 2006 Sep 1;23(5):733-42 PMID: 16949368
  52. Interchromosomal associations between alternatively expressed loci.
    Nature. 2005 Jun 2;435(7042):637-45 PMID: 15880101
  53. Flanking HS-62.5 and 3' HS1, and regions upstream of the LCR, are not required for beta-globin transcription.
    Blood. 2006 Aug 15;108(4):1395-401 PMID: 16645164
  54. Nucleosome positioning signals in the DNA sequence of the human and mouse H19 imprinting control regions.
    J Mol Biol. 2003 Jan 31;325(5):873-87 PMID: 12527297
  55. Chromatin dynamics and gene positioning.
    Cell. 2008 Mar 21;132(6):929-34 PMID: 18358806
  56. The testis-specific factor CTCFL cooperates with the protein methyltransferase PRMT7 in H19 imprinting control region methylation.
    PLoS Biol. 2006 Oct;4(11):e355 PMID: 17048991
  57. YB-1 and CTCF differentially regulate the 5-HTT polymorphic intron 2 enhancer which predisposes to a variety of neurological disorders.
    J Neurosci. 2004 Jun 30;24(26):5966-73 PMID: 15229244
  58. Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF.
    Mol Cell. 2005 Nov 11;20(3):483-9 PMID: 16285929
  59. Identification of a Ctcf cofactor, Yy1, for the X chromosome binary switch.
    Mol Cell. 2007 Jan 12;25(1):43-56 PMID: 17218270
  60. Impact of chromatin structures on DNA processing for genomic analyses.
    PLoS One. 2009 Aug 20;4(8):e6700 PMID: 19693276
  61. Chromosome territories, nuclear architecture and gene regulation in mammalian cells.
    Nat Rev Genet. 2001 Apr;2(4):292-301 PMID: 11283701
  62. Genetics and epigenetics of the multifunctional protein CTCF.
    Curr Top Dev Biol. 2008;80:337-60 PMID: 17950379
  63. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter tts DNA-binding specificity.
    Cancer Res. 2002 Jan 1;62(1):48-52 PMID: 11782357
  64. Transcriptional repression by the insulator protein CTCF involves histone deacetylases.
    Nucleic Acids Res. 2000 Apr 15;28(8):1707-13 PMID: 10734189
  65. Regulatory factor interactions and somatic silencing of the germ cell-specific ALF gene.
    J Biol Chem. 2006 Nov 10;281(45):34288-98 PMID: 16966320
  66. High-resolution profiling of histone methylations in the human genome.
    Cell. 2007 May 18;129(4):823-37 PMID: 17512414
  67. A 5' element of the chicken beta-globin domain serves as an insulator in human erythroid cells and protects against position effect in Drosophila.
    Cell. 1993 Aug 13;74(3):505-14 PMID: 8348617
  68. Human gamma-satellite DNA maintains open chromatin structure and protects a transgene from epigenetic silencing.
    Genome Res. 2009 Apr;19(4):533-44 PMID: 19141594
  69. The evolution of epigenetic regulators CTCF and BORIS/CTCFL in amniotes.
    PLoS Genet. 2008 Aug 29;4(8):e1000169 PMID: 18769711
  70. CTCF regulates cell cycle progression of alphabeta T cells in the thymus.
    EMBO J. 2008 Nov 5;27(21):2839-50 PMID: 18923423
  71. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes.
    Nat Genet. 2006 Nov;38(11):1278-88 PMID: 17057718
  72. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting.
    Nature. 2009 Jul 2;460(7251):128-32 PMID: 19536159
  73. The zinc finger protein CTCF binds to the APBbeta domain of the amyloid beta-protein precursor promoter. Evidence for a role in transcriptional activation.
    J Biol Chem. 1997 Dec 26;272(52):33353-9 PMID: 9407128
  74. Nuclear organization of the genome and the potential for gene regulation.
    Nature. 2007 May 24;447(7143):413-7 PMID: 17522674
  75. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains.
    Genome Res. 2009 Jan;19(1):24-32 PMID: 19056695
  76. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells.
    Cell. 2008 Jun 13;133(6):1106-17 PMID: 18555785
  77. The LPS-induced transcriptional upregulation of the chicken lysozyme locus involves CTCF eviction and noncoding RNA transcription.
    Mol Cell. 2008 Oct 10;32(1):129-39 PMID: 18851839
  78. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease.
    Trends Genet. 2001 Sep;17(9):520-7 PMID: 11525835
  79. Gene regulation in the third dimension.
    Science. 2008 Mar 28;319(5871):1793-4 PMID: 18369139
  80. Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation.
    Nat Genet. 2004 Oct;36(10):1105-10 PMID: 15361875
  81. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions.
    Nat Rev Genet. 2007 Feb;8(2):104-15 PMID: 17230197
  82. Active promoters and insulators are marked by the centrosomal protein 190.
    EMBO J. 2009 Apr 8;28(7):877-88 PMID: 19229299
  83. BORIS, a novel male germ-line-specific protein associated with epigenetic reprogramming events, shares the same 11-zinc-finger domain with CTCF, the insulator protein involved in reading imprinting marks in the soma.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6806-11 PMID: 12011441
  84. Global expression analysis of cancer/testis genes in uterine cancers reveals a high incidence of BORIS expression.
    Clin Cancer Res. 2007 Mar 15;13(6):1713-9 PMID: 17363524
  85. Genetics. Widespread monoallelic expression.
    Science. 2007 Nov 16;318(5853):1077-8 PMID: 18006729
  86. CTCFBSDB: a CTCF-binding site database for characterization of vertebrate genomic insulators.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D83-7 PMID: 17981843
  87. Three subclasses of a Drosophila insulator show distinct and cell type-specific genomic distributions.
    Genes Dev. 2009 Jun 1;23(11):1338-50 PMID: 19443682
  88. CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region.
    Mol Cell Biol. 2008 Feb;28(3):1124-35 PMID: 18039862
  89. BORIS, a paralogue of the transcription factor, CTCF, is aberrantly expressed in breast tumours.
    Br J Cancer. 2008 Feb 12;98(3):571-9 PMID: 18195709
  90. Cell cycle control of Kaposi's sarcoma-associated herpesvirus latency transcription by CTCF-cohesin interactions.
    J Virol. 2009 Jun;83(12):6199-210 PMID: 19369356
  91. Molecular cloning and expression of the chromatin insulator protein CTCF in Xenopus laevis.
    Mech Dev. 2002 Apr;113(1):95-8 PMID: 11900981
  92. Cohesin mediates transcriptional insulation by CCCTC-binding factor.
    Nature. 2008 Feb 14;451(7180):796-801 PMID: 18235444
  93. Chromosome crosstalk in three dimensions.
    Nature. 2009 Sep 10;461(7261):212-7 PMID: 19741702
  94. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus.
    Genes Dev. 2006 Sep 1;20(17):2349-54 PMID: 16951251
  95. Cohesins localize with CTCF at the KSHV latency control region and at cellular c-myc and H19/Igf2 insulators.
    EMBO J. 2008 Feb 20;27(4):654-66 PMID: 18219272
  96. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus.
    Nature. 2000 May 25;405(6785):486-9 PMID: 10839547
  97. Physical and functional interaction between two pluripotent proteins, the Y-box DNA/RNA-binding factor, YB-1, and the multivalent zinc finger factor, CTCF.
    J Biol Chem. 2000 Sep 22;275(38):29915-21 PMID: 10906122
  98. Gene regulation through nuclear organization.
    Nat Struct Mol Biol. 2007 Nov;14(11):1049-55 PMID: 17984967
  99. The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome.
    PLoS Genet. 2008 Jul 25;4(7):e1000138 PMID: 18654629
  100. Modular structure of a chicken lysozyme silencer: involvement of an unusual thyroid hormone receptor binding site.
    Cell. 1990 May 4;61(3):505-14 PMID: 2159385
  101. Position-effect protection and enhancer blocking by the chicken beta-globin insulator are separable activities.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6883-8 PMID: 12011446
  102. Chromatin insulators: regulatory mechanisms and epigenetic inheritance.
    Mol Cell. 2008 Oct 10;32(1):1-9 PMID: 18851828
  103. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome.
    Cell. 2007 Mar 23;128(6):1231-45 PMID: 17382889
  104. Epigenetic boundaries of tumour suppressor gene promoters: the CTCF connection and its role in carcinogenesis.
    J Cell Mol Med. 2006 Jul-Sep;10(3):554-68 PMID: 16989720
  105. CTCF genomic binding sites in Drosophila and the organisation of the bithorax complex.
    PLoS Genet. 2007 Jul;3(7):e112 PMID: 17616980
  106. Inter-chromosomal gene regulation in the mammalian cell nucleus.
    Curr Opin Genet Dev. 2007 Oct;17(5):456-64 PMID: 17884460
  107. The human enhancer blocker CTC-binding factor interacts with the transcription factor Kaiso.
    J Biol Chem. 2005 Dec 30;280(52):43017-23 PMID: 16230345
  108. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations.
    PLoS Biol. 2006 May;4(5):e138 PMID: 16623600
  109. Capturing chromosome conformation.
    Science. 2002 Feb 15;295(5558):1306-11 PMID: 11847345
  110. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions.
    Nat Genet. 2006 Nov;38(11):1341-7 PMID: 17033624
  111. Cloning and characterization of zebrafish CTCF: Developmental expression patterns, regulation of the promoter region, and evolutionary aspects of gene organization.
    Gene. 2006 Jun 21;375:26-36 PMID: 16647825
  112. How are cohesin rings opened and closed?
    Trends Biochem Sci. 2007 Apr;32(4):154-7 PMID: 17320400
  113. Epigenetic regulation of the human retinoblastoma tumor suppressor gene promoter by CTCF.
    Cancer Res. 2007 Mar 15;67(6):2577-85 PMID: 17363576
  114. Transvection mediated by the translocated cyclin D1 locus in mantle cell lymphoma.
    J Exp Med. 2008 Aug 4;205(8):1843-58 PMID: 18625744
  115. CTCF cis-regulates trinucleotide repeat instability in an epigenetic manner: a novel basis for mutational hot spot determination.
    PLoS Genet. 2008 Nov;4(11):e1000257 PMID: 19008940
  116. Chromatin structure is implicated in "late" elongation checkpoints on the U2 snRNA and beta-actin genes.
    Mol Cell Biol. 2009 Jul;29(14):4002-13 PMID: 19451231
  117. Chromatin organization in the mammalian nucleus.
    Int Rev Cytol. 2005;242:283-336 PMID: 15598472
  118. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide.
    Mol Cell Biol. 2007 Mar;27(5):1631-48 PMID: 17210645
  119. Beyond the sequence: cellular organization of genome function.
    Cell. 2007 Feb 23;128(4):787-800 PMID: 17320514
  120. The nucleotides responsible for the direct physical contact between the chromatin insulator protein CTCF and the H19 imprinting control region manifest parent of origin-specific long-distance insulation and methylation-free domains.
    Genes Dev. 2003 Mar 1;17(5):586-90 PMID: 12629040
  121. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators.
    Cell. 1999 Aug 6;98(3):387-96 PMID: 10458613
  122. The meaning of gene positioning.
    Cell. 2008 Oct 3;135(1):9-13 PMID: 18854147
  123. CTCF, a conserved nuclear factor required for optimal transcriptional activity of the chicken c-myc gene, is an 11-Zn-finger protein differentially expressed in multiple forms.
    Mol Cell Biol. 1993 Dec;13(12):7612-24 PMID: 8246978
  124. CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2.
    Proc Natl Acad Sci U S A. 2006 Jul 11;103(28):10684-9 PMID: 16815976
  125. Geometric analysis and comparison of protein-DNA interfaces: why is there no simple code for recognition?
    J Mol Biol. 2000 Aug 18;301(3):597-624 PMID: 10966773
Article Info
Journal
BioEssays : news and reviews in molecular, cellular and developmental biology
Abbr.
Bioessays
ISSN
1521-1878
DOI
10.1002/bies.200900118
Email
rolf.ohlsson@ki.se
Published
2010-01-00
Pages
37-50
Language
English
Region
United States
NLM ID
8510851
PMCID
PMC6375297
Subset
IM
Grants
Medical Research Council · G0401088 · United Kingdom
Intramural NIH HHS · Z99 AI999999 · United States
External Links
PubMed source DOI: 10.1002/bies.200900118 PMC Full Text View journal details
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: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2