The role of nuclear organization in cancer

The functional significance of changes in nuclear structure and organization in transformed cells remains one of the most enigmatic questions in cancer biology. In this review, we discuss relationships between nuclear organization and transcription in terms of the three‐dimensional arrangement of genes in the interphase cancer nucleus and the regulatory functions of nuclear matrix proteins. We also analyse the role of nuclear topology in the generation of gene fusions. We speculate that this type of multi‐layered analysis will one day provide a framework for a more comprehensive understanding of the genetic origins of cancer and the identification of new therapeutic targets. Copyright © 2009 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.

[1]  P. Edwards.  Fusion genes and chromosome translocations in the common epithelial cancers , 2009, The Journal of pathology.

[2]  D. Bell.  Our changing view of the genomic landscape of cancer , 2009, The Journal of pathology.

[3]  F. Real,et al.  The epigenetic regulators Bmi1 and Ring1B are differentially regulated in pancreatitis and pancreatic ductal adenocarcinoma , 2009, The Journal of pathology.

[4]  E. Klenova,et al.  Decreased Poly(ADP-Ribosyl)ation of CTCF, a Transcription Factor, Is Associated with Breast Cancer Phenotype and Cell Proliferation , 2009, Clinical Cancer Research.

[5]  Jian-ming Li,et al.  Down‐regulated expression of SATB2 is associated with metastasis and poor prognosis in colorectal cancer , 2009, The Journal of pathology.

[6]  R. Mansel,et al.  The mRNA expression of SATB1 and SATB2 in human breast cancer , 2009, Cancer Cell International.

[7]  S. Stifani,et al.  'Runxs and regulations' of sensory and motor neuron subtype differentiation: implications for hematopoietic development. , 2009, Blood cells, molecules & diseases.

[8]  A. Paradowska,et al.  Aberrant epigenetic modifications in the CTCF binding domain of the IGF2/H19 gene in prostate cancer compared with benign prostate hyperplasia. , 2009, International journal of oncology.

[9]  V. Corces,et al.  CTCF: Master Weaver of the Genome , 2009, Cell.

[10]  Eberhard Schmitt,et al.  Spatial allelic imbalance of BCL2 genes and chromosome 18 territories in nonneoplastic and neoplastic cervical squamous epithelium , 2009, European Biophysics Journal.

[11]  Jing Ma,et al.  Activation of the ERK/MAPK pathway: a signature genetic defect in posterior fossa pilocytic astrocytomas , 2009, The Journal of pathology.

[12]  B. Emerson,et al.  Epigenetic silencing of the p16(INK4a) tumor suppressor is associated with loss of CTCF binding and a chromatin boundary. , 2009, Molecular cell.

[13]  C. Muchardt,et al.  The PRC1 Polycomb group complex interacts with PLZF/RARA to mediate leukemic transformation. , 2009, Genes & development.

[14]  L. Kenner,et al.  SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. , 2009, Developmental cell.

[15]  M. Stratton,et al.  The cancer genome , 2009, Nature.

[16]  Goberdhan P Dimri,et al.  BMI1 Cooperates with H-RAS to Induce an Aggressive Breast Cancer Phenotype with Brain Metastases , 2009, Oncogene.

[17]  Steven S. Chang,et al.  Coordinated Activation of Candidate Proto-Oncogenes and Cancer Testes Antigens via Promoter Demethylation in Head and Neck Cancer and Lung Cancer , 2009, PloS one.

[18]  T. Misteli,et al.  The emerging role of nuclear architecture in DNA repair and genome maintenance , 2009, Nature Reviews Molecular Cell Biology.

[19]  Christopher K. Glass,et al.  Tyrosine Dephosphorylation of H2AX Modulates Apoptosis and Survival Decisions , 2009, Nature.

[20]  C. Jimenez,et al.  Unravelling the nuclear matrix proteome. , 2009, Journal of proteomics.

[21]  米満 裕.  Distinct expression of polycomb group proteins EZH2 and BMI1 in hepatocellular carcinoma , 2009 .

[22]  Paul Tempst,et al.  WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase , 2009 .

[23]  F. Zhou,et al.  Expression of Bmi-1 is a prognostic marker in bladder cancer , 2009, BMC Cancer.

[24]  L. Vives,et al.  Bivalent domains enforce transcriptional memory of DNA methylated genes in cancer cells , 2008, Proceedings of the National Academy of Sciences.

[25]  E. Cameron,et al.  Gene array analysis reveals a common Runx transcriptional programme controlling cell adhesion and survival , 2008, Oncogene.

[26]  H. Zentgraf,et al.  The enhancer of zeste homolog 2 gene contributes to cell proliferation and apoptosis resistance in renal cell carcinoma cells , 2008, International journal of cancer.

[27]  L. True,et al.  The cancer nuclear microenvironment: Interface between light microscopic cytology and molecular phenotype , 2008, Journal of cellular biochemistry.

[28]  R. Getzenberg,et al.  Nuclear structure as a source of cancer specific biomarkers , 2008, Journal of cellular biochemistry.

[29]  O. Bogdanović,et al.  Loss of imprinting of IGF2 and H19, loss of heterozygosity of IGF2R and CTCF, and Helicobacter pylori infection in laryngeal squamous cell carcinoma , 2008, Journal of Molecular Medicine.

[30]  T. Misteli,et al.  On the contribution of spatial genome organization to cancerous chromosome translocations. , 2008, Journal of the National Cancer Institute. Monographs.

[31]  Kelly M. McGarvey,et al.  A novel 6C assay uncovers Polycomb-mediated higher order chromatin conformations. , 2008, Genome research.

[32]  D. Gold,et al.  Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation , 2008, Nature Genetics.

[33]  V P Collins,et al.  Array painting reveals a high frequency of balanced translocations in breast cancer cell lines that break in cancer-relevant genes , 2008, Oncogene.

[34]  J. Russo,et al.  SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis , 2008, Nature.

[35]  Elizabeth Kerr,et al.  Recruitment to the Nuclear Periphery Can Alter Expression of Genes in Human Cells , 2008, PLoS genetics.

[36]  F. Brasseur,et al.  Expression of BORIS in melanoma: Lack of association with MAGE‐A1 activation , 2008, International journal of cancer.

[37]  Prabhakar R. Gudla,et al.  Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP. , 2008, Genes & development.

[38]  S. Mcconnell,et al.  Satb2 Regulates Callosal Projection Neuron Identity in the Developing Cerebral Cortex , 2008, Neuron.

[39]  T. Tammela,et al.  EZH2, Ki‐67 and MCM7 are prognostic markers in prostatectomy treated patients , 2008, International journal of cancer.

[40]  D. Sheer,et al.  Anchoring the genome , 2008, Genome Biology.

[41]  Victor V Lobanenkov,et al.  BORIS, a paralogue of the transcription factor, CTCF, is aberrantly expressed in breast tumours , 2008, British Journal of Cancer.

[42]  D. Spector,et al.  A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence , 2008, The Journal of cell biology.

[43]  Tom Misteli,et al.  Locus-specific and activity-independent gene repositioning during early tumorigenesis , 2008, The Journal of cell biology.

[44]  Andrew R. Green,et al.  Loss of expression of chromosome 16q genes DPEP1 and CTCF in lobular carcinoma in situ of the breast , 2008, Breast Cancer Research and Treatment.

[45]  D. Ghosh,et al.  A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. , 2007, Cancer research.

[46]  O. van Tellingen,et al.  Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. , 2007, Cancer cell.

[47]  W. Schulz,et al.  Expression changes in EZH2, but not in BMI-1, SIRT1, DNMT1 or DNMT3B are associated with DNA methylation changes in prostate cancer , 2007, Cancer biology & therapy.

[48]  J. Carroll,et al.  Oestrogen-receptor-mediated transcription and the influence of co-factors and chromatin state , 2007, Nature Reviews Cancer.

[49]  Cameron S. Osborne,et al.  Myc Dynamically and Preferentially Relocates to a Transcription Factory Occupied by Igh , 2007, PLoS biology.

[50]  T. Nakazawa,et al.  Conservation and alteration of chromosome territory arrangements in thyroid carcinoma cell nuclei. , 2007, Thyroid : official journal of the American Thyroid Association.

[51]  D. Schrump,et al.  Dynamic transcriptional regulatory complexes including BORIS, CTCF and Sp1 modulate NY-ESO-1 expression in lung cancer cells , 2007, Oncogene.

[52]  D. Chan,et al.  Initial analyses of colon cancer-specific antigen (CCSA)-3 and CCSA-4 as colorectal cancer-associated serum markers. , 2007, Cancer research.

[53]  S. K. Zaidi,et al.  Nuclear microenvironments in biological control and cancer , 2007, Nature Reviews Cancer.

[54]  Gaudenz Danuser,et al.  Positional stability of single double-strand breaks in mammalian cells , 2007, Nature Cell Biology.

[55]  P. Fraser,et al.  Nuclear organization of the genome and the potential for gene regulation , 2007, Nature.

[56]  M. Duffy.  Role of tumor markers in patients with solid cancers: A critical review. , 2007, European journal of internal medicine.

[57]  M. Fraga,et al.  The Polycomb group protein EZH2 directly controls DNA methylation , 2007, Nature.

[58]  B. Johansson,et al.  The impact of translocations and gene fusions on cancer causation , 2007, Nature Reviews Cancer.

[59]  M. Ohtaki,et al.  Expression of Polycomb-group (PcG) protein BMI-1 predicts prognosis in patients with acute myeloid leukemia , 2007, Leukemia.

[60]  F. Recillas-Targa,et al.  Epigenetic regulation of the human retinoblastoma tumor suppressor gene promoter by CTCF. , 2007, Cancer research.

[61]  A. Berchuck,et al.  Global Expression Analysis of Cancer/Testis Genes in Uterine Cancers Reveals a High Incidence of BORIS Expression , 2007, Clinical Cancer Research.

[62]  Thomas Cremer,et al.  Radial chromatin positioning is shaped by local gene density, not by gene expression , 2007, Chromosoma.

[63]  Daniel Chourrout,et al.  Genome Regulation by Polycomb and Trithorax Proteins , 2007, Cell.

[64]  P. Jelinic,et al.  Loss of imprinting and cancer , 2007, The Journal of pathology.

[65]  T. Cremer,et al.  Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions , 2007, Nature Reviews Genetics.

[66]  Victor V Lobanenkov,et al.  A CTCF-binding silencer regulates the imprinted genes AWT1 and WT1-AS and exhibits sequential epigenetic defects during Wilms' tumourigenesis. , 2007, Human molecular genetics.

[67]  R. Getzenberg,et al.  Characterization of nuclear matrix protein alterations associated with renal cell carcinoma. , 2006, Urology.

[68]  D. Chan,et al.  EPCA-2: a highly specific serum marker for prostate cancer. , 2006, Urology.

[69]  D. Butcher,et al.  Epigenetic inactivation of BRCA1 is associated with aberrant expression of CTCF and DNA methyltransferase (DNMT3B) in some sporadic breast tumours. , 2007, European journal of cancer.

[70]  A. Dejean,et al.  Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus , 2007, Nature Cell Biology.

[71]  K. Odunsi,et al.  DNA methylation-dependent regulation of BORIS/CTCFL expression in ovarian cancer. , 2007, Cancer immunity.

[72]  S. Kozubek,et al.  Distinct nuclear arrangement of active and inactive c-myc genes in control and differentiated colon carcinoma cells. , 2006, Experimental cell research.

[73]  T. Kawabe,et al.  Dysregulated Expression of Stem Cell Factor Bmi1 in Precancerous Lesions of the Gastrointestinal Tract , 2006, Clinical Cancer Research.

[74]  Karl Rohr,et al.  Chromatin domains and the interchromatin compartment form structurally defined and functionally interacting nuclear networks , 2006, Chromosome Research.

[75]  Anke Sparmann,et al.  Polycomb silencers control cell fate, development and cancer , 2006, Nature Reviews Cancer.

[76]  C. Richard,et al.  The Potential of BORIS Detected in the Leukocytes of Breast Cancer Patients as an Early Marker of Tumorigenesis , 2006, Clinical Cancer Research.

[77]  P. Fraser.  Transcriptional control thrown for a loop. , 2006, Current opinion in genetics & development.

[78]  I. Fariñas,et al.  SATB2 Is a Multifunctional Determinant of Craniofacial Patterning and Osteoblast Differentiation , 2006, Cell.

[79]  Y. Okada,et al.  Erasure of methylation imprint at the promoter and CTCF-binding site upstream of H19 in human testicular germ cell tumors of adolescents indicate their fetal germ cell origin , 2006, Oncogene.

[80]  T. Kohwi-Shigematsu,et al.  SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes , 2006, Nature Genetics.

[81]  J. Zeitlinger,et al.  Polycomb complexes repress developmental regulators in murine embryonic stem cells , 2006, Nature.

[82]  A. Pombo,et al.  Intermingling of Chromosome Territories in Interphase Suggests Role in Translocations and Transcription-Dependent Associations , 2006, PLoS biology.

[83]  Jiri Bartek,et al.  Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks , 2006, The Journal of cell biology.

[84]  Sanjeev Galande,et al.  Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. , 2006, Molecular cell.

[85]  Megan F. Cole,et al.  Control of Developmental Regulators by Polycomb in Human Embryonic Stem Cells , 2006, Cell.

[86]  James A. Cuff,et al.  A Bivalent Chromatin Structure Marks Key Developmental Genes in Embryonic Stem Cells , 2006, Cell.

[87]  S. Merajver,et al.  Identification of EZH2 as a molecular marker for a precancerous state in morphologically normal breast tissues. , 2006, Cancer research.

[88]  Y. Nikiforov,et al.  Interphase chromosome folding determines spatial proximity of genes participating in carcinogenic RET/PTC rearrangements , 2006, Oncogene.

[89]  K. Nowak,et al.  BMI1 is a target gene of E2F-1 and is strongly expressed in primary neuroblastomas , 2006, Nucleic acids research.

[90]  Johan Eide,et al.  Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. , 2006, Clinical cancer research : an official journal of the American Association for Cancer Research.

[91]  C. Osborne,et al.  Scaffold attachment factor SAFB1 suppresses estrogen receptor alpha-mediated transcription in part via interaction with nuclear receptor corepressor. , 2006, Molecular endocrinology.

[92]  S. Bae,et al.  Phosphorylation, acetylation and ubiquitination: the molecular basis of RUNX regulation. , 2006, Gene.

[93]  O. Halvorsen,et al.  EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[94]  P. Boccuni,et al.  Combinatorial action of RUNX1 and PU.1 in the regulation of hematopoiesis. , 2006, Critical reviews in eukaryotic gene expression.

[95]  R. Pfundt,et al.  Genomic and expression profiling of human spermatocytic seminomas: primary spermatocyte as tumorigenic precursor and DMRT1 as candidate chromosome 9 gene. , 2006, Cancer research.

[96]  Stephen A Boorjian,et al.  Increased Expression of the Polycomb Group Gene, EZH2, in Transitional Cell Carcinoma of the Bladder , 2005, Clinical Cancer Research.

[97]  M. Babjuk,et al.  Highly specific urine-based marker of bladder cancer. , 2005, Urology.

[98]  J. Auwerx,et al.  Scaffold attachment factor B1 directly interacts with nuclear receptors in living cells and represses transcriptional activity. , 2005, Journal of molecular endocrinology.

[99]  N. Palavan-Unsal,et al.  Increased Expression of EZH2, a Polycomb Group Protein, in Bladder Carcinoma , 2005, Urologia Internationalis.

[100]  Victor V Lobanenkov,et al.  Reciprocal binding of CTCF and BORIS to the NY-ESO-1 promoter coincides with derepression of this cancer-testis gene in lung cancer cells. , 2005, Cancer research.

[101]  R. Getzenberg,et al.  Mechanistic analysis of the role of BLCA-4 in bladder cancer pathobiology. , 2005, Cancer research.

[102]  J. Köllermann,et al.  Expression levels of the EZH2 polycomb transcriptional repressor correlate with aggressiveness and invasive potential of bladder carcinomas. , 2005, International journal of molecular medicine.

[103]  R. Haba,et al.  Expression of a novel biomarker, EPCA, in adenocarcinomas and precancerous lesions in the prostate. , 2005, The Journal of urology.

[104]  S. Kozubek,et al.  Nuclear topography and expression of the BCR/ABL fusion gene and its protein level influenced by cell differentiation and RNA interference. , 2005, Leukemia research.

[105]  T. Naoe,et al.  BMI-1 is Highly Expressed in M0-Subtype Acute Myeloid Leukemia , 2005, International journal of hematology.

[106]  D. Landsittel,et al.  Use of the novel marker BLCA-1 for the detection of bladder cancer. , 2005, The Journal of urology.

[107]  A. Mackay,et al.  Heightened expression of CTCF in breast cancer cells is associated with resistance to apoptosis. , 2005, Cancer research.

[108]  A. Feinberg,et al.  Association of chromosome arm 16q loss with loss of imprinting of insulin‐like growth factor–II in Wilms tumor , 2005, Genes, chromosomes & cancer.

[109]  K. Mimori,et al.  Clinical significance of enhancer of zeste homolog 2 expression in colorectal cancer cases. , 2005, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[110]  Karen Blyth,et al.  The runx genes: gain or loss of function in cancer , 2005, Nature Reviews Cancer.

[111]  R. Eils,et al.  Three-Dimensional Maps of All Chromosomes in Human Male Fibroblast Nuclei and Prometaphase Rosettes , 2005, PLoS biology.

[112]  T. Utsunomiya,et al.  Clinicopathological significance of EZH2 mRNA expression in patients with hepatocellular carcinoma , 2005, British Journal of Cancer.

[113]  M. Pierotti,et al.  Proximity of TPR and NTRK1 rearranging loci in human thyrocytes. , 2005, Cancer research.

[114]  Peter Schmidtke,et al.  Microdeletion of target sites for insulator protein CTCF in a chromosome 11p15 imprinting center in Beckwith-Wiedemann syndrome and Wilms' tumor. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[115]  M. Nikiforova,et al.  Oncogenic AKAP9-BRAF fusion is a novel mechanism of MAPK pathway activation in thyroid cancer. , 2005, The Journal of clinical investigation.

[116]  C. Yoshida,et al.  Role of Runx proteins in chondrogenesis. , 2005, Critical reviews in eukaryotic gene expression.

[117]  G. Robertson,et al.  A novel human homologue of Drosophila polycomblike gene is up-regulated in multiple cancers. , 2004, Gene.

[118]  Rolf Ohlsson,et al.  Poly(ADP-ribosyl)ation regulates CTCF-dependent chromatin insulation , 2004, Nature Genetics.

[119]  D. Butcher,et al.  DNA binding sites for putative methylation boundaries in the unmethylated region of the BRCA1 promoter , 2004, International journal of cancer.

[120]  N. Sjakste,et al.  Role of the nuclear matrix proteins in malignant transformation and cancer diagnosis. , 2004, Experimental oncology.

[121]  Daniele Zink,et al.  Nuclear structure in cancer cells , 2004, Nature Reviews Cancer.

[122]  Tom Misteli,et al.  Tissue-specific spatial organization of genomes , 2004, Genome Biology.

[123]  Adrian V. Lee,et al.  Structure-function analysis of the estrogen receptor alpha corepressor scaffold attachment factor-B1: identification of a potent transcriptional repression domain. , 2004, The Journal of biological chemistry.

[124]  D. Landsittel,et al.  Early identification of individuals with prostate cancer in negative biopsies. , 2004, The Journal of urology.

[125]  M. Lohuizen,et al.  Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas , 2004, Nature.

[126]  B. Konety,et al.  Functional Characterization of the Bladder Cancer Marker, BLCA-4 , 2004, Clinical Cancer Research.

[127]  M. Kozubek,et al.  Spatial arrangement of genes, centromeres and chromosomes in human blood cell nuclei and its changes during the cell cycle, differentiation and after irradiation , 2004, Chromosome Research.

[128]  H. Heng,et al.  From DNA structure to gene expression: mediators of nuclear compartmentalization and dynamics , 2004, Chromosome Research.

[129]  D. Spector,et al.  The dynamics of chromosome organization and gene regulation. , 2003, Annual review of biochemistry.

[130]  S. Oesterreich.  Scaffold attachment factors SAFB1 and SAFB2: Innocent bystanders or critical players in breast tumorigenesis? , 2003, Journal of cellular biochemistry.

[131]  P. V. van Diest,et al.  Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. , 2003, Neoplasia.

[132]  Debashis Ghosh,et al.  EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[133]  T. Cremer,et al.  Inheritance of gene density–related higher order chromatin arrangements in normal and tumor cell nuclei , 2003, The Journal of cell biology.

[134]  Tom Misteli,et al.  Spatial proximity of translocation-prone gene loci in human lymphomas , 2003, Nature Genetics.

[135]  Adrian V. Lee,et al.  SAFB2, a New Scaffold Attachment Factor Homolog and Estrogen Receptor Corepressor* , 2003, Journal of Biological Chemistry.

[136]  G. Sauvageau,et al.  Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells , 2003, Nature.

[137]  T. Kohwi-Shigematsu,et al.  Tissue-specific nuclear architecture and gene expession regulated by SATB1 , 2003, Nature Genetics.

[138]  Y. Shiloh.  ATM and related protein kinases: safeguarding genome integrity , 2003, Nature Reviews Cancer.

[139]  D. S. Coffey,et al.  Nuclear matrix localization of high mobility group protein I(Y) in a transgenic mouse model for prostate cancer , 2003, Journal of cellular biochemistry.

[140]  P. Farnham,et al.  Identification of the polycomb group protein SU(Z)12 as a potential molecular target for human cancer therapy. , 2003, Molecular cancer therapeutics.

[141]  S. Dhanasekaran,et al.  The polycomb group protein EZH2 is involved in progression of prostate cancer , 2002, Nature.

[142]  Victor V Lobanenkov,et al.  The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. , 2002, Seminars in cancer biology.

[143]  R. Schoen,et al.  Nuclear matrix protein alterations associated with colon cancer metastasis to the liver. , 2002, Clinical cancer research : an official journal of the American Association for Cancer Research.

[144]  R. Schoen,et al.  Identification of nuclear matrix protein alterations associated with human colon cancer. , 2002, Cancer research.

[145]  Roy Riblet,et al.  Subnuclear Compartmentalization of Immunoglobulin Loci During Lymphocyte Development , 2002, Science.

[146]  T. Cremer,et al.  Evolutionary conservation of chromosome territory arrangements in cell nuclei from higher primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[147]  A. Feinberg,et al.  Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter tts DNA-binding specificity. , 2002, Cancer research.

[148]  D. Gray,et al.  Nonequivalent nuclear location of immunoglobulin alleles in B lymphocytes , 2001, Nature Immunology.

[149]  R Ohlsson,et al.  CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. , 2001, Trends in genetics : TIG.

[150]  A. Feinberg,et al.  Loss of imprinting of insulin-like growth factor-II in Wilms' tumor commonly involves altered methylation but not mutations of CTCF or its binding site. , 2001, Cancer research.

[151]  C. Meijer,et al.  Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. , 2001, Blood.

[152]  M. Lohuizen,et al.  The bmi-1 oncoprotein is differentially expressed in non-small cell lung cancer and correlates with INK4A-ARF locus expression , 2001, British Journal of Cancer.

[153]  T. Cremer,et al.  Chromosome territories, nuclear architecture and gene regulation in mammalian cells , 2001, Nature Reviews Genetics.

[154]  E. Campo,et al.  BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphomas. , 2001, Cancer research.

[155]  R. Willemze,et al.  The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma , 2001, British journal of haematology.

[156]  J. Nickerson,et al.  Experimental observations of a nuclear matrix. , 2001, Journal of cell science.

[157]  C. Plass,et al.  Loss of imprinting of the insulin-like growth factor II gene occurs by biallelic methylation in a core region of H19-associated CTCF-binding sites in colorectal cancer. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[158]  S. Nishiguchi,et al.  Lack of the Polycomb-group gene rae28 causes maturation arrest at the early B-cell developmental stage. , 2001, Experimental hematology.

[159]  M. Nikiforova,et al.  Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. , 2000, Science.

[160]  C. Meijer,et al.  Coexpression of BMI-1 and EZH2 polycomb group genes in Reed-Sternberg cells of Hodgkin's disease. , 2000, The American journal of pathology.

[161]  G. Brenes,et al.  Clinical usefulness of the novel marker BLCA-4 for the detection of bladder cancer. , 2000, The Journal of urology.

[162]  C. Osborne,et al.  HET/SAF-B overexpression causes growth arrest and multinuclearity and is associated with aneuploidy in human breast cancer. , 2000, Clinical cancer research : an official journal of the American Association for Cancer Research.

[163]  R. Day,et al.  Detection of bladder cancer using a novel nuclear matrix protein, BLCA-4. , 2000, Clinical cancer research : an official journal of the American Association for Cancer Research.

[164]  J. Ragoussis,et al.  Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. , 2000, Journal of cell science.

[165]  C. Osborne,et al.  Tamoxifen-bound estrogen receptor (ER) strongly interacts with the nuclear matrix protein HET/SAF-B, a novel inhibitor of ER-mediated transactivation. , 2000, Molecular endocrinology.

[166]  M Kozubek,et al.  Nuclear topography of the c-myc gene in human leukemic cells. , 2000, Gene.

[167]  W. Bickmore,et al.  Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts , 2000, Current Biology.

[168]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[169]  R. Getzenberg,et al.  Nuclear matrix proteins as cancer markers , 2000, Journal of cellular biochemistry. Supplement.

[170]  V. Kroha,et al.  The topological organization of chromosomes 9 and 22 in cell nuclei has a determinative role in the induction of t(9,22) translocations and in the pathogenesis of t(9,22) leukemias , 1999, Chromosoma.

[171]  M. Hutchinson,et al.  Preclinical Feasibility Study of NMP179, a Nuclear Matrix Protein Marker for Cervical Dysplasia , 1999, Acta Cytologica.

[172]  Peter Teague,et al.  Differences in the Localization and Morphology of Chromosomes in the Human Nucleus , 1999, The Journal of cell biology.

[173]  A. Parreira,et al.  The nuclear topography of ABL, BCR, PML, and RARalpha genes: evidence for gene proximity in specific phases of the cell cycle and stages of hematopoietic differentiation. , 1999, Blood.

[174]  J. Marchese,et al.  Human cervical cancer-associated nuclear matrix proteins. , 1998, Experimental cell research.

[175]  M. Becich,et al.  Identification of nuclear matrix protein alterations associated with renal cell carcinoma. , 1998, The Journal of urology.

[176]  Michal Kozubek,et al.  Localisation and distance between ABL and BCR genes in interphase nuclei of bone marrow cells of control donors and patients with chronic myeloid leukaemia , 1997, Human Genetics.

[177]  J. Davie,et al.  Nuclear matrix proteins in well and poorly differentiated human breast cancer cell lines , 1997, Journal of cellular biochemistry.

[178]  G Horneck,et al.  Distribution of ABL and BCR genes in cell nuclei of normal and irradiated lymphocytes. , 1997, Blood.

[179]  M. Becich,et al.  Bladder cancer-associated nuclear matrix proteins. , 1996, Cancer research.

[180]  J. Yanagisawa,et al.  A matrix attachment region (MAR)-binding activity due to a p114 kilodalton protein is found only in human breast carcinomas and not in normal and benign breast disease tissues. , 1996, Cancer research.

[181]  S. Shurtleff,et al.  TEL/AML1 fusion resulting from a cryptic t(12;21) is the most common genetic lesion in pediatric ALL and defines a subgroup of patients with an excellent prognosis. , 1995, Leukemia.

[182]  R. Berezney,et al.  The nuclear matrix: a structural milieu for genomic function. , 1995, International review of cytology.

[183]  P. Neiman,et al.  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 , 1993, Molecular and cellular biology.

[184]  Y. Haupt,et al.  bmi-1 transgene induces lymphomas and collaborates with myc in tumorigenesis. , 1993, Oncogene.

[185]  K. Pienta,et al.  Nuclear matrix proteins in normal and breast cancer cells. , 1993, Cancer research.

[186]  Y. Kohwi,et al.  Torsional stress stabilizes extended base unpairing in suppressor sites flanking immunoglobulin heavy chain enhancer. , 1990, Biochemistry.