EVI1 and hematopoietic disorders: history and perspectives.

The ecotropic viral integration site 1 (EVI1) gene was identified almost 20 years ago as the integration site of an ecotropic retrovirus leading to murine myeloid leukemia. Since its identification, EVI1 has slowly been recognized as one of the most aggressive oncogenes associated with human leukemia. Despite the effort of many investigators, still very little is known about this gene. The mechanism by which EVI1 operates in the transformation of hematopoietic cells is not known, but it is clear that EVI1 upregulates cell proliferation, impairs cell differentiation, and induces cell transformation. In this review, we summarize the biochemical properties of EVI1 and the effects of EVI1 in biological models.

[1]  S. Potter,et al.  The Evil proto-oncogene is required at midgestation for neural, heart, and paraxial mesenchyme development , 1997, Mechanisms of Development.

[2]  R. Ren,et al.  Both AML1 and EVI1 oncogenic components are required for the cooperation of AML1/MDS1/EVI1 with BCR/ABL in the induction of acute myelogenous leukemia in mice , 2004, Oncogene.

[3]  L. Liu,et al.  The Retinoblastoma Interacting Zinc Finger Gene RIZ Produces a PR Domain-lacking Product through an Internal Promoter* , 1997, The Journal of Biological Chemistry.

[4]  E. Solary,et al.  New case of t(3;17)(q26;q22) as an additional change in a Philadelphia-positive chronic myelogenous leukemia in acceleration. , 1992, Cancer genetics and cytogenetics.

[5]  C. von Kalle,et al.  Recurrent retroviral vector integration at the Mds1/Evi1 locus in nonhuman primate hematopoietic cells. , 2005, Blood.

[6]  K. Irie,et al.  The oncoprotein Evi-1 represses TGF-β signalling by inhibiting Smad3 , 1998, Nature.

[7]  S. Huang,et al.  The yin-yang of PR-domain family genes in tumorigenesis. , 2000, Histology and histopathology.

[8]  B. Fehse,et al.  Clonal Dominance of Hematopoietic Stem Cells Triggered by Retroviral Gene Marking , 2005, Science.

[9]  J. M. Boyd,et al.  Molecular cloning and characterization of a cellular phosphoprotein that interacts with a conserved C-terminal domain of adenovirus E1A involved in negative modulation of oncogenic transformation. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Kurokawa,et al.  The corepressor CtBP interacts with Evi-1 to repress transforming growth factor beta signaling. , 2001, Blood.

[11]  J. Rowley,et al.  The chimeric genes AML1/MDS1 and AML1/EAP inhibit AML1B activation at the CSF1R promoter, but only AML1/MDS1 has tumor-promoter properties. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G. Shao,et al.  The PR Domain of the Rb-binding Zinc Finger Protein RIZ1 Is a Protein Binding Interface and Is Related to the SET Domain Functioning in Chromatin-mediated Gene Expression* , 1998, The Journal of Biological Chemistry.

[13]  G. Nucifora,et al.  P/CAF and GCN5 acetylate the AML1/MDS1/EVI1 fusion oncoprotein. , 2003, Biochemical and biophysical research communications.

[14]  J. Rowley,et al.  Intergenic splicing of MDS1 and EVI1 occurs in normal tissues as well as in myeloid leukemia and produces a new member of the PR domain family. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  D. Levanon,et al.  Structure and regulated expression of mammalian RUNX genes , 2004, Oncogene.

[16]  B. Löwenberg,et al.  Low expression of MDS1-EVI1-like-1 (MEL1) and EVI1-like-1 (EL1) genes in favorable-risk acute myeloid leukemia. , 2003, Experimental hematology.

[17]  Andrew J. Bannister,et al.  Unsafe SETs: histone lysine methyltransferases and cancer. , 2002, Trends in biochemical sciences.

[18]  S. Fichelson,et al.  Alternative splicing of the Evi-1 zinc finger gene generates mRNAs which differ by the number of zinc finger motifs. , 1990, Oncogene.

[19]  P. Marynen,et al.  Fusion of ETV6 to MDS1/EVI1 as a result of t(3;12)(q26;p13) in myeloproliferative disorders. , 1997, Cancer research.

[20]  R. Sood,et al.  Forced expression of the leukemia-associated gene EVI1 in ES cells: a model for myeloid leukemia with 3q26 rearrangements , 1999, Leukemia.

[21]  M. Crossley,et al.  Evi-1 Transforming and Repressor Activities Are Mediated by CtBP Co-repressor Proteins* , 2001, The Journal of Biological Chemistry.

[22]  S. Fujita,et al.  Novel RUNX1‐PRDM16 fusion transcripts in a patient with acute myeloid leukemia showing t(1;21)(p36;q22) , 2005, Genes, chromosomes & cancer.

[23]  G. Stein,et al.  Nomenclature for Runt-related (RUNX) proteins , 2004, Oncogene.

[24]  J. Ihle,et al.  Expression of the Evi-1 zinc finger gene in 32Dc13 myeloid cells blocks granulocytic differentiation in response to granulocyte colony-stimulating factor , 1992, Molecular and cellular biology.

[25]  Y. Kwong Translocation (2;3) and myeloid disorders. , 1996, Cancer genetics and cytogenetics.

[26]  S. Orkin,et al.  Loss of erythropoietin responsiveness in erythroid progenitors due to expression of the Evi-1 myeloid-transforming gene. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A. Kilbey,et al.  The Evi-1 proto-oncogene encodes a transcriptional repressor activity associated with transformation , 1997, Oncogene.

[28]  Y. Yazaki,et al.  Evi-1 raises AP-1 activity and stimulates c-fos promoter transactivation with dependence on the second zinc finger domain. , 1994, The Journal of biological chemistry.

[29]  R. Espinosa,et al.  Involvement of the AML1 gene in the t(3;21) in therapy-related leukemia and in chronic myeloid leukemia in blast crisis. , 1993, Blood.

[30]  L. Platanias,et al.  EVI1 Abrogates Interferon-α Response by Selectively Blocking PML Induction* , 2005, Journal of Biological Chemistry.

[31]  N. Speck,et al.  Core-binding factors in hematopoiesis and immune function , 2004, Oncogene.

[32]  G. Nucifora,et al.  Interaction of EVI1 with cAMP-responsive Element-binding Protein-binding Protein (CBP) and p300/CBP-associated Factor (P/CAF) Results in Reversible Acetylation of EVI1 and in Co-localization in Nuclear Speckles* , 2001, The Journal of Biological Chemistry.

[33]  N. Copeland,et al.  Patterns of Evi-1 expression in embryonic and adult tissues suggest that Evi-1 plays an important regulatory role in mouse development. , 1991, Development.

[34]  R. Sood,et al.  MDS1/EVI1 enhances TGF-β1 signaling and strengthens its growth-inhibitory effect, but the leukemia-associated fusion protein AML1/MDS1/EVI1, product of the t(3;21), abrogates growth-inhibition in response to TGF-β1 , 1999, Leukemia.

[35]  J. Ihle,et al.  The carboxyl domain of zinc fingers of the Evi-1 myeloid transforming gene binds a consensus sequence of GAAGATGAG. , 1994, Oncogene.

[36]  J. Winter,et al.  t(3;21)(q26;q22): A Recurring Chromosomal Abnormality in Therapy-Related Myelodysplastic Syndrome and Acute Myeloid Leukemia , 1990 .

[37]  R. Verhaak,et al.  Prognostically useful gene-expression profiles in acute myeloid leukemia. , 2004, The New England journal of medicine.

[38]  G. Nucifora,et al.  A discriminating screening is necessary to ascertain EVI1 expression by RT-PCR in malignant cells from the myeloid lineage without 3q26 rearrangement , 2003, Leukemia.

[39]  M. Kurokawa,et al.  The t(3;21) fusion product, AML1/Evi-1 blocks AML1-induced transactivation by recruiting CtBP , 2002, Oncogene.

[40]  J. Rowley,et al.  The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the gene for EAP, a highly conserved protein associated with the Epstein-Barr virus small RNA EBER 1. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Ogawa,et al.  The Evi‐1 oncoprotein inhibits c‐Jun N‐terminal kinase and prevents stress‐induced cell death , 2000, The EMBO journal.

[42]  Y. Yazaki,et al.  The AML1/Evi-1 fusion protein in the t(3;21) translocation exhibits transforming activity on Rat1 fibroblasts with dependence on the Evi-1 sequence. , 1995, Oncogene.

[43]  T. Yamagata,et al.  Dysplastic definitive hematopoiesis in AML1/EVI1 knock-in embryos. , 2005, Blood.

[44]  J. Rowley,et al.  Consistent intergenic splicing and production of multiple transcripts between AML1 at 21q22 and unrelated genes at 3q26 in (3;21)(q26;q22) translocations. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[45]  H. Nawata,et al.  Expression of EVI1 and the retinoblastoma genes in acute myelogenous leukemia with t(3;13)(q26;q13–14) , 1996, American journal of hematology.

[46]  G. Nucifora,et al.  EVI1 induces myelodysplastic syndrome in mice. , 2004, The Journal of clinical investigation.

[47]  G. Nucifora,et al.  The leukemia-associated gene MDS1/EVI1 is a new type of GATA-binding transactivator , 1997, Leukemia.

[48]  P. Venugopal,et al.  Arsenic trioxide and thalidomide combination produces multi-lineage hematological responses in myelodysplastic syndromes patients, particularly in those with high pre-therapy EVI1 expression. , 2004, Leukemia research.

[49]  J. Yokota,et al.  A novel gene, MEL1, mapped to 1p36.3 is highly homologous to the MDS1/EVI1 gene and is transcriptionally activated in t(1;3)(p36;q21)-positive leukemia cells. , 2000, Blood.

[50]  B. Bain,et al.  EVI1 expression in acute myeloid leukaemia , 2001, British journal of haematology.

[51]  H. Horvitz,et al.  Migrations of the Caenorhabditis elegans HSNs are regulated by egl-43, a gene encoding two zinc finger proteins. , 1993, Genes & development.

[52]  B. Johansson,et al.  Cytogenetic and Molecular Genetic Evolution of Chronic Myeloid Leukemia , 2002, Acta Haematologica.

[53]  Bob Löwenberg,et al.  High EVI1 expression predicts poor survival in acute myeloid leukemia: a study of 319 de novo AML patients. , 2003, Blood.

[54]  G. Nucifora,et al.  EVI1 Promotes Cell Proliferation by Interacting with BRG1 and Blocking the Repression of BRG1 on E2F1 Activity* , 2003, Journal of Biological Chemistry.

[55]  N. Kamada,et al.  Establishment of an Undifferentiated Leukemia Cell Line (Kasumi‐3) with t(3;7)(q27;q22) and Activation of the EVI1 Gene , 1996, Japanese journal of cancer research : Gann.

[56]  F. Mikhail,et al.  The leukemia-associated transcription repressor AML1/MDS1/EVI1 requires CtBP to induce abnormal growth and differentiation of murine hematopoietic cells , 2002, Oncogene.

[57]  Y. Yazaki,et al.  Dual functions of the AML1/Evi-1 chimeric protein in the mechanism of leukemogenesis in t(3;21) leukemias , 1995, Molecular and cellular biology.

[58]  G. Nucifora,et al.  Human AML1/MDS1/EVI1 fusion protein induces an acute myelogenous leukemia (AML) in mice: a model for human AML. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[59]  J. Rowley,et al.  The leukemic fusion gene AML1-MDS1-EVI1 suppresses CEBPA in acute myeloid leukemia by activation of Calreticulin. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[60]  R. Marmorstein Structure of SET domain proteins: a new twist on histone methylation. , 2003, Trends in biochemical sciences.

[61]  J. Ihle,et al.  Four of the seven zinc fingers of the Evi-1 myeloid-transforming gene are required for sequence-specific binding to GA(C/T)AAGA(T/C)AAGATAA , 1993, Molecular and cellular biology.

[62]  G. Martinelli,et al.  3q21 and 3q26 cytogenetic abnormalities in acute myeloblastic leukemia: biological and clinical features. , 1999, Haematologica.

[63]  F. Mikhail,et al.  The distal zinc finger domain of AML1/MDS1/EVI1 is an oligomerization domain involved in induction of hematopoietic differentiation defects in primary cells in vitro. , 2005, Cancer research.

[64]  M. Rocchi,et al.  A novel chromosomal translocation t(3;7)(q26;q21) in myeloid leukemia resulting in overexpression of EVI1 , 2003, Annals of Hematology.

[65]  D. Meijer,et al.  Erythroid defects and increased retrovirally-induced tumor formation in Evi1 transgenic mice , 2000, Leukemia.

[66]  N. Copeland,et al.  Identification of a common ecotropic viral integration site, Evi-1, in the DNA of AKXD murine myeloid tumors , 1988, Molecular and cellular biology.

[67]  K. Calame,et al.  Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. , 1997, Science.

[68]  J. Ihle,et al.  Unique expression of the human Evi-1 gene in an endometrial carcinoma cell line: sequence of cDNAs and structure of alternatively spliced transcripts. , 1990, Oncogene.

[69]  S. Huang,et al.  PFM1 (PRDM4), a new member of the PR-domain family, maps to a tumor suppressor locus on human chromosome 12q23-q24.1. , 1999, Genomics.

[70]  T. Jenuwein,et al.  SET domain proteins modulate chromatin domains in eu- and heterochromatin , 1998, Cellular and Molecular Life Sciences CMLS.