Oncogenic role of Pax5 in the T-lymphoid lineage upon ectopic expression from the immunoglobulin heavy-chain locus

Blood. 2007 Jan 1;109(1):281-9. doi: 10.1182/blood-2006-03-009670. Epub 2006 Sep 12.

Abstract

Four of 9 PAX transcription factor genes have been associated with chromosomal translocations in human tumors, although their oncogenic potential has not yet been demonstrated in transgenic mouse models. The B-lymphoidPAX5 gene participates in the generation of the t(9;14)(p13;q32) translocation in germinal center B cells, which leads to deregulated PAX5 expression under the control of the immunoglobulin heavy-chain (IgH) locus in a subset of B-cell non-Hodgkin lymphomas. Here we reconstructed a human t(9;14) translocation in a knock-in mouse by inserting a PAX5 minigene into the IgH locus. The IgH(P5ki) allele, which corresponds to a germline rather than somatic mutation, is activated in multipotent hematopoietic progenitors and is subsequently expressed in dendritic cells (DCs) and in natural killer (NK), T, and B cells. Ectopic Pax5 expression interferes with normal T-cell development and causes immature T-lymphoblastic lymphomas in IgH(P5ki/+) and IgH(P5ki/P5ki) mice. Aggressive T-cell lymphomas develop even faster in Ik(Pax5/+) mice expressing Pax5 from the Ikaros locus. Pax5 expression in thymocytes activates B-cell-specific genes and represses T-lymphoid genes, suggesting that Pax5 contributes to lymphomagenesis by deregulating the T-cell gene-expression program. These data identify Pax5 as a potent oncogene and demonstrate that the T-lymphoid lineage is particularly sensitive to the oncogenic action of Pax5.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • B-Lymphocytes / metabolism
  • B-Lymphocytes / pathology
  • Bone Marrow Transplantation
  • Cell Differentiation / genetics*
  • Cell Lineage
  • Cell Transformation, Neoplastic / genetics*
  • Chromosomes, Human, Pair 14 / genetics*
  • Chromosomes, Human, Pair 14 / ultrastructure
  • Chromosomes, Human, Pair 9 / genetics*
  • Chromosomes, Human, Pair 9 / ultrastructure
  • Dendritic Cells / metabolism
  • Dendritic Cells / pathology
  • Embryonal Carcinoma Stem Cells
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Ikaros Transcription Factor / genetics
  • Immunoglobulin Heavy Chains / genetics*
  • Killer Cells, Natural / metabolism
  • Killer Cells, Natural / pathology
  • Lymphocytes / metabolism
  • Lymphocytes / pathology
  • Lymphoma, B-Cell / genetics
  • Lymphoma, B-Cell / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mutagenesis, Insertional
  • Neoplasm Transplantation
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology*
  • PAX5 Transcription Factor / genetics
  • PAX5 Transcription Factor / physiology*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Promoter Regions, Genetic*
  • Radiation Chimera
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology*
  • Translocation, Genetic*

Substances

  • Immunoglobulin Heavy Chains
  • PAX5 Transcription Factor
  • PAX5 protein, human
  • Pax5 protein, mouse
  • Zfpn1a1 protein, mouse
  • Ikaros Transcription Factor