Cell of origin in radiation-induced premalignant thymocytes with differentiation capability in mice conditionally losing one Bcl11b allele

Cancer Sci. 2013 Aug;104(8):1009-16. doi: 10.1111/cas.12193. Epub 2013 Jun 17.

Abstract

Bcl11b is a haploinsufficient tumor suppressor, mutations or deletion of which has been found in 10-16% of T-cell acute lymphoblastic leukemias. Bcl11b(KO) (/+) heterozygous mice are susceptible to thymic lymphomas, a model of T-cell acute lymphoblastic leukemia, when γ-irradiated, and irradiated Bcl11b(KO) (/+) mice generate clonally expanding or premalignant thymocytes before thymic lymphoma development. Cells with radiation-induced DNA damages are assumed to be the cells of origin in tumors; however, which thymocyte is the tumor cell origin remains obscure. In this study we generated Bcl11b(flox/+) ;Lck-Cre and Bcl11b(flox/+) ;CD4-Cre mice; in the former, loss of one Bcl11b allele occurs in thymocytes at the immature CD4(-) CD8(-) stage, whereas in the latter the loss occurs in the more differentiated CD4(+) CD8(+) double-positive stage. We examined clonal expansion and differentiation of thymocytes in mice 60 days after 3 Gy γ-irradiation. Half (9/18) of the thymuses in the Bcl11b(flox/+) ;Lck-Cre group showed limited rearrangement sites at the T-cell receptor-β (TCRβ) locus, indicating clonal cell expansion, but none in the Bcl11b(flox/+) ;CD4-Cre group did. This indicates that the origin of the premalignant thymocytes is not in double-positive cells but immature thymocytes. Interestingly, those premalignant thymocytes underwent rearrangement at various different sites of the TCRα locus and the majority showed a higher expression of TCRβ and CD8, and more differentiated phenotypes. This suggests the existence of a subpopulation of immature cells within the premalignant cells that is capable of proliferating and continuously producing differentiated thymocytes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles*
  • Animals
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • CD4-Positive T-Lymphocytes / radiation effects
  • CD8-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / pathology
  • CD8-Positive T-Lymphocytes / radiation effects
  • Cell Cycle / genetics
  • Cell Cycle / radiation effects
  • Cell Differentiation / genetics
  • Cell Differentiation / radiation effects
  • Cell Proliferation / radiation effects
  • Gamma Rays / adverse effects
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms, Radiation-Induced / genetics*
  • Neoplasms, Radiation-Induced / metabolism
  • Neoplasms, Radiation-Induced / pathology
  • Precancerous Conditions / genetics*
  • Precancerous Conditions / metabolism
  • Precancerous Conditions / pathology
  • Receptors, Antigen, T-Cell, alpha-beta / genetics
  • Receptors, Antigen, T-Cell, alpha-beta / metabolism
  • Repressor Proteins / genetics*
  • Thymocytes / metabolism
  • Thymocytes / pathology*
  • Thymocytes / radiation effects*
  • Thymus Neoplasms / genetics*
  • Thymus Neoplasms / metabolism
  • Thymus Neoplasms / pathology
  • Tumor Suppressor Proteins / genetics*

Substances

  • Bcl11b protein, mouse
  • Receptors, Antigen, T-Cell, alpha-beta
  • Repressor Proteins
  • Tumor Suppressor Proteins