Abstract
The TCL1 gene at 14q32.1 is involved in chromosomal translocations and inversions in mature T cell leukemias. These leukemias are classified either as T prolymphocytic leukemias, which occur very late in life, or as T chronic lymphocytic leukemias, which often arise in patients with ataxia telangiectasia (AT) at a young age. In transgenic animals, the deregulated expression of TCL1 leads to mature T cell leukemia, demonstrating the role of TCL1 in the initiation of malignant transformation in T cell neoplasia. Expression of high levels of Tcl1 have also been found in a variety of human tumor-derived B cell lines ranging from pre-B cell to mature B cell. Here we describe the phenotype of transgenic mice, E mu-TCL1, established with TCL1 under the control of a V(H) promoter-Ig(H)-E mu enhancer to target TCL1 expression to immature and mature B cells. Flow cytometric analysis reveals a markedly expanded CD5(+) population in the peritoneal cavity of E mu-TCL1 mice starting at 2 mo of age that becomes evident in the spleen by 3-5 mo and in the bone marrow by 5-8 mo. Analysis of Ig gene rearrangements indicates monoclonality or oligoclonality in these populations, suggesting a preneoplastic expansion of CD5(+) B cell clones, with the elder mice eventually developing a chronic lymphocytic leukemia (CLL)-like disorder resembling human B-CLL. Our findings provide an animal model for CLL, the most common human leukemia, and demonstrate that deregulation of the Tcl1 pathway plays a crucial role in CLL pathogenesis.
MeSH Terms
Aging
Animals
CD5 Antigens
Cell Cycle
DNA-Binding Proteins/genetics,metabolism,physiology
Disease Models, Animal
G1 Phase
Gene Targeting
Humans
Immunoenzyme Techniques
Immunoglobulin Heavy Chains
Immunoglobulin M
Immunoglobulin Variable Region
Immunophenotyping
Leukemia, Lymphocytic, Chronic, B-Cell/etiology,genetics,metabolism
Mice
Mice, Transgenic
Plasmids
Proto-Oncogene Proteins
Resting Phase, Cell Cycle
Transcription Factors/genetics,metabolism,physiology
Chemicals
CD5 Antigens
DNA-Binding Proteins
Immunoglobulin Heavy Chains
Immunoglobulin M
Immunoglobulin Variable Region
Proto-Oncogene Proteins
TCL1A protein, human
Tcl1 protein, mouse
Transcription Factors
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Bichi Roberta
Kimmel Cancer Center, Jefferson Medical College, 233 South 10th Street, Philadelphia, PA 19107, USA.
Shinton Susan A
Martin Eric S
Koval Anatoliy
Calin George A
Cesari Rossano
Russo Giandomenico
Hardy Richard R
Croce Carlo M
References (27)
27 references, click to expand
-
Regulation of TCL1 expression in B- and T-cell lymphomas and reactive lymphoid tissues.
Cancer Res. 2000 Apr 15;60(8):2095-100
PMID: 10786666
-
Activated Ras signals developmental progression of recombinase-activating gene (RAG)-deficient pro-B lymphocytes.
J Exp Med. 1999 Jan 4;189(1):123-9
PMID: 9874569
-
Discrimination of human leukemia subtypes by flow cytometric analysis of cellular DNA and RNA.
Blood. 1980 Feb;55(2):282-93
PMID: 6928106
-
Expression of Lyt-1 antigen on certain murine B cell lymphomas.
J Exp Med. 1981 Apr 1;153(4):998-1003
PMID: 6788882
-
Infrequent normal B lymphocytes express features of B-chronic lymphocytic leukemia.
J Exp Med. 1982 Feb 1;155(2):623-8
PMID: 6977012
-
Human c-myc onc gene is located on the region of chromosome 8 that is translocated in Burkitt lymphoma cells.
Proc Natl Acad Sci U S A. 1982 Dec;79(24):7824-7
PMID: 6961453
-
Differential expression of the translocated and the untranslocated c-myc oncogene in Burkitt lymphoma.
Science. 1983 Oct 28;222(4622):390-3
PMID: 6414084
-
Role of chromosome translocations in human neoplasia.
Cell. 1987 Apr 24;49(2):155-6
PMID: 3494520
-
Normal, autoimmune, and malignant CD5+ B cells: the Ly-1 B lineage?
Annu Rev Immunol. 1988;6:197-218
PMID: 3289567
-
Restricted Ig variable region gene expression among Ly-1+ B cell lymphomas.
J Immunol. 1988 Oct 15;141(8):2788-96
PMID: 3139765
-
Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow.
J Exp Med. 1991 May 1;173(5):1213-25
PMID: 1827140
-
The NZB mouse as a model for chronic lymphocytic leukemia.
Cancer Res. 1992 Jan 15;52(2):437-43
PMID: 1370214
-
The development and repertoire of B-1 cells (CD5 B cells).
Immunol Today. 1991 Nov;12(11):389-91
PMID: 1723875
-
Origin of murine B cell lineages.
Annu Rev Immunol. 1993;11:501-38
PMID: 8476571
-
The regulated expression of B lineage associated genes during B cell differentiation in bone marrow and fetal liver.
J Exp Med. 1993 Sep 1;178(3):951-60
PMID: 8350062
-
Distinctive developmental origins and specificities of murine CD5+ B cells.
Immunol Rev. 1994 Feb;137:91-118
PMID: 7518415
-
Identification of the TCL1 gene involved in T-cell malignancies.
Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12530-4
PMID: 7809072
-
Expression of either the TCL1 oncogene, or transcripts from its homologue MTCP1/c6.1B, in leukaemic and non-leukaemic T cells from ataxia telangiectasia patients.
Oncogene. 1996 Jan 18;12(2):379-86
PMID: 8570215
-
Identification of the earliest B lineage stage in mouse bone marrow.
Immunity. 1996 Dec;5(6):527-35
PMID: 8986713
-
An unbiased analysis of V(H)-D-J(H) sequences from B-1a, B-1b, and conventional B cells.
J Immunol. 1997 Feb 1;158(3):1175-86
PMID: 9013957
-
Evidence for selection of a population of multi-reactive B cells into the splenic marginal zone.
Int Immunol. 1997 Jan;9(1):27-41
PMID: 9043945
-
Rapid molecular cloning of rearrangements of the IGHJ locus using long-distance inverse polymerase chain reaction.
Blood. 1997 Sep 15;90(6):2456-64
PMID: 9310498
-
TCL1 is overexpressed in patients affected by adult T-cell leukemias.
Cancer Res. 1997 Dec 15;57(24):5452-6
PMID: 9407948
-
Cancer statistics, 1998.
CA Cancer J Clin. 1998 Jan-Feb;48(1):6-29
PMID: 9449931
-
Deregulated expression of TCL1 causes T cell leukemia in mice.
Proc Natl Acad Sci U S A. 1998 Mar 31;95(7):3885-9
PMID: 9520462
-
Expression of the TCL1 gene at 14q32 in B-cell malignancies but not in adult T-cell leukemia.
Jpn J Cancer Res. 1998 Jul;89(7):712-8
PMID: 9738977
-
Some chronic lymphocytic leukemia cells bearing surface immunoglobulins share determinants with T cells.
Eur J Immunol. 1978 Dec;8(12):900-4
PMID: 83236