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Blood, 1 November 2001, Vol. 98, No. 9, pp. 2837-2844
NEOPLASIA
Cyclin D3 is a target gene of t(6;14)(p21.1;q32.3) of mature
B-cell malignancies
Takashi Sonoki,
Lana Harder,
Doug E. Horsman,
Loraine Karran,
Izumi Taniguchi,
Tony G. Willis,
Stefan Gesk,
Doris Steinemann,
Emanuele Zucca,
Brigitte Schlegelberger,
Francesc Solé,
Andrew J. Mungall,
Randy D. Gascoyne,
Reiner Siebert, and
Martin J. S. Dyer
From the Academic Department of Haematology and
Cytogenetics, Institute of Cancer Research, Sutton, United Kingdom;
Institute of Human Genetics, University Hospital, Kiel, Germany;
Department of Pathology, British Columbia Cancer Agency, Vancouver,
Canada; Internal Medicine II, Kumamoto University School of Medicine,
Kumamoto, Japan; Oncology Institute of Southern Switzerland,
Bellinzona, Switzerland; Laboratory of Cytogenetics and Molecular
Genetics, Department of Pathology, Hospital del Mar IMAs IMIM,
Barcelona, Spain; and The Sanger Centre, Wellcome Trust Genome Campus,
Cambridge, United Kingdom.
Chromosomal translocation t(6;14)(p21.1;q32.3) has been reported as
a rare but recurrent event not only in myeloma and plasma cell leukemia
but also in diffuse large B-cell non-Hodgkin lymphoma (B-NHL)
(diffuse large B-cell lymphoma [DLBCL]) and splenic lymphoma with
villous lymphocytes (SLVL); however, the nature of the target gene(s)
has not been determined. This study identified t(6;14)(p21.1;q32.3) in
3 cases of transformed extranodal marginal zone B-NHL, in 1 case of
SLVL, and in 1 case of a low-grade B-cell lymphoproliferative disorder.
In a sixth case, a CD5+ DLBCL, the translocation was
identified by molecular cloning in the absence of cytogenetically
detectable change. Two chromosomal translocation breakpoints were
cloned by using long-distance inverse polymerase chain reaction
methods. Comparison with the genomic sequence for chromosome 6p21.1
showed breakpoints approximately 59 and 73.5 kilobases 5' of the cyclin
D3 (CCND3) gene with no other identifiable transcribed
sequences in the intervening region. Although Southern blotting with
derived genomic 6p21.1 probes failed to detect other rearrangements,
fluorescent in situ hybridization assays, using BAC (bacterial
artificial chromosome) clones spanning and flanking the
CCND3 locus, along with probes for IGH
confirmed localization of 6p21.1 breakpoints within the same region, as well as fusion of the CCND3 and IGH loci.
Furthermore, in all cases, high-level expression of CCND3
was demonstrated at RNA and/or protein levels by Northern and Western
blotting and by immunohistochemistry. These data implicate
CCND3 as a dominant oncogene in the pathogenesis and
transformation in several histologic subtypes of mature B-cell
malignancies with t(6;14)(p21.1;q32.3) and suggest that
CCND3 overexpression seen in about 10% of DLBCL cases may
have a genetic basis.
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