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Vol. 16, No. 24, pp. 3277-3289, December 15, 2002
1 Department of Cancer Biology, Dana-Farber Cancer
Institute and Department of Pathology, Harvard Medical School, Boston,
Massachusetts 02115, USA; 2 Department of Pediatric Oncology,
Dana-Farber Cancer Institute and Harvard Medical School, Boston,
Massachusetts 02115, USA; 3 Department of Pathology, Brigham
and Women's Hospital, Harvard Medical School, Boston, Massachusetts
02115, USA; 4 Tufts University School of Veterinary Medicine,
North Grafton, Massachusetts 01536, USA; 5 Biogen, Cambridge,
Massachusetts 02142, USA
D-cyclins (cyclins D1, D2, and D3) are components of the core cell
cycle machinery. To directly test the ability of each D-cyclin to drive
development of various lineages, we generated mice expressing only
cyclin D1, or only cyclin D2, or only cyclin D3. We found that these
"single-cyclin" embryos develop normally until late gestation. Our
analyses revealed that in single-cyclin embryos, the tissue-specific
expression pattern of D-cyclins was lost. Instead, mutant embryos
ubiquitously expressed the remaining D-cyclin. These findings suggest
that the functions of the three D-cyclins are largely exchangeable at
this stage. Later in life, single-cyclin mice displayed focused
abnormalities, resulting in premature mortality. "Cyclin D1-only"
mice developed severe megaloblastic anemia, "cyclin D2-only" mice
presented neurological abnormalities, and "cyclin D3-only" mice
lacked normal cerebella. Analyses of the affected tissues revealed that
these compartments failed to sufficiently up-regulate the remaining,
intact D-cyclin. In particular, we found that in cerebellar granule
neuron precursors, the N-myc transcription factor communicates with the
cell cycle machinery via cyclins D1 and D2, but not D3, explaining the
inability of D3-only mice to up-regulate cyclin D3 in this compartment.
Hence, the requirement for a particular cyclin in a given tissue is
likely caused by specific transcription factors, rather than by unique properties of cyclins.
[Key Words: Cell cycle; D-cyclins; mouse development; cell proliferation]
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