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Vol. 16, No. 13, pp. 1721-1737, July 1, 2002
1 Molecular Medicine Unit, University of Leeds, St.
James's University Hospital, Leeds LS9 7TF, UK; 2 Institute
for Molecular Biosciences and ARC Special Research Centre for
Functional and Applied Genomics, University of Queensland Q4072,
Brisbane, Australia; 3 Deptartment of Immunology, Erasmus MC,
University Medical Center, 3000 DR Rotterdam, The Netherlands;
4 Department of Biology, Beckman Institute of City of Hope,
Duarte, California 91010, USA
Expression of the gene for the macrophage colony stimulating factor
receptor (CSF-1R), c-fms, has been viewed as a hallmark of the
commitment of multipotent precursor cells to macrophages. Lineage-restricted expression of the gene is controlled by conserved elements in the proximal promoter and within the first intron. To
investigate the developmental regulation of c-fms at the level of
chromatin structure, we developed an in vitro system to examine the
maturation of multipotent myeloid precursor cells into mature macrophages. The dynamics of chromatin fine structure alterations and
transcription factor occupancy at the c-fms promoter and intronic enhancer was examined by in vivo DMS and UV-footprinting. We show that
the c-fms gene is already transcribed at low levels in early myeloid
precursors on which no CSF-1R surface expression can be detected. At
this stage of myelopoiesis, the formation of transcription factor
complexes on the promoter was complete. By contrast, occupancy of the
enhancer was acutely regulated during macrophage differentiation. Our
data show that cell-intrinsic differentiation decisions at the c-fms
locus precede the appearance of c-fms on the cell surface. They also
suggest that complex lineage-specific enhancers such as the c-fms
intronic enhancer regulate local chromatin structure through the
coordinated assembly and disassembly of distinct transcription factor complexes.
[Key Words: CSF-1 receptor; chromatin; in vivo footprinting; myeloid progenitor cells; macrophage differentiation]
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