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HEMATOPOIESIS
From the Department of Developmental and Molecular
Biology, Albert Einstein College of Medicine, Bronx, NY.
The effects of colony-stimulating factor 1 (CSF-1), the primary
regulator of mononuclear phagocyte production, are thought to be
mediated by the CSF-1 receptor (CSF-1R), encoded by the c-fms proto-oncogene. To investigate the in vivo
specificity of CSF-1 for the CSF-1R, the mouse Csf1r gene
was inactivated. The phenotype of
Csf1 Colony-stimulating factor 1 (CSF-1) regulates the
survival, proliferation, and differentiation of mononuclear phagocytic
cells and is the primary regulator of mononuclear phagocyte production in vivo.1,2 However, CSF-1 also regulates cells of the
female reproductive tract and plays an important role in
fertility.3,4 The effects of CSF-1 are mediated by a
high-affinity receptor tyrosine kinase (CSF-1R)5-8 encoded
by the c-fms proto-oncogene.9 The CSF-1R is
expressed on primitive multipotent hematopoietic cells,10,11 mononuclear phagocyte progenitor
cells,12 monoblasts, promonocytes,
monocytes,5,6 tissue macrophages,6,13-15
osteoclasts,16 B cells,17,18 smooth muscle
cells,19 and neurons.20,21 CSF-1R messenger
RNA (mRNA) is expressed in Langerhans cells,22 in the
female reproductive tract, in oocytes and embryonic cells of the inner
cell mass and trophectoderm,23 in decidual
cells,24-26 and in cells of the
trophoblast.24,25 The expression of the CSF-1R on
primitive hematopoietic cells that are unable to proliferate in vitro
in response to CSF-1 alone10,11 but are able to
proliferate and differentiate if stimulated with combinations of CSF-1
and other hematopoietic growth factors10,11,27 suggests
that CSF-1R is involved in the regulation of more primitive
hematopoietic cells than those that form macrophage colonies in vitro
in response to CSF-1 alone.
Mice homozygous for the mutation
osteopetrotic28 possess an inactivating
mutation in the coding region of the CSF-1 gene and are devoid of
detectable CSF-1.29,30 These
Csf1op/Csf1op mice are
osteopetrotic because of an early and marked deficiency of
osteoclasts28 that spontaneously recovers with
age,31,32 probably because of the action of vascular
endothelial growth factor.33 However, the phenotype of
these mice is pleiotropic.3 They are toothless; have low
body weight, low growth rate, and skeletal abnormalities; and are
deficient in tissue macrophages.2,28,30,34,35 They have
defects in both male and female fertility, neural development, the
dermis, and synovial membranes.3 The pleiotropic phenotype of the Csf1op/Csf1op mouse may be
due to a reduction in trophic and/or scavenger functions of the tissue
macrophages regulated by CSF-1, secondary to the reduction of
their concentration in tissues,2 because outside the
female reproductive tract the CSF-1R is primarily expressed in
mononuclear phagocytes.1,3 However, it is possible that some of these effects may also be due to loss of function of other cells such as neuronal cells and muscle precursors, which have also
been reported to express the CSF-1R.20,36
To address the questions of whether CSF-1 activates other receptors
besides the CSF-1R and, conversely, whether the CSF-1R mediates the
response to ligands other than CSF-1, we have carried out the targeted
inactivation of the CSF-1R gene. The present study describes the
phenotype of mice homozygous for a targeted CSF-1R-null mutation and
compares it with the phenotype of
Csf1op/Csf1op mice. The
slightly more severe phenotype of
Csf1r Construction of the Csf1r gene-targeting
vector
ES cell culture and chimeric mouse production
Mice
Radiographic analysis of mouse skeletal structure and CSF-1 radioimmunoassay Radiographs were produced by exposing euthanized or anesthetized mice in a Faxitron pathology specimen x-ray cabinet (Faxitron X-Ray, Buffalo Grove, IL). The animals were posed immediately above a fine-grained Polaroid 665 instant negative film package. Exposure was set at 50 kV for 1.5 minutes. The negatives were developed and printed according to the manufacturer's instructions (Polaroid, Cambridge, MA). CSF-1 in mouse sera was determined by a radioimmunoassay that selectively detects biologically active CSF-1.38,39Immunohistochemistry and histochemistry Rat monoclonal antibody to F4/80 was a gift from Dr David Hume (Department of Microbiology, University of Queensland). For immunostaining with F4/80 antibodies and histochemical localization of tartrate-resistant acid phosphatase (TRAP), siblings of the different genotypes were perfused and tissues were fixed, decalcified (knee joint only), embedded, sectioned, and immunostained as described.2,40 TRAP staining was carried out as described.40 Quantitative histomorphometric analyses of the hematoxylin and eosin-stained sections were performed using a digital camera to capture images. Image analysis was performed by using Image-Pro Plus (Media Cybernetics, Silver Spring, MD). F4/80+ cells in tissue sections of at least 2 mice of a particular genotype at each age were quantitated as described.2 Whole-mount preparations of the 4th inguinal mammary gland were stained with alum carmine as described.41 For the estrus cycle analyses, daily vaginal smears were stained with hematoxylin and eosin. Mice were assessed as being in one of the 4 stages: proestrus (100% intact live epithelial cells), estrus (100% cornified epithelial cells), metestrus (50% cornified epithelial cells and 50% leukocytes), or diestrus (80%-100% leukocytes).42Hematologic analysis and hematopoietic progenitor cell assays Mice (6- to 8-week-old) were euthanized by exposure to a high concentration of CO2. Blood was collected in heparinized tubes. Total white blood cells were counted in 6% CH3COOH by using a hemocytometer. Red cell parameters were analyzed by using an automatic blood cell counter. Monocytes, granulocytes, and lymphocytes were resolved by differential flow cytometry analysis as described.43 Spleen and bone marrow cell suspensions were assayed for high-proliferative potential colony-forming cells (HPP-CFCs) and CSF-1-dependent colony-forming units (CFU-Cs) in agar cultures as previously described.31 Erythroid burst-forming unit (BFU-E) and granulocyte, erythroid, megakaryocyte, and macrophage colony-forming unit (CFU-GEMM) assays were performed by using reagents supplied by Stem Cell Technology (Vancouver, BC, Canada) in methylcellulose cultures as described by the manufacturers. The growth factors used for HPP-CFC agar cultures were stem cell factor, interleukin-6 (IL-6), IL-3, and granulocyte-macrophage CSF (GM-CSF). CFU-GEMM assays were performed in methylcellulose culture medium containing stem cell factor, IL-6, IL-3, and EPO.Reverse transcriptase-PCR and Western blot To assess Csf1r gene expression, bone marrow-derived macrophages (BMMs) were prepared from siblings of the different genotypes as previously described44 but with GM-CSF replacing CSF-1. BMM cultured in mouse GM-CSF (R & D Systems, MN) was solubilized in sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) running buffer,45 subjected to SDS-PAGE, and Western blotted with a 1:1 mixture of 2 affinity purified goat antimouse CSF-1R cytoplasmic domain peptide antibodies.46 Total RNA samples were prepared from BMM using the Trizol reagent (Gibco) and assayed by reverse transcriptase (RT)-PCR with primers that bind to exon 2 of the Csf1r gene and 5' coding sequence of the GFP gene (P5 and P6, Figure 1A; P5 [5'-CTAGCAGCTGGGAGCCCCGTGCCCAGCCGACTC-3']; P6 [5'-GGGTAGCGGCTGAAGCACTGCACGCCGTAGGTC-3']). RT-PCR was carried out with an Advantage one-step RT-PCR kit (Clontech, Palo Alto, CA).Statistical analyses The mean, SD, or SEM of all numeric data was calculated. Data were analyzed by either Student t test or chi-square test, where appropriate. Comparisons of data sets yielding P > .05 were considered as not statistically significant.
Targeted disruption of the mouse CSF-1R gene A P1 clone containing the entire coding region and flanking DNA of CSF-1R gene was used to prepare the targeting construct (Figure 1A) as described in "Materials and methods." This vector was linearized and electroporated into 129SvJ strain ES cells, and clones of transfected cells resistant to both G418 and Ganc were screened for homologous recombinants by Southern blotting and PCR (Figure 1B). Of the 164 G418/Ganc-resistant clones obtained, 20 were identified as homologous recombinants and 2 of these (2C5 and 6D3) were injected into blastocysts. Of the 5 chimeras obtained, 3 (2 derived from 6D3 and one from 2C5) were transmitted to the germline. These lines were maintained on the same C57BL/6J × C3Heb/FeJ-a/a background as the Csf1op/Csf1op mice. Western blot analysis of whole cell lysates of BMM prepared from Csf1r /Csf1r and littermate
control mice indicated that the
Csf1r/Csf1r cells were devoid of
CSF-1R (Figure 1C, top panel). Consistent with these results, RT-PCR
analysis using primers P5 and P6 (Figure 1A) indicated that both
Csf1r/Csf1r and
Csf1r+/Csf1r cells expressed mRNA
encoding the CSF-1R-hGFP fusion protein (Figure 1C, lower panels).
However, no significant expression of GFP could be detected in
Csf1r/Csf1r or
Csf1r+/Csf1r cells by fluorescence
microscopy or flow cytometry (data not shown).
Gross phenotype of
Csf1r /Csf1r mice were
identical in appearance to
Csf1op/Csf1op mice. They
were small (see below) and toothless and possessed truncated limbs, a
domed skull, and, occasionally, a kinked tail. Studies with
Csf1op/Csf1op mice
indicate that they have a low body weight and a low growth rate.28,37 Mice homozygous for the
Csf1op or Csf1r
mutations possessed a significantly lower growth rate and lower adult
weight than double-positive control mice or mice heterozygous for the
mutations and were indistinguishable from each other in this respect
(Figure 1D). Furthermore, the growth curves of the double mutants were
indistinguishable from those of mice homozygous for either mutation.
The Csf1r/Csf1r mice, like
Csf1op/Csf1op
mice,47 were also deaf (data not shown).
A comparison of the genotypic frequencies for single heterozygous
crosses (Csf1+/Csf1op × Csf1+/Csf1op and
Csf1r+/Csf1r
Previous studies from our laboratory indicated that 95% of the
circulating CSF-1 is cleared by CSF-1R-mediated endocytosis and
intracellular destruction by sinusoidally located macrophages and that
circulating CSF-1 has a half-life of only 10 minutes.48 We
therefore determined the CSF-1 concentration in the sera of Csf1r Comparison of the osteopetrotic phenotypes of
Csf1r /Csf1r mice. Compared with
wild-type littermates, the long bones of their limbs were short (Figure
2) with increased bone density at the metaphyses (Figure 2),
deformities in the flat bony plates result in a domed skull (Figure 2),
and the increased bone density in the mandible presumably leads to the
failure of tooth eruption (Figure 2). Interestingly, a radiograph
analysis of the temporal changes in the femurs of wild-type and mutant
mice with age (Figure 2) indicates that there is significantly more
radiopacity in the distal metaphysis of the femurs of
Csf1r/Csf1r than of
Csf1op/Csf1op mice.
Similar results were obtained with
Csf1r/Csf1r mice derived from
both 2C5 and 6D3 ES cell lines. All further experiments were carried
out with Csf1r/Csf1r mice
derived from 2C5 ES cells.
The metaphyseal radiopacity of the long bones of
Csf1op/Csf1op and
Csf1r
Consequent to their decreased volume of femoral bone marrow, the total
femoral marrow cellularity of
Csf1op/Csf1op and
Csf1r
Reduced mononuclear phagocyte production in
Csf1r /Csf1r mice
and that they were not significantly different from
Csf1op/Csf1op mice in
this respect (Figure 4A). Similarly, the
total cellularities of the pleural and peritoneal cavities of
Csf1r/Csf1r mice were reduced to
the same extent as in
Csf1op/Csf1op mice
(Figure 4B) as were the frequencies of Mac1(CD11b)+ cells
in these cavities (Figure 4C). Tissue macrophages expressing macrophage-specific cell-surface protein, F4/80, are significantly decreased in many tissues of
Csf1op/Csf1op
mice.2 The F4/80+ cell densities of several
such tissues were determined in wild-type, Csf1op/Csf1op, and
Csf1r/Csf1r mice at ages in
which the F4/80+ macrophage density had previously been
shown2 to be maximum for the particular wild-type tissue
(Figure 5, Table
4).2,50,51 As previously
shown,2 the F4/80+ cell densities of the
tissues of Csf1op/Csf1op
mice were significantly lower than those of wild-type control mice
(including the Langerhans cells of the epidermis, previously reported
to be normal in
Csf1op/Csf1op
mice2). There was no difference between the lowered
F4/80+ cell densities of these tissues and those of
Csf1r/Csf1r mice, except
that the F4/80+ cell density in the kidney was
significantly lower in
Csf1r/Csf1r mice than in
Csf1op/Csf1op mice (Table
4). Thus, apart from this difference, the mononuclear phagocyte numbers
were equivalently reduced in
Csf1r/Csf1r and
Csf1op/Csf1op
mice.
Hematopoietic progenitor cells in
Csf1r /Csf1r mice
(5.1 ± 0.5) were significantly elevated compared with those of
littermate control wild-type mice (3.0 ± 0.3 [± SD], n = 3). The hematopoietic status of the wild-type,
Csf1op/Csf1op, and
Csf1r/Csf1r mice was examined by
determining bone marrow and splenic frequency of hematopoietic
progenitor cells at 6 weeks of age (Figure
6). Splenic BFU-Es and HPP-CFCs were
elevated to a similar extent in both types of mutant mouse. There was
no significant effect of either mutation on CFU-GM or CFU-GEMM. As
expected, in contrast to the elevated frequency of CSF-1-responsive
splenic CFU-C in the
Csf1op/Csf1op mice, there
were no CSF-1-responsive progenitors in spleens of the
Csf1r/Csf1r mice. In the bone
marrow of both
Csf1op/Csf1op and
Csf1r/Csf1r mice, there was no
difference in the frequency of these progenitors compared with their
frequency in wild-type mice, save for the absence of CFU-Cs in the
Csf1r/Csf1r mice. These results
reflect a negative regulatory role of CSF-1 on the in vivo frequencies
of splenic BFU-Es and HPP-CFCs.
Reproductive phenotype of
Csf1r /Csf1r mice, determined by
the appearance in the vagina of exfoliated anuclear cornified cells and
the absence of macrophages, although lower (8.0 ± 2.0, n = 40;
Figure 7A) than the previously reported cycling time for
Csf1op/Csf1op mice
(~14.5 days), was significantly higher than the duration of estrus in
wild-type mice (5.9 ± 0.5, n = 40; Figure 7 A). As previously
reported for the
Csf1op/Csf1op mice, this
increase in cycling time was primarily due to an increase in the
duration of the diestrus period (Figure 7B). In pregnant Csf1op/Csf1op mice, the
lactating mammary gland fails to develop normally because of a failure
of branching morphogenesis of the ductal epithelium.56 As
shown in the whole-mount stained mammary glands in Figure 7C, a similar
phenotype was observed for mammary glands from pregnant Csf1r/Csf1r mice.
Compared with normal males,
Csf1op/Csf1op male mice
had low testosterone levels, low libido, and reduced viable sperm
numbers, as well as mating infrequently and displaying a long latency
between mating when presented serially with female mice in
estrous.42 A similar phenotype was observed for
Csf1r
In this study, we have shown that BMM from mice in which both
Csf1r alleles have been targeted by the insertion of a
PGKneo cassette containing stop codons into exon 3 fail to express
detectable CSF-1R mRNA or protein. In contrast, BMM from wild- type
mice express approximately 50 000 cell surface CSF-1R molecules per cell.7 Consistent with this observation, neither bone
marrow nor splenic cells from the
Csf1r The phenotype of the
Csf1r Despite the overall similarity of the
Csf1r It has previously been suggested, in part because of the residual
tissue macrophage production seen in certain tissues in Csf1op/Csf1op mice and in
part because of the nature of the mutation, that this mouse is not
completely devoid of a mutated yet active form of CSF-1.59
However, as indicated above, the
Csf1op/Csf1op and
Csf1r It has previously been reported that the percentage of blood monocytes
and lymphocytes is reduced34,37,49 and the percentage of
blood granulocytes increased37,49 in
Csf1op/Csf1op mice,
without significant changes in the circulating leukocyte concentration.
These changes in monocytes and granulocytes are not unexpected, given
the specificity of CSF-1 for the mononuclear phagocytic
lineage13,38 and the existence of progenitors capable of
giving rise to both granulocytes and macrophages.61
However, the decrease in the percentage of blood lymphocytes, which we also observed in both
Csf1op/Csf1op and
Csf1r The development of the CSF-1R-nullizygous mouse permits new
approaches to be taken to the analysis of CSF-1 action. In studies of
CSF-1R signal transduction, a powerful approach to our understanding of
CSF-1R structure-function has been to introduce mutated forms of the
receptor into fibroblast or myeloid cell lines that do not express the
CSF-1R.64-68 However, the functions affected by particular
CSF-1R mutations have been found to differ substantially, indicating
the importance of cellular context for experiments of this kind
(reviewed in Hamilton69,70). By using BMM and progenitor
cells from Csf1r Circulating CSF-1 is composed of both proteoglycan and glycoprotein
forms.71 The analysis of these forms and their regulation has been limited by the amounts of mouse serum needed and the low
specific activity of serum CSF-1 per unit serum protein. The 20-fold
elevation of the concentration (and specific activity) of serum CSF-1
in Csf1r Perhaps the area of most immediate import is the assessment of the role
of CSF-1 in the regulation of primitive hematopoietic cells. Previous
studies have indicated that, although CFU-Cs are the most primitive
cells that can be stimulated to proliferate and differentiate by CSF-1
alone in vitro, CSF-1 can cause the proliferation and differentiation
of precursors of the CFU-Cs, by synergizing with other growth factors
that alone have limited or no effect on the proliferation of the
primitive cells.10,11,27,72 Indeed, the observation in the
present study that splenic BFU-E and HPP-CFC levels in
Csf1op/Csf1op and
Csf1r
We thank members of the AECOM analytical imaging, FACS, histopathology, hybridoma, and transgenic and gene targeting facilities for assistance in different aspects of the work; Dr Paula E. Cohen for advice on the fertility analysis; Dr Sandy C. Marks Jr for advice on TRAP staining; David Gebhard of the AECOM FACS facility for assistance with the FACS analyses; Dr Thomas Graf for reviewing the manuscript; and Xiao-Hua Zong for technical assistance.
Submitted May 23, 2001; accepted August 31, 2001.
Supported by grant CA32551 from the National Institutes of Health (E.R.S.); grant 5P30-CA13330 from the Albert Einstein College of Medicine Cancer Center; an American Cancer Society Fellowship (A.J.H.); a Yamagiwa-Yoshida Memorial UICC International Cancer Study Grant (A.J.H.); and an American Society of Hematology fellowship (G.R.R.).
The publication costs of this article were defrayed in part by page charge payment. Therefore, and solely to indicate this fact, this article is hereby marked "advertisement" in accordance with 18 U.S.C. section 1734.
Reprints: E. Richard Stanley, Dept of Developmental and Molecular Biology, Albert Einstein College of Medicine, 1300 Morris Park Ave, Bronx, NY 10461; e-mail: rstanley{at}aecom.yu.edu.
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R. Feng, S. C. Desbordes, H. Xie, E. S. Tillo, F. Pixley, E. R. Stanley, and T. Graf PU.1 and C/EBP{alpha}/{beta} convert fibroblasts into macrophage-like cells PNAS, April 22, 2008; 105(16): 6057 - 6062. [Abstract] [Full Text] [PDF]
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H. Ha, J.-H. Lee, H.-N. Kim, H. B. Kwak, H.-M. Kim, S. E. Lee, J. H. Rhee, H.-H. Kim, and Z. H. Lee Stimulation by TLR5 Modulates Osteoclast Differentiation through STAT1/IFN-{beta} J. Immunol., February 1, 2008; 180(3): 1382 - 1389. [Abstract] [Full Text] [PDF]
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J. Lattin, D. A. Zidar, K. Schroder, S. Kellie, D. A. Hume, and M. J. Sweet G-protein-coupled receptor expression, function, and signaling in macrophages J. Leukoc. Biol., July 1, 2007; 82(1): 16 - 32. [Abstract] [Full Text] [PDF]
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M. L. Hibbs, C. Quilici, N. Kountouri, J. F. Seymour, J. E. Armes, A. W. Burgess, and A. R. Dunn Mice Lacking Three Myeloid Colony-Stimulating Factors (G-CSF, GM-CSF, and M-CSF) Still Produce Macrophages and Granulocytes and Mount an Inflammatory Response in a Sterile Model of Peritonitis J. Immunol., May 15, 2007; 178(10): 6435 - 6443. [Abstract] [Full Text] [PDF]
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A. Khanna-Gupta, H. Sun, T. Zibello, H. M. Lee, R. Dahl, L. A. Boxer, and N. Berliner Growth factor independence-1 (Gfi-1) plays a role in mediating specific granule deficiency (SGD) in a patient lacking a gene-inactivating mutation in the C/EBP{epsilon} gene Blood, May 15, 2007; 109(10): 4181 - 4190. [Abstract] [Full Text] [PDF]
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Z. Yao, P. Li, Q. Zhang, E. M. Schwarz, P. Keng, A. Arbini, B. F. Boyce, and L. Xing Tumor Necrosis Factor-{alpha} Increases Circulating Osteoclast Precursor Numbers by Promoting Their Proliferation and Differentiation in the Bone Marrow through Up-regulation of c-Fms Expression J. Biol. Chem., April 28, 2006; 281(17): 11846 - 11855. [Abstract] [Full Text] [PDF]
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S. R. Himes, D. P. Sester, T. Ravasi, S. L. Cronau, T. Sasmono, and D. A. Hume The JNK Are Important for Development and Survival of Macrophages J. Immunol., February 15, 2006; 176(4): 2219 - 2228. [Abstract] [Full Text] [PDF]
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P. Palmqvist, P. Lundberg, E. Persson, A. Johansson, I. Lundgren, A. Lie, H. H. Conaway, and U. H. Lerner Inhibition of Hormone and Cytokine-stimulated Osteoclastogenesis and Bone Resorption by Interleukin-4 and Interleukin-13 Is Associated with Increased Osteoprotegerin and Decreased RANKL and RANK in a STAT6-dependent Pathway J. Biol. Chem., February 3, 2006; 281(5): 2414 - 2429. [Abstract] [Full Text] [PDF]
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S. Nandi, M. P. Akhter, M. F. Seifert, X.-M. Dai, and E. R. Stanley Developmental and functional significance of the CSF-1 proteoglycan chondroitin sulfate chain Blood, January 15, 2006; 107(2): 786 - 795. [Abstract] [Full Text] [PDF]
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J. Dauffy, G. Mouchiroud, and R. P. Bourette The interferon-inducible gene, Ifi204, is transcriptionally activated in response to M-CSF, and its expression favors macrophage differentiation in myeloid progenitor cells J. Leukoc. Biol., January 1, 2006; 79(1): 173 - 183. [Abstract] [Full Text] [PDF]
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M. Witcher, H. Y. Shiu, Q. Guo, and W. H. Miller Jr Combination of retinoic acid and tumor necrosis factor overcomes the maturation block in a variety of retinoic acid-resistant acute promyelocytic leukemia cells Blood, November 15, 2004; 104(10): 3335 - 3342. [Abstract] [Full Text] [PDF]
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D. M. Lenda, E. R. Stanley, and V. R. Kelley Negative Role of Colony-Stimulating Factor-1 in Macrophage, T Cell, and B Cell Mediated Autoimmune Disease in MRL-Faslpr Mice J. Immunol., October 1, 2004; 173(7): 4744 - 4754. [Abstract] [Full Text] [PDF]
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P. J. Hanley, B. Musset, V. Renigunta, S. H. Limberg, A. H. Dalpke, R. Sus, K. M. Heeg, R. Preisig-Muller, and J. Daut Extracellular ATP induces oscillations of intracellular Ca2+ and membrane potential and promotes transcription of IL-6 in macrophages PNAS, June 22, 2004; 101(25): 9479 - 9484. [Abstract] [Full Text] [PDF]
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A. C. Bharti, Y. Takada, and B. B. Aggarwal Curcumin (Diferuloylmethane) Inhibits Receptor Activator of NF-{kappa}B Ligand-Induced NF-{kappa}B Activation in Osteoclast Precursors and Suppresses Osteoclastogenesis J. Immunol., May 15, 2004; 172(10): 5940 - 5947. [Abstract] [Full Text] [PDF]
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P. H. Correll, A. C. Morrison, and M. A. Lutz Receptor tyrosine kinases and the regulation of macrophage activation J. Leukoc. Biol., May 1, 2004; 75(5): 731 - 737. [Full Text] [PDF]
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 C. N. Wrobel, J. Debnath, E. Lin, S. Beausoleil, M. F. Roussel, and J. S. Brugge Autocrine CSF-1R activation promotes Src-dependent disruption of mammary epithelial architecture J. Cell Biol., April 26, 2004; 165(2): 263 - 273. [Abstract] [Full Text] [PDF]
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S. H. Burnett, E. J. Kershen, J. Zhang, L. Zeng, S. C. Straley, A. M. Kaplan, and D. A. Cohen Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene J. Leukoc. Biol., April 1, 2004; 75(4): 612 - 623. [Abstract] [Full Text] [PDF]
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B. J. Jenkins, D. Grail, M. Inglese, C. Quilici, S. Bozinovski, P. Wong, and M. Ernst Imbalanced gp130-Dependent Signaling in Macrophages Alters Macrophage Colony-Stimulating Factor Responsiveness via Regulation of c-fms Expression Mol. Cell. Biol., February 15, 2004; 24(4): 1453 - 1463. [Abstract] [Full Text] [PDF]
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X.-M. Dai, X.-H. Zong, V. Sylvestre, and E. R. Stanley Incomplete restoration of colony-stimulating factor 1 (CSF-1) function in CSF-1-deficient Csf1op/Csf1op mice by transgenic expression of cell surface CSF-1 Blood, February 1, 2004; 103(3): 1114 - 1123. [Abstract] [Full Text] [PDF]
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K. Wilhelmsen and P. van der Geer Phorbol 12-Myristate 13-Acetate-Induced Release of the Colony-Stimulating Factor 1 Receptor Cytoplasmic Domain into the Cytosol Involves Two Separate Cleavage Events Mol. Cell. Biol., January 1, 2004; 24(1): 454 - 464. [Abstract] [Full Text] [PDF]
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 E. Sapi The Role of CSF-1 in Normal Physiology of Mammary Gland and Breast Cancer: An Update Experimental Biology and Medicine, January 1, 2004; 229(1): 1 - 11. [Abstract] [Full Text] [PDF]
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M. Amoui, D. J. Baylink, J. B. Tillman, and K.-H. W. Lau Expression of a Structurally Unique Osteoclastic Protein-tyrosine Phosphatase Is Driven by an Alternative Intronic, Cell Type-specific Promoter J. Biol. Chem., November 7, 2003; 278(45): 44273 - 44280. [Abstract] [Full Text] [PDF]
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 Y.-G. Yeung and E. R. Stanley Proteomic Approaches to the Analysis of Early Events in Colony-stimulating Factor-1 Signal Transduction Mol. Cell. Proteomics, November 1, 2003; 2(11): 1143 - 1155. [Abstract] [Full Text] [PDF]
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 G. A. Follows, H. Tagoh, P. Lefevre, G. J. Morgan, and C. Bonifer Differential transcription factor occupancy but evolutionarily conserved chromatin features at the human and mouse M-CSF (CSF-1) receptor loci Nucleic Acids Res., October 15, 2003; 31(20): 5805 - 5816. [Abstract] [Full Text] [PDF]
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F. Schonlau, C. Schlesiger, J. Ehrehen, S. Grabbe, C. Sorg, and C. Sunderkotter Monocyte and macrophage functions in M-CSF-deficient op/op mice during experimental leishmaniasis J. Leukoc. Biol., May 1, 2003; 73(5): 564 - 573. [Abstract] [Full Text] [PDF]
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D. M. Lenda, E. Kikawada, E. R. Stanley, and V. R. Kelley Reduced Macrophage Recruitment, Proliferation, and Activation in Colony-Stimulating Factor-1-Deficient Mice Results in Decreased Tubular Apoptosis During Renal Inflammation J. Immunol., March 15, 2003; 170(6): 3254 - 3262. [Abstract] [Full Text] [PDF]
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D. M. Parichy and J. M. Turner Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development Development, March 1, 2003; 130(5): 817 - 833. [Abstract] [Full Text] [PDF]
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R. T. Sasmono, D. Oceandy, J. W. Pollard, W. Tong, P. Pavli, B. J. Wainwright, M. C. Ostrowski, S. R. Himes, and D. A. Hume A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse Blood, February 1, 2003; 101(3): 1155 - 1163. [Abstract] [Full Text] [PDF]
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H. Ide, D. B. Seligson, S. Memarzadeh, L. Xin, S. Horvath, P. Dubey, M. B. Flick, B. M. Kacinski, A. Palotie, and O. N. Witte Expression of colony-stimulating factor 1 receptor during prostate development and prostate cancer progression PNAS, October 29, 2002; 99(22): 14404 - 14409. [Abstract] [Full Text] [PDF]
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D. A. Hume, I. L. Ross, S. R. Himes, R. T. Sasmono, C. A. Wells, and T. Ravasi The mononuclear phagocyte system revisited J. Leukoc. Biol., October 1, 2002; 72(4): 621 - 627. [Abstract] [Full Text] [PDF]
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O. M. Mitrasinovic and G. M. Murphy Jr. Accelerated Phagocytosis of Amyloid-beta by Mouse and Human Microglia Overexpressing the Macrophage Colony-stimulating Factor Receptor J. Biol. Chem., August 9, 2002; 277(33): 29889 - 29896. [Abstract] [Full Text] [PDF]
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 H. Tagoh, R. Himes, D. Clarke, P. J.M. Leenen, A. D. Riggs, D. Hume, and C. Bonifer Transcription factor complex formation and chromatin fine structure alterations at the murine c-fms (CSF-1 receptor) locus during maturation of myeloid precursor cells Genes & Dev., July 1, 2002; 16(13): 1721 - 1737. [Abstract] [Full Text] [PDF]
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Top
Abstract
Introduction
-actin (lower
panel) are shown. (D) Growth curves of progeny of double
heterozygote
(Csf1r+/Csf1r
5 for each genotype). (E) Serum CSF-1 concentration
determined by a radioimmunoassay that selectively detects biologically
active CSF-1 (± SD; n 
.01).
a mononuclear phagocyte lineage-specific hemopoietic growth factor.
J Cell Biochem.
1983;21:151-159