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Rac2 Controls Tumor Growth, Metastasis and M1-M2 Macrophage Differentiation In Vivo

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Abstract

Although it is well-established that the macrophage M1 to M2 transition plays a role in tumor progression, the molecular basis for this process remains incompletely understood. Herein, we demonstrate that the small GTPase, Rac2 controls macrophage M1 to M2 differentiation and the metastatic phenotype in vivo. Using a genetic approach, combined with syngeneic and orthotopic tumor models we demonstrate that Rac2-/- mice display a marked defect in tumor growth, angiogenesis and metastasis. Microarray, RT-PCR and metabolomic analysis on bone marrow derived macrophages isolated from the Rac2-/- mice identify an important role for Rac2 in M2 macrophage differentiation. Furthermore, we define a novel molecular mechanism by which signals transmitted from the extracellular matrix via the α4β1 integrin and MCSF receptor lead to the activation of Rac2 and potentially regulate macrophage M2 differentiation. Collectively, our findings demonstrate a macrophage autonomous process by which the Rac2 GTPase is activated downstream of the α4β1 integrin and the MCSF receptor to control tumor growth, metastasis and macrophage differentiation into the M2 phenotype. Finally, using gene expression and metabolomic data from our Rac2-/- model, and information related to M1-M2 macrophage differentiation curated from the literature we executed a systems biologic analysis of hierarchical protein-protein interaction networks in an effort to develop an iterative interactome map which will predict additional mechanisms by which Rac2 may coordinately control macrophage M1 to M2 differentiation and metastasis.

Overview

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Written from the paper’s full text.

TL;DR

Rac2 is required in macrophages for tumor growth, angiogenesis, invasion, metastasis, and M1-to-M2 differentiation in mouse tumor models. The authors propose a macrophage-autonomous axis in which MCSF receptor and α4β1 integrin co-signal through Rac2 to promote M2 polarization and tumor progression.

Key findings

  • Rac2-/- mice showed significantly reduced growth of syngeneic LLC, B16 melanoma, and NB9464D tumors (p<0.001), reduced tumor angiogenesis by CD31 microvessel density (P<0.05), and less invasion into muscularis compared with WT mice.
  • Rac2-/- mice had an 80% reduction in B16F10 lung metastatic nodules (p<0.001), reduced orthotopic Panc02 pancreatic tumor growth (P<0.05), and reduced regional colonic lymph node metastasis.
  • Macrophages sorted from LLC tumors in WT mice expressed higher M2 markers (Cox2, uPA, MMP9, MMR, arginase, VEGF), while Rac2-/- tumor macrophages expressed higher M1 markers IL1 and TNFα; WT tumor macrophages also had higher arginase activity (p<0.05) and lower nitrite production (p<0.001).
  • α4Y991A knock-in mice were defective in tumor growth (p<0.001), metastasis by 90% (p<0.001), and M2 macrophage differentiation; MCSF stimulation activated Rac2 but not Rac1 about 5-fold, and injection of WT BMDMs—but not WT GBMDMs or Rac2-/- BMDMs—reversed tumor growth and metastatic defects in Rac2-/- mice.

Methods

  • Genetic mouse models: Rac2-/- and α4Y991A knock-in mice, with syngeneic/orthotopic tumor implants including LLC, B16F10, NB9464D, and Panc02; tumor growth, angiogenesis, invasion, experimental metastasis, and spontaneous lymph node metastasis were assessed.
  • Bone marrow-derived macrophages (BMDM) and GMCSF-cultured macrophages (GBMDM) were analyzed by RT-PCR, FACS, arginase/NOS assays, Rac2 GTP pull-down, haptotaxis/invasion assays, microarray (Affymetrix Mouse Genome 1.0 ST; FDR<5%), and metabolomic profiling (UHLC/MS/MS2 and GC/MS).
  • Macrophage autonomy was tested by injecting WT, Rac2-/-, or GBMDM into Rac2-/- mice; interactome analysis used literature-curated M1/M2 drivers, BioGRID protein interactions, and network propagation.

Limitations

  • The paper states that the molecular mechanisms controlling the M1-M2 transition remain incompletely understood, that M1/M2 classification is “somewhat inexact and artificial,” and that future studies are needed to validate additional cooperating signaling elements.
  • Evident from the text: all experiments are in mouse models, with no human validation; some supporting data are described as “data not shown”; and the interactome map is predictive/iterative rather than fully experimentally validated.

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Registry

Crossref · 10.1371/journal.pone.0095893

Cites

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Statistics

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Figures

Figure 1 Rac2 promotes tumor growth, angiogenesis and invasion. (A & B) WT and Rac2-/- mice (n = 8-10) were subcutaneously implanted with 1×105 LLC, B16F10 and 2×106 NB9464D cells on the dorsal flank. Tumor growth was monitored regularly, until tumors were harvested on day 21. Mean tumor volume (A) and mass (B) for each group (n = 8) is plotted. Graphs present mean ± SEM of 8 mice in each group. Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. Experiment was repeated 7–8 times with similar results. (C) Left panel shows representative immunofluorescent staining of tumor vasculature by CD31 (green) and counterstain by DAPI (blue) on frozen tumor sections of LLC and B16 tumors implanted subcutaneously in WT and Rac2-/- mice. Right panel shows reduced microvascular density (MVD) in tumors isolated from Rac2-/- animals as compared to WT animals. MVD was determined by counting the number of microvessels per high-power field (HPF) in the section with an antibody reactive to CD31. Microvessels were counted blindly in 5–10 randomly chosen fields and data is representative of three independent experiments with 4–5 mice. * P<0.05 vs. WT. (D) H & E stained images (magnification 4X and 20X) showing invasive interface between the skin and muscularis layer of subcutaneous implanted LLC tumor into WT and Rac2-/- animals. The invasive interface is shown by arrows. Same results were obtained with 7–8 mice in each group and experiment is repeated 7–8 times.
Figure 1 Rac2 promotes tumor growth, angiogenesis and invasion. (A & B) WT and Rac2-/- mice (n = 8-10) were subcutaneously implanted with 1×105 LLC, B16F10 and 2×106 NB9464D cells on the dorsal flank. Tumor growth was monitored regularly, until tumors were harvested on day 21. Mean tumor volume (A) and mass (B) for each group (n = 8) is plotted. Graphs present mean ± SEM of 8 mice in each group. Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. Experiment was repeated 7–8 times with similar results. (C) Left panel shows representative immunofluorescent staining of tumor vasculature by CD31 (green) and counterstain by DAPI (blue) on frozen tumor sections of LLC and B16 tumors implanted subcutaneously in WT and Rac2-/- mice. Right panel shows reduced microvascular density (MVD) in tumors isolated from Rac2-/- animals as compared to WT animals. MVD was determined by counting the number of microvessels per high-power field (HPF) in the section with an antibody reactive to CD31. Microvessels were counted blindly in 5–10 randomly chosen fields and data is representative of three independent experiments with 4–5 mice. * P<0.05 vs. WT. (D) H & E stained images (magnification 4X and 20X) showing invasive interface between the skin and muscularis layer of subcutaneous implanted LLC tumor into WT and Rac2-/- animals. The invasive interface is shown by arrows. Same results were obtained with 7–8 mice in each group and experiment is repeated 7–8 times.CC BY · PubMed Central
Figure 2 Rac2 promotes both experimental as well as spontaneous metastasis. (A) Experimental metastasis of B16 melanoma cells in WT and Rac2-/- mice (n = 5). B16 F10 melanoma cells (5×105 cells) were injected through the tail vein, and after 15 days, the lungs were removed and the photographs were taken shown as upper panel in the figure. Lower panel shows mean number of tumor nodules visible on the surface of the lungs in WT and Rac2-/- mice. Surface tumor nodules in lungs were counted under dissecting microscope. Values are mean ± SEM (n = 5 or 6; P<0.001; pair wise two-sided Student's t test). A marked suppression in the number of metastatic nodules was observed in Rac2-/- mice.(B) H&E-stained lung tissues demonstrating large macroscopic nodules (black arrows) were greatly increased in number and size in the WT vs. Rac2-/- mice, 15 d after B16 tumor cell injection. (C) Upper panel shows tumor mass of pancreatic tumors implanted orthotopically in WT and Rac2-/- mice. Panc02 (1×106) cells were injected in the pancreas of WT and Rac2-/- mice (n = 10). Tumors were removed 30 days after tumor implantation. Values are mean ± SEM (n = 10; P<0.05; pair wise two-sided Student's t test). Bottom panel shows representative images of pancreatic tumors isolated from pancreas of WT and Rac2-/- mice. (D) Left panel shows macroscopic view of Panc02 metastatic mesenteric lymph nodes from WT and Rac2-/- mice. Right panel shows number of metastatic mesenteric lymph nodes/mesentery. Values are mean ± SEM (n = 5 or 6; P<0.001; pair wise two-sided Student's t test). The data are representative of three independent experiments performed.
Figure 2 Rac2 promotes both experimental as well as spontaneous metastasis. (A) Experimental metastasis of B16 melanoma cells in WT and Rac2-/- mice (n = 5). B16 F10 melanoma cells (5×105 cells) were injected through the tail vein, and after 15 days, the lungs were removed and the photographs were taken shown as upper panel in the figure. Lower panel shows mean number of tumor nodules visible on the surface of the lungs in WT and Rac2-/- mice. Surface tumor nodules in lungs were counted under dissecting microscope. Values are mean ± SEM (n = 5 or 6; P<0.001; pair wise two-sided Student's t test). A marked suppression in the number of metastatic nodules was observed in Rac2-/- mice.(B) H&E-stained lung tissues demonstrating large macroscopic nodules (black arrows) were greatly increased in number and size in the WT vs. Rac2-/- mice, 15 d after B16 tumor cell injection. (C) Upper panel shows tumor mass of pancreatic tumors implanted orthotopically in WT and Rac2-/- mice. Panc02 (1×106) cells were injected in the pancreas of WT and Rac2-/- mice (n = 10). Tumors were removed 30 days after tumor implantation. Values are mean ± SEM (n = 10; P<0.05; pair wise two-sided Student's t test). Bottom panel shows representative images of pancreatic tumors isolated from pancreas of WT and Rac2-/- mice. (D) Left panel shows macroscopic view of Panc02 metastatic mesenteric lymph nodes from WT and Rac2-/- mice. Right panel shows number of metastatic mesenteric lymph nodes/mesentery. Values are mean ± SEM (n = 5 or 6; P<0.001; pair wise two-sided Student's t test). The data are representative of three independent experiments performed.CC BY · PubMed Central
Figure 3 Rac2 signaling is required for specific α4β1 integrin signaling. (A) Left panel shows BMDMs from WT, and Rac2-/- mice were tested in haptotaxis assay for capacity to migrate on different matrix proteins or fragments of fibronectin, vitronectin (via αvβ3/αvβ5); H296, via α4β1; CH271, via α5β1 and collagen via α2β1/α2β2. Comparison of WT to Rac2-/- BMDMs shows significant difference on H296 peptide (P<0.001), CH271 peptide (P<0.05), VN protein (P<0.01). Data represent mean ± SEM, representative of 4 independent experiments performed (n = 3). Right Upper panel shows Rac2 pull down assay indicating the extent of Rac2 activation in WT BMDMs under conditions of adhesion to: NS, no stimulation; Vitronectin (αvβ3/αvβ5); H296, fibronectin fragment for α4β1; CH271, fibronectin fragment for α5β1; and Collagen (α2β1/α2β2). Conversion of GDP-Rac2/Rac1 to GTP-Rac2/Rac1 was determined by using GST fusion protein representing the GTP-Rac-binding CRIB domain of the PAK-1 kinase. Cell lysate used in this comparison contained equal amounts of protein per lane. Total Rac1 and Rac2 protein was loaded for control. Right Lower panel shows Rac2 pull down assay indicating the extent of Rac2 activation in WT and α4Y991A knock in BMDMs under conditions of adhesion to H296, fibronectin fragment for α4β1. Experiments were repeated 2-3 times with similar results. (B) LLC cells were inoculated subcutaneously in WT and α4Y991A mice (n = 6–8) and tumor growth was recorded as described in Methods. Values represent mean ± SEM (n = 6–8 mice per group; P<0.001) (C) Quantitative PCR analysis of mRNA for M1, M2 specific genes in the macrophages sorted from LLC tumors grown in WT and α4Y991A mice (n = 3–4). LLC tumors implanted in WT and α4Y991A mice were used for FACS sorting of macrophages on the basis of F4/80 and CD11b staining as described in Materials and Methods. RNA was isolated from these macrophages and was used for real-time PCR analysis of the indicated genes described in Methods. Values are mean ± SEM (n = 3–4). Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001.). (D) Left panel shows representative photograph of pulmonary metastatic foci produced 15 days after intravenous injection of B16F10 cells in WT and α4Y991A mice (n = 6–8). Right panel shows mean number of tumor nodules visible on the surface of the lungs in WT and α4Y991A mice. Values are mean ± SEM (n = 6; P<0.001; pair wise two-sided Student's t test). (E), Quantitative PCR analysis of mRNA for IL 1, uPA, TNFα, MMP9, Mgl1, MMR, YM1 and TGF-β in BMDMs isolated from WT and α4Y991A knock in mice and cultured in MCSF in vitro. Data are representative of three independent experiments, shown are mean ± SEM, *P<0.05, **P<0.01 and ***P<0.001 vs. WT, t test.
Figure 3 Rac2 signaling is required for specific α4β1 integrin signaling. (A) Left panel shows BMDMs from WT, and Rac2-/- mice were tested in haptotaxis assay for capacity to migrate on different matrix proteins or fragments of fibronectin, vitronectin (via αvβ3/αvβ5); H296, via α4β1; CH271, via α5β1 and collagen via α2β1/α2β2. Comparison of WT to Rac2-/- BMDMs shows significant difference on H296 peptide (P<0.001), CH271 peptide (P<0.05), VN protein (P<0.01). Data represent mean ± SEM, representative of 4 independent experiments performed (n = 3). Right Upper panel shows Rac2 pull down assay indicating the extent of Rac2 activation in WT BMDMs under conditions of adhesion to: NS, no stimulation; Vitronectin (αvβ3/αvβ5); H296, fibronectin fragment for α4β1; CH271, fibronectin fragment for α5β1; and Collagen (α2β1/α2β2). Conversion of GDP-Rac2/Rac1 to GTP-Rac2/Rac1 was determined by using GST fusion protein representing the GTP-Rac-binding CRIB domain of the PAK-1 kinase. Cell lysate used in this comparison contained equal amounts of protein per lane. Total Rac1 and Rac2 protein was loaded for control. Right Lower panel shows Rac2 pull down assay indicating the extent of Rac2 activation in WT and α4Y991A knock in BMDMs under conditions of adhesion to H296, fibronectin fragment for α4β1. Experiments were repeated 2-3 times with similar results. (B) LLC cells were inoculated subcutaneously in WT and α4Y991A mice (n = 6–8) and tumor growth was recorded as described in Methods. Values represent mean ± SEM (n = 6–8 mice per group; P<0.001) (C) Quantitative PCR analysis of mRNA for M1, M2 specific genes in the macrophages sorted from LLC tumors grown in WT and α4Y991A mice (n = 3–4). LLC tumors implanted in WT and α4Y991A mice were used for FACS sorting of macrophages on the basis of F4/80 and CD11b staining as described in Materials and Methods. RNA was isolated from these macrophages and was used for real-time PCR analysis of the indicated genes described in Methods. Values are mean ± SEM (n = 3–4). Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001.). (D) Left panel shows representative photograph of pulmonary metastatic foci produced 15 days after intravenous injection of B16F10 cells in WT and α4Y991A mice (n = 6–8). Right panel shows mean number of tumor nodules visible on the surface of the lungs in WT and α4Y991A mice. Values are mean ± SEM (n = 6; P<0.001; pair wise two-sided Student's t test). (E), Quantitative PCR analysis of mRNA for IL 1, uPA, TNFα, MMP9, Mgl1, MMR, YM1 and TGF-β in BMDMs isolated from WT and α4Y991A knock in mice and cultured in MCSF in vitro. Data are representative of three independent experiments, shown are mean ± SEM, *P<0.05, **P<0.01 and ***P<0.001 vs. WT, t test.CC BY · PubMed Central
Figure 4 Rac2 promotes M2 macrophage polarization with no substantial change in macrophage recruitment. (A) Identification of F4/80+ macrophages by immunofluorescence microscopy in the frozen sections of LLC and B16 tumors stained with antibodies against F4/80 and imaged by fluorescence microscopy. The average no. of macrophages per HPF for 3 different experiments were 42±8, (WT) 38±6 (Rac2-/-) for LLC tumors and 50±5, (WT) 45±10, (Rac2-/-) for B16 tumors. Macrophages were counted blindly by 3 individuals in 5-10 randomly chosen fields and data is representative of three independent experiments with 4 mice. (B) Figure represents FACS data showing the quantification of CD11b and F480+ macrophages infiltrated in LLC tumors implanted in WT and Rac2-/- mice. Experiment was repeated 4-5 times with 3-4 mice in each group and similar results were obtained. (C) Quantitative PCR analysis of mRNA for M1, M2 specific genes in the macrophages sorted from LLC tumors grown in WT and Rac2-/- mice (n = 3–4) as described in Methods. Values are mean ± SEM. Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. (D) Arginase activity was measured in macrophages sorted from LLC tumors injected in WT and Rac2-/- mice as described in Methods. (E) Nitrite production in macrophages sorted from LLC tumors injected in WT and Rac2-/- and stimulated with 10 ng/ml LPS for 24 h. Supernatants were collected, and nitrite concentration was measured as described in Methods. Results are mean ± SEM (n = 3–4 mice) for 3 independent experiments performed in triplicate (P<0.05 for arginase activity and P<0.001 for nitrite assay; student's t test).
Figure 4 Rac2 promotes M2 macrophage polarization with no substantial change in macrophage recruitment. (A) Identification of F4/80+ macrophages by immunofluorescence microscopy in the frozen sections of LLC and B16 tumors stained with antibodies against F4/80 and imaged by fluorescence microscopy. The average no. of macrophages per HPF for 3 different experiments were 42±8, (WT) 38±6 (Rac2-/-) for LLC tumors and 50±5, (WT) 45±10, (Rac2-/-) for B16 tumors. Macrophages were counted blindly by 3 individuals in 5-10 randomly chosen fields and data is representative of three independent experiments with 4 mice. (B) Figure represents FACS data showing the quantification of CD11b and F480+ macrophages infiltrated in LLC tumors implanted in WT and Rac2-/- mice. Experiment was repeated 4-5 times with 3-4 mice in each group and similar results were obtained. (C) Quantitative PCR analysis of mRNA for M1, M2 specific genes in the macrophages sorted from LLC tumors grown in WT and Rac2-/- mice (n = 3–4) as described in Methods. Values are mean ± SEM. Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. (D) Arginase activity was measured in macrophages sorted from LLC tumors injected in WT and Rac2-/- mice as described in Methods. (E) Nitrite production in macrophages sorted from LLC tumors injected in WT and Rac2-/- and stimulated with 10 ng/ml LPS for 24 h. Supernatants were collected, and nitrite concentration was measured as described in Methods. Results are mean ± SEM (n = 3–4 mice) for 3 independent experiments performed in triplicate (P<0.05 for arginase activity and P<0.001 for nitrite assay; student's t test).CC BY · PubMed Central
Figure 5 Rac2 promotes differentiation of M2 macrophages in vitro. (A) Quantitative PCR analysis of mRNA for IL 1, uPA, TNFα, MMP9, Mgl1, MMR, YM1 and TGF-β in BMDMs isolated from WT and Rac2-/- mice and cultured in MCSF in vitro. Values are mean ± SEM (n = 3-4 mice). Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. (B) & (C), Heat map generated from microarray analysis of BMDMs isolated from WT and Rac2-/- mice (n = 5 in each group) as described in Materials and Methods. Colors illustrate fold changes, Red: up-regulation; green: down-regulation; black: no change. The bar code on the bottom represents the color scale of the log 2 values. The differential expression of genes related to cell cycle, angiogenesis and invasion are shown in B and M1-M2 polarization are shown in (C). (D) & (E), Heatmap representation of metabolites across BMDMs from WT (n = 5) and Rac2-/- (n = 5) mice. Shades of yellow represent elevation of a metabolite and shades of blue represent decrease of a metabolite relative to the median metabolite levels (see color scale). Colors illustrate fold changes, Yellow: up-regulation; blue: down-regulation; black: no change. Data shows higher expression of metabolites related to carbohydrate (D) and lipid metabolism (E) in Rac2-/- BMDMs.
Figure 5 Rac2 promotes differentiation of M2 macrophages in vitro. (A) Quantitative PCR analysis of mRNA for IL 1, uPA, TNFα, MMP9, Mgl1, MMR, YM1 and TGF-β in BMDMs isolated from WT and Rac2-/- mice and cultured in MCSF in vitro. Values are mean ± SEM (n = 3-4 mice). Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. (B) & (C), Heat map generated from microarray analysis of BMDMs isolated from WT and Rac2-/- mice (n = 5 in each group) as described in Materials and Methods. Colors illustrate fold changes, Red: up-regulation; green: down-regulation; black: no change. The bar code on the bottom represents the color scale of the log 2 values. The differential expression of genes related to cell cycle, angiogenesis and invasion are shown in B and M1-M2 polarization are shown in (C). (D) & (E), Heatmap representation of metabolites across BMDMs from WT (n = 5) and Rac2-/- (n = 5) mice. Shades of yellow represent elevation of a metabolite and shades of blue represent decrease of a metabolite relative to the median metabolite levels (see color scale). Colors illustrate fold changes, Yellow: up-regulation; blue: down-regulation; black: no change. Data shows higher expression of metabolites related to carbohydrate (D) and lipid metabolism (E) in Rac2-/- BMDMs.CC BY · PubMed Central
Figure 6 Reversal of the metastatic defect by injection of macrophages cultured in MCSF. (A) Upper panel shows that MCSF signaling differentially activates Rac2 while GMCSF signaling does not result in significant Rac2 activation. BMDMs or GBMDMs cultured in MCSF or GMCSF for 7 days were serum starved for 4 hrs and stimulated with 50 ng/ml of MCSF or GMCSF for 15 min followed by Rac2 GTP pull down assays as described in Materials and Methods. Lower panel shows the differential activation of Rac2 when Mθs are costimulated through the MCSFR and α4β1 integrin. WT BMDMs cultured in MCSF for 7 days were serum starved for 4 hrs, trypsinized and were allowed to engage with α4β1 ligand (H296) or α2β1 ligand (collagen), followed by MCSF stimulation (50 ng/ml) for 15 min and Rac2 GTP pull down assay as described before. (B & C) Tumor volume (B) and mass (C) of LLC tumors grown in Rac2-/- mice treated with or without 1 million WT BMDMs or Rac2-/- BMDMs or WT GBMDMs. After 5 days of LLC tumor inoculation, Rac2-/- mice were treated either with 1 million WT BMDMs or GBMDMs or Rac2-/- BMDMs or every third day, until tumors were removed on day 21. Values are mean ± SEM (n = 6-8). Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. Experiment was repeated three times with similar results. (D) Reversal of B16 metastasis by injection of WT BMDMs and not by WT GBMDMs in Rac2-/- mice. Figure shows representative photograph of pulmonary metastatic foci produced 15 days after intravenous injection of B16F10 cells in Rac2-/- mice and treated with 1 million WT BMDMs or WT GBMDMs. One dose of 1 million BMDMs or GBMDMs were given to Rac2-/- mice two days before inoculating 5×105 B16F10 cells intravenously followed by treatment with 1 million BMDM or GBMDM every third day, lungs were harvested on day 15. Data are representative of three independent experiments with 6–8 mice in each group. (E) Reversal of metastatic defect in Rac2-/- mice by local injections of 1 million WT BMDMs in the right lobe of lungs and 1 million WT GBMDMs or Rac2-/- BMDMs in the left lobe of Rac2-/- mice, followed by tail vein injections of B16 luciferase cells (5×105) after 2 days. The luciferase signal was monitored every third day on IVIS by injecting luciferin, until lungs were harvested on day 15 (n = 5). Data are representative of two independent experiments with 5–6 mice in each group.
Figure 6 Reversal of the metastatic defect by injection of macrophages cultured in MCSF. (A) Upper panel shows that MCSF signaling differentially activates Rac2 while GMCSF signaling does not result in significant Rac2 activation. BMDMs or GBMDMs cultured in MCSF or GMCSF for 7 days were serum starved for 4 hrs and stimulated with 50 ng/ml of MCSF or GMCSF for 15 min followed by Rac2 GTP pull down assays as described in Materials and Methods. Lower panel shows the differential activation of Rac2 when Mθs are costimulated through the MCSFR and α4β1 integrin. WT BMDMs cultured in MCSF for 7 days were serum starved for 4 hrs, trypsinized and were allowed to engage with α4β1 ligand (H296) or α2β1 ligand (collagen), followed by MCSF stimulation (50 ng/ml) for 15 min and Rac2 GTP pull down assay as described before. (B & C) Tumor volume (B) and mass (C) of LLC tumors grown in Rac2-/- mice treated with or without 1 million WT BMDMs or Rac2-/- BMDMs or WT GBMDMs. After 5 days of LLC tumor inoculation, Rac2-/- mice were treated either with 1 million WT BMDMs or GBMDMs or Rac2-/- BMDMs or every third day, until tumors were removed on day 21. Values are mean ± SEM (n = 6-8). Statistical significance is assessed by two sample t-test where *denotes P<0.05, ** denotes P<0.01 and *** denotes P<0.001. Experiment was repeated three times with similar results. (D) Reversal of B16 metastasis by injection of WT BMDMs and not by WT GBMDMs in Rac2-/- mice. Figure shows representative photograph of pulmonary metastatic foci produced 15 days after intravenous injection of B16F10 cells in Rac2-/- mice and treated with 1 million WT BMDMs or WT GBMDMs. One dose of 1 million BMDMs or GBMDMs were given to Rac2-/- mice two days before inoculating 5×105 B16F10 cells intravenously followed by treatment with 1 million BMDM or GBMDM every third day, lungs were harvested on day 15. Data are representative of three independent experiments with 6–8 mice in each group. (E) Reversal of metastatic defect in Rac2-/- mice by local injections of 1 million WT BMDMs in the right lobe of lungs and 1 million WT GBMDMs or Rac2-/- BMDMs in the left lobe of Rac2-/- mice, followed by tail vein injections of B16 luciferase cells (5×105) after 2 days. The luciferase signal was monitored every third day on IVIS by injecting luciferin, until lungs were harvested on day 15 (n = 5). Data are representative of two independent experiments with 5–6 mice in each group.CC BY · PubMed Central
Figure 7 Identification of Rac2 regulated signaling pathways controlling differentiation of macrophages into M2 phenotype. (A) Graphic representation of novel integrin-Rac2 signaling axis in macrophages required for tumor growth, invasion, metastasis and the polarization of macrophages into M2 phenotype. (B) Interactome map developed from multiple-omic data which predicts how Rac2 regulates macrophage M2 differentiation. Nodes indicate genes either preselected for hierarchical analysis (colored borderer) or prioritized directly by the network propagation algorithm. Edges indicate protein-protein interactions. Node color indicates the protein or gene expression change in the Rac2-/- vs. WT condition.
Figure 7 Identification of Rac2 regulated signaling pathways controlling differentiation of macrophages into M2 phenotype. (A) Graphic representation of novel integrin-Rac2 signaling axis in macrophages required for tumor growth, invasion, metastasis and the polarization of macrophages into M2 phenotype. (B) Interactome map developed from multiple-omic data which predicts how Rac2 regulates macrophage M2 differentiation. Nodes indicate genes either preselected for hierarchical analysis (colored borderer) or prioritized directly by the network propagation algorithm. Edges indicate protein-protein interactions. Node color indicates the protein or gene expression change in the Rac2-/- vs. WT condition.CC BY · PubMed Central

Verification

Claims the paper makes

47 Own result · 15 Own interpretation · 11 No full text of the sources · 6 Partly supported · 6 Own method · 3 Couldn’t confirm · 2 Supported so far · 1 Supported · 1 Not checked yet · 1 No basis given · accuracy not yet measured

Show all 48 claims

  • Probably not a substantial claim. 26
  • It may state two separate claims as one. 24
  • The quote only partly states this claim. 1
45 of 45
  • The paper relies on this without support.

    The α4Y991A knock-in mutation specifically disrupts α4β1 integrin signaling relevant to Rac2 activation and does not have confounding effects on other pathways.

    “We next examined if α4Y991A knock-in mice bearing a point mutation in α4 integrin tail (Y991A), has any defect in activating Rac2.”
    “We observed that the α4Y991A k/in mice are defective in tumor growth (p<0.001), polarization of macrophages and metastasis (by 90%, p<0.001) (Figure 3B–D).”
  • The paper relies on this without support.

    The molecular entities involved in the global rearrangement of the transcriptional profile during alternative macrophage activation are still largely unknown.

    “Despite considerable progress, the molecular entities involved in the global rearrangement of the transcriptional profile occurring during alternative macrophage activation are still largely unknown.”
  • The paper relies on this without support.

    The coordinate regulation of the macrophage transcriptomic program downstream of CSF1R/α4β1 stimulation required for the complex physiologic transition from M1 to M2 remains unclear.

    “The coordinate regulation of the macrophage transcriptomic program downstream of CSF1R/α4β1 stimulation is required for the complex physiologic transition from M1 to M2 remains unclear.”
  • The paper relies on this without support.

    There is no literature on the interaction of CSF-1 receptor and α4β1 integrin.

    “Although there is no literature on the interaction of CSF-1 receptor and α4β1 integrin”
4 of 4

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Each contradiction between two passages listed here was confirmed by an independent check.

5 of 5

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Metadata

Authors
Joshi, S., Singh, A. R., Zulcic, M., Bao, L., Messer, K., Ideker, T., Dutkowski, J., & Durden, D. L.
Affiliations
University of California San Diego (US)
Corresponding author
Durden, Donald L.
Venue
PLoS ONE
Published
2014-04-25
Volume
9
Issue
4
Pages
e95893
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2058100343
Cited by
128
References
66
Citations by year
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FWCI
4.15
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (submittedVersion, other-oa)
  • PubMed Central (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Institutes of Health (CA23100, CA94233, HL091385)
  • University of California, San Diego (P30 CA23100)
  • National Heart, Lung, and Blood Institute (R21 HL091385, HL091385)
  • National Cancer Institute (CA94233-09, R01 CA094233, P30CA023100, P30 CA23100-22, R56 CA094233)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
  • Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
Keywords
Rac2, small GTPases, tumor-associated macrophages, macrophage polarization, macrophage differentiation, metastasis, tumor growth, angiogenesis, alpha4beta1 integrin, macrophage colony-stimulating factor receptor, extracellular matrix signaling, bone marrow-derived macrophages, protein-protein interaction network, systems biology
MeSH terms
RAC2 GTP-Binding Protein, Animals, Cell Differentiation, Enzyme Activation, Lung Neoplasms, Macrophages, Melanoma, Experimental, Mice, Inbred C57BL, Neoplasm Invasiveness, Neoplasm Transplantation, Neovascularization, Pathologic, Signal Transduction, Receptor, Macrophage Colony-Stimulating Factor, Mice, Knockout, Platelet Endothelial Cell Adhesion Molecule-1, rac GTP-Binding Proteins, Integrin alpha4beta1, Cell Line, Tumor, Tumor Burden

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

A language model drew the claims from the paper on 2026-10-19, under version 3 of the claim definition (model deepseek-v4.1-flash, prompt extract-v3).

A second model labelled each claim on 2026-10-19 (model jev-1.13-20260917, definition revision gold-guideline-v0.2).

Cited sources are checked with a language model’s help (gpt-6-sol).

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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