CSF-1R inhibition alters macrophage polarization and blocks glioma progression (original) (raw)

• Stupp, R. et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987–996 (2005).
  Article CAS PubMed Google Scholar
• Wen, P.Y. & Kesari, S. Malignant gliomas in adults. N. Engl. J. Med. 359, 492–507 (2008).
  Article CAS PubMed Google Scholar
• Dunn, G.P. et al. Emerging insights into the molecular and cellular basis of glioblastoma. Genes Dev. 26, 756–784 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Verhaak, R.G. et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17, 98–110 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Balkwill, F.R. & Mantovani, A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin. Cancer Biol. 22, 33–40 (2012).
  Article CAS PubMed Google Scholar
• Joyce, J.A. & Pollard, J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer 9, 239–252 (2009).
  Article CAS PubMed Google Scholar
• Bingle, L., Brown, N.J. & Lewis, C.E. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196, 254–265 (2002).
  Article CAS PubMed Google Scholar
• Hussain, S.F. et al. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro-oncol. 8, 261–279 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Komohara, Y., Ohnishi, K., Kuratsu, J. & Takeya, M. Possible involvement of the M2 anti-inflammatory macrophage phenotype in growth of human gliomas. J. Pathol. 216, 15–24 (2008).
  Article CAS PubMed Google Scholar
• Wyckoff, J. et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 64, 7022–7029 (2004).
  Article CAS PubMed Google Scholar
• Coniglio, S.J. et al. Microglial stimulation of glioblastoma invasion involves EGFR and CSF-1R signaling. Mol. Med. 18, 519–527 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Ruffell, B., Affara, N.I. & Coussens, L.M. Differential macrophage programming in the tumor microenvironment. Trends Immunol. 33, 119–126 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Manthey, C.L. et al. JNJ-28312141, a novel orally active colony-stimulating factor-1 receptor/FMS-related receptor tyrosine kinase-3 receptor tyrosine kinase inhibitor with potential utility in solid tumors, bone metastases, and acute myeloid leukemia. Mol. Cancer Ther. 8, 3151–3161 (2009).
  Article CAS PubMed Google Scholar
• Patel, S. & Player, M.R. Colony-stimulating factor-1 receptor inhibitors for the treatment of cancer and inflammatory disease. Curr. Top. Med. Chem. 9, 599–610 (2009).
  Article CAS PubMed Google Scholar
• Fomchenko, E.I. et al. Recruited cells can become transformed and overtake PDGF-induced murine gliomas in vivo during tumor progression. PLoS ONE 6, e20605 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Hambardzumyan, D., Amankulor, N.M., Helmy, K.Y., Becher, O.J. & Holland, E.C. Modeling adult gliomas using RCAS/t-va technology. Transl. Oncol. 2, 89–95 (2009).
  Article PubMed PubMed Central Google Scholar
• Huse, J.T. & Holland, E.C. Genetically engineered mouse models of brain cancer and the promise of preclinical testing. Brain Pathol. 19, 132–143 (2009).
  Article CAS PubMed Google Scholar
• Kennedy, B.C. et al. Dynamics of central and peripheral immunomodulation in a murine glioma model. BMC Immunol. 10, 11 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Hambardzumyan, D., Parada, L.F., Holland, E.C. & Charest, A. Genetic modeling of gliomas in mice: new tools to tackle old problems. Glia 59, 1155–1168 (2011).
  Article PubMed PubMed Central Google Scholar
• Serrano, M. et al. Role of the INK4a locus in tumor suppression and cell mortality. Cell 85, 27–37 (1996).
  Article CAS PubMed Google Scholar
• Wang, T. et al. Investigation of correlation among safety biomarkers in serum, histopathological examination, and toxicogenomics. Int. J. Toxicol. 30, 300–312 (2011).
  Article CAS PubMed Google Scholar
• Kilic, T. et al. Intracranial inhibition of platelet-derived growth factor–mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class. Cancer Res. 60, 5143–5150 (2000).
  CAS PubMed Google Scholar
• Takeuchi, H., Kanzawa, T., Kondo, Y. & Kondo, S. Inhibition of platelet-derived growth factor signalling induces autophagy in malignant glioma cells. Br. J. Cancer 90, 1069–1075 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Shih, A.H. et al. Dose-dependent effects of platelet-derived growth factor-B on glial tumorigenesis. Cancer Res. 64, 4783–4789 (2004).
  Article CAS PubMed Google Scholar
• Chitu, V. & Stanley, E.R. Colony-stimulating factor-1 in immunity and inflammation. Curr. Opin. Immunol. 18, 39–48 (2006).
  Article CAS PubMed Google Scholar
• Luo, J. et al. Colony-stimulating factor 1 receptor (CSF1R) signaling in injured neurons facilitates protection and survival. J. Exp. Med. 210, 157–172 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Erblich, B., Zhu, L., Etgen, A.M., Dobrenis, K. & Pollard, J.W. Absence of colony stimulation factor-1 receptor results in loss of microglia, disrupted brain development and olfactory deficits. PLoS ONE 6, e26317 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Lin, H. et al. Discovery of a cytokine and its receptor by functional screening of the extracellular proteome. Science 320, 807–811 (2008).
  Article CAS PubMed Google Scholar
• Bradley, E.W., Ruan, M.M. & Oursler, M.J. Novel pro-survival functions of the Kruppel-like transcription factor Egr2 in promotion of macrophage colony-stimulating factor–mediated osteoclast survival downstream of the MEK/ERK pathway. J. Biol. Chem. 283, 8055–8064 (2008).
  Article CAS PubMed Google Scholar
• Friedman, J., Hastie, T. & Tibshirani, R. Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).
  Article PubMed PubMed Central Google Scholar
• Croucher, D.R., Saunders, D.N., Lobov, S. & Ranson, M. Revisiting the biological roles of PAI2 (SERPINB2) in cancer. Nat. Rev. Cancer 8, 535–545 (2008).
  Article CAS PubMed Google Scholar
• Biswas, S.K. & Mantovani, A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 11, 889–896 (2010).
  Article CAS PubMed Google Scholar
• Töröcsik, D. et al. Factor XIII-A is involved in the regulation of gene expression in alternatively activated human macrophages. Thromb. Haemost. 104, 709–717 (2010).
  Article CAS PubMed Google Scholar
• Probst-Cousin, S., Rickert, C.H. & Gullotta, F. Factor XIIIa-immunoreactivity in tumors of the central nervous system. Clin. Neuropathol. 17, 79–84 (1998).
  CAS PubMed Google Scholar
• Chen, P. et al. Tumor-associated macrophages promote angiogenesis and melanoma growth via adrenomedullin in a paracrine and autocrine manner. Clin. Cancer Res. 17, 7230–7239 (2011).
  Article CAS PubMed Google Scholar
• Schroder, W.A., Major, L. & Suhrbier, A. The role of SerpinB2 in immunity. Crit. Rev. Immunol. 31, 15–30 (2011).
  Article CAS PubMed Google Scholar
• Solinas, G. et al. Tumor-conditioned macrophages secrete migration-stimulating factor: a new marker for M2-polarization, influencing tumor cell motility. J. Immunol. 185, 642–652 (2010).
  Article CAS PubMed Google Scholar
• Sica, A., Schioppa, T., Mantovani, A. & Allavena, P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur. J. Cancer 42, 717–727 (2006).
  Article CAS PubMed Google Scholar
• Fleetwood, A.J., Lawrence, T., Hamilton, J.A. & Cook, A.D. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J. Immunol. 178, 5245–5252 (2007).
  Article CAS PubMed Google Scholar
• Sierra-Filardi, E. et al. Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood 117, 5092–5101 (2011).
  Article CAS PubMed Google Scholar
• Wu, A. et al. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro-oncol. 12, 1113–1125 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Squatrito, M. et al. Loss of ATM/Chk2/p53 pathway components accelerates tumor development and contributes to radiation resistance in gliomas. Cancer Cell 18, 619–629 (2010).
  Article CAS PubMed Google Scholar
• Cancer Genome Atlas Research Network. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061–1068 (2008).
• Freije, W.A. et al. Gene expression profiling of gliomas strongly predicts survival. Cancer Res. 64, 6503–6510 (2004).
  Article CAS PubMed Google Scholar
• Phillips, H.S. et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9, 157–173 (2006).
  Article CAS PubMed Google Scholar
• Murat, A. et al. Stem cell–related “self-renewal” signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma. J. Clin. Oncol. 26, 3015–3024 (2008).
  Article CAS PubMed Google Scholar
• Noushmehr, H. et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17, 510–522 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• DeNardo, D.G. et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discovery 1, 54–67 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Shree, T. et al. Macrophages and cathepsin proteases blunt chemotherapeutic response in breast cancer. Genes Dev. 25, 2465–2479 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Kioi, M. et al. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice. J. Clin. Invest. 120, 694–705 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Dai, C. et al. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev. 15, 1913–1925 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Tchougounova, E. et al. Loss of Arf causes tumor progression of PDGFB-induced oligodendroglioma. Oncogene 26, 6289–6296 (2007).
  Article CAS PubMed Google Scholar
• Hohl, T.M. et al. Inflammatory monocytes facilitate adaptive CD4 T cell responses during respiratory fungal infection. Cell Host Microbe 6, 470–481 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Cailhier, J.F. et al. Conditional macrophage ablation demonstrates that resident macrophages initiate acute peritoneal inflammation. J. Immunol. 174, 2336–2342 (2005).
  Article CAS PubMed Google Scholar
• Duffield, J.S. et al. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J. Clin. Invest. 115, 56–65 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Ueno, M. et al. Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 16, 543–551 (2013).
  Article CAS PubMed Google Scholar
• Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. & Nishimune, Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 407, 313–319 (1997).
  Article CAS PubMed Google Scholar
• Pontén, J. & Macintyre, E.H. Long term culture of normal and neoplastic human glia. Acta Pathol. Microbiol. Scand. 74, 465–486 (1968).
  Article PubMed Google Scholar
• Walker, W.S. Establishment of mononuclear phagocyte cell lines. J. Immunol. Methods 174, 25–31 (1994).
  Article CAS PubMed Google Scholar
• Bocchini, V. et al. An immortalized cell line expresses properties of activated microglial cells. J. Neurosci. Res. 31, 616–621 (1992).
  Article CAS PubMed Google Scholar
• Szerlip, N.J. et al. Intratumoral heterogeneity of receptor tyrosine kinases EGFR and PDGFRA amplification in glioblastoma defines subpopulations with distinct growth factor response. Proc. Natl. Acad. Sci. USA 109, 3041–3046 (2012).
  Article PubMed PubMed Central Google Scholar
• Ponomarev, V. et al. A novel triple-modality reporter gene for whole-body fluorescent, bioluminescent, and nuclear noninvasive imaging. Eur. J. Nucl. Med. Mol. Imaging 31, 740–751 (2004).
  Article CAS PubMed Google Scholar
• Jensen, J.B. & Parmar, M. Strengths and limitations of the neurosphere culture system. Mol. Neurobiol. 34, 153–161 (2006).
  Article CAS PubMed Google Scholar
• Florey, O., Kim, S.E., Sandoval, C.P., Haynes, C.M. & Overholtzer, M. Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat. Cell Biol. 13, 1335–1343 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Hirai, H. et al. MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol. Cancer Ther. 9, 1956–1967 (2010).
  Article CAS PubMed Google Scholar
• Irizarry, R.A. et al. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Gautier, L., Cope, L., Bolstad, B.M. & Irizarry, R.A. affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20, 307–315 (2004).
  Article CAS PubMed Google Scholar
• Smyth, G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
  Article PubMed Google Scholar
• Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102, 15545–15550 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Therneau, T. A package for survival analysis in S. (R package version 2.36–12, 2012).
• Warnes, G.R. et al. gplots: various R programming tools for plotting data (R package version 2.10.1, 2011).
• Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, New York, 2009).