Suppression of microRNA activity amplifies IFN-γ-induced macrophage activation and promotes anti-tumour immunity (original) (raw)

• Wynn, T. A., Chawla, A. & Pollard, J. W. Macrophage biology in development, homeostasis and disease. Nature 496, 445–455 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Noy, R. & Pollard, J. W. Tumor-associated macrophages: from mechanisms to therapy. Immunity 41, 49–61 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Lahmar, Q. et al. Tissue-resident versus monocyte-derived macrophages in the tumor microenvironment. Biochim. Biophys. Acta 1865, 23–34 (2016).
  CAS PubMed Google Scholar
• Heusinkveld, M. & van der Burg, S. H. Identification and manipulation of tumor associated macrophages in human cancers. J. Trans. Med. 9, 216 (2011).
  Article CAS 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
• Sica, A. & Mantovani, A. Macrophage plasticity and polarization: in vivo veritas. J. Clin. Invest. 122, 787–795 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Pucci, F. et al. A distinguishing gene signature shared by tumor-infiltrating Tie2-expressing monocytes, blood ”resident” monocytes, and embryonic macrophages suggests common functions and developmental relationships. Blood 114, 901–914 (2009).
  Article CAS PubMed Google Scholar
• Movahedi, K. et al. Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res. 70, 5728–5739 (2010).
  Article CAS PubMed Google Scholar
• Squadrito, M. L. et al. miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep. 1, 141–154 (2012).
  Article CAS PubMed Google Scholar
• Duluc, D. et al. Interferon-gamma reverses the immunosuppressive and protumoral properties and prevents the generation of human tumor-associated macrophages. Int. J. Cancer 125, 367–373 (2009).
  Article CAS PubMed Google Scholar
• Kratochvill, F. et al. TNF counterbalances the emergence of M2 tumor macrophages. Cell Rep. 12, 1902–1914 (2015).
  Article CAS PubMed PubMed Central Google Scholar
• Guiducci, C., Vicari, A. P., Sangaletti, S., Trinchieri, G. & Colombo, M. P. Redirecting in vivo elicited tumor infiltrating macrophages and dendritic cells towards tumor rejection. Cancer Res. 65, 3437–3446 (2005).
  Article CAS PubMed Google Scholar
• De Palma, M. et al. Tumor-targeted interferon-alpha delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis. Cancer Cell 14, 299–311 (2008).
  Article CAS PubMed Google Scholar
• Rolny, C. et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19, 31–44 (2011).
  Article CAS PubMed Google Scholar
• Pyonteck, S. M. et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat. Med. 19, 1264–1272 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ha, M. & Kim, V. N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15, 509–524 (2014).
  Article CAS PubMed Google Scholar
• Bernstein, E. et al. Dicer is essential for mouse development. Nat. Genet. 35, 215–217 (2003).
  Article CAS PubMed Google Scholar
• Park, C. Y. et al. A resource for the conditional ablation of microRNAs in the mouse. Cell Rep. 1, 385–391 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Park, C. Y., Choi, Y. S. & McManus, M. T. Analysis of microRNA knockouts in mice. Hum. Mol. Genet. 19, R169–175 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Squadrito, M. L. et al. Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells. Cell Rep. 8, 1432–1446 (2014).
  Article CAS PubMed Google Scholar
• Graff, J. W., Dickson, A. M., Clay, G., McCaffrey, A. P. & Wilson, M. E. Identifying functional microRNAs in macrophages with polarized phenotypes. J. Biol. Chem. 287, 21816–21825 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Bleckmann, A. et al. Integrated miRNA and mRNA profiling of tumor-educated macrophages identifies prognostic subgroups in estrogen receptor-positive breast cancer. Mol. Oncol. 9, 155–166 (2015).
  Article CAS PubMed Google Scholar
• Squadrito, M. L., Etzrodt, M., De Palma, M. & Pittet, M. J. MicroRNA-mediated control of macrophages and its implications for cancer. Trends Immunol. 34, 350–359 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Sonda, N. et al. miR-142-3p prevents macrophage differentiation during cancer-induced myelopoiesis. Immunity 38, 1236–1249 (2013).
  Article CAS PubMed Google Scholar
• Zonari, E. et al. A role for miR-155 in enabling tumor-infiltrating innate immune cells to mount effective antitumor responses in mice. Blood 122, 243–252 (2013).
  Article CAS PubMed Google Scholar
• Xu, S. et al. Effect of miR-142-3p on the M2 macrophage and therapeutic efficacy against murine glioblastoma. J. Natl Cancer Inst. 106 (2014).
• Clausen, B. E., Burkhardt, C., Reith, W., Renkawitz, R. & Forster, I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res. 8, 265–277 (1999).
  Article CAS PubMed Google Scholar
• Harfe, B. D., McManus, M. T., Mansfield, J. H., Hornstein, E. & Tabin, C. J. The RNaseIII enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl Acad. Sci. USA 102, 10898–10903 (2005).
  Article CAS PubMed Google Scholar
• Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global double-fluorescent Cre reporter mouse. Genesis 45, 593–605 (2007).
  Article CAS PubMed Google Scholar
• De Palma, M. et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8, 211–226 (2005).
  Article CAS PubMed Google Scholar
• Coffelt, S. B. et al. Angiopoietin 2 stimulates TIE2-expressing monocytes to suppress T cell activation and to promote regulatory T cell expansion. J. Immunol. 186, 4183–4190 (2011).
  Article CAS PubMed Google Scholar
• Ries, C. H. et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 25, 846–859 (2014).
  Article CAS PubMed Google Scholar
• Lin, E. Y., Nguyen, A. V., Russell, R. G. & Pollard, J. W. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J. Exp. Med. 193, 727–740 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Mullokandov, G. et al. High-throughput assessment of microRNA activity and function using microRNA sensor and decoy libraries. Nat. Methods 9, 840–846 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Lewis, B. P., Burge, C. B. & Bartel, D. P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15–20 (2005).
  Article CAS PubMed Google Scholar
• Eichhorn, S. W. et al. mRNA destabilization is the dominant effect of mammalian microRNAs by the time substantial repression ensues. Mol. Cell 56, 104–115 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Ooi, C. H. et al. A densely interconnected genome-wide network of microRNAs and oncogenic pathways revealed using gene expression signatures. PLoS Genet. 7, e1002415 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Yang, J. S. et al. Conserved vertebrate mir-451 provides a platform for Dicer-independent, Ago2-mediated microRNA biogenesis. Proc. Natl Acad. Sci. USA 107, 15163–15168 (2010).
  Article CAS PubMed Google Scholar
• Viswanathan, S. R., Daley, G. Q. & Gregory, R. I. Selective blockade of microRNA processing by Lin28. Science 320, 97–100 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Gilfillan, S. et al. DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J. Exp. Med. 205, 2965–2973 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Freeman, G. J. et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192, 1027–1034 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Topalian, S. L. et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443–2454 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Vonderheide, R. H. & Glennie, M. J. Agonistic CD40 antibodies and cancer therapy. Clin. Cancer Res. 19, 1035–1043 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Pardoll, D. M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252–264 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Yona, S. et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38, 79–91 (2013).
  Article CAS PubMed Google Scholar
• Guo, S. et al. MicroRNA miR-125a controls hematopoietic stem cell number. Proc. Natl Acad. Sci. USA 107, 14229–14234 (2010).
  Article CAS PubMed Google Scholar
• Alemdehy, M. F. et al. Dicer1 deletion in myeloid-committed progenitors causes neutrophil dysplasia and blocks macrophage/dendritic cell development in mice. Blood 119, 4723–4730 (2012).
  Article CAS PubMed Google Scholar
• Mizoguchi, F. et al. Osteoclast-specific Dicer gene deficiency suppresses osteoclastic bone resorption. J. Cell. Biochem. 109, 866–875 (2010).
  CAS PubMed Google Scholar
• Kuipers, H., Schnorfeil, F. M., Fehling, H. J., Bartels, H. & Brocker, T. Dicer-dependent microRNAs control maturation, function, and maintenance of Langerhans cells in vivo. J. Immunol. 185, 400–409 (2010).
  Article CAS PubMed Google Scholar
• Ikeda, H., Old, L. J. & Schreiber, R. D. The roles of IFN gamma in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev. 13, 95–109 (2002).
  Article CAS PubMed Google Scholar
• Ellis, S. L. et al. The cell-specific induction of CXC chemokine ligand 9 mediated by IFN-gamma in microglia of the central nervous system is determined by the myeloid transcription factor PU.1. J. Immunol. 185, 1864–1877 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Tannenbaum, C. S. et al. The CXC chemokines IP-10 and Mig are necessary for IL-12-mediated regression of the mouse RENCA tumor. J. Immunol. 161, 927–932 (1998).
  CAS PubMed Google Scholar
• Harlin, H. et al. Chemokine expression in melanoma metastases associated with CD8 + T-cell recruitment. Cancer Res. 69, 3077–3085 (2009).
  Article CAS PubMed Google Scholar
• De Palma, M. & Lewis, C. E. Macrophage regulation of tumor responses to anticancer therapies. Cancer Cell 23, 277–286 (2013).
  Article CAS PubMed Google Scholar
• Coffelt, S. B. & de Visser, K. E. Immune-mediated mechanisms influencing the efficacy of anticancer therapies. Trends Immunol. 36, 198–216 (2015).
  Article CAS PubMed Google Scholar
• Ries, C. H., Hoves, S., Cannarile, M. A. & Ruttinger, D. CSF-1/CSF-1R targeting agents in clinical development for cancer therapy. Curr. Opin. Pharmacol. 23, 45–51 (2015).
  Article CAS PubMed Google Scholar
• Curtale, G. et al. Negative regulation of Toll-like receptor 4 signaling by IL-10-dependent microRNA-146b. Proc. Natl Acad. Sci. USA 110, 11499–11504 (2013).
  Article CAS PubMed Google Scholar
• Cobos Jimenez, V. et al. Next-generation sequencing of microRNAs uncovers expression signatures in polarized macrophages. Physiol. Genomics 46, 91–103 (2014).
  Article PubMed Google Scholar
• Banerjee, S. et al. MicroRNA let-7c regulates macrophage polarization. J. Immunol. 190, 6542–6549 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Mathsyaraja, H. et al. CSF1-ETS2-induced microRNA in myeloid cells promote metastatic tumor growth. Oncogene 34, 3651–3661 (2015).
  Article CAS PubMed Google Scholar
• Chen, X. M., Splinter, P. L., O’Hara, S. P. & LaRusso, N. F. A cellular micro-RNA, let-7i, regulates Toll-like receptor 4 expression and contributes to cholangiocyte immune responses against Cryptosporidium parvum infection. J. Biol. Chem. 282, 28929–28938 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Teng, G. G. et al. Let-7b is involved in the inflammation and immune responses associated with Helicobacter pylori infection by targeting Toll-like receptor 4. PLoS ONE 8, e56709 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• O’ Neill, L. A., Sheedy, F. J. & McCoy, C. E. MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat. Rev. Immunol. 11, 163–175 (2011).
  Article Google Scholar
• Amendola, M., Venneri, M. A., Biffi, A., Vigna, E. & Naldini, L. Coordinate dual-gene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat. Biotechnol. 23, 108–116 (2005).
  Article CAS PubMed Google Scholar
• De Palma, M. & Naldini, L. Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol. 346, 514–529 (2002).
  Article CAS PubMed Google Scholar
• Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
  Article CAS PubMed Google Scholar
• Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628 (2008).
  Article CAS PubMed Google Scholar
• Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368, 2059–2074 (2013).
  Article Google Scholar
• Sandmann, T., Kummerfeld, S. K., Gentleman, R. & Bourgon, R. gCMAP: user-friendly connectivity mapping with R. Bioinformatics 30, 127–128 (2014).
  Article CAS PubMed Google Scholar