Microenvironmental control of breast cancer subtype elicited through paracrine platelet-derived growth factor-CC signaling

  • 1.

    Perou, C.M. et al. Molecular portraits of human breast tumours. Nature 406, 747–752 (2000).

  • 2.

    Goldhirsch, A. et al. Thresholds for therapies: highlights of the St Gallen International Expert Consensus on the primary therapy of early breast cancer 2009. Ann. Oncol. 20, 1319–1329 (2009).

  • 3.

    Sørlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. USA 98, 10869–10874 (2001).

  • 4.

    Goldhirsch, A. et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann. Oncol. 24, 2206–2223 (2013).

  • 5.

    Goldhirsch, A. et al. Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann. Oncol. 22, 1736–1747 (2011).

  • 6.

    Prat, A. et al. Clinical implications of the intrinsic molecular subtypes of breast cancer. Breast 24 (Suppl. 2), S26–S35 (2015).

  • 7.

    Ignatiadis, M. & Sotiriou, C. Luminal breast cancer: from biology to treatment. Nat. Rev. Clin. Oncol. 10, 494–506 (2013).

  • 8.

    Voduc, K.D. et al. Breast cancer subtypes and the risk of local and regional relapse. J. Clin. Oncol. 28, 1684–1691 (2010).

  • 9.

    Prat, A. & Perou, C.M. Deconstructing the molecular portraits of breast cancer. Mol. Oncol. 5, 5–23 (2011).

  • 10.

    Hanahan, D. & Coussens, L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 21, 309–322 (2012).

  • 11.

    Pietras, K. & Ostman, A. Hallmarks of cancer: interactions with the tumor stroma. Exp. Cell Res. 316, 1324–1331 (2010).

  • 12.

    Kalluri, R. & Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 6, 392–401 (2006).

  • 13.

    Cortez, E., Roswall, P. & Pietras, K. Functional subsets of mesenchymal cell types in the tumor microenvironment. Semin. Cancer Biol. 25, 3–9 (2014).

  • 14.

    Augsten, M. Cancer-associated fibroblasts as another polarized cell type of the tumor microenvironment. Front. Oncol. 4, 62 (2014).

  • 15.

    Kim, H.M., Jung, W.H. & Koo, J.S. Expression of cancer-associated fibroblast related proteins in metastatic breast cancer: an immunohistochemical analysis. J. Transl. Med. 13, 222 (2015).

  • 16.

    Anderberg, C. et al. Paracrine signaling by platelet-derived growth factor-CC promotes tumor growth by recruitment of cancer-associated fibroblasts. Cancer Res. 69, 369–378 (2009).

  • 17.

    Pietras, K., Pahler, J., Bergers, G. & Hanahan, D. Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacolo
    gical targeting
    . PLoS Med. 5, e19 (2008).

  • 18.

    Li, X. et al. PDGF-C is a new protease-activated ligand for the PDGF α-receptor. Nat. Cell Biol. 2, 302–309 (2000).

  • 19.

    Cao, R. et al. Angiogenesis stimulated by PDGF-CC, a novel member in the PDGF family, involves activation of PDGFR-αα and -αβ receptors. FASEB J. 16, 1575–1583 (2002).

  • 20.

    Theurillat, J.P. et al. NY-ESO-1 protein expression in primary breast carcinoma and metastases: correlation with CD8+ T-cell and CD79a+ plasmacytic/B-cell infiltration. Int. J. Cancer 120, 2411–2417 (2007).

  • 21.

    Falck, A.K. et al. Biomarker expression and St Gallen molecular subtype classification in primary tumours, synchronous lymph node metastases and asynchronous relapses in primary breast cancer patients with 10 years’ follow-up. Breast Cancer Res. Treat. 140, 93–104 (2013).

  • 22.

    Falck, A.K. et al. Analysis of and prognostic information from disseminated tumour cells in bone marrow in primary breast cancer: a prospective observational study. BMC Cancer 12, 403 (2012).

  • 23.

    Guy, C.T., Cardiff, R.D. & Muller, W.J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954–961 (1992).

  • 24.

    Lin, E.Y. et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 163, 2113–2126 (2003).

  • 25.

    Ding, H. et al. A specific requirement for PDGF-C in palate formation and PDGFR-alpha signaling. Nat. Genet. 36, 1111–1116 (2004).

  • 26.

    Cancer Genome Atlas, N.; Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature 490, 61–70 (2012).

  • 27.

    Badve, S. et al. FOXA1 expression in breast cancer—correlation with luminal subtype A and survival. Clin. Cancer Res. 13, 4415–4421 (2007).

  • 28.

    Thorat, M.A. et al. Forkhead box A1 expression in breast cancer is associated with luminal subtype and good prognosis. J. Clin. Pathol. 61, 327–332 (2008).

  • 29.

    Neve, R.M. et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515–527 (2006).

  • 30.

    Kong, S.L., Li, G., Loh, S.L., Sung, W.K. & Liu, E.T. Cellular reprogramming by the conjoint action of ERα, FOXA1, and GATA3 to a ligand-inducible growth state. Mol. Syst. Biol. 7, 526 (2011).

  • 31.

    Kojima, Y. et al. Autocrine TGF-β and stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc. Natl. Acad. Sci. USA 107, 20009–20014 (2010).

  • 32.

    Ray, P.S. et al. FOXC1 is a potential prognostic biomarker with functional significance in basal-like breast cancer. Cancer Res. 70, 3870–3876 (2010).

  • 33.

    Chebil, G., Bendahl, P.O., Idvall, I. & Fernö, M. Comparison of immunohistochemical and biochemical assay of steroid receptors in primary breast cancer—clinical associations and reasons for discrepancies. Acta Oncol. 42, 719–725 (2003).

  • 34.

    Hammond, M.E. et al. American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J. Clin. Oncol. 28, 2784–2795 (2010).

  • 35.

    Polyak, K. Breast cancer: origins and evolution. J. Clin. Invest. 117, 3155–3163 (2007).

  • 36.

    Gupta, P.B. et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146, 633–644 (2011).

  • 37.

    Lim, E. et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat. Med. 15, 907–913 (2009).

  • 38.

    Molyneux, G. & Smalley, M.J. The cell of origin of BRCA1 mutation-associated breast cancer: a cautionary tale of gene expression profiling. J. Mammary Gland Biol. Neoplasia 16, 51–55 (2011).

  • 39.

    Liu, S. et al. BRCA1 regulates human mammary stem/progenitor cell fate. Proc. Natl. Acad. Sci. USA 105, 1680–1685 (2008).

  • 40.

    Molyneux, G. et al. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 7, 403–417 (2010).

  • 41.

    Su, Y. et al. Somatic cell fusions reveal extensive heterogeneity in basal-like breast cancer. Cell Rep. 11, 1549–1563 (2015).

  • 42.

    Yamamoto, S. et al. JARID1B is a luminal lineage-driving oncogene in breast cancer. Cancer Cell 25, 762–777 (2014).

  • 43.

    Bernardo, G.M. et al. FOXA1 represses the molecular phenotype of basal breast cancer cells. Oncogene 32, 554–563 (2013).

  • 44.

    Sflomos, G. et al. A preclinical model for ERα-positive breast cancer points to the epithelial microenvironment as determinant of luminal phenotype and hormone response. Cancer Cell 29, 407–422 (2016).

  • 45.

    Tam, W.L. et al. Protein kinase C α is a central signaling node and therapeutic target for breast cancer stem cells. Cancer Cell 24, 347–364 (2013).

  • 46.

    Meng, F. et al. PDGFRα and β play critical roles in mediating Foxq1-driven breast cancer stemness and chemoresistance. Cancer Res. 75, 584–593 (2015).

  • 47.

    Jansson, S. et al. The three receptor tyrosine kinases c-KIT, VEGFR2 and PDGFRα, closely spaced at 4q12, show increased protein expression in triple-negative breast cancer. PLoS One 9, e102176 (2014).

  • 48.

    Horikawa, S. et al. PDGFRα plays a crucial role in connective tissue remodeling. Sci. Rep. 5, 17948 (2015).

  • 49.

    Kim, Y.J. et al. MET is a potential target for use in combination therapy with EGFR inhibition in triple-negative/basal-like breast cancer. Int. J. Cancer 134, 2424–2436 (2014).

  • 50.

    Ho-Yen, C.M. et al. C-Met in invasive breast cancer: is there a relationship with the basal-like subtype? Cancer 120, 163–171 (2014).

  • 51.

    Ponzo, M.G. et al. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc. Natl. Acad. Sci. USA 106, 12903–12908 (2009).

  • 52.

    Graveel, C.R. et al. Met induces diverse mammary carcinomas in mice and is associated with human basal breast cancer. Proc. Natl. Acad. Sci. USA 106, 12909–12914 (2009).

  • 53.

    Gastaldi, S. et al. Met signaling regulates growth, repopulating potential and basal cell-fate commitment of mammary luminal progenitors: implications for basal-like breast cancer. Oncogene 32, 1428–1440 (2013).

  • 54.

    Marzec, K.A., Baxter, R.C. & Martin, J.L. Targeting insulin-like growth factor binding protein-3 signaling in triple-negative breast cancer. BioMed Res. Int. 2015, 638526 (2015).

  • 55.

    Bissell, M.J. & Hines, W.C. Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat. Med. 17, 320–329 (2011).

  • 56.

    Marsh, T., Pietras, K. & McAllister, S.S. Fibroblasts as architects of cancer pathogenesis. Biochim. Biophys. Acta 1832, 1070–1078 (2013).

  • 57.

    Gascard, P. & Tlsty, T.D. Carcinoma-associated fibroblasts: orchestrating the composition of malignancy. Genes Dev. 30, 1002–1019 (2016).

  • 58.

    Brechbuhl, H.M. et al. Fibroblast subtypes regulate responsiveness of luminal breast cancer to estrogen. Clin. Cancer Res. 23, 1710–1721 (2017).

  • 59.

    Özdemir, B.C. et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 25, 719–734 (2014).

  • 60.

    Rhim, A.D. et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 25, 735–747 (2014).

  • 61.

    Parker, J.S. et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J. Clin. Oncol. 27, 1160–1167 (2009).

  • 62.

    Bray, N.L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).

  • 63.

    Pimentel, H. et al. Differential analysis of RNA-seq incorporating quantification uncertainty. Nat. Methods 14, 687–690 (2017).

  • 64.

    Mei, S. et al. Cistrome Data Browser: a data portal for ChIP–seq and chromatin accessibility data in human and mouse. Nucleic Acids Res. 45 D1, D658–D662 (2017).

  • 65.

    Sikora-Wohlfeld, W., Ackermann, M., Christodoulou, E.G., Singaravelu, K. & Beyer, A. Assessing computational methods for transcription factor target gene identification based on ChIP–seq data. PLOS Comput. Biol. 9, e1003342 (2013).

  • 66.

    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).

  • 67.

    Mootha, V.K. et al. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).

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