Interleukin 7-expressing fibroblasts promote breast cancer growth through sustenance of tumor cell stemness

References

• Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017;67:7–30. doi:10.3322/caac.21387.
   PubMed Web of Science ®Google Scholar
• Sledge GW, Mamounas EP, Hortobagyi GN, Burstein HJ, Goodwin PJ, Wolff AC. Past, present, and future challenges in breast cancer treatment. J Clin Oncol. 2014;32:1979–1986. doi:10.1200/JCO.2014.55.4139. PMID:24888802.
   PubMed Web of Science ®Google Scholar
• Braun S, Vogl FD, Naume B, Janni W, Osborne MP, Coombes RC, Schlimok G, Diel IJ, Gerber B, Gebauer G, et al. A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med. 2005;353:793–802. doi:10.1056/NEJMoa050434. PMID:16120859.
   PubMed Web of Science ®Google Scholar
• Hosseini H, Obradović MM, Hoffmann M, Harper KL, Sosa MS, Werner-Klein M, Nanduri LK, Werno C, Ehrl C, Maneck M, et al. Early dissemination seeds metastasis in breast cancer. Nature. 2016. doi:10.1038/nature20785.
   Web of Science ®Google Scholar
• Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983–88. doi:10.1073/pnas.0530291100. PMID:12629218.
   PubMed Web of Science ®Google Scholar
• Liu S, Wicha MS. Targeting breast cancer stem cells. J Clin Oncol. 2010;28:4006–12. doi:10.1200/JCO.2009.27.5388. PMID:20498387.
   PubMed Web of Science ®Google Scholar
• Al-Ejeh F, Smart CE, Morrison BJ, Chenevix-Trench G, López JA, Lakhani SR, Brown MP, Khanna KK. Breast cancer stem cells: treatment resistance and therapeutic opportunities. Carcinogenesis. 2011;32:650–8. doi:10.1093/carcin/bgr028. PMID:21310941.
   PubMed Web of Science ®Google Scholar
• Boesch M, Zeimet AG, Rumpold H, Gastl G, Sopper S, Wolf D. Drug Transporter-Mediated Protection of Cancer Stem Cells From Ionophore Antibiotics. Stem Cells Transl Med. 2015;4:1028–32. doi:10.5966/sctm.2015-0054. PMID:26136502.
   PubMed Web of Science ®Google Scholar
• Boesch M, Zeimet AG, Reimer D, Schmidt S, Gastl G, Parson W, Spoeck F, Hatina J, Wolf D, Sopper S. The side population of ovarian cancer cells defines a heterogeneous compartment exhibiting stem cell characteristics. Oncotarget. 2014;5:7027–39. doi:10.18632/oncotarget.2053. PMID:25216521.
   PubMed Web of Science ®Google Scholar
• Boesch M, Sopper S, Zeimet AG, Reimer D, Gastl G, Ludewig B, Wolf D. Heterogeneity of Cancer Stem Cells: Rationale for Targeting the Stem Cell Niche. Biochim Biophys Acta. 2016;1866:276–89. PMID:27751894.
   PubMed Web of Science ®Google Scholar
• Borovski T, De Sousa EMF, Vermeulen L, Medema JP. Cancer stem cell niche: the place to be. Cancer Res. 2011;71:634–9. doi:10.1158/0008-5472.CAN-10-3220. PMID:21266356.
   PubMed Web of Science ®Google Scholar
• Mao Y, Keller ET, Garfield DH, Shen K, Wang J. Stromal cells in tumor microenvironment and breast cancer. Cancer Metastasis Rev. 2013;32:303–15. doi:10.1007/s10555-012-9415-3. PMID:23114846.
   PubMed Web of Science ®Google Scholar
• Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449:557–63. doi:10.1038/nature06188. PMID:17914389.
   PubMed Web of Science ®Google Scholar
• Zhang XH, Jin X, Malladi S, Zou Y, Wen YH, Brogi E, Smid M, Foekens JA, Massagué J. Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma. Cell. 2013;154:1060–73. doi:10.1016/j.cell.2013.07.036. PMID:23993096.
   PubMed Web of Science ®Google Scholar
• Tsuyada A, Chow A, Wu J, Somlo G, Chu P, Loera S, Luu T, Li AX, Wu X, Ye W, et al. CCL2 mediates cross-talk between cancer cells and stromal fibroblasts that regulates breast cancer stem cells. Cancer Res. 2012;72:2768–79. doi:10.1158/0008-5472.CAN-11-3567. PMID:22472119.
   PubMed Web of Science ®Google Scholar
• Malanchi I, Santamaria-Martínez A, Susanto E, Peng H, Lehr HA, Delaloye JF, Huelsken J. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2011;481:85–9. doi:10.1038/nature10694. PMID:22158103.
   PubMed Web of Science ®Google Scholar
• Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva EN, Saunders T, Becerra CP, Tattersall IW, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell. 2014;25:735–47. doi:10.1016/j.ccr.2014.04.021. PMID:24856585.
   PubMed Web of Science ®Google Scholar
• Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy SV, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell. 2014;25:719–34. doi:10.1016/j.ccr.2014.04.005. PMID:24856586.
   PubMed Web of Science ®Google Scholar
• Fletcher AL, Acton SE, Knoblich K. Lymph node fibroblastic reticular cells in health and disease. Nat Rev Immunol. 2015;15:350–61. doi:10.1038/nri3846. PMID:25998961.
   PubMed Web of Science ®Google Scholar
• Turley SJ, Cremasco V, Astarita JL. Immunological hallmarks of stromal cells in the tumour microenvironment. Nat. Rev. Immunol. 2015;15:669–82. doi:10.1038/nri3902. PMID:26471778.
   PubMed Web of Science ®Google Scholar
• Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 2007;8:1255–65. doi:10.1038/ni1513. PMID:17893676.
   PubMed Web of Science ®Google Scholar
• Onder L, Narang P, Scandella E, Chai Q, Iolyeva M, Hoorweg K, Halin C, Richie E, Kaye P, Westermann J, et al. IL-7-producing stromal cells are critical for lymph node remodeling. Blood. 2012;120:4675–83. doi:10.1182/blood-2012-03-416859. PMID:22955921.
   PubMed Web of Science ®Google Scholar
• Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC. Dev. Biol. 2001;1:4. doi:10.1186/1471-213X-1-4. PMID:11299042.
   PubMedGoogle Scholar
• Buch T, Heppner FL, Tertilt C, Heinen TJ, Kremer M, Wunderlich FT, Jung S, Waisman A. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods. 2005;2:419–26. doi:10.1038/nmeth762. PMID:15908920.
   PubMed Web of Science ®Google Scholar
• Vaillant F, Asselin-Labat ML, Shackleton M, Forrest NC, Lindeman GJ, Visvader JE. The mammary progenitor marker CD61/beta3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res. 2008;68:7711–17. doi:10.1158/0008-5472.CAN-08-1949. PMID:18829523.
   PubMed Web of Science ®Google Scholar
• Zhang M, Behbod F, Atkinson RL, Landis MD, Kittrell F, Edwards D, Medina D, Tsimelzon A, Hilsenbeck S, Green JE, et al. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 2008;68:4674–82. doi:10.1158/0008-5472.CAN-07-6353. PMID:18559513.
   PubMed Web of Science ®Google Scholar
• Zhang M, Tsimelzon A, Chang CH, Fan C, Wolff A, Perou CM, Hilsenbeck SG, Rosen JM. Intratumoral heterogeneity in a Trp53-null mouse model of human breast cancer. Cancer Discov. 2015;5:520–33. doi:10.1158/2159-8290.CD-14-1101. PMID:25735774.
   PubMed Web of Science ®Google Scholar
• Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, Kim JK, Patel LR, Ying C, Ziegler AM, et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest. 2011;121:1298–312. doi:10.1172/JCI43414. PMID:21436587.
   PubMed Web of Science ®Google Scholar
• Lu J, Ye X, Fan F, Xia L, Bhattacharya R, Bellister S, Tozzi F, Sceusi E, Zhou Y, Tachibana I, et al. Endothelial cells promote the colorectal cancer stem cell phenotype through a soluble form of Jagged-1. Cancer Cell. 2013;23:171–85. doi:10.1016/j.ccr.2012.12.021. PMID:23375636.
   PubMed Web of Science ®Google Scholar
• Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, Downey RJ, Manova-Todorova K, Brogi E, Massagué J. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17:867–74. doi:10.1038/nm.2379. PMID:21706029.
   PubMed Web of Science ®Google Scholar
• Le Coz V, Zhu C, Devocelle A, Vazquez A, Boucheix C, Azzi S, Gallerne C, Eid P, Lecourt S, Giron-Michel J. IGF-1 contributes to the expansion of melanoma-initiating cells through an epithelial-mesenchymal transition process. Oncotarget. 2016;7:82511–527. PMID:27764776.
   PubMed Web of Science ®Google Scholar
• Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, et al. Involvement of chemokine receptors in breast cancer metastasis. Nature. 2001;410:50–6. doi:10.1038/35065016. PMID:11242036.
   PubMed Web of Science ®Google Scholar
• Yoshihara K, Shahmoradgoli M, Martínez E, Vegesna R, Kim H, Torres-Garcia W, Treviño V, Shen H, Laird PW, Levine DA, et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat Commun. 2013;4:2612. doi:10.1038/ncomms3612. PMID:24113773.
   PubMed Web of Science ®Google Scholar
• Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell. 2007;1:313–23. doi:10.1016/j.stem.2007.06.002. PMID:18371365.
   PubMed Web of Science ®Google Scholar
• Tape CJ, Ling S, Dimitriadi M, McMahon KM, Worboys JD, Leong HS, Norrie IC, Miller CJ, Poulogiannis G, Lauffenburger DA, et al. Oncogenic KRAS Regulates Tumor Cell Signaling via Stromal Reciprocation. Cell. 2016;165:910–20. doi:10.1016/j.cell.2016.03.029. PMID:27087446.
   PubMed Web of Science ®Google Scholar
• Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity. 2006;25:977–88. doi:10.1016/j.immuni.2006.10.016. PMID:17174120.
   PubMed Web of Science ®Google Scholar
• Rhodes LV, Short SP, Neel NF, Salvo VA, Zhu Y, Elliott S, Wei Y, Yu D, Sun M, Muir SE, et al. Cytokine receptor CXCR4 mediates estrogen-independent tumorigenesis, metastasis, and resistance to endocrine therapy in human breast cancer. Cancer Res. 2011;71:603–13. doi:10.1158/0008-5472.CAN-10-3185. PMID:21123450.
   PubMed Web of Science ®Google Scholar
• Sauve K, Lepage J, Sanchez M, Heveker N, Tremblay A. Positive feedback activation of estrogen receptors by the CXCL12-CXCR4 pathway. Cancer Res. 2009;69:5793–800. doi:10.1158/0008-5472.CAN-08-4924. PMID:19584281.
   PubMed Web of Science ®Google Scholar
• Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer. 2008;8:755–68. doi:10.1038/nrc2499. PMID:18784658.
   PubMed Web of Science ®Google Scholar
• Hiratsuka S, Duda DG, Huang Y, Goel S, Sugiyama T, Nagasawa T, Fukumura D, Jain RK. C-X-C receptor type 4 promotes metastasis by activating p38 mitogen-activated protein kinase in myeloid differentiation antigen (Gr-1)-positive cells. Proc Natl Acad Sci U S A. 2011;108:302–7. doi:10.1073/pnas.1016917108. PMID:21173223.
   PubMed Web of Science ®Google Scholar
• Dubrovska A, Hartung A, Bouchez LC, Walker JR, Reddy VA, Cho CY, Schultz PG. CXCR4 activation maintains a stem cell population in tamoxifen-resistant breast cancer cells through AhR signalling. Br J Cancer. 2012;107:43–52. doi:10.1038/bjc.2012.105. PMID:22644306.
   PubMed Web of Science ®Google Scholar
• Cordeiro Gomes A, Hara T, Lim VY, Herndler-Brandstetter D, Nevius E, Sugiyama T, Tani-Ichi S, Schlenner S, Richie E, Rodewald HR, et al. Hematopoietic Stem Cell Niches Produce Lineage-Instructive Signals to Control Multipotent Progenitor Differentiation. Immunity. 2016;45:1219–31. doi:10.1016/j.immuni.2016.11.004. PMID:27913094.
   PubMed Web of Science ®Google Scholar
• Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, Nagasawa T, Link DC. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature. 2013;495:227–30. doi:10.1038/nature11926. PMID:23434756.
   PubMed Web of Science ®Google Scholar
• Asada N, Kunisaki Y, Pierce H, Wang Z, Fernandez NF, Birbrair A, Ma'ayan A, Frenette PS. Differential cytokine contributions of perivascular haematopoietic stem cell niches. Nat Cell Biol. 2017;19:214–23. doi:10.1038/ncb3475. PMID:28218906.
   PubMed Web of Science ®Google Scholar
• Metzger-Filho O, Tutt A, de Azambuja E, Saini KS, Viale G, Loi S, Bradbury I, Bliss JM, Azim HA Jr, Ellis P, et al. Dissecting the heterogeneity of triple-negative breast cancer. J Clin Oncol. 2012;30:1879–87. doi:10.1200/JCO.2011.38.2010. PMID:22454417.
   PubMed Web of Science ®Google Scholar
• Fang M, Li Y, Huang K, Qi S, Zhang J, Zgodzinski W, Majewski M, Wallner G, Gozdz S, Macek P, et al. IL33 Promotes Colon Cancer Cell Stemness via JNK Activation and Macrophage Recruitment. Cancer Res. 2017;77:2735–45. doi:10.1158/0008-5472.CAN-16-1602. PMID:28249897.
   PubMed Web of Science ®Google Scholar
• Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, Sevillano M, Palomo-Ponce S, Tauriello DV, Byrom D, et al. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet. 2015;47:320–9. doi:10.1038/ng.3225. PMID:25706628.
   PubMed Web of Science ®Google Scholar
• Ewens A, Mihich E, Ehrke MJ. Distant metastasis from subcutaneously grown E0771 medullary breast adenocarcinoma. Anticancer Res. 2005;25:3905–15. PMID:16312045.
   PubMed Web of Science ®Google Scholar
• Bove K, Lincoln DW, Tsan MF. Effect of resveratrol on growth of 4T1 breast cancer cells in vitro and in vivo. Biochem Biophys Res Commun. 2002;291:1001–5. doi:10.1006/bbrc.2002.6554. PMID:11866465.
   PubMed Web of Science ®Google Scholar
• Repass JF, Laurent MN, Carter C, Reizis B, Bedford MT, Cardenas K, Narang P, Coles M, Richie ER. IL7-hCD25 and IL7-Cre BAC transgenic mouse lines: new tools for analysis of IL-7 expressing cells. Genesis. 2009;47:281–7. doi:10.1002/dvg.20497. PMID:19263498.
   PubMed Web of Science ®Google Scholar
• Jensen MM, Jorgensen JT, Binderup T, Kjaer A. Tumor volume in subcutaneous mouse xenografts measured by microCT is more accurate and reproducible than determined by 18 F-FDG-microPET or external caliper. BMC Med Imaging. 2008;8:16. doi:10.1186/1471-2342-8-16.
   PubMedGoogle Scholar
• Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80. doi:10.1186/gb-2004-5-10-r80. PMID:15461798.
   PubMed Web of Science ®Google Scholar
• Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249–264. doi:10.1093/biostatistics/4.2.249. PMID:12925520.
   PubMed Web of Science ®Google Scholar
• Carvalho BS, Irizarry RA. A framework for oligonucleotide microarray preprocessing. Bioinformatics. 2010;26:2363–67. doi:10.1093/bioinformatics/btq431. PMID:20688976.
   PubMed Web of Science ®Google Scholar
• Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004;3: 1–25. doi:10.2202/1544-6115.1027. PMID:16646809
   PubMedGoogle Scholar
• Wettenhall JM, Smyth GK. limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics. 2004;20;3705–06. doi:10.1093/bioinformatics/bth449. PMID:15297296.
   PubMed Web of Science ®Google Scholar
• Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102:15545–50. doi:10.1073/pnas.0506580102. PMID:16199517.
   PubMed Web of Science ®Google Scholar