The Wnt Signaling Landscape of Mammary Stem Cells and Breast Tumors

Saito-Diaz, 2013, The way Wnt works: components and mechanism, Growth Factors, 31, 1, 10.3109/08977194.2012.752737 Alexander, 2012, Wnt signaling in mammary glands: plastic cell fates and combinatorial signaling, Cold Spring Harb Perspect Biol, 4, a008037, 10.1101/cshperspect.a008037 Makarem, 2013, Stem cells and the developing mammary gland, J Mammary Gland Biol Neoplasia, 18, 209, 10.1007/s10911-013-9284-6 Wend, 2010, Wnt signaling in stem and cancer stem cells, Semin Cell Dev Biol, 21, 855, 10.1016/j.semcdb.2010.09.004 van Amerongen, 2009, Towards an integrated view of Wnt signaling in development, Development, 136, 3205, 10.1242/dev.033910 Nusse, 2017, Wnt/beta-catenin signaling, disease, and emerging therapeutic modalities, Cell, 169, 985, 10.1016/j.cell.2017.05.016 Daley, 2015, Stem cells and the evolving notion of cellular identity, Philos Trans R Soc Lond B Biol Sci, 370, 20140376, 10.1098/rstb.2014.0376 Xu, 2017, WNT10A mutation causes ectodermal dysplasia by impairing progenitor cell proliferation and KLF4-mediated differentiation, Nat Commun, 8, 15397, 10.1038/ncomms15397 Visvader, 2016, Tissue-specific designs of stem cell hierarchies, Nat Cell Biol, 18, 349, 10.1038/ncb3332 Bruno, 2017, Mammary extracellular matrix directs differentiation of testicular and embryonic stem cells to form functional mammary glands in vivo, Sci Rep, 7, 40196, 10.1038/srep40196 Van Keymeulen, 2015, Reactivation of multipotency by oncogenic PIK3CA induces breast tumour heterogeneity, Nature, 525, 119, 10.1038/nature14665 Jones, 2007, Sic transit gloria: farewell to the epidermal transit amplifying cell?, Cell Stem Cell, 1, 371, 10.1016/j.stem.2007.09.014 Paguirigan, 2007, Simulating mouse mammary gland development: cell ageing and its relation to stem and progenitor activity, Cell Prolif, 40, 106, 10.1111/j.1365-2184.2007.00416.x Wang, 2015, Self-renewing diploid Axin2(+) cells fuel homeostatic renewal of the liver, Nature, 524, 180, 10.1038/nature14863 Kopp, 2016, Stem cells versus plasticity in liver and pancreas regeneration, Nat Cell Biol, 18, 238, 10.1038/ncb3309 Van Keymeulen, 2011, Distinct stem cells contribute to mammary gland development and maintenance, Nature, 479, 189, 10.1038/nature10573 van Amerongen, 2012, Developmental stage and time dictate the fate of Wnt/beta-catenin-responsive stem cells in the mammary gland, Cell Stem Cell, 11, 387, 10.1016/j.stem.2012.05.023 Eirew, 2010, Quantitation of human mammary epithelial stem cells with in vivo regenerative properties using a subrenal capsule xenotransplantation assay, Nat Protoc, 5, 1945, 10.1038/nprot.2010.148 Visvader, 2014, Mammary stem cells and the differentiation hierarchy: current status and perspectives, Genes Dev, 28, 1143, 10.1101/gad.242511.114 Stingl, 2006, Purification and unique properties of mammary epithelial stem cells, Nature, 439, 993, 10.1038/nature04496 Shackleton, 2006, Generation of a functional mammary gland from a single stem cell, Nature, 439, 84, 10.1038/nature04372 Magee, 2012, Cancer stem cells: impact, heterogeneity, and uncertainty, Cancer Cell, 21, 283, 10.1016/j.ccr.2012.03.003 Wuidart, 2016, Quantitative lineage tracing strategies to resolve multipotency in tissue-specific stem cells, Genes Dev, 30, 1261, 10.1101/gad.280057.116 Choi, 2012, Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation, Cancer Cell, 21, 253, 10.1016/j.ccr.2012.01.005 Wang, 2013, Lineage analysis of basal epithelial cells reveals their unexpected plasticity and supports a cell-of-origin model for prostate cancer heterogeneity, Nat Cell Biol, 15, 274, 10.1038/ncb2697 Moser, 1995, ApcMin: a mouse model for intestinal and mammary tumorigenesis, Eur J Cancer, 31, 1061, 10.1016/0959-8049(95)00181-H Chin, 2015, Lrp5 has a Wnt-independent role in glucose uptake and growth for mammary epithelial cells, Mol Cell Biol, 36, 871, 10.1128/MCB.00800-15 Ball, 1988, Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line, EMBO J, 7, 2089, 10.1002/j.1460-2075.1988.tb03048.x Danielson, 1984, Epithelial mouse mammary cell line exhibiting normal morphogenesis in vivo and functional differentiation in vitro, Proc Natl Acad Sci USA, 81, 3756, 10.1073/pnas.81.12.3756 Campbell, 1988, A clonal derivative of mammary epithelial cell line COMMA-D retains stem cell characteristics of unique morphological and functional heterogeneity, Exp Cell Res, 177, 109, 10.1016/0014-4827(88)90029-8 Merlo, 1995, p53-Dependent and p53-independent activation of apoptosis in mammary epithelial cells reveals a survival function of EGF and insulin, J Cell Biol, 128, 1185, 10.1083/jcb.128.6.1185 Yu, 2014, Updating the Wnt pathways, Biosci Rep, 34, e00142, 10.1042/BSR20140119 Nile, 2017, Unsaturated fatty acyl recognition by Frizzled receptors mediates dimerization upon Wnt ligand binding, Proc Natl Acad Sci USA, 114, 4147, 10.1073/pnas.1618293114 Ahn, 2013, Lrp4 and wise interplay controls the formation and patterning of mammary and other skin appendage placodes by modulating Wnt signaling, Development, 140, 583, 10.1242/dev.085118 Ohazama, 2010, Lrp4: A novel modulator of extracellular signaling in craniofacial organogenesis, Am J Med Genet A, 152A, 2974, 10.1002/ajmg.a.33372 Ahn, 2010, Inhibition of Wnt signaling by Wise (Sostdc1) and negative feedback from Shh controls tooth number and patterning, Development, 137, 3221, 10.1242/dev.054668 Kessenbrock, 2017, Diverse regulation of mammary epithelial growth and branching morphogenesis through noncanonical Wnt signaling, Proc Natl Acad Sci USA, 114, 3121, 10.1073/pnas.1701464114 Roarty, 2015, Ror2 regulates branching, differentiation, and actin-cytoskeletal dynamics within the mammary epithelium, J Cell Biol, 208, 351, 10.1083/jcb.201408058 van Tienen, 2017, Constitutive scaffolding of multiple Wnt enhanceosome components by Legless/BCL9, Elife, 6, e20882, 10.7554/eLife.20882 Langton, 2016, Making, exporting, and modulating Wnts, Trends Cell Biol, 26, 756, 10.1016/j.tcb.2016.05.011 Goel, 2012, Both LRP5 and LRP6 receptors are required to respond to physiological Wnt ligands in mammary epithelial cells and fibroblasts, J Biol Chem, 287, 16454, 10.1074/jbc.M112.362137 Macdonald, 2011, Dissecting molecular differences between Wnt coreceptors LRP5 and LRP6, PLoS One, 6, e23537, 10.1371/journal.pone.0023537 Cruciat, 2013, Secreted and transmembrane wnt inhibitors and activators, Cold Spring Harb Perspect Biol, 5, a015081, 10.1101/cshperspect.a015081 Larraguibel, 2015, Wnt ligand-dependent activation of the negative feedback regulator Nkd1, Mol Biol Cell, 26, 2375, 10.1091/mbc.E14-12-1648 Yan, 2017, Non-equivalence of Wnt and R-spondin ligands during Lgr5+ intestinal stem-cell self-renewal, Nature, 545, 238, 10.1038/nature22313 Kumar, 2014, Structure and function of LGR5: an enigmatic G-protein coupled receptor marking stem cells, Protein Sci, 23, 551, 10.1002/pro.2446 Carmon, 2014, RSPO-LGR4 functions via IQGAP1 to potentiate Wnt signaling, Proc Natl Acad Sci USA, 111, E1221, 10.1073/pnas.1323106111 Cai, 2014, R-spondin1 is a novel hormone mediator for mammary stem cell self-renewal, Genes Dev, 28, 2205, 10.1101/gad.245142.114 Kimura, 2016, CKAP4 is a Dickkopf1 receptor and is involved in tumor progression, J Clin Invest, 126, 2689, 10.1172/JCI84658 Wang, 2015, Identification of multipotent mammary stem cells by protein C receptor expression, Nature, 517, 81, 10.1038/nature13851 Callahan, 2008, Common integration sites for MMTV in viral induced mouse mammary tumors, J Mammary Gland Biol Neoplasia, 13, 309, 10.1007/s10911-008-9092-6 Veltmaat, 2004, Identification of the mammary line in mouse by Wnt10b expression, Dev Dyn, 229, 349, 10.1002/dvdy.10441 Kendrick, 2008, Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate, BMC Genomics, 9, 591, 10.1186/1471-2164-9-591 Ugolini, 2001, WNT pathway and mammary carcinogenesis: loss of expression of candidate tumor suppressor gene SFRP1 in most invasive carcinomas except of the medullary type, Oncogene, 20, 5810, 10.1038/sj.onc.1204706 Howe, 2004, Wnt signaling and breast cancer, Cancer Biol Ther, 3, 36, 10.4161/cbt.3.1.561 Xie, 2013, Interaction with both ZNRF3 and LGR4 is required for the signalling activity of R-spondin, EMBO Rep, 14, 1120, 10.1038/embor.2013.167 Valenta, 2012, The many faces and functions of beta-catenin, EMBO J, 31, 2714, 10.1038/emboj.2012.150 Roarty, 2013, Pygopus 2: tilting the Wnt-Notch balance in mammary epithelial lineage determination, Breast Cancer Res, 15, 322, 10.1186/bcr3592 Zanconato, 2016, YAP/TAZ at the roots of cancer, Cancer Cell, 29, 783, 10.1016/j.ccell.2016.05.005 Dupont, 2011, Role of YAP/TAZ in mechanotransduction, Nature, 474, 179, 10.1038/nature10137 Aragona, 2013, A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors, Cell, 154, 1047, 10.1016/j.cell.2013.07.042 Butler, 2017, Planar cell polarity in development and disease, Nat Rev Mol Cell Biol, 18, 375, 10.1038/nrm.2017.11 Nguyen-Ngoc, 2015, 3D culture assays of murine mammary branching morphogenesis and epithelial invasion, Methods Mol Biol, 1189, 135, 10.1007/978-1-4939-1164-6_10 Jamieson, 2017, Derivation of a robust mouse mammary organoid system for studying tissue dynamics, Development, 144, 1065, 10.1242/dev.145045 Linnemann, 2017, An organotypic 3D assay for primary human mammary epithelial cells that recapitulates branching morphogenesis, Methods Mol Biol, 1612, 125, 10.1007/978-1-4939-7021-6_9 Chu, 2004, Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis, Development, 131, 4819, 10.1242/dev.01347 Badders, 2009, The Wnt receptor, Lrp5, is expressed by mouse mammary stem cells and is required to maintain the basal lineage, PLoS One, 4, e6594, 10.1371/journal.pone.0006594 Brisken, 2010, Hormone action in the mammary gland, Cold Spring Harb Perspect Biol, 2, a003178, 10.1101/cshperspect.a003178 Cai, 2017, A quiescent Bcl11b high stem cell population is required for maintenance of the mammary gland, Cell Stem Cell, 20, 247, 10.1016/j.stem.2016.11.007 Lim, 2009, Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers, Nat Med, 15, 907, 10.1038/nm.2000 Chepko, 1997, Three division-competent, structurally-distinct cell populations contribute to murine mammary epithelial renewal, Tissue Cell, 29, 239, 10.1016/S0040-8166(97)80024-9 Kreuzaler, 2011, Stat3 controls lysosomal-mediated cell death in vivo, Nat Cell Biol, 13, 303, 10.1038/ncb2171 Liu, 2004, The transforming ability of Wnt effectors correlates with their ability to induce the accumulation of mammary progenitor cells, Proc Natl Acad Sci USA, 101, 4158, 10.1073/pnas.0400699101 Li, 2003, Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells, Proc Natl Acad Sci USA, 100, 15853, 10.1073/pnas.2136825100 Teuliere, 2005, Targeted activation of beta-catenin signaling in basal mammary epithelial cells affects mammary development and leads to hyperplasia, Development, 132, 267, 10.1242/dev.01583 Zhang, 2017, Establishing estrogen-responsive mouse mammary organoids from single Lgr5+ cells, Cell Signal, 29, 41, 10.1016/j.cellsig.2016.08.001 Plaks, 2013, Lgr5-expressing cells are sufficient and necessary for postnatal mammary gland organogenesis, Cell Rep, 3, 70, 10.1016/j.celrep.2012.12.017 Wang, 2013, Lgr4 regulates mammary gland development and stem cell activity through the pluripotency transcription factor Sox2, Stem Cells, 31, 1921, 10.1002/stem.1438 Rajaram, 2015, Progesterone and Wnt4 control mammary stem cells via myoepithelial crosstalk, EMBO J, 34, 641, 10.15252/embj.201490434 Joshi, 2010, Progesterone induces adult mammary stem cell expansion, Nature, 465, 803, 10.1038/nature09091 Nusse, 1982, Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome, Cell, 31, 99, 10.1016/0092-8674(82)90409-3 Yu, 2016, Mammary development and breast cancer: a Wnt perspective, Cancers, 8, 65, 10.3390/cancers8070065 MacDonald, 2009, Wnt/beta-catenin signaling: components, mechanisms, and diseases, Dev Cell, 17, 9, 10.1016/j.devcel.2009.06.016 Mahler-Araujo, 2008, Reduction of E-cadherin expression is associated with non-lobular breast carcinomas of basal-like and triple negative phenotype, J Clin Pathol, 61, 615, 10.1136/jcp.2007.053991 Parker, 2001, E-cadherin as a prognostic indicator in primary breast cancer, Br J Cancer, 85, 1958, 10.1054/bjoc.2001.2178 2012, Comprehensive molecular portraits of human breast tumours, Nature, 490, 61, 10.1038/nature11412 Canas-Marques, 2016, E-cadherin immunohistochemistry in breast pathology: uses and pitfalls, Histopathology, 68, 57, 10.1111/his.12869 Rakha, 2010, Clinical and biological significance of E-cadherin protein expression in invasive lobular carcinoma of the breast, Am J Surg Pathol, 34, 1472, 10.1097/PAS.0b013e3181f01916 Gumbiner, 1998, Propagation and localization of Wnt signaling, Curr Op Gen Dev, 8, 430, 10.1016/S0959-437X(98)80114-7 Geyer, 2011, β-Catenin pathway activation in breast cancer is associated with triple-negative phenotype but not with CTNNB1 mutation, Mod Pathol, 24, 209, 10.1038/modpathol.2010.205 van de Wetering, 2001, Mutant E-cadherin breast cancer cells do not display constitutive Wnt signaling, Cancer Res, 61, 278 Incassati, 2010, Key signaling nodes in mammary gland development and cancer: beta-catenin, Breast Cancer Res, 12, 213, 10.1186/bcr2723 Lu, 2016, Wnt drug discovery: weaving through the screens, patents and clinical trials, Cancers, 8, E82, 10.3390/cancers8090082 Anastas, 2013, WNT signalling pathways as therapeutic targets in cancer, Nat Rev Cancer, 13, 11, 10.1038/nrc3419 Coussy, 2017, Clinical value of R-spondins in triple-negative and metaplastic breast cancers, Br J Cancer, 116, 1595, 10.1038/bjc.2017.131 Jamieson, 2014, Targeting the beta-catenin nuclear transport pathway in cancer, Semin Cancer Biol, 27, 20, 10.1016/j.semcancer.2014.04.012 Polakis, 2000, Wnt signaling and cancer, Genes Dev, 14, 1837, 10.1101/gad.14.15.1837 Ayyanan, 2006, Increased Wnt signaling triggers oncogenic conversion of human breast epithelial cells by a Notch-dependent mechanism, Proc Natl Acad Sci USA, 103, 3799, 10.1073/pnas.0600065103 Weigelt, 2014, Metaplastic breast carcinoma: more than a special type, Nat Rev Cancer, 14, 147, 10.1038/nrc3637 Lawrence, 2014, Discovery and saturation analysis of cancer genes across 21 tumour types, Nature, 505, 495, 10.1038/nature12912 Jiang, 2016, Comprehensive comparison of molecular portraits between cell lines and tumors in breast cancer, BMC Genomics, 17, 525, 10.1186/s12864-016-2911-z Mackay, 2009, A high-resolution integrated analysis of genetic and expression profiles of breast cancer cell lines, Breast Cancer Res Treat, 118, 481, 10.1007/s10549-008-0296-7 Hollestelle, 2007, Phosphatidylinositol-3-OH kinase or RAS pathway mutations in human breast cancer cell lines, Mol Cancer Res, 5, 195, 10.1158/1541-7786.MCR-06-0263 Hollestelle, 2010, Distinct gene mutation profiles among luminal-type and basal-type breast cancer cell lines, Breast Cancer Res Treat, 121, 53, 10.1007/s10549-009-0460-8 Riaz, 2009, Low-risk susceptibility alleles in 40 human breast cancer cell lines, BMC Cancer, 9, 236, 10.1186/1471-2407-9-236 Timmerman, 2013, Glutamine sensitivity analysis identifies the xCT antiporter as a common triple-negative breast tumor therapeutic target, Cancer Cell, 24, 450, 10.1016/j.ccr.2013.08.020 Matsuda, 2009, WNT signaling enhances breast cancer cell motility and blockade of the WNT pathway by sFRP1 suppresses MDA-MB-231 xenograft growth, Breast Cancer Res, 11, R32, 10.1186/bcr2317 Liu, 2010, LRP6 overexpression defines a class of breast cancer subtype and is a target for therapy, Proc Natl Acad Sci USA, 107, 5136, 10.1073/pnas.0911220107 Chen, 2014, XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway, Nature, 508, 103, 10.1038/nature13119 Kim, 2012, A phenotypic mouse model of basaloid breast tumors, PLoS One, 7, e30979, 10.1371/journal.pone.0030979 Clevers, 2012, Wnt/beta-catenin signaling and disease, Cell, 149, 1192, 10.1016/j.cell.2012.05.012 Gunther, 2002, A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology, Faseb J, 16, 283, 10.1096/fj.01-0551com Gunther, 2003, Impact of p53 loss on reversal and recurrence of conditional Wnt-induced tumorigenesis, Genes Dev, 17, 488, 10.1101/gad.1051603 Scheel, 2012, Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links, Semin Cancer Biol, 22, 396, 10.1016/j.semcancer.2012.04.001 Kim, 2011, Differentiation generates paracrine cell pairs that maintain basaloid mouse mammary tumors: proof of concept, PLoS One, 6, e19310, 10.1371/journal.pone.0019310 Wang, 2016, PAF-Wnt signaling-induced cell plasticity is required for maintenance of breast cancer cell stemness, Nat Commun, 7, 10633, 10.1038/ncomms10633 Smalley, 2008, BRCA1 and stem cells: tumour typecasting, Nat Cell Biol, 10, 377, 10.1038/ncb0408-377 Agliano, 2017, The challenge of targeting cancer stem cells to halt metastasis, Semin Cancer Biol, 44, 25, 10.1016/j.semcancer.2017.03.003 Tammela, 2017, A Wnt-producing niche drives proliferative potential and progression in lung adenocarcinoma, Nature, 545, 355, 10.1038/nature22334 Lien, 2014, Wnt some lose some: transcriptional governance of stem cells by Wnt/beta-catenin signaling, Genes Dev, 28, 1517, 10.1101/gad.244772.114 Dobrolecki, 2016, Patient-derived xenograft (PDX) models in basic and translational breast cancer research, Cancer Metastasis Rev, 35, 547, 10.1007/s10555-016-9653-x Green, 2013, Paracrine Wnt signaling both promotes and inhibits human breast tumor growth, Proc Natl Acad Sci USA, 110, 6991, 10.1073/pnas.1303671110 Pond, 2010, Fibroblast growth factor receptor signaling dramatically accelerates tumorigenesis and enhances oncoprotein translation in the mouse mammary tumor virus-Wnt-1 mouse model of breast cancer, Cancer Res, 70, 4868, 10.1158/0008-5472.CAN-09-4404 Brady, 2013, The FGF/FGFR axis as a therapeutic target in breast cancer, Expert Rev Endocrinol Metab, 8, 391, 10.1586/17446651.2013.811910 Giannakis, 2014, RNF43 is frequently mutated in colorectal and endometrial cancers, Nat Genet, 46, 1264, 10.1038/ng.3127 Koo, 2012, Tumour suppressor RNF43 is a stem-cell E3 ligase that induces endocytosis of Wnt receptors, Nature, 488, 665, 10.1038/nature11308 Zheng, 2016, Comprehensive pan-genomic characterization of adrenocortical carcinoma, Cancer Cell, 30, 363, 10.1016/j.ccell.2016.07.013 Wu, 2011, Whole-exome sequencing of neoplastic cysts of the pancreas reveals recurrent mutations in components of ubiquitin-dependent pathways, Proc Natl Acad Sci USA, 108, 21188, 10.1073/pnas.1118046108 Jiang, 2013, Inactivating mutations of RNF43 confer Wnt dependency in pancreatic ductal adenocarcinoma, Proc Natl Acad Sci USA, 110, 12649, 10.1073/pnas.1307218110 Steinhart, 2017, Genome-wide CRISPR screens reveal a Wnt-FZD5 signaling circuit as a druggable vulnerability of RNF43-mutant pancreatic tumors, Nat Med, 23, 60, 10.1038/nm.4219