Notch ligand Dll1 mediates cross-talk between mammary stem cells and the macrophageal niche

Science

Volumn 360, Issue 6396, 2018, Pages

  Chakrabarti, Rumela ^a,b   Celià Terrassa, Toni ^a,g   Kumar, Sushil ^b   Hang, Xiang ^a   Wei, Yong ^a   Choudhury, Abrar ^a   Hwang, Julie ^a   Peng, Jia ^a   Nixon, Briana ^c   Grady, John J ^a   DeCoste, Christina ^a   Gao, Jie ^d   van Es, Johan H ^e   Li, Ming O ^c   Aifantis, Iannis ^d   Clevers, Hans ^d   Kang, Yibin ^a,f  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^f RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^g HOSPITAL DEL MAR   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

NOTCH LIGAND DLL1; NOTCH RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; UNCLASSIFIED DRUG; WNT PROTEIN; WNT10 PROTEIN; WNT16 PROTEIN; WNT3 PROTEIN; DLK1 PROTEIN, MOUSE; LIGAND; SIGNAL PEPTIDE;

CELL; GENE EXPRESSION; GENETIC ANALYSIS; LIGAND; MORPHOGENESIS; NICHE;

ANIMAL CELL; ARTICLE; BASAL CELL; BREAST CELL; BREAST DEVELOPMENT; BREAST EPITHELIUM CELL; CELL COUNT; CELL FUNCTION; CELL LINEAGE; CELL POPULATION; CELLS BY BODY ANATOMY; COCULTURE; CONTROLLED STUDY; FEMALE; LACTATION; LUMINAL CELL; LUNG ALVEOLUS; MACROPHAGE; MOLECULAR INTERACTION; MORPHOGENESIS; MOUSE; NONHUMAN; NOTCH SIGNALING; PREGNANCY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; STEM CELL; WNT SIGNALING; ANIMAL; CYTOLOGY; GENE KNOCKOUT; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; STEM CELL NICHE; STROMA CELL; UDDER;

ANIMALS; CELL COUNT; FEMALE; GENE KNOCKOUT TECHNIQUES; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MACROPHAGES; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; MORPHOGENESIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELLS; STROMAL CELLS; WNT PROTEINS;

EID: 85047263264     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aan4153     Document Type: Article

References (48)

1. J. E. Visvader, J. Stingl, Mammary stem cells and the differentiation hierarchy: Current status and perspectives. Genes Dev. 28, 1143–1158 (2014). doi: 10.1101/gad.242511.114; pmid: 24888586
2. M. Makarem et al., Stem cells and the developing mammary gland. J. Mammary Gland Biol. Neoplasia 18, 209–219 (2013). doi: 10.1007/s10911-013-9284-6; pmid: 23624881
3. M. Shackleton et al., Generation of a functional mammary gland from a single stem cell. Nature 439, 84–88 (2006). doi: 10.1038/nature04372; pmid: 16397499
4. J. Stingl et al., Purification and unique properties of mammary epithelial stem cells. Nature 439, 993–997 (2006). pmid: 16395311
5. A. C. Rios, N. Y. Fu, G. J. Lindeman, J. E. Visvader, In situ identification of bipotent stem cells in the mammary gland. Nature 506, 322–327 (2014). doi: 10.1038/nature12948; pmid: 24463516
6. A. Van Keymeulen et al., Distinct stem cells contribute to mammary gland development and maintenance. Nature 479, 189–193 (2011). doi: 10.1038/nature10573; pmid: 21983963
7. J. L. Inman, C. Robertson, J. D. Mott, M. J. Bissell, Mammary gland development: Cell fate specification, stem cells and the microenvironment. Development 142, 1028–1042 (2015). doi: 10.1242/dev.087643; pmid: 25758218
8. R. C. Hovey, L. Aimo, Diverse and active roles for adipocytes during mammary gland growth and function. J. Mammary Gland Biol. Neoplasia 15, 279–290 (2010). doi: 10.1007/ s10911-010-9187-8; pmid: 20717712
9. M. F. Gregor et al., The role of adipocyte XBP1 in metabolic regulation during lactation. Cell Rep. 3, 1430–1439 (2013). doi: 10.1016/j.celrep.2013.03.042; pmid: 23623498
10. K. L. Schwertfeger, J. M. Rosen, D. A. Cohen, Mammary gland macrophages: Pleiotropic functions in mammary development. J. Mammary Gland Biol. Neoplasia 11, 229–238 (2006). doi: 10.1007/s10911-006-9028-y; pmid: 17115264
11. J. O’Brien, H. Martinson, C. Durand-Rougely, P. Schedin, Macrophages are crucial for epithelial cell death and adipocyte repopulation during mammary gland involution. Development 139, 269–275 (2012). doi: 10.1242/dev.071696; pmid: 22129827
12. V. Gouon-Evans, M. E. Rothenberg, J. W. Pollard, Postnatal mammary gland development requires macrophages and eosinophils. Development 127, 2269–2282 (2000). pmid: 10804170
13. D. E. Gyorki, M. L. Asselin-Labat, N. van Rooijen, G. J. Lindeman, J. E. Visvader, Resident macrophages influence stem cell activity in the mammary gland. Breast Cancer Res. 11, R62 (2009). doi: 10.1186/bcr2353; pmid: 19706193
14. A. Unsworth, R. Anderson, K. Britt, Stromal fibroblasts and the immune microenvironment: Partners in mammary gland biology and pathology? J. Mammary Gland Biol. Neoplasia 19, 169–182 (2014). doi: 10.1007/s10911-014-9326-8; pmid: 24984900
15. T. Bouras et al., Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 3, 429–441 (2008). doi: 10.1016/j.stem.2008.08.001; pmid: 18940734
16. R. Callahan, S. E. Egan, Notch signaling in mammary development and oncogenesis. J. Mammary Gland Biol. Neoplasia 9, 145–163 (2004). doi: 10.1023/B:JOMG.0000037159.63644.81; pmid: 15300010
17. G. Dontu et al., Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res. 6, R605–R615 (2004). doi: 10.1186/ bcr920; pmid: 15535842
18. Y. A. Zeng, R. Nusse, Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 6, 568–577 (2010). doi: 10.1016/ j.stem.2010.03.020; pmid: 20569694
19. R. van Amerongen, A. N. Bowman, R. Nusse, Developmental stage and time dictate the fate of Wnt/b-catenin-responsive stem cells in the mammary gland. Cell Stem Cell 11, 387–400 (2012). doi: 10.1016/j.stem.2012.05.023; pmid: 22863533
20. V. Plaks et al., Lgr5-expressing cells are sufficient and necessary for postnatal mammary gland organogenesis. Cell Rep. 3, 70–78 (2013). doi: 10.1016/j.celrep.2012.12.017; pmid: 23352663
21. V. Rodilla et al., Luminal progenitors restrict their lineage potential during mammary gland development. PLOS Biol. 13, e1002069 (2015). doi: 10.1371/journal.pbio.1002069; pmid: 25688859
22. S. Šale, D. Lafkas, S. Artavanis-Tsakonas, Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nat. Cell Biol. 15, 451–460 (2013). doi: 10.1038/ncb2725; pmid: 23604318
23. H. Clevers, K. M. Loh, R. Nusse, An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346, 1248012 (2014). doi: 10.1126/science.1248012; pmid: 25278615
24. N. M. Badders et al., The Wnt receptor, Lrp5, is expressed by mouse mammary stem cells and is required to maintain the basal lineage. PLOS ONE 4, e6594 (2009). doi: 10.1371/journal. pone.0006594; pmid: 19672307
25. R. D. Rajaram et al., Progesterone and Wnt4 control mammary stem cells via myoepithelial crosstalk. EMBO J. 34, 641–652 (2015). doi: 10.15252/embj.201490434; pmid: 25603931
26. R. Chakrabarti et al., DNp63 promotes stem cell activity in mammary gland development and basal-like breast cancer by enhancing Fzd7 expression and Wnt signalling. Nat. Cell Biol. 16, 1004–1015 (2014). doi: 10.1038/ncb3040; pmid: 25241036
27. Y. S. Choi, R. Chakrabarti, R. Escamilla-Hernandez, S. Sinha, Elf5 conditional knockout mice reveal its role as a master regulator in mammary alveolar development: Failure of Stat5 activation and functional differentiation in the absence of Elf5. Dev. Biol. 329, 227–241 (2009). doi: 10.1016/ j.ydbio.2009.02.032; pmid: 19269284
28. K. Hozumi et al., Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nat. Immunol. 5, 638–644 (2004). doi: 10.1038/ni1075; pmid: 15146182
29. K. Miyoshi et al., Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J. Cell Biol. 155, 531–542 (2001). doi: 10.1083/jcb.200107065 pmid: 11706048
30. M. L. Asselin-Labat et al., Control of mammary stem cell function by steroid hormone signalling. Nature 465, 798–802 (2010). doi: 10.1038/nature09027; pmid: 20383121
31. J. H. van Es et al., Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14, 1099–1104 (2012). doi: 10.1038/ncb2581; pmid: 23000963
32. N. van Rooijen, E. Hendrikx, Liposomes for specific depletion of macrophages from organs and tissues. Methods Mol. Biol. 605, 189–203 (2010). doi: 10.1007/978-1-60327-360-2_13; pmid: 20072882
33. C. H. Ries et al., Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 25, 846–859 (2014). doi: 10.1016/j. ccr.2014.05.016; pmid: 24898549
34. S. H. Burnett et al., Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J. Leukoc. Biol. 75, 612–623 (2004). doi: 10.1189/jlb.0903442; pmid: 14726498
35. R. A. Franklin et al., The cellular and molecular origin of tumor-associated macrophages. Science 344, 921–925 (2014). doi: 10.1126/science.1252510; pmid: 24812208
36. R. Chakrabarti et al., Elf5 regulates mammary gland stem/ progenitor cell fate by influencing notch signaling. Stem Cells 30, 1496–1508 (2012). doi: 10.1002/stem.1112; pmid: 22523003
37. D. Wang et al., Identification of multipotent mammary stem cells by protein C receptor expression. Nature 517, 81–84 (2015). doi: 10.1038/nature13851; pmid: 25327250
38. I. G. Winkler et al., Bone marrow macrophages maintain hematopoietic stem cell (HSC) niches and their depletion mobilizes HSCs. Blood 116, 4815–4828 (2010). doi: 10.1182/ blood-2009-11-253534; pmid: 20713966
39. T. DeFalco et al., Macrophages Contribute to the Spermatogonial Niche in the Adult Testis. Cell Rep. 12, 1107–1119 (2015). doi: 10.1016/j.celrep.2015.07.015; pmid: 26257171
40. H. Clevers, The intestinal crypt, a prototype stem cell compartment. Cell 154, 274–284 (2013). doi: 10.1016/ j.cell.2013.07.004; pmid: 23870119
41. T. Sato et al., Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415–418 (2011). doi: 10.1038/nature09637; pmid: 21113151
42. J. A. Kim et al., Identification of a stroma-mediated Wnt/ beta-catenin signal promoting self-renewal of hematopoietic stem cells in the stem cell niche. Stem Cells 27, 1318–1329 (2009). doi: 10.1002/stem.52; pmid: 19489023
43. K. B. Deome, L. J. Faulkin Jr., H. A. Bern, P. B. Blair, Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 19, 515–520 (1959). pmid: 13663040
44. R. Chakrabarti, Y. Kang, Transplantable mouse tumor models of breast cancer metastasis. Methods Mol. Biol. 1267, 367–380 (2015). doi: 10.1007/978-1-4939-2297-0_18; pmid: 25636479
45. E. Lim et al., Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat. Med. 15, 907–913 (2009). doi: 10.1038/ nm.2000; pmid: 19648928
46. B. J. Tiede, L. A. Owens, F. Li, C. DeCoste, Y. Kang, A novel mouse model for non-invasive single marker tracking of mammary stem cells in vivo reveals stem cell dynamics throughout pregnancy. PLOS ONE 4, e8035 (2009). doi: 10.1371/journal.pone.0008035; pmid: 19946375
47. V. K. Mootha et al., Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115, 629–640 (2003). doi: 10.1016/S0092-8674(03) 00926-7; pmid: 14651853
48. A. Subramanian et al., Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545–15550 (2005). doi: 10.1073/pnas.0506580102; pmid: 16199517