Establishing estrogen-responsive mouse mammary organoids from single Lgr5+ cells

Cellular Signalling

Volumn 29, Issue , 2017, Pages 41-51

  Zhang, Lixing ^a,b,c   Adileh, Mohammad ^b   Martin, Maria Laura ^b   Klingler, Stefan ^b   White, Julie ^b   Ma, Xiaojing ^a,c   Howe, Louise R ^c   Brown, Anthony M C ^c   Kolesnick, Richard ^b  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Lgr5+; Mammary gland; Organoid; Stem cells

Indexed keywords

ALPHA6 INTEGRIN; BETA CATENIN; CD24 ANTIGEN; CYTOKERATIN 14; EPIDERMAL GROWTH FACTOR; ESTRADIOL; LGR5 PROTEIN; PEPTIDES AND PROTEINS; R SPONDIN 1; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WNT3A PROTEIN; ESTROGEN; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, MOUSE;

ADULT; AMINO ACID SEQUENCE; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; BREAST CELL; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; CELL SELF-RENEWAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; EPITHELIUM CELL; FEMALE; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; YOUNG ADULT; ANIMAL; C57BL MOUSE; CFU COUNTING; CYTOLOGY; DRUG EFFECTS; METABOLISM; ORGANOID; UDDER;

ANIMALS; CELL DIFFERENTIATION; COLONY-FORMING UNITS ASSAY; ESTROGENS; FEMALE; MAMMARY GLANDS, ANIMAL; MICE, INBRED C57BL; ORGANOIDS; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84992058698     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2016.08.001     Document Type: Article

References (47)

1. [1] Deome, K.B., Faulkin, L.J. Jr., Bern, H.A., Blair, P.B., Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res. 19 (1959), 515–520.
2. [2] Smith, G.H., Experimental mammary epithelial morphogenesis in an in vivo model: evidence for distinct cellular progenitors of the ductal and lobular phenotype. Breast Cancer Res. Treat. 39 (1996), 21–31.
3. [3] Shackleton, M., Vaillant, F., Simpson, K.J., Stingl, J., Smyth, G.K., Asselin-Labat, M.L., et al. Generation of a functional mammary gland from a single stem cell. Nature 439 (2006), 84–88.
4. [4] Stingl, J., Eirew, P., Ricketson, I., Shackleton, M., Vaillant, F., Choi, D., et al. Purification and unique properties of mammary epithelial stem cells. Nature 439 (2006), 993–997.
5. [5] Barker, N., van Es, J.H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007), 1003–1007.
6. [6] Jaks, V., Barker, N., Kasper, M., van Es, J.H., Snippert, H.J., Clevers, H., et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 40 (2008), 1291–1299.
7. [7] Schuijers, J., Clevers, H., Adult mammalian stem cells: the role of Wnt, Lgr5 and R-spondins. EMBO J. 31 (2012), 2685–2696.
8. [8] de Lau, W., Peng, W.C., Gros, P., Clevers, H., The R-spondin/Lgr5/Rnf43 module: regulator of Wnt signal strength. Genes Dev. 28 (2014), 305–316.
9. [9] de Visser, K.E., Ciampricotti, M., Michalak, E.M., Tan, D.W., Speksnijder, E.N., Hau, C.S., et al. Developmental stage-specific contribution of LGR5(+) cells to basal and luminal epithelial lineages in the postnatal mammary gland. J. Pathol. 228 (2012), 300–309.
10. [10] Rios, A.C., Fu, N.Y., Lindeman, G.J., Visvader, J.E., In situ identification of bipotent stem cells in the mammary gland. Nature 506 (2014), 322–327.
11. [11] Plaks, V., Brenot, A., Lawson, D.A., Linnemann, J.R., Van Kappel, E.C., Wong, K.C., et al. Lgr5-expressing cells are sufficient and necessary for postnatal mammary gland organogenesis. Cell Rep. 3 (2013), 70–78.
12. [12] Wang, D., Cai, C., Dong, X., Yu, Q.C., Zhang, X.O., Yang, L., et al. Identification of multipotent mammary stem cells by protein C receptor expression. Nature 517 (2015), 81–84.
13. [13] Baker, R., Kent, C.V., Silbermann, R.A., Hassell, J.A., Young, L.J., Howe, L.R., Pea3 transcription factors and wnt1-induced mouse mammary neoplasia. PLoS One, 5, 2010, e8854.
14. [14] Van Keymeulen, A., Rocha, A.S., Ousset, M., Beck, B., Bouvencourt, G., Rock, J., et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature 479 (2011), 189–193.
15. [15] Rowland, B., Purkayastha, A., Monserrat, C., Casart, Y., Takiff, H., McDonough, K.A., Fluorescence-based detection of lacZ reporter gene expression in intact and viable bacteria including mycobacterium species. FEMS Microbiol. Lett. 179 (1999), 317–325.
16. [16] Brisken, C., Heineman, A., Chavarria, T., Elenbaas, B., Tan, J., Dey, S.K., et al. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev. 14 (2000), 650–654.
17. [17] Brown, A.M., Wildin, R.S., Prendergast, T.J., Varmus, H.E., A retrovirus vector expressing the putative mammary oncogene int-1 causes partial transformation of a mammary epithelial cell line. Cell 46 (1986), 1001–1009.
18. [18] Santiago, F., Oguma, J., Brown, A.M., Laurence, J., Noncanonical Wnt signaling promotes osteoclast differentiation and is facilitated by the human immunodeficiency virus protease inhibitor ritonavir. Biochem. Biophys. Res. Commun. 417 (2012), 223–230.
19. [19] Ootani, A., Li, X., Sangiorgi, E., Ho, Q.T., Ueno, H., Toda, S., et al. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med. 15 (2009), 701–706.
20. [20] Wang, Y., Dong, J., Li, D., Lai, L., Siwko, S., Li, Y., et al. Lgr4 regulates mammary gland development and stem cell activity through the pluripotency transcription factor Sox2. Stem Cells 31 (2013), 1921–1931.
21. [21] van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111 (2002), 241–250.
22. [22] Barker, N., Clevers, H., Lineage tracing in the intestinal epithelium. Curr. Protoc. Stem Cell Biol., 2010 (Chapter 5:Unit5A 4).
23. [23] Hua, G., Thin, T.H., Feldman, R., Haimovitz-Friedman, A., Clevers, H., Fuks, Z., et al. Crypt base columnar stem cells in small intestines of mice are radioresistant. Gastroenterology 143 (2012), 1266–1276.
24. [24] Sale, S., Lafkas, D., Artavanis-Tsakonas, S., Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nat. Cell Biol. 15 (2013), 451–460.
25. [25] Huch, M., Bonfanti, P., Boj, S.F., Sato, T., Loomans, C.J., van de Wetering, M., et al. Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J. 32 (2013), 2708–2721.
26. [26] Kendrick, H., Regan, J.L., Magnay, F.A., Grigoriadis, A., Mitsopoulos, C., Zvelebil, M., et al. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics, 9, 2008, 591.
27. [27] Asselin-Labat, M.L., Vaillant, F., Sheridan, J.M., Pal, B., Wu, D., Simpson, E.R., et al. Control of mammary stem cell function by steroid hormone signalling. Nature 465 (2010), 798–802.
28. [28] Kleinberg, D.L., Early mammary development: growth hormone and IGF-1. J. Mammary Gland Biol. Neoplasia 2 (1997), 49–57.
29. [29] Soyal, S., Ismail, P.M., Li, J., Mulac-Jericevic, B., Conneely, O.M., Lydon, J.P., Progesterone's role in mammary gland development and tumorigenesis as disclosed by experimental mouse genetics. Breast Cancer Res. 4 (2002), 191–196.
30. [30] Cornog, J.L., Mobini, J., Steiger, E., Enterline, H.T., Squamous carcinoma of the breast. Am. J. Clin. Pathol. 55 (1971), 410–417.
31. [31] Hassan, M.O., Olaizola, M.Y., Ultrastructural observations on gynecomastia. Arch. Pathol. Lab. Med. 103 (1979), 624–630.
32. [32] Salm, R., Massive epidermoid metaplasia with keratin cyst formation in a giant fibro-adenoma of breast. J. Pathol. Bacteriol. 77 (1959), 297–299.
33. [33] Gobbi, H., Simpson, J.F., Jensen, R.A., Olson, S.J., Page, D.L., Metaplastic spindle cell breast tumors arising within papillomas, complex sclerosing lesions, and nipple adenomas. Mod. Pathol. 16 (2003), 893–901.
34. [34] Reddick, R.L., Jennette, J.C., Askin, F.B., Squamous metaplasia of the breast. An ultrastructural and immunologic evaluation. Am. J. Clin. Pathol. 84 (1985), 530–533.
35. [35] Smith, G.H., Medina, D., A morphologically distinct candidate for an epithelial stem cell in mouse mammary gland. J. Cell Sci. 90:Pt 1 (1988), 173–183.
36. [36] Visvader, J.E., Stingl, J., Mammary stem cells and the differentiation hierarchy: current status and perspectives. Genes Dev. 28 (2014), 1143–1158.
37. [37] Williams, J.M., Daniel, C.W., Mammary ductal elongation: differentiation of myoepithelium and basal lamina during branching morphogenesis. Dev. Biol. 97 (1983), 274–290.
38. [38] Fernandez-Gonzalez, R., Illa-Bochaca, I., Welm, B.E., Fleisch, M.C., Werb, Z., Ortiz-de-Solorzano, C., et al. Mapping mammary gland architecture using multi-scale in situ analysis. Integr. Biol. (Camb.) 1 (2009), 80–89.
39. [39] Neville, M.C., McFadden, T.B., Forsyth, I., Hormonal regulation of mammary differentiation and milk secretion. J. Mammary Gland Biol. Neoplasia 7 (2002), 49–66.
40. [40] Meier-Abt, F., Bentires-Alj, M., How pregnancy at early age protects against breast cancer. Trends Mol. Med. 20 (2014), 143–153.
41. [41] Mulac-Jericevic, B., Lydon, J.P., DeMayo, F.J., Conneely, O.M., Defective mammary gland morphogenesis in mice lacking the progesterone receptor B isoform. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 9744–9749.
42. [42] Cai, C., Yu, Q.C., Jiang, W., Liu, W., Song, W., Yu, H., et al. R-spondin1 is a novel hormone mediator for mammary stem cell self-renewal. Genes Dev. 28 (2014), 2205–2218.
43. [43] Miyoshi, K., Rosner, A., Nozawa, M., Byrd, C., Morgan, F., Landesman-Bollag, E., et al. Activation of different Wnt/beta-catenin signaling components in mammary epithelium induces transdifferentiation and the formation of Pilar tumors. Oncogene 21 (2002), 5548–5556.
44. [44] Kuraguchi, M., Ohene-Baah, N.Y., Sonkin, D., Bronson, R.T., Kucherlapati, R., Genetic mechanisms in Apc-mediated mammary tumorigenesis. PLoS Genet., 5, 2009, e1000367.
45. [45] Hennessy, B.T., Krishnamurthy, S., Giordano, S., Buchholz, T.A., Kau, S.W., Duan, Z., et al. Squamous cell carcinoma of the breast. J. Clin. Oncol. 23 (2005), 7827–7835.
46. [46] Mailleux, A.A., Overholtzer, M., Schmelzle, T., Bouillet, P., Strasser, A., Brugge, J.S., BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev. Cell 12 (2007), 221–234.
47. [47] Schaefer, F.V., Custer, R.P., Sorof, S., Squamous metaplasia in human breast culture: induction by cyclic adenine nucleotide and prostaglandins, and influence of menstrual cycle. Cancer Res. 43 (1983), 279–286.