Epithelial-Mesenchymal Micro-niches Govern Stem Cell Lineage Choices

Cell

Volumn 169, Issue 3, 2017, Pages 483-496.e13

  Yang, Hanseul ^a   Adam, Rene C ^a   Ge, Yejing ^a   Hua, Zhong L ^a   Fuchs, Elaine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

epithelial mesenchymal interactions; lineage determination; single cell analyses; stem cells; tissue regeneration

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL COMPARTMENTALIZATION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL INTERACTION; CELL LINEAGE; CELL MATURATION; CELL PLASTICITY; CELL POPULATION; CELL REGENERATION; CELL ULTRASTRUCTURE; CHROMATIN; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM BASAL CELL; G2 PHASE CELL CYCLE CHECKPOINT; GENE TARGETING; HAIR FOLLICLE CELL; HAIR ROOT; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MALE; MITOCHONDRIAL GENOME; MORPHOGENESIS; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; RNA SEQUENCE; SINGLE CELL ANALYSIS; STEM CELL NICHE; STEM CELL SELF-RENEWAL; TISSUE REGENERATION; WNT SIGNALING PATHWAY; ADULT STEM CELL; ANIMAL; C57BL MOUSE; CYTOLOGY; HAIR FOLLICLE; METABOLISM; SEQUENCE ANALYSIS;

BONE MORPHOGENETIC PROTEIN;

ADULT STEM CELLS; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; HAIR FOLLICLE; MICE; MICE, INBRED C57BL; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS; STEM CELL NICHE; WNT SIGNALING PATHWAY;

EID: 85017423588     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.03.038     Document Type: Article

References (51)

1. Adam, R.C., Yang, H., Rockowitz, S., Larsen, S.B., Nikolova, M., Oristian, D.S., Polak, L., Kadaja, M., Asare, A., Zheng, D., Fuchs, E., Pioneer factors govern super-enhancer dynamics in stem cell plasticity and lineage choice. Nature 521 (2015), 366–370.
2. Alonso, L., Okada, H., Pasolli, H.A., Wakeham, A., You-Ten, A.I., Mak, T.W., Fuchs, E., Sgk3 links growth factor signaling to maintenance of progenitor cells in the hair follicle. J. Cell Biol. 170 (2005), 559–570.
3. Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol., 11, 2010, R106.
4. Barker, N., Ridgway, R.A., van Es, J.H., van de Wetering, M., Begthel, H., van den Born, M., Danenberg, E., Clarke, A.R., Sansom, O.J., Clevers, H., Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457 (2009), 608–611.
5. Beronja, S., Livshits, G., Williams, S., Fuchs, E., Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nat. Med. 16 (2010), 821–827.
6. Blanpain, C., Fuchs, E., Stem cell plasticity. Plasticity of epithelial stem cells in tissue regeneration. Science, 344, 2014, 1242281.
7. Brennecke, P., Anders, S., Kim, J.K., Kołodziejczyk, A.A., Zhang, X., Proserpio, V., Baying, B., Benes, V., Teichmann, S.A., Marioni, J.C., Heisler, M.G., Accounting for technical noise in single-cell RNA-seq experiments. Nat. Methods 10 (2013), 1093–1095.
8. Bryder, D., Rossi, D.J., Weissman, I.L., Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am. J. Pathol. 169 (2006), 338–346.
9. Buenrostro, J.D., Giresi, P.G., Zaba, L.C., Chang, H.Y., Greenleaf, W.J., Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10 (2013), 1213–1218.
10. Clayton, E., Doupé, D.P., Klein, A.M., Winton, D.J., Simons, B.D., Jones, P.H., A single type of progenitor cell maintains normal epidermis. Nature 446 (2007), 185–189.
11. Enshell-Seijffers, D., Lindon, C., Kashiwagi, M., Morgan, B.A., β-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Dev. Cell 18 (2010), 633–642.
12. Fraley, C., Raftery, A.E., Model-based clustering, discriminant analysis, and density estimation. J. Am. Stat. Assoc. 97 (2002), 611–631.
13. Genander, M., Cook, P.J., Ramsköld, D., Keyes, B.E., Mertz, A.F., Sandberg, R., Fuchs, E., BMP signaling and its pSMAD1/5 target genes differentially regulate hair follicle stem cell lineages. Cell Stem Cell 15 (2014), 619–633.
14. Greco, V., Chen, T., Rendl, M., Schober, M., Pasolli, H.A., Stokes, N., Dela Cruz-Racelis, J., Fuchs, E., A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4 (2009), 155–169.
15. Hsu, Y.-C., Li, L., Fuchs, E., Transit-amplifying cells orchestrate stem cell activity and tissue regeneration. Cell 157 (2014), 935–949.
16. Hsu, Y.-C., Pasolli, H.A., Fuchs, E., Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144 (2011), 92–105.
17. Huang, W., Sherman, B.T., Lempicki, R.A., Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4 (2009), 44–57.
18. Joost, S., Zeisel, A., Jacob, T., Sun, X., La Manno, G., Lönnerberg, P., Linnarsson, S., Kasper, M., Single-cell transcriptomics reveals that differentiation and spatial signatures shape epidermal and hair follicle heterogeneity. Cell Syst. 3 (2016), 221–237.e9.
19. Kaufman, C.K., Zhou, P., Pasolli, H.A., Rendl, M., Bolotin, D., Lim, K.-C., Dai, X., Alegre, M.-L., Fuchs, E., GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 17 (2003), 2108–2122.
20. Kondo, M., Lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. Immunol. Rev. 238 (2010), 37–46.
21. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
22. Legué, E., Nicolas, J.-F., Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors. Development 132 (2005), 4143–4154.
23. Legué, E., Sequeira, I., Nicolas, J.-F., Hair follicle renewal: authentic morphogenesis that depends on a complex progression of stem cell lineages. Development 137 (2010), 569–577.
24. Li, B., Dewey, C.N., RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 2011, 323.
25. Lien, W.-H., Guo, X., Polak, L., Lawton, L.N., Young, R.A., Zheng, D., Fuchs, E., Genome-wide maps of histone modifications unwind in vivo chromatin states of the hair follicle lineage. Cell Stem Cell 9 (2011), 219–232.
26. Losick, V.P., Morris, L.X., Fox, D.T., Spradling, A., Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev. Cell 21 (2011), 159–171.
27. Maaten, L.V.D., Hinton, G., Visualizing data using t-SNE. J. Mach. Learn. Res. 9 (2008), 2579–2605.
28. McKinney-Freeman, S., Cahan, P., Li, H., Lacadie, S.A., Huang, H.-T., Curran, M., Loewer, S., Naveiras, O., Kathrein, K.L., Konantz, M., et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell 11 (2012), 701–714.
29. Morrison, S.J., Weissman, I.L., The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1 (1994), 661–673.
30. Morrison, S.J., Spradling, A.C., Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132 (2008), 598–611.
31. Orkin, S.H., Zon, L.I., Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132 (2008), 631–644.
32. Oshimori, N., Fuchs, E., Paracrine TGF-β signaling counterbalances BMP-mediated repression in hair follicle stem cell activation. Cell Stem Cell 10 (2012), 63–75.
33. Ouspenskaia, T., Matos, I., Mertz, A.F., Fiore, V.F., Fuchs, E., WNT-SHH antagonism specifies and expands stem cells prior to niche formation. Cell 164 (2016), 156–169.
34. Paul, F., Arkin, Y., Giladi, A., Jaitin, D.A., Kenigsberg, E., Keren-Shaul, H., Winter, D., Lara-Astiaso, D., Gury, M., Weiner, A., et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163 (2015), 1663–1677.
35. Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Prettenhofer, P., Weiss, R., Dubourg, V., et al. Scikit-learn: Machine learning in Python. J. Mach. Learn. Res. 12 (2011), 2825–2830.
36. Perié, L., Duffy, K.R., Kok, L., de Boer, R.J., Schumacher, T.N., The branching point in erythro-myeloid differentiation. Cell 163 (2015), 1655–1662.
37. Picelli, S., Björklund, Å.K., Faridani, O.R., Sagasser, S., Winberg, G., Sandberg, R., Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 10 (2013), 1096–1098.
38. Rendl, M., Polak, L., Fuchs, E., BMP signaling in dermal papilla cells is required for their hair follicle-inductive properties. Genes Dev. 22 (2008), 543–557.
39. Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer. Nat. Biotechnol. 29 (2011), 24–26.
40. Rompolas, P., Mesa, K.R., Greco, V., Spatial organization within a niche as a determinant of stem-cell fate. Nature 502 (2013), 513–518.
41. Scadden, D.T., Nice neighborhood: emerging concepts of the stem cell niche. Cell 157 (2014), 41–50.
42. Schofield, R., The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4 (1978), 7–25.
43. Scialdone, A., Natarajan, K.N., Saraiva, L.R., Proserpio, V., Teichmann, S.A., Stegle, O., Marioni, J.C., Buettner, F., Computational assignment of cell-cycle stage from single-cell transcriptome data. Methods 85 (2015), 54–61.
44. Sequeira, I., Nicolas, J.-F., Redefining the structure of the hair follicle by 3D clonal analysis. Development 139 (2012), 3741–3751.
45. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
46. Tetteh, P.W., Basak, O., Farin, H.F., Wiebrands, K., Kretzschmar, K., Begthel, H., van den Born, M., Korving, J., de Sauvage, F., van Es, J.H., et al. Replacement of lost Lgr5-positive stem cells through plasticity of their enterocyte-lineage daughters. Cell Stem Cell 18 (2016), 203–213.
47. Tian, H., Biehs, B., Warming, S., Leong, K.G., Rangell, L., Klein, O.D., de Sauvage, F.J., A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478 (2011), 255–259.
48. Wilson, N.K., Kent, D.G., Buettner, F., Shehata, M., Macaulay, I.C., Calero-Nieto, F.J., Sánchez Castillo, M., Oedekoven, C.A., Diamanti, E., Schulte, R., et al. Combined single-cell functional and gene expression analysis resolves heterogeneity within stem cell populations. Cell Stem Cell 16 (2015), 712–724.
49. Woo, W.-M., Zhen, H.H., Oro, A.E., Shh maintains dermal papilla identity and hair morphogenesis via a Noggin-Shh regulatory loop. Genes Dev. 26 (2012), 1235–1246.
50. Yu, V.W.C., Yusuf, R.Z., Oki, T., Wu, J., Saez, B., Wang, X., Cook, C., Baryawno, N., Ziller, M.J., Lee, E., et al. Epigenetic memory underlies cell-autonomous heterogeneous behavior of hematopoietic stem cells. Cell 167 (2016), 1310–1322.e17.
51. Zhou, F., Li, X., Wang, W., Zhu, P., Zhou, J., He, W., Ding, M., Xiong, F., Zheng, X., Li, Z., et al. Tracing haematopoietic stem cell formation at single-cell resolution. Nature 533 (2016), 487–492.