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Intestinal Enteroendocrine Lineage Cells Possess Homeostatic and Injury-Inducible Stem Cell Activity

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Yan, Kelley S., Gevaert, Olivier, Zheng, Grace X.Y., Anchang, Benedict, Probert, Christopher S., Larkin, Kathryn A., Davies, Paige S., Cheng, Zhuan-fen, Kaddis, John S., Han, Arnold, Roelf, Kelly, Calderon, Ruben I., Cynn, Esther, Hu, Xiaoyi, Mandleywala, Komal, Wilhelmy, Julie, Grimes, Sue M., Corney, David C., Boutet, Stéphane C., Terry, Jessica M., Belgrader, Phillip, Ziraldo, Solongo B., Mikkelsen, Tarjei S., Wang, Fengchao, von Furstenberg, Richard J., Smith, Nicholas R., Chandrakesan, Parthasarathy, May, Randal, Chrissy, Mary Ann S., Jain, Rajan, Cartwright, Christine A., Niland, Joyce C., Hong, Young-Kwon, Carrington, Jill, Breault, David T., Epstein, Jonathan, Houchen, Courtney W., Lynch, John P., Martin, Martin G., Plevritis, Sylvia K., Curtis, Christina, Ji, Hanlee P., Li, Linheng, Henning, Susan J., Wong, Melissa H., Kuo, Calvin J.·2017·Cell Stem Cell

DOI 10.1016/j.stem.2017.06.014

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Abstract

SUMMARY Several cell populations have been reported to possess intestinal stem cell (ISC) activity during homeostasis and injury-induced regeneration. Here, we explored inter-relationships between putative mouse ISC populations by comparative RNA-sequencing (RNA-seq). The transcriptomes of multiple cycling ISC populations closely resembled Lgr5+ ISCs, the most well-defined ISC pool, but Bmi1-GFP+ cells were distinct and enriched for enteroendocrine (EE) markers including Prox1. Prox1-GFP+ cells exhibited sustained clonogenic growth in vitro, and lineage-tracing of Prox1+ cells revealed long-lived clones during homeostasis and after radiation-induced injury in vivo. Single-cell mRNA-seq revealed two subsets of Prox1-GFP+ cells, one of which resembled mature EE cells while the other displayed low level EE gene expression but co-expressed tuft cell markers, Lgr5 and Ascl2, reminiscent of label-retaining secretory progenitors. Our data suggest that the EE lineage, including mature EE cells, comprise a reservoir of homeostatic and injury-inducible ISCs, extending our understanding of cellular plasticity and stemness.

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Magness, S. T., Puthoff, B. J., Crissey, M. A. S., Dunn, J., Henning, S., Houchen, C. W., Kaddis, J. S., Kuo, C. J., Li, L., Lynch, J. P., et al. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00481.2012 · Cited by 31
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Nkx2.2 is expressed in a subset of enteroendocrine cells with expanded lineage potential
Groß, S., Balderes, D. A., Liu, J., Asfaha, S., Gu, G., Wang, T. C., & Sussel, L. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00244.2015 · Cited by 23
Side population sorting separates subfractions of cycling and non-cycling intestinal stem cells
von Furstenberg, R. J., Buczacki, S. J. A., Smith, B. J., Seiler, K. M., Winton, D. J., & Henning, S. (2013) · Stem Cell Research · doi:10.1016/j.scr.2013.10.012 · Cited by 20
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The rewards of roughing it
Lu, X. B. (2015) · Science · doi:10.1126/science.350.6258.350 · Cited by 10

A single-cell survey of the small intestinal epithelium
Haber, A. L., Biton, M., Rogel, N., Herbst, R. H., Shekhar, K., Smillie, C., Burgin, G., Delorey, T. M., Howitt, M. R., Katz, Y., et al. (2017) · Nature · doi:10.1038/nature24489 · Cited by 1,750
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Serra, D., Mayr, U., Boni, A., Lukonin, I., Rempfler, M., Challet Meylan, L., Stadler, M. B., Strnad, P., Papasaikas, P., Vischi, D., et al. (2019) · Nature · doi:10.1038/s41586-019-1146-y · Cited by 561
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Moor, A. E., Harnik, Y., Ben-Moshe, S., Massasa, E. E., Rozenberg, M., Eilam, R., Bahar Halpern, K., & Itzkovitz, S. (2018) · Cell · doi:10.1016/j.cell.2018.08.063 · Cited by 480
Identification of Enteroendocrine Regulators by Real-Time Single-Cell Differentiation Mapping
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Differential pre-malignant programs and microenvironment chart distinct paths to malignancy in human colorectal polyps
Chen, B., Scurrah, C. R., McKinley, E. T., Simmons, A. J., Ramirez-Solano, M. A., Zhu, X., Markham, N. O., Heiser, C. N., Vega, P. N., Rolong, A., et al. (2021) · Cell · doi:10.1016/j.cell.2021.11.031 · Cited by 325

See all 361

Authors: Yan, K. S., Gevaert, O., Zheng, G. X. Y., Anchang, B., Probert, C. S., Larkin, K. A., Davies, P. S., Cheng, Z.-F., Kaddis, J. S., Han, A., Roelf, K., Calderon, R. I., Cynn, E., Hu, X., Mandleywala, K., Wilhelmy, J., Grimes, S. M., Corney, D. C., Boutet, S. C., Terry, J. M., Belgrader, P., Ziraldo, S. B., Mikkelsen, T. S., Wang, F., von Furstenberg, R. J., Smith, N. R., Chandrakesan, P., May, R., Chrissy, M. A. S., Jain, R., Cartwright, C. A., Niland, J. C., Hong, Y.-K., Carrington, J., Breault, D. T., Epstein, J., Houchen, C. W., Lynch, J. P., Martin, M. G., Plevritis, S. K., Curtis, C., Ji, H. P., Li, L., Henning, S. J., Wong, M. H., & Kuo, C. J.
Venue: Cell Stem Cell
Publisher: Elsevier BV
Published: 2017-07
Volume: 21
Issue: 1
Pages: 78-90.e6
ISSN: 1875-9777 (ISSN-L)
1934-5909
DOI: 10.1016/j.stem.2017.06.014
OpenAlex: W2729843964
Cited by: 361
References: 78
FWCI: 27.17
Type: journal article
Language: en
Open access: bronze

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Intestinal Enteroendocrine Lineage Cells Possess Homeostatic and Injury-Inducible Stem Cell Activity

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