Enteroendocrine cells are generated from stem cells through a distinct progenitor in the adult drosophila posterior midgut

Development (Cambridge)

Volumn 142, Issue 4, 2015, Pages 644-653

  Zeng, Xiankun ^a   Hou, Steven X ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Drosophila; Intestinal stem cell; Pre enteroendocrine cell; Prospero; Secretory enteroendocrine cell

Indexed keywords

ACHAETE SCUTE COMPLEX; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; DROSOPHILA; ENTEROENDOCRINE CELL; FEMALE; INTESTINAL STEM CELL; INTESTINE CELL; MALE; MIDGUT; NONHUMAN; PRIORITY JOURNAL; STEM CELL; ANIMAL; CYTOLOGY; GASTROINTESTINAL TRACT; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

PROSPERO;

DROSOPHILA PROTEIN;

ANIMALS; CELL DIFFERENTIATION; DROSOPHILA; DROSOPHILA PROTEINS; ENTEROENDOCRINE CELLS; FEMALE; GASTROINTESTINAL TRACT; MALE; RNA INTERFERENCE; STEM CELLS;

EID: 84922553419     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.113357     Document Type: Article

References (47)

1. Bardin, A. J., Perdigoto, C. N., Southall, T. D., Brand, A. H. and Schweisguth, F. (2010). Transcriptional control of stem cell maintenance in the Drosophila intestine. Development 137, 705-714.
2. Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J. et al. (2007). Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007.
3. Beebe, K., Lee, W.-C. and Micchelli, C. A. (2010). JAK/STAT signaling coordinates stem cell proliferation and multilineage differentiation in the Drosophila intestinal stem cell lineage. Dev. Biol. 338, 28-37.
4. Biteau, B. and Jasper, H. (2014). Slit/Robo signaling regulates cell fate decisions in the intestinal stem cell lineage of Drosophila. Cell Rep. 7, 1867-1875.
5. Biteau, B., Hochmuth, C. E. and Jasper, H. (2011). Maintaining tissue homeostasis: dynamic control of somatic stem cell activity. Cell Stem Cell 9, 402-411.
6. Buchon, N., Osman, D., David, F. P. A., Fang, H. Y., Boquete, J.-P., Deplancke, B. and Lemaitre, B. (2013). Morphological and molecular characterization of adult midgut compartmentalization in Drosophila. Cell Rep. 3, 1725-1738.
7. Buczacki, S. J. A., Zecchini, H. I., Nicholson, A. M., Russell, R., Vermeulen, L., Kemp, R. and Winton, D. J. (2013). Intestinal label-retaining cells are secretory precursors expressing Lgr5. Nature 495, 65-69.
8. Chou, T. B. and Perrimon, N. (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
9. Cook, T., Pichaud, F., Sonneville, R., Papatsenko, D. and Desplan, C. (2003). Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev. Cell 4, 853-864.
10. Decotto, E. and Spradling, A. C. (2005). The Drosophila ovarian and testis stem cell niches: similar somatic stem cells and signals. Dev. Cell 9, 501-510.
11. Evans, C. J., Olson, J. M., Ngo, K. T., Kim, E., Lee, N. E., Kuoy, E., Patananan, A. N., Sitz, D., Tran, P., Do, M.-T. et al. (2009). G-TRACE: rapid Gal4-based cell lineage analysis in Drosophila. Nat. Methods 6, 603-605.
12. Golic, K. G. and Lindquist, S. (1989). The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509.
13. Guo, L., Karpac, J., Tran, S. L. and Jasper, H. (2014). PGRP-SC2 promotes gut immune homeostasis to limit commensal dysbiosis and extend lifespan. Cell 156, 109-122.
14. Hakim, R. S., Baldwin, K. and Smagghe, G. (2010). Regulation of midgut growth, development, and metamorphosis. Annu. Rev. Entomol. 55, 593-608.
15. Hampel, S., Chung, P., McKellar, C. E., Hall, D., Looger, L. L. and Simpson, J. H. (2011). Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns. Nat. Methods 8, 253-259.
16. Heidmann, D. and Lehner, C. F. (2001). Reduction of Cre recombinase toxicity in proliferating Drosophila cells by estrogen-dependent activity regulation. Dev. Genes Evol. 211, 458-465.
17. Hur, J. H., Bahadorani, S., Graniel, J., Koehler, C. L., Ulgherait, M., Rera, M., Jones, D. L. and Walker, D. W. (2013). Increased longevity mediated by yeast NDI1 expression in Drosophila intestinal stem and progenitor cells. Aging 5, 662-681.
18. Jiang, H. and Edgar, B. A. (2011). Intestinal stem cells in the adult Drosophila midgut. Exp. Cell Res. 317, 2780-2788.
19. Jiang, H., Patel, P. H., Kohlmaier, A., Grenley, M. O., McEwen, D. G. and Edgar, B. A. (2009). Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355.
20. Kapuria, S., Karpac, J., Biteau, B., Hwangbo, D. and Jasper, H. (2012). Notchmediated suppression of TSC2 expression regulates cell differentiation in the Drosophila intestinal stem cell lineage. PLoS Genet. 8, e1003045.
21. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
22. Mardon, G., Solomon, N. M. and Rubin, G. M. (1994). dachshund encodes a nuclear protein required for normal eye and leg development in Drosophila. Development 120, 3473-3486.
23. Marianes, A. and Spradling, A. C. (2013). Physiological and stem cell compartmentalization within the Drosophila midgut. Elife 2, e00886.
24. Mathur, D., Bost, A., Driver, I. and Ohlstein, B. (2010). A transient niche regulates the specification of Drosophila intestinal stem cells. Science 327, 210-213.
25. McGuire, S. E., Le, P. T., Osborn, A. J., Matsumoto, K. and Davis, R. L. (2003). Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302, 1765-1768.
26. Micchelli, C. A. and Perrimon, N. (2006). Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479.
27. Nicholson, L., Singh, G. K., Osterwalder, T., Roman, G. W., Davis, R. L. and Keshishian, H. (2008). Spatial and temporal control of gene expression in Drosophila using the inducible GeneSwitch GAL4 system. I. Screen for larval nervous system drivers. Genetics 178, 215-234.
28. Ohlstein, B. and Spradling, A. (2006). The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474.
29. Ohlstein, B. and Spradling, A. (2007). Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315, 988-992.
30. O’Brien, L. E., Soliman, S. S., Li, X. and Bilder, D. (2011). Altered modes of stem cell division drive adaptive intestinal growth. Cell 147, 603-614.
31. Perdigoto, C. N., Schweisguth, F. and Bardin, A. J. (2011). Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine. Development 138, 4585-4595.
32. Sato, T., van Es, J. H., Snippert, H. J., Stange, D. E., Vries, R. G., van den Born, M., Barker, N., Shroyer, N. F., van de Wetering, M. and Clevers, H. (2011). Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418.
33. Simons, B. D. and Clevers, H. (2011). Strategies for homeostatic stem cell selfrenewal in adult tissues. Cell 145, 851-862.
34. Singh, S. R., Liu, W. and Hou, S. X. (2007). The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 1, 191-203.
35. Singh, S. R., Zeng, X., Zheng, Z. and Hou, S. X. (2011). The adult Drosophila gastric and stomach organs are maintained by a multipotent stem cell pool at the foregut/midgut junction in the cardia (proventriculus). Cell Cycle 10, 1109-1120.
36. Snippert, H. J., van der Flier, L. G., Sato, T., van Es, J. H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A. M., van Rheenen, J., Simons, B. D. et al. (2010). Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134-144.
37. Strand, M. and Micchelli, C. A. (2011). Quiescent gastric stem cells maintain the adult Drosophila stomach. Proc. Natl. Acad. Sci. USA 108, 17696-17701.
38. Takeda, N., Jain, R., LeBoeuf, M. R., Wang, Q., Lu, M. M. and Epstein, J. A. (2011). Interconversion between intestinal stem cell populations in distinct niches. Science 334, 1420-1424.
39. Tulina, N. and Matunis, E. (2001). Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
40. Wang, P. and Hou, S. X. (2010). Regulation of intestinal stem cells in mammals and Drosophila. J. Cell. Physiol. 222, 33-37.
41. Wang, L., Zeng, X., Ryoo, H. D. and Jasper, H. (2014). Integration of UPRER and oxidative stress signaling in the control of intestinal stem cell proliferation. PLoS Genet. 10, e1004568.
42. Weissman, I. L. (2000). Stem cells: units of development, units of regeneration, and units in evolution. Cell 100, 157-168.
43. Xie, T. and Spradling, A. C. (1998). decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94, 251-260.
44. Xu, T. and Rubin, G.M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
45. Zeng, X., Chauhan, C. and Hou, S. X. (2010). Characterization of midgut stem celland enteroblast-specific Gal4 lines in Drosophila. Genesis 48, 607-611.
46. Zeng, X., Lin, X. and Hou, S. X. (2013). The Osa-containing SWI/SNF chromatinremodeling complex regulates stem cell commitment in the adult Drosophila intestine. Development 140, 3532-3540.
47. Zielke, N., Korzelius, J., van Straaten, M., Bender, K., Schuhknecht, G. F. P., Dutta, D., Xiang, J. and Edgar, B. A. (2014). Fly-FUCCI: a versatile tool for studying cell proliferation in complex tissues. Cell Rep. 7, 588-598.