Trop2 marks transient gastric fetal epithelium and adult regenerating cells after epithelial damage

Development (Cambridge)

Volumn 143, Issue 9, 2016, Pages 1452-1463

  Fernandez Vallone, Valeria ^a   Leprovots, Morgane ^a   Strollo, Sandra ^a   Vasile, Gabriela ^a   Lefort, Anne ^a   Libert, Frederick ^a   Vassart, Gilbert ^a   Garcia, Marie Isabelle ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Embryonic; Indomethacin; Lgr5; Spheroids; Stomach; Tacstd2

Indexed keywords

CONNEXIN 43; GLYCOPROTEIN; GLYCOPROTEIN TROP2; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CELL ADHESION MOLECULE; INDOMETACIN; TROP2 PROTEIN, MOUSE; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL REGENERATION; CONTROLLED STUDY; CYTOPLASM; FORESTOMACH; GLANDULAR STOMACH; HOMEOSTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH EPITHELIUM; TRANSIENT EXPRESSION; ADULT STEM CELL; ANIMAL; CELL CULTURE; CYTOLOGY; EMBRYO DEVELOPMENT; EMBRYOLOGY; EPITHELIUM; GROWTH, DEVELOPMENT AND AGING; INJURIES; METABOLISM; MULTICELLULAR SPHEROID; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; REGENERATION; STOMACH MUCOSA; TRANSGENIC MOUSE;

ADULT STEM CELLS; ANIMALS; ANTIGENS, NEOPLASM; BIOMARKERS; CELL ADHESION MOLECULES; CELLS, CULTURED; EMBRYONIC DEVELOPMENT; EPITHELIUM; GASTRIC MUCOSA; INDOMETHACIN; MICE; MICE, TRANSGENIC; ORGAN CULTURE TECHNIQUES; REGENERATION; SPHEROIDS, CELLULAR;

EID: 84964856856     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.131490     Document Type: Article

References (33)

1. Anthony, A., Pounder, R. E., Dhillon, A. P. and Wakefield, A. J. (2000). Similarities between ileal Crohn's disease and indomethacin experimental jejunal ulcers in the rat. Aliment. Pharmacol. Ther. 14, 241-245.
2. Arnold, K., Sarkar, A., Yram, M. A., Polo, J. M., Bronson, R., Sengupta, S., Seandel, M., Geijsen, N. and Hochedlinger, K. (2011). Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 9, 317-329.
3. Barbera, M., di Pietro, M., Walker, E., Brierley, C., MacRae, S., Simons, B. D., Jones, P. H., Stingl, J. and Fitzgerald, R. C. (2015). The human squamous oesophagus has widespread capacity for clonal expansion from cells at diverse stages of differentiation. Gut 64, 11-19.
4. 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.
5. Barker, N., Huch, M., Kujala, P., van de Wetering, M., Snippert, H. J., van Es, J. H., Sato, T., Stange, D. E., Begthel, H., van den Born, M. et al. (2010). Lgr5 (+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6, 25-36.
6. Chen, X., Rosenfeld, C. S., Roberts, R. M. and Green, J. A. (2001). An aspartic proteinase expressed in the yolk sac and neonatal stomach of the mouse. Biol. Reprod. 65, 1092-1101.
7. Fordham, R. P., Yui, S., Hannan, N. R. F., Soendergaard, C., Madgwick, A., Schweiger, P. J., Nielsen, O. H., Vallier, L., Pedersen, R. A., Nakamura, T. et al. (2013). Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury. Cell Stem Cell 13, 734-744.
8. Fornaro, M., Dell'Arciprete, R., Stella, M., Bucci, C., Nutini, M., Capri, M. G. and Alberti, S. (1995). Cloning of the gene encoding Trop-2, a cell-surface glycoprotein expressed by human carcinomas. Int. J. Cancer 62, 610-618.
9. Garcia, M. I., Ghiani, M., Lefort, A., Libert, F., Strollo, S. and Vassart, G. (2009). LGR5 deficiency deregulates Wnt signaling and leads to precocious Paneth cell differentiation in the fetal intestine. Dev. Biol. 331, 58-67.
10. Goldstein, A. S., Lawson, D. A., Cheng, D., Sun, W., Garraway, I. P. and Witte, O. N. (2008). Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proc. Natl. Acad. Sci. USA 105, 20882-20887.
11. Hoffmann, W. (2015). Current status on stem cells and cancers of the gastric epithelium. Int. J. Mol. Sci. 16, 19153-19169.
12. Huch, M., Bonfanti, P., Boj, S. F., Sato, T., Loomans, C. J. M., van de Wetering, M., Sojoodi, M., Li, V. S., Schuijers, J., Gracanin, A. et al. (2013a). Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/Rspondin axis. EMBO J. 32, 2708-2721.
13. Huch, M., Dorrell, C., Boj, S. F., van Es, J. H., Li, V. S. M., van de Wetering, M., Sato, T., Hamer, K., Sasaki, N., Finegold, M. J. et al. (2013b). In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature 494, 247-250.
14. Jeong, Y., Rhee, H., Martin, S., Klass, D., Lin, Y., Nguyen, L. X., Feng, W. and Diehn, M. (2015). Identification and genetic manipulation of human and mouse oesophageal stem cells. Gut (in press).
15. Liu, Q., Rehman, H., Krishnasamy, Y., Haque, K., Schnellmann, R. G., Lemasters, J. J. and Zhong, Z. (2012). Amphiregulin stimulates liver regeneration after small-for-size mouse liver transplantation. Am. J. Transplant. 12, 2052-2061.
16. McCracken, K. W., Catá, E. M., Crawford, C. M., Sinagoga, K. L., Schumacher, M., Rockich, B. E., Tsai, Y.-H., Mayhew, C. N., Spence, J. R., Zavros, Y. et al. (2014). Modelling human development and disease in pluripotent stem-cellderived gastric organoids. Nature 516, 400-404.
17. McDougall, A. R. A., Tolcos, M., Hooper, S. B., Cole, T. J. and Wallace, M. J. (2015). Trop2: from development to disease. Dev. Dyn. 244, 99-109.
18. Mustata, R. C., Vasile, G., Fernandez-Vallone, V., Strollo, S., Lefort, A., Libert, F., Monteyne, D., Pérez-Morga, D., Vassart, G. and Garcia, M.-I. (2013). Identification of Lgr5-independent spheroid-generating progenitors of the mouse fetal intestinal epithelium. Cell Rep. 5, 421-432.
19. Nagai, K., Arai, H., Okudera, M., Yamamura, T., Oki, H. and Komiyama, K. (2014). Epiregulin is critical for the acinar cell regeneration of the submandibular gland in a mouse duct ligation model. J. Oral Pathol. Med. 43, 378-387.
20. Nam, K. T., Lee, H.-J., Sousa, J. F., Weis, V. G., O'Neal, R. L., Finke, P. E., Romero-Gallo, J., Shi, G., Mills, J. C., Peek, R. M., Jr et al. (2010). Mature chief cells are cryptic progenitors for metaplasia in the stomach. Gastroenterology 139, 2028-2037. e9.
21. Noguchi, T.-a. K., Ninomiya, N., Sekine, M., Komazaki, S., Wang, P.-C., Asashima, M. and Kurisaki, A. (2015). Generation of stomach tissue from mouse embryonic stem cells. Nat. Cell Biol. 17, 984-993.
22. Okabe, M., Tsukahara, Y., Tanaka, M., Suzuki, K., Saito, S., Kamiya, Y., Tsujimura, T., Nakamura, K. and Miyajima, A. (2009). Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse liver. Development 136, 1951-1960.
23. Qiao, X. T., Ziel, J. W., McKimpson, W., Madison, B. B., Todisco, A., Merchant, J. L., Samuelson, L. C. and Gumucio, D. L. (2007). Prospective identification of a multilineage progenitor in murine stomach epithelium. Gastroenterology 133, 1989-1998. e3.
24. Quante, M., Marrache, F., Goldenring, J. R. andWang, T. C. (2010). TFF2 mRNA transcript expression marks a gland progenitor cell of the gastric oxyntic mucosa. Gastroenterology 139, 2018-2027. e2.
25. Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., van Es, J. H., Abo, A., Kujala, P., Peters, P. J. et al. (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265.
26. Sherwood, R. I., Maehr, R., Mazzoni, E. O. and Melton, D. A. (2011). Wnt signaling specifies and patterns intestinal endoderm. Mech. Dev. 128, 387-400.
27. Shvartsur, A. and Bonavida, B. (2015). Trop2 and its overexpression in cancers: regulation and clinical/therapeutic implications. Genes Cancer 6, 84-105.
28. Singh, B. N., Koyano-Nakagawa, N., Donaldson, A., Weaver, C. V., Garry, M. G. and Garry, D. J. (2015). Hedgehog signaling during appendage development and regeneration. Genes 6, 417-435.
29. Stange, D. E., Koo, B.-K., Huch, M., Sibbel, G., Basak, O., Lyubimova, A., Kujala, P., Bartfeld, S., Koster, J., Geahlen, J. H. et al. (2013). Differentiated Troy+ chief cells act as reserve stem cells to generate all lineages of the stomach epithelium. Cell 155, 357-368.
30. Sun, C., Fukui, H., Hara, K., Kitayama, Y., Eda, H., Yang, M., Yamagishi, H., Tomita, T., Oshima, T., Watari, J. et al. (2015). Expression of Reg family genes in the gastrointestinal tract of mice treated with indomethacin. Am. J. Physiol. Gastrointest. Liver Physiol. 308, G736-G744.
31. Tata, P. R., Mou, H., Pardo-Saganta, A., Zhao, R., Prabhu, M., Law, B. M., Vinarsky, V., Cho, J. L., Breton, S., Sahay, A. et al. (2013). Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503, 218-223.
32. Tian, H., Biehs, B., Warming, S., Leong, K. G., Rangell, L., Klein, O. D. and de Sauvage, F. J. (2011). A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478, 255-259.
33. van Es, J. H., Sato, T., van de Wetering, M., Lyubimova, A., Yee Nee, A. N., Gregorieff, A., Sasaki, N., Zeinstra, L., van den Born, M., Korving, J. et al. (2012). Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14, 1099-1104.