Identification of Stem Cells in the Epithelium of the Stomach Corpus and Antrum of Mice

Gastroenterology

Volumn 152, Issue 1, 2017, Pages 218-231.e14

  Matsuo, Junichi ^a   Kimura, Shunichi ^a,b   Yamamura, Akihiro ^a,b   Koh, Cai Ping ^a   Hossain, Md Zakir ^a   Heng, Dede Liana ^a   Kohu, Kazuyoshi ^a   Voon, Dominic Chih Cheng ^a   Hiai, Hiroshi ^c   Unno, Michiaki ^b   So, Jimmy Bok Yan ^d   Zhu, Feng ^e   Srivastava, Supriya ^a   Teh, Ming ^f   Yeoh, Khay Guan ^e,f   Osato, Motomi ^a,d,g,h   Ito, Yoshiaki ^a,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c Kyoto Prefectural Technology Center   (Japan)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e Dept Medicine Endocrinol Diabet   (Singapore)

^f NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^g INSTITUTE OF BIOENGINEERING AND NANOTECHNOLOGY   (Singapore)

^h KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Cancer Stem Cell; Mouse Model; Oncogene; Stomach Cancer

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; MESSENGER RNA; MUCIN 5AC; MUCIN 6; TAMOXIFEN; TRANSCRIPTION FACTOR CDX2; TRANSCRIPTION FACTOR RUNX1; GREEN FLUORESCENT PROTEIN; KI 67 ANTIGEN; MUC5AC PROTEIN, MOUSE; RUNX1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; ENHANCER REGION; EPITHELIUM CELL; GENE EXPRESSION; GENE MUTATION; HISTOLOGY; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; IN VITRO STUDY; METAPLASIA; MOUSE; MOUSE MODEL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PYLORUS GLAND; STEM CELL; STOMACH; STOMACH ANTRUM; STOMACH ATROPHY; STOMACH EPITHELIUM; ANIMAL; C57BL MOUSE; CELL LINEAGE; GENETICS; HUMAN; METABOLISM; PATHOLOGY; STOMACH MUCOSA; STOMACH TUMOR; TISSUE CULTURE TECHNIQUE; TRANSGENIC MOUSE;

ANIMALS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA 2 SUBUNIT; ENHANCER ELEMENTS, GENETIC; GASTRIC MUCOSA; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; HUMANS; KI-67 ANTIGEN; METAPLASIA; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUCIN 5AC; PYLORIC ANTRUM; RNA, MESSENGER; STEM CELLS; STOMACH NEOPLASMS; TISSUE CULTURE TECHNIQUES;

EID: 85006237792     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2016.09.018     Document Type: Article

References (54)

1. 1 Barker, N., Ridgway, R.A., van Es, J.H., et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457 (2009), 608–611.
2. 2 Friedmann-Morvinski, D., Bushong, E.A., Ke, E., et al. Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338 (2012), 1080–1084.
3. 3 Nam, K.T., Lee, H.J., Sousa, J.F., et al. Mature chief cells are cryptic progenitors for metaplasia in the stomach. Gastroenterology 139 (2010), 2028–2037 e9.
4. 4 Stange, D.E., Koo, B.K., Huch, M., et al. Differentiated Troy+ chief cells act as reserve stem cells to generate all lineages of the stomach epithelium. Cell 155 (2013), 357–368.
5. 5 Asfaha, S., Hayakawa, Y., Muley, A., et al. Krt19(+)/Lgr5(-) cells are radioresistant cancer-initiating stem cells in the colon and intestine. Cell Stem Cell 16 (2015), 627–638.
6. 6 Barker, N., van Es, J.H., Kuipers, J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007), 1003–1007.
7. 7 Sangiorgi, E., Capecchi, M.R., Bmi1 is expressed in vivo in intestinal stem cells. Nature Genet 40 (2008), 915–920.
8. 8 Global Burden of Disease Cancer Collaboration, Fitzmaurice, C., Dicker, D., et al. The Global Burden of Cancer 2013. JAMA Oncol 1 (2015), 505–527.
9. 9 Mills, J.C., Shivdasani, R.A., Gastric epithelial stem cells. Gastroenterology 140 (2011), 412–424.
10. 10 Kim, T.H., Shivdasani, R.A., Notch signaling in stomach epithelial stem cell homeostasis. J Exp Med 208 (2011), 677–688.
11. 11 Karam, S.M., Leblond, C.P., Dynamics of epithelial cells in the corpus of the mouse stomach. Anat Rec 236 (1993), 259–273.
12. 12 Ito, Y., Bae, S.C., Chuang, L.S., The RUNX family: developmental regulators in cancer. Nat Rev Cancer 15 (2015), 81–95.
13. 13 Chen, M.J., Yokomizo, T., Zeigler, B.M., et al. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 457 (2009), 887–891.
14. 14 Jacob, B., Osato, M., Yamashita, N., et al. Stem cell exhaustion due to Runx1 deficiency is prevented by Evi5 activation in leukemogenesis. Blood 115 (2009), 1610–1620.
15. 15 Okuda, T., van Deursen, J., Hiebert, S.W., et al. AML1, the target of multiple choromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84 (1996), 321–330.
16. 16 Papaemmanuil, E., Gerstung, M., Bullinger, L., et al. Genomic classification and prognosis in acute myeloid leukemia. N Engl J Med 374 (2016), 2209–2221.
17. 17 Ng, C.E., Yokomizo, T., Yamashita, N., et al. A Runx1 intronic enhancer marks hemogenic endothelial cells and hematopoietic stem cells. Stem Cells 28 (2010), 1869–1881.
18. 18 Nottingham, W.T., Jarratt, A., Burgess, M., et al. Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer. Blood 110 (2007), 4188–4197.
19. 19 Scheitz, C.J., Lee, T.S., McDermitt, D.J., et al. Defining a tissue stem cell-driven Runx1/Stat3 signalling axis in epithelial cancer. EMBO J 31 (2012), 4124–4139.
20. 20 Banerji, S., Cibulskis, K., Rangel-Escareno, C., et al. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature 486 (2012), 405–409.
21. 21 Ellis, M.J., Ding, L., Shen, D., et al. Whole-genome analysis informs breast cancer response to aromatase inhibition. Nature 486 (2012), 353–360.
22. 22 Giannakis, M., Stappenbeck, T.S., Mills, J.C., et al. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J Biol Chem 281 (2006), 11292–11300.
23. 23 Osorio, K.M., Lilja, K.C., Tumbar, T., Runx1 modulates adult hair follicle stem cell emergence and maintenance from distinct embryonic skin compartments. J Cell Biol 193 (2011), 235–250.
24. 24 Quante, M., Marrache, F., Goldenring, J.R., et al. TFF2 mRNA transcript expression marks a gland progenitor cell of the gastric oxyntic mucosa. Gastroenterology 139 (2010), 2018–2027 e2.
25. 25 Huh, W.J., Khurana, S.S., Geahlen, J.H., et al. Tamoxifen induces rapid, reversible atrophy, and metaplasia in mouse stomach. Gastroenterology 142 (2012), 21–24 e7.
26. 26 Barker, N., Huch, M., Kujala, P., et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6 (2010), 25–36.
27. 27 Sato, T., Vries, R.G., Snippert, H.J., et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459 (2009), 262–265.
28. 28 Hayakawa, Y., Ariyama, H., Stancikova, J., et al. Mist1 expressing gastric stem cells maintain the normal and neoplastic gastric epithelium and are supported by a perivascular stem cell niche. Cancer Cell 28 (2015), 800–814.
29. 29 Okumura, T., Ericksen, R.E., Takaishi, S., et al. K-ras mutation targeted to gastric tissue progenitor cells results in chronic inflammation, an altered microenvironment, and progression to intraepithelial neoplasia. Cancer Res 70 (2010), 8435–8445.
30. 30 Ray, K.C., Bell, K.M., Yan, J., et al. Epithelial tissues have varying degrees of susceptibility to KrasG12D-initiated tumorigenesis in a mouse model. PLoS One, 6, 2011, e16786.
31. 31 Lee, E.R., Leblond, C.P., Dynamic histology of the antral epithelium in the mouse stomach: II. ultrastructure and renewal of isthmal cells. Am J Anat 172 (1985), 205–224.
32. 32 Watson, S.A., Grabowska, A.M., El-Zaatari, M., et al. Gastrin—active participant or bystander in gastric carcinogenesis?. Nat Rev Cancer 6 (2006), 936–946.
33. 33 Goldenring, J.R., Nam, K.T., Wang, T.C., et al. Spasmolytic polypeptide-expressing metaplasia and intestinal metaplasia: time for reevaluation of metaplasias and the origins of gastric cancer. Gastroenterology 138 (2010), 2207–2210.
34. 34 Nomura, S., Baxter, T., Yamaguchi, H., et al. Spasmolytic polypeptide expressing metaplasia to preneoplasia in H. felis-infected mice. Gastroenterology 127 (2004), 582–594.
35. 35 Hatakeyama, M., SagA of CagA in Helicobacter pylori pathogenesis. Curr Opin Microbiol 11 (2008), 30–37.
36. 36 Yang, H., Rivera, Z., Jube, S., et al. Programmed necrosis induced by asbestos in human mesothelial cells causes high-mobility group box 1 protein release and resultant inflammation. Proc Natl Acad Sci U S A 107 (2010), 12611–12616.
37. 37 Eskelinen, E.L., Doctor Jekyll and Mister Hyde: autophagy can promote both cell survival and cell death. Cell Death Differ 12:Suppl 2 (2005), 1468–1472.
38. 38 Hwang, J.J., Kim, H.N., Kim, J., et al. Zinc(II) ion mediates tamoxifen-induced autophagy and cell death in MCF-7 breast cancer cell line. Biometals 23 (2010), 997–1013.
39. 39 Yamauchi, H., Matsumaru, T., Morita, T., et al. The cell competition-based high-throughput screening identifies small compounds that promote the elimination of RasV12-transformed cells from epithelia. Sci Rep, 5, 2015, 15336.
40. 40 Ramsey, V.G., Doherty, J.M., Chen, C.C., et al. The maturation of mucus-secreting gastric epithelial progenitors into digestive-enzyme secreting zymogenic cells requires Mist1. Development 134 (2007), 211–222.
41. 41 Choi, E., Hendley, A.M., Bailey, J.M., et al. Expression of activated Ras in gastric chief cells of mice leads to the full spectrum of metaplastic lineage transitions. Gastroenterology 150 (2016), 918–930 e13.
42. 42 Hayakawa, Y., Jin, G., Wang, H., et al. CCK2R identifies and regulates gastric antral stem cell states and carcinogenesis. Gut 64 (2015), 544–553.
43. 43 Arnold, K., Sarkar, A., Yram, M.A., et al. Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 9 (2011), 317–329.
44. 44 Khurana, S.S., Riehl, T.E., Moore, B.D., et al. The hyaluronic acid receptor CD44 coordinates normal and metaplastic gastric epithelial progenitor cell proliferation. J Biol Chem 288 (2013), 16085–16097.
45. 45 Bertaux-Skeirik, N., Feng, R., Schumacher, M.A., et al. CD44 plays a functional role in Helicobacter pylori-induced epithelial cell proliferation. PLoS Pathog, 11, 2015, e1004663.
46. 46 Matkar, S.S., Durham, A., Brice, A., et al. Systemic activation of K-ras rapidly induces gastric hyperplasia and metaplasia in mice. Am J Cancer Res 1 (2011), 432–445.
47. 47 Coffey, R.J., Washington, M.K., Corless, C.L., et al. Menetrier disease and gastrointestinal stromal tumors: hyperproliferative disorders of the stomach. J Clin Invest 117 (2007), 70–80.
48. 48 Nomura, S., Settle, S.H., Leys, C.M., et al. Evidence for repatterning of the gastric fundic epithelium associated with Ménétrier's eisease and TGFα overexpression. Gastroenterology 128 (2005), 1292–1305.
49. 1 Barker, N., van Es, J.H., Kuipers, J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007), 1003–1007.
50. 2 Huh, W.J., Khurana, S.S., Geahlen, J.H., et al. Tamoxifen induces rapid, reversible atrophy, and metaplasia in mouse stomach. Gastroenterology 142 (2012), 21–24 e27.
51. 3 Srivastava, S., Liew, M.S., McKeon, F., et al. Immunohistochemical analysis of metaplastic non-goblet columnar lined oesophagus shows phenotypic similarities to Barrett's oesophagus: a study in an Asian population. Dig Liver Dis 46 (2014), 170–175.
52. 4 Wakamatsu, Y., Watanabe, Y., Shimono, A., et al. Transition of localization of the N-Myc protein from nucleus to cytoplasm in differentiating neurons. Neuron 10 (1993), 1–9.
53. 5 Mahe, M.M., Aihara, E., Schumacher, M.A., et al. Establishment of gastrointestinal epithelial organoids. Curr Protoc Mouse Biol 3 (2013), 217–240.
54. 6 Pinto, M.P., Jacobsen, B.M., Horwitz, K.B., An immunohistochemical method to study breast cancer cell subpopulations and their growth regulation by hormones in three-dimensional cultures. Front Endocrinol, 2, 2011, 15.