Notch signaling regulates gastric antral LGR5 stem cell function

EMBO Journal

Volumn 34, Issue 20, 2015, Pages 2522-2536

  Demitrack, Elise S ^a   Gifford, Gail B ^a   Keeley, Theresa M ^a   Carulli, Alexis J ^a   VanDussen, Kelli L ^b   Thomas, Dafydd ^a   Giordano, Thomas J ^a   Liu, Zhenyi ^b   Kopan, Raphael ^c   Samuelson, Linda C ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

gastric cancer; gastric organoids; gastric stem cells; gland fission; mTOR

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; NOTCH RECEPTOR; G PROTEIN COUPLED RECEPTOR; LGR5 PROTEIN, MOUSE; MTOR PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; ENDOCRINE CELL; EPITHELIUM; FEMALE; HOMEOSTASIS; MALE; MOUSE; MUCOUS CELL; NONHUMAN; POLYP; PRIORITY JOURNAL; PYLORUS GLAND; STEM CELL; STOMACH ANTRUM; TISSUE EXPANSION; ANALYSIS OF VARIANCE; ANIMAL; CELL LINEAGE; CONFOCAL MICROSCOPY; CYTOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HISTOLOGY; IN SITU HYBRIDIZATION; METABOLISM; MORPHOMETRY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; BODY WEIGHTS AND MEASURES; CELL DIFFERENTIATION; CELL LINEAGE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HISTOLOGICAL TECHNIQUES; HOMEOSTASIS; IN SITU HYBRIDIZATION; MICE; MICROSCOPY, CONFOCAL; PYLORIC ANTRUM; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; STEM CELLS; TOR SERINE-THREONINE KINASES;

EID: 84944442090     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201490583     Document Type: Article

References (53)

1. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H, (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007
2. Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M, Danenberg E, van den Brink S, Korving J, Abo A, Peters PJ, Wright N, Poulsom R, Clevers H, (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
3. Bell SM, Schreiner CM, Wert SE, Mucenski ML, Scott WJ, Whitsett JA, (2008) R-spondin 2 is required for normal laryngeal-tracheal, lung and limb morphogenesis. Development 135: 1049-1058
4. Bellacosa A, Kumar CC, Di Cristofano A, Testa JR, (2005) Activation of AKT kinases in cancer: implications for therapeutic targeting. Adv Cancer Res 94: 29-86
5. Carulli AJ, Keeley TM, Demitrack ES, Chung J, Maillard I, Samuelson LC, (2015) Notch receptor regulation of intestinal stem cell homeostasis and crypt regeneration. Dev Biol 402: 98-108
6. Chan SM, Weng AP, Tibshirani R, Aster JC, Utz PJ, (2007) Notch signals positively regulate activity of the mTOR pathway in T-cell acute lymphoblastic leukemia. Blood 110: 278-286
7. Dehmer JJ, Garrison AP, Speck KE, Dekaney CM, Van Landeghem L, Sun X, Henning SJ, Helmrath MA, (2011) Expansion of intestinal epithelial stem cells during murine development. PLoS ONE 6: e27070
8. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H, (2005) Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435: 959-963
9. van der Flier LG, van Gijn ME, Hatzis P, Kujala P, Haegebarth A, Stange DE, Begthel H, van den Born M, Guryev V, Oving I, van Es JH, Barker N, Peters PJ, van de Wetering M, Clevers H, (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136: 903-912
10. Fre S, Huyghe M, Mourikis P, Robine S, Louvard D, Artavanis-Tsakonas S, (2005) Notch signals control the fate of immature progenitor cells in the intestine. Nature 435: 964-968
11. Gutierrez-Gonzalez L, Graham TA, Rodriguez-Justo M, Leedham SJ, Novelli MR, Gay LJ, Ventayol-Garcia T, Green A, Mitchell I, Stoker DL, Preston SL, Bamba S, Yamada E, Kishi Y, Harrison R, Jankowski JA, Wright NA, McDonald SA, (2011) The clonal origins of dysplasia from intestinal metaplasia in the human stomach. Gastroenterology 140: 1251-1260 e1251-1256
12. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, Dirisina R, Porter-Westpfahl KS, Hembree M, Johnson T, Wiedermann LM, Barrett TA, Hood L, Wu H, Li L, (2007) PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 39: 189-198
13. Horst D, Gu X, Bhasin M, Yang Q, Verzi M, Lin D, Joseph M, Zhang X, Chen W, Li YP, Shivdasani RA, Libermann TA, (2010) Requirement of the epithelium-specific Ets transcription factor Spdef for mucous gland cell function in the gastric antrum. J Biol Chem 285: 35047-35055
14. Hsu KW, Hsieh RH, Huang KH, Fen-Yau LA, Chi CW, Wang TY, Tseng MJ, Wu KJ, Yeh TS, (2012) Activation of the Notch1/STAT3/Twist signaling axis promotes gastric cancer progression. Carcinogenesis 33: 1459-1467
15. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H, Toftgard R, (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40: 1291-1299
16. Jensen J, Pedersen EE, Galante P, Hald J, Heller RS, Ishibashi M, Kageyama R, Guillemot F, Serup P, Madsen OD, (2000) Control of endodermal endocrine development by Hes-1. Nat Genet 24: 36-44
17. Karam SM, Leblond CP, (1993a) Dynamics of epithelial cells in the corpus of the mouse stomach. II. Outward migration of pit cells. Anat Rec 236: 280-296
18. Karam SM, Leblond CP, (1993b) Dynamics of epithelial cells in the corpus of the mouse stomach. III. Inward migration of neck cells followed by progressive transformation into zymogenic cells. Anat Rec 236: 297-313
19. Keeley TM, Samuelson LC, (2010) Cytodifferentiation of the postnatal mouse stomach in normal and Huntingtin-interacting protein 1-related-deficient mice. Am J Physiol Gastrointest Liver Physiol 299: G1241-G1251
20. Kim TH, Shivdasani RA, (2011) Notch signaling in stomach epithelial stem cell homeostasis. J Exp Med 208: 677-688
21. Kokubu H, Ohtsuka T, Kageyama R, (2008) Mash1 is required for neuroendocrine cell development in the glandular stomach. Genes Cells 13: 41-51
22. Lang SA, Gaumann A, Koehl GE, Seidel U, Bataille F, Klein D, Ellis LM, Bolder U, Hofstaedter F, Schlitt HJ, Geissler EK, Stoeltzing O, (2007) Mammalian target of rapamycin is activated in human gastric cancer and serves as a target for therapy in an experimental model. Int J Cancer 120: 1803-1810
23. Lee CS, Perreault N, Brestelli JE, Kaestner KH, (2002) Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev 16: 1488-1497
24. Leushacke M, Ng A, Galle J, Loeffler M, Barker N, (2013) Lgr5(+) gastric stem cells divide symmetrically to effect epithelial homeostasis in the pylorus. Cell Rep 5: 349-356
25. Loeffler M, Bratke T, Paulus U, Li YQ, Potten CS, (1997) Clonality and life cycles of intestinal crypts explained by a state dependent stochastic model of epithelial stem cell organization. J Theor Biol 186: 41-54
26. Lopez-Diaz L, Hinkle KL, Jain RN, Zavros Y, Brunkan CS, Keeley T, Eaton KA, Merchant JL, Chew CS, Samuelson LC, (2006) Parietal cell hyperstimulation and autoimmune gastritis in cholera toxin transgenic mice. Am J Physiol Gastrointest Liver Physiol 290: G970-G979
27. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H, (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13: 133-140
28. Magness ST, Puthoff BJ, Crissey MA, Dunn J, Henning SJ, Houchen C, Kaddis JS, Kuo CJ, Li L, Lynch J, Martin MG, May R, Niland JC, Olack B, Qian D, Stelzner M, Swain JR, Wang F, Wang J, Wang X, et al, (2013) A multicenter study to standardize reporting and analyses of fluorescence-activated cell-sorted murine intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 305: G542-G551
29. McDonald SA, Greaves LC, Gutierrez-Gonzalez L, Rodriguez-Justo M, Deheragoda M, Leedham SJ, Taylor RW, Lee CY, Preston SL, Lovell M, Hunt T, Elia G, Oukrif D, Harrison R, Novelli MR, Mitchell I, Stoker DL, Turnbull DM, Jankowski JA, Wright NA, (2008) Mechanisms of field cancerization in the human stomach: the expansion and spread of mutated gastric stem cells. Gastroenterology 134: 500-510
30. Miyoshi H, Ajima R, Luo CT, Yamaguchi TP, Stappenbeck TS, (2012) Wnt5a potentiates TGF-beta signaling to promote colonic crypt regeneration after tissue injury. Science 338: 108-113
31. Miyoshi H, Stappenbeck TS, (2013) In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat Protoc 8: 2471-2482
32. Murayama T, Inokuchi M, Takagi Y, Yamada H, Kojima K, Kumagai J, Kawano T, Sugihara K, (2009) Relation between outcomes and localisation of p-mTOR expression in gastric cancer. Br J Cancer 100: 782-788
33. Murtaugh LC, Stanger BZ, Kwan KM, Melton DA, (2003) Notch signaling controls multiple steps of pancreatic differentiation. Proc Natl Acad Sci USA 100: 14920-14925
34. Nomura S, Esumi H, Job C, Tan SS, (1998) Lineage and clonal development of gastric glands. Dev Biol 204: 124-135
35. Palomero T, Sulis ML, Cortina M, Real PJ, Barnes K, Ciofani M, Caparros E, Buteau J, Brown K, Perkins SL, Bhagat G, Agarwal AM, Basso G, Castillo M, Nagase S, Cordon-Cardo C, Parsons R, Zuniga-Pflucker JC, Dominguez M, Ferrando AA, (2007) Mutational loss of PTEN induces resistance to NOTCH1 inhibition in T-cell leukemia. Nat Med 13: 1203-1210
36. Pellegrinet L, Rodilla V, Liu Z, Chen S, Koch U, Espinosa L, Kaestner KH, Kopan R, Lewis J, Radtke F, (2011) Dll1- and dll4-mediated notch signaling are required for homeostasis of intestinal stem cells. Gastroenterology 140: 1230-1240 e1231-1237
37. Qiao XT, Ziel JW, McKimpson W, Madison BB, Todisco A, Merchant JL, Samuelson LC, Gumucio DL, (2007) Prospective identification of a multilineage progenitor in murine stomach epithelium. Gastroenterology 133: 1989-1998
38. Sangiorgi E, Capecchi MR, (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40: 915-920
39. Shroyer NF, Helmrath MA, Wang VY, Antalffy B, Henning SJ, Zoghbi HY, (2007) Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 132: 2478-2488
40. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, Barker N, Klein AM, van Rheenen J, Simons BD, Clevers H, (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143: 134-144
41. Snippert HJ, Schepers AG, van Es JH, Simons BD, Clevers H, (2014) Biased competition between Lgr5 intestinal stem cells driven by oncogenic mutation induces clonal expansion. EMBO Rep 15: 62-69
42. Stanger BZ, Datar R, Murtaugh LC, Melton DA, (2005) Direct regulation of intestinal fate by Notch. Proc Natl Acad Sci USA 102: 12443-12448
43. Sun Y, Gao X, Liu J, Kong QY, Wang XW, Chen XY, Wang Q, Cheng YF, Qu XX, Li H, (2011) Differential Notch1 and Notch2 expression and frequent activation of Notch signaling in gastric cancers. Arch Pathol Lab Med 135: 451-458
44. Tanigaki K, Han H, Yamamoto N, Tashiro K, Ikegawa M, Kuroda K, Suzuki A, Nakano T, Honjo T, (2002) Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat Immunol 3: 443-450
45. Thiem S, Pierce TP, Palmieri M, Putoczki TL, Buchert M, Preaudet A, Farid RO, Love C, Catimel B, Lei Z, Rozen S, Gopalakrishnan V, Schaper F, Hallek M, Boussioutas A, Tan P, Jarnicki A, Ernst M, (2013) mTORC1 inhibition restricts inflammation-associated gastrointestinal tumorigenesis in mice. J Clin Invest 123: 767-781
46. Tian H, Biehs B, Chiu C, Siebel CW, Wu Y, Costa M, de Sauvage FJ, Klein OD, (2015) Opposing activities of Notch and Wnt signaling regulate intestinal stem cells and gut homeostasis. Cell Rep 11: 33-42
47. Totafurno J, Bjerknes M, Cheng H, (1987) The crypt cycle. Crypt and villus production in the adult intestinal epithelium. Biophys J 52: 279-294
48. VanDussen KL, Samuelson LC, (2010) Mouse atonal homolog 1 directs intestinal progenitors to secretory cell rather than absorptive cell fate. Dev Biol 346: 215-223
49. VanDussen KL, Carulli AJ, Keeley TM, Patel SR, Puthoff BJ, Magness ST, Tran IT, Maillard I, Siebel C, Kolterud A, Grosse AS, Gumucio DL, Ernst SA, Tsai YH, Dempsey PJ, Samuelson LC, (2012) Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 139: 488-497
50. Verzi MP, Khan AH, Ito S, Shivdasani RA, (2008) Transcription factor foxq1 controls mucin gene expression and granule content in mouse stomach surface mucous cells. Gastroenterology 135: 591-600
51. Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY, (2001) Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294: 2155-2158
52. Yeh TS, Wu CW, Hsu KW, Liao WJ, Yang MC, Li AF, Wang AM, Kuo ML, Chi CW, (2009) The activated Notch1 signal pathway is associated with gastric cancer progression through cyclooxygenase-2. Cancer Res 69: 5039-5048
53. Yu G, Wang J, Chen Y, Wang X, Pan J, Li G, Jia Z, Li Q, Yao JC, Xie K, (2009) Overexpression of phosphorylated mammalian target of rapamycin predicts lymph node metastasis and prognosis of chinese patients with gastric cancer. Clin Cancer Res 15: 1821-1829