Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium

Journal of Cell Biology

Volumn 192, Issue 5, 2011, Pages 767-780

  Gerbe, François ^a,b   Van Es, Johan H ^c   Makrini, Leila ^a,b   Brulin, Bénédicte ^a,b   Mellitzer, Georg ^d   Robine, Sylvie ^e   Romagnolo, Béatrice ^f   Shroyer, Noah F ^g   Bourgaux, Jean François ^h   Pignodel, Christine ^h   Clevers, Hans ^c   Jay, Philippe ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e INSTITUT CURIE   (France)

^f INSTITUT COCHIN   (France)

^g CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^h NÎMES UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROGENIN 3; PROSTAGLANDIN SYNTHASE; TRANSCRIPTION FACTOR SOX9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; ENTEROENDOCRINE CELL; GOBLET CELL; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; INTESTINE TUMOR; MOUSE; NONHUMAN; PANETH CELL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY CELL;

ADENOCARCINOMA; ADENOMA; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; HUMANS; INTESTINAL MUCOSA; INTESTINAL NEOPLASMS; INTESTINE, LARGE; INTESTINE, SMALL; ISOMERASES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; SOX9 TRANSCRIPTION FACTOR;

EID: 79952418471     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201010127     Document Type: Article

References (62)

1. Barker, N., and H. Clevers. 2010. Leucine-rich repeat-containing G-protein-coupled receptors as markers of adult stem cells. Gastroenterology. 138:1681-1696. doi:10.1053/j.gastro.2010.03.002
2. Barker, N., J.H. van Es, J. Kuipers, P. Kujala, M. van den Born, M. Cozijnsen, A. Haegebarth, J. Korving, H. Begthel, P.J. Peters, and H. Clevers. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 449:1003-1007. doi:10.1038/nature06196 (Pubitemid 350014593)
3. Bastide, P., C. Darido, J. Pannequin, R. Kist, S. Robine, C. Marty-Double, F. Bibeau, G. Scherer, D. Joubert, F. Hollande, et al. 2007. Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J. Cell Biol. 178:635-648. doi:10.1083/jcb.200704152 (Pubitemid 47267275)
4. Bezençon, C., J. le Coutre, and S. Damak. 2007. Taste-signaling proteins are co-expressed in solitary intestinal epithelial cells. Chem. Senses. 32:41-49. doi:10.1093/chemse/bjl034 (Pubitemid 46017873)
5. Bezençon, C., A. Fürholz, F. Raymond, R. Mansourian, S. Métairon, J. Le Coutre, and S. Damak. 2008. Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J. Comp. Neurol. 509:514-525. doi:10.1002/cne.21768
6. Bjerknes, M., and H. Cheng. 1999. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology. 116:7-14. doi:10.1016/S0016-5085(99) 70222-2 (Pubitemid 29013487)
7. Bjerknes, M., and H. Cheng. 2006. Neurogenin 3 and the enteroendocrine cell lineage in the adult mouse small intestinal epithelium. Dev. Biol. 300:722-735. doi:10.1016/j.ydbio.2006.07.040 (Pubitemid 44914135)
8. Bjerknes, M., and H. Cheng. 2010. Cell Lineage metastability in Gfi1-deficient mouse intestinal epithelium. Dev. Biol. 345:49-63. doi:10.1016/j.ydbio.2010.06.021
9. Blache, P., M. van de Wetering, I. Duluc, C. Domon, P. Berta, J.N. Freund, H. Clevers, and P. Jay. 2004. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J. Cell Biol. 166:37-47. doi:10.1083/jcb.200311021 (Pubitemid 38931915)
10. Colnot, S., M. Niwa-Kawakita, G. Hamard, C. Godard, S. Le Plenier, C. Houbron, B. Romagnolo, D. Berrebi, M. Giovannini, and C. Perret. 2004. Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab. Invest. 84:1619-1630. doi:10.1038/labinvest.3700180 (Pubitemid 39600569)
11. Dekaney, C.M., A.S. Gulati, A.P. Garrison, M.A. Helmrath, and S.J. Henning. 2009. Regeneration of intestinal stem/progenitor cells following doxorubicin treatment of mice. Am. J. Physiol. Gastrointest. Liver Physiol. 297:G461-G470. doi:10.1152/ajpgi.90446.2008
12. el Marjou, F., K.P. Janssen, B.H. Chang, M. Li, V. Hindie, L. Chan, D. Louvard, P. Chambon, D. Metzger, and S. Robine. 2004. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis. 39:186-193. doi:10.1002/gene.20042
13. Formeister, E.J., A.L. Sionas, D.K. Lorance, C.L. Barkley, G.H. Lee, and S.T. Magness. 2009. Distinct SOX9 levels differentially mark stem/progenitor populations and enteroendocrine cells of the small intestine epithelium. Am. J. Physiol. Gastrointest. Liver Physiol. 296:G1108-G1118. doi:10.1152/ajpgi.00004. 2009
14. Fre, S., M. Huyghe, P. Mourikis, S. Robine, D. Louvard, and S. Artavanis-Tsakonas. 2005. Notch signals control the fate of immature progenitor cells in the intestine. Nature. 435:964-968. doi:10.1038/nature03589 (Pubitemid 40896323)
15. Gebert, A., K. al-Samir, K. Werner, S. Fassbender, and A. Gebhard. 2000. The apical membrane of intestinal brush cells possesses a specialised, but species-specific, composition of glycoconjugates - on-section and in vivo lectin labelling in rats, guinea-pigs and mice. Histochem. Cell Biol. 113:389-399. doi:10.1007/s004180000148
16. Gebhard, A., and A. Gebert. 1999. Brush cells of the mouse intestine possess a specialized glycocalyx as revealed by quantitative lectin histochemistry. Further evidence for a sensory function. J. Histochem. Cytochem. 47:799-808. doi:10.1177/002215549904700609 (Pubitemid 29244518)
17. Gerbe, F., B. Brulin, L. Makrini, C. Legraverend, and P. Jay. 2009. DCAMKL-1 expression identifies Tuft cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology. 137:2179-2180, author reply :2180-2181. doi:10.1053/j.gastro.2009.06.072
18. Giannakis, M., T.S. Stappenbeck, J.C. Mills, D.G. Leip, M. Lovett, S.W. Clifton, J.E. Ippolito, J.I. Glasscock, M. Arumugam, M.R. Brent, and J.I. Gordon. 2006. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J. Biol. Chem. 281:11292-11300. doi:10.1074/jbc.M512118200 (Pubitemid 43855554)
19. Gregorieff, A., D.E. Stange, P. Kujala, H. Begthel, M. van den Born, J. Korving, P.J. Peters, and H. Clevers. 2009. The ets-domain transcription factor Spdef promotes maturation of goblet and paneth cells in the intestinal epithelium. Gastroenterology. 137:1333-1345: e1-e3. doi:10.1053/j.gastro.2009. 06.044
20. Höfer, D., and D. Drenckhahn. 1992. Identification of brush cells in the alimentary and respiratory system by antibodies to villin and fimbrin. Histochemistry. 98:237-242. doi:10.1007/BF00271037
21. Höfer, D., and D. Drenckhahn. 1996. Cytoskeletal markers allowing discrimination between brush cells and other epithelial cells of the gut including enteroendocrine cells. Histochem. Cell Biol. 105:405-412. doi:10.1007/BF01463662 (Pubitemid 26174083)
22. Höfer, D., and D. Drenckhahn. 1998. Identification of the taste cell G-protein, alpha-gustducin, in brush cells of the rat pancreatic duct system. Histochem. Cell Biol. 110:303-309. doi:10.1007/s004180050292 (Pubitemid 28401738)
23. Höfer, D., B. Püschel, and D. Drenckhahn. 1996. Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc. Natl. Acad. Sci. USA. 93:6631-6634. doi:10.1073/pnas.93.13.6631
24. Holzer, P. 2009. Opioid receptors in the gastrointestinal tract. Regul. Pept. 155:11-17. doi:10.1016/j.regpep.2009.03.012
25. Iseki, S., T. Kanda, M. Hitomi, and T. Ono. 1991. Ontogenic appearance of three fatty acid binding proteins in the rat stomach. Anat. Rec. 229:51-60. doi:10.1002/ar.1092290107
26. Jang, H.J., Z. Kokrashvili, M.J. Theodorakis, O.D. Carlson, B.J. Kim, J. Zhou, H.H. Kim, X. Xu, S.L. Chan, M. Juhaszova, et al. 2007. Gut-expressed gustducin and taste receptors regulate secretion of glucagon-like peptide-1. Proc. Natl. Acad. Sci. USA. 104:15069-15074. doi:10.1073/pnas.0706890104 (Pubitemid 47619594)
27. Janssen, K.P., F. el-Marjou, D. Pinto, X. Sastre, D. Rouillard, C. Fouquet, T. Soussi, D. Louvard, and S. Robine. 2002. Targeted expression of oncogenic K-ras in intestinal epithelium causes spontaneous tumorigenesis in mice. Gastroenterology. 123:492-504. doi:10.1053/gast.2002.34786
28. Jarvi, O., and O. Keyrilainen. 1956. On the cellular structures of the epithelial invasions in the glandular stomach of mice caused by intramural application of 20-methylcholantren. Acta Pathol Microbiol Scand Suppl. 39(Suppl 111):72-73.
29. Jenny, M., C. Uhl, C. Roche, I. Duluc, V. Guillermin, F. Guillemot, J. Jensen, M. Kedinger, and G. Gradwohl. 2002. Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J. 21:6338-6347. doi:10.1093/emboj/cdf649 (Pubitemid 35448412)
30. Jensen, J., E.E. Pedersen, P. Galante, J. Hald, R.S. Heller, M. Ishibashi, R. Kageyama, F. Guillemot, P. Serup, and O.D. Madsen. 2000. Control of endodermal endocrine development by Hes-1. Nat. Genet. 24:36-44. doi:10.1038/71657 (Pubitemid 30041417)
31. Jin, G., V. Ramanathan, M. Quante, G.H. Baik, X. Yang, S.S. Wang, S. Tu, S.A. Gordon, D.M. Pritchard, A. Varro, et al. 2009. Inactivating cholecystokinin-2 receptor inhibits progastrin-dependent colonic crypt fission, proliferation, and colorectal cancer in mice. J. Clin. Invest. 119:2691-2701. doi:10.1172/JCI38918
32. Katz, J.P., N. Perreault, B.G. Goldstein, C.S. Lee, P.A. Labosky, V.W. Yang, and K.H. Kaestner. 2002. The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development. 129:2619-2628. (Pubitemid 34874246)
33. Kist, R., H. Schrewe, R. Balling, and G. Scherer. 2002. Conditional inactivation of Sox9: a mouse model for campomelic dysplasia. Genesis. 32:121-123. doi:10.1002/gene.10050 (Pubitemid 34211715)
34. Kokrashvili, Z., D. Rodriguez, V. Yevshayeva, H. Zhou, R.F. Margolskee, and B. Mosinger. 2009. Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology. 137:598-606: 606:e1-e2. doi:10.1053/j.gastro.2009.02.070
35. Korinek, V., N. Barker, P. Moerer, E. van Donselaar, G. Huls, P.J. Peters, and H. Clevers. 1998. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19:379-383. doi:10.1038/1270 (Pubitemid 28357912)
36. Kugler, P., D. Höfer, B. Mayer, and D. Drenckhahn. 1994. Nitric oxide synthase and NADP-linked glucose-6-phosphate dehydrogenase are co-localized in brush cells of rat stomach and pancreas. J. Histochem. Cytochem. 42:1317-1321. doi:10.1177/42.10.7523487 (Pubitemid 24307721)
37. May, R., T.E. Riehl, C. Hunt, S.M. Sureban, S. Anant, and C.W. Houchen. 2008. Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem Cells. 26:630-637. doi:10.1634/stemcells.2007-0621
38. May, R., S.M. Sureban, N. Hoang, T.E. Riehl, S.A. Lightfoot, R. Ramanujam, J.H. Wyche, S. Anant, and C.W. Houchen. 2009. Doublecortin and CaM kinase-like-1 and leucine-rich-repeat-containing G-protein-coupled receptor mark quiescent and cycling intestinal stem cells, respectively. Stem Cells. 27:2571-2579. doi:10.1002/stem.193
39. Mellitzer, G., A. Beucher, V. Lobstein, P. Michel, S. Robine, M. Kedinger, and G. Gradwohl. 2010. Loss of enteroendocrine cells in mice alters lipid absorption and glucose homeostasis and impairs postnatal survival. J. Clin. Invest. 120:1708-1721. doi:10.1172/JCI40794
40. Mori-Akiyama, Y., M. van den Born, J.H. van Es, S.R. Hamilton, H.P. Adams, J. Zhang, H. Clevers, and B. de Crombrugghe. 2007. SOX9 is required for the differentiation of paneth cells in the intestinal epithelium. Gastroenterology. 133:539-546. doi:10.1053/j.gastro.2007.05.020 (Pubitemid 47187347)
41. Moxey, P.C., and J.S. Trier. 1978. Specialized cell types in the human fetal small intestine. Anat. Rec. 191:269-285. doi:10.1002/ar.1091910302 (Pubitemid 8362054)
42. Noah, T.K., A. Kazanjian, J. Whitsett, and N.F. Shroyer. 2010. SAM pointed domain ETS factor (SPDEF) regulates terminal differentiation and maturation of intestinal goblet cells. Exp. Cell Res. 316:452-465. doi:10.1016/j.yexcr.2009.09.020
43. Pinto, D., A. Gregorieff, H. Begthel, and H. Clevers. 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 17:1709-1713. doi:10.1101/gad.267103 (Pubitemid 36870334)
44. Rhodin, J., and T. Dalhamn. 1956. Electron microscopy of the tracheal ciliated mucosa in rat. Z. Zellforsch. Mikrosk. Anat. 44:345-412. doi:10.1007/BF00345847
45. Sancho, E., E. Batlle, and H. Clevers. 2004. Signaling pathways in intestinal development and cancer. Annu. Rev. Cell Dev. Biol. 20:695-723. doi:10.1146/annurev.cellbio.20.010403.092805 (Pubitemid 39488655)
46. Sangiorgi, E., and M.R. Capecchi. 2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40:915-920. doi:10.1038/ng.165 (Pubitemid 351913652)
47. Sato, A. 2007. Tuft cells. Anat. Sci. Int. 82:187-199. doi:10.1111/j.1447-073X.2007.00188.x (Pubitemid 350090512)
48. Sato, T., J.H. van Es, H.J. Snippert, D.E. Stange, R.G. Vries, M. van den Born, N. Barker, N.F. Shroyer, M. van de Wetering, and H. Clevers. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 469:415-418. doi:10.1038/nature09637
49. Schonhoff, S.E., M. Giel-Moloney, and A.B. Leiter. 2004. Neurogenin 3-expressing progenitor cells in the gastrointestinal tract differentiate into both endocrine and non-endocrine cell types. Dev. Biol. 270:443-454. doi:10.1016/j.ydbio.2004.03.013 (Pubitemid 38748564)
50. Shroyer, N.F., D. Wallis, K.J. Venken, H.J. Bellen, and H.Y. Zoghbi. 2005. Gfi1 functions downstream of Math1 to control intestinal secretory cell subtype allocation and differentiation. Genes Dev. 19:2412-2417. doi:10.1101/gad.1353905 (Pubitemid 41483688)
51. Shroyer, N.F., M.A. Helmrath, V.Y. Wang, B. Antalffy, S.J. Henning, and H.Y. Zoghbi. 2007. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology. 132:2478-2488. doi:10.1053/j.gastro.2007.03.047 (Pubitemid 46890862)
52. Stenson, W.F. 2008. What is the function of cyclooxygenases in the normal and inflamed intestine? Inflamm. Bowel Dis. 14:S104-S105. doi:10.1002/ibd.20700
53. Sureban, S.M., R. May, S. Ramalingam, D. Subramaniam, G. Natarajan, S. Anant, and C.W. Houchen. 2009. Selective blockade of DCAMKL-1 results in tumor growth arrest by a Let-7a MicroRNA-dependent mechanism. Gastroenterology. 137:649-659: 659: e1-e2. doi:10.1053/j.gastro.2009.05.004
54. Sutherland, K., R.L. Young, N.J. Cooper, M. Horowitz, and L.A. Blackshaw. 2007. Phenotypic characterization of taste cells of the mouse small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1420-G1428. doi:10.1152/ajpgi.00504.2006 (Pubitemid 47084658)
55. Suzuki, K., H. Fukui, T. Kayahara, M. Sawada, H. Seno, H. Hiai, R. Kageyama, H. Okano, and T. Chiba. 2005. Hes1-deficient mice show precocious differentiation of Paneth cells in the small intestine. Biochem. Biophys. Res. Commun. 328:348-352. doi:10.1016/j.bbrc.2004.12.174 (Pubitemid 40164675)
56. van der Flier, L.G., and H. Clevers. 2009. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 71:241-260. doi:10.1146/annurev.physiol.010908.163145
57. van der Flier, L.G., M.E. van Gijn, P. Hatzis, P. Kujala, A. Haegebarth, D.E. Stange, H. Begthel, M. van den Born, V. Guryev, I. Oving, et al. 2009. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell. 136:903-912. doi:10.1016/j.cell.2009.01.031
58. van Es, J.H., P. Jay, A. Gregorieff, M.E. van Gijn, S. Jonkheer, P. Hatzis, A. Thiele, M. van den Born, H. Begthel, T. Brabletz, et al. 2005a. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat. Cell Biol. 7:381-386. doi:10.1038/ncb1240 (Pubitemid 40533127)
59. van Es, J.H., M.E. van Gijn, O. Riccio, M. van den Born, M. Vooijs, H. Begthel, M. Cozijnsen, S. Robine, D.J. Winton, F. Radtke, and H. Clevers. 2005b. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature. 435:959-963. doi:10.1038/nature03659 (Pubitemid 40896322)
60. van Es, J.H., N. de Geest, M. van de Born, H. Clevers, and B.A. Hassan. 2010. Intestinal stem cells lacking the Math1 tumour suppressor are refractory to Notch inhibitors. Nat. Commun.. 1:1-5. doi:10.1038/ncomms1017
61. Wang, D., and R.N. Dubois. 2010. Eicosanoids and cancer. Nat. Rev. Cancer. 10:181-193. doi:10.1038/nrc2809
62. Yang, Q., N.A. Bermingham, M.J. Finegold, and H.Y. Zoghbi. 2001. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science. 294:2155-2158. doi:10.1126/science.1065718 (Pubitemid 33150670)