Intestinal stem cells and mucosal gut development

Current Opinion in Gastroenterology

Volumn 19, Issue 6, 2003, Pages 583-590

  Vidrich, Alda ^a   Buzan, Jenny M ^a   Cohn, Steven M ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

Epithelial differentiation; Intestinal development; Intestinal epithelium; Stem cells

Indexed keywords

BETA CATENIN; WNT PROTEIN;

CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CRYPT CELL; DEVELOPMENTAL STAGE; HUMAN; INTESTINE EPITHELIUM; INTESTINE MUCOSA; INTESTINE VILLUS; MESENCHYME; NONHUMAN; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TISSUE REGENERATION; TISSUE REPAIR;

EID: 0142247091     PISSN: 02671379     EISSN: None     Source Type: Journal    
DOI: 10.1097/00001574-200311000-00012     Document Type: Review

References (59)

1. Cheng H, Leblond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine, V: unitarian theory of the origin of the four epithelial cell types. Am J Anat 1974, 141:537-562.
2. Cheng H, LeBlond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I: columnar cells. Am J Anat 1974, 141:461-480.
3. Cheng H, LeBlond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine, IV: Paneth cells. Am J Anat 1974, 141:521-536.
4. Cheng H, LeBlond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine, II: mucous cells. Am J Anat 1974, 141:481-502.
5. Cheng H, Leblond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine, III: enteroendocrine cells. Am J Anat 1974, 141:503-520.
6. Cohn SM, Roth KA, Birkenmeier EH, et al.: Temporal and spatial patterns of transgene expression in aging adult mice provide insights about the origins, organization and differentiation of the intestinal epithelium. Proc Natl Acad Sci U S A 1991, 88:1034-1038.
7. Schmidt GH, Winton DJ, Ponder BAJ: Development of the pattern of cell renewal in the crypt villus unit of chimeric mouse intestine. Development 1988, 103:785-790.
8. Ponder BAJ, Schmidt GH, Wilkinson MM, et al.: Deviation of mouse intestinal crypts from single progenitor cells. Nature 1985, 313:689-691.
9. Schmidt GH, Wilkinson MM, Ponder BAJ: Cell migration pathway in the intestinal epithelium: an in situ marker system using mouse aggregation chimeras. Cell 1985, 40:425-429.
10. Griffiths DFR, Davies SJ, Williams D, et al.: Demonstration of somatic mutation and crypt clonality by X-linked enzyme histochemistry. Nature 1988, 333:461-463.
11. Winton DJ, Blount MA, Ponder BAJ: A clonal marker induced by mutation in mouse intestinal epithelium. Nature 1988, 333:463-466.
12. Winton DJ, Ponder BAJ: Stem cell organization in mouse small intestine. Proc R Soc Lond B 1990, 241:13-18.
13. Bjerknes M: Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 1999, 116:7-14.
14. Potten CS: Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 1998, 353:821-830.
15. Potten CS: A comprehensive study of the radiobiological response of murine (BDF1) small intestine. Int J Radiat Biol 1990, 58:925-973.
16. Potten CS, Loeffler M: Stem cells: attributes, cycles, spirals, pitfalls and uncertainties: lessons for and from the crypt. Development 1990, 110:1001-1020.
17. Colony PC, Neutra MR: Macromolecular transport in the fetal rat intestine. Gastroenterology 1985, 89:294-306.
18. Madara JL, Neutra MR, Trier JS: Junctional complexes in the fetal rat small intestine during morphogenesis. Dev Biol 1981, 86:170-178.
19. Trier JS, Moxey PC: Morphogenesis of the small intestine during fetal development. Ciba Found Symp 1979, 70:3-29.
20. Lee YJ, Swencki B, Shoichet S, et al.: A possible role for the high mobility group box transcription factor Tcf-4 in vertebrate gut epithelial cell differentiation. J Biol Chem 1999, 274:1566-1572.
21. Korinek V, Barker N, Moerer P, et al.: Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 1998, 19:379-383.
22. van de Wetering M, Sancho E, Verweij C, et al.: The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002, 111:241-250. Gene array methodology is used to identify those genes transcriptionally modulated by the β-catenin/Tcf-4 nuclear complex in colorectal cancer cells by introducing dominant-negative TCFs to disrupt the native activity of this complex. The relevance of genes found to be either upregulated or downmodulated is examined in vivo by determining their expression during normal fetal gut development and in the intestine of animals bearing a null mutation for Tcf-4.
23. van Noort M, Meeldijk J, van der Zee R, et al.: Wnt signaling controls the phosphorylation status of beta-catenin. J Biol Chem 2002, 277:17901-17905. An antibody recognizing the unphosphorylated and active form of β-catenin is described and used to demonstrate the presence of nuclear active β-catenin in intervillus epithelial cells during the genesis of the stem cell compartment.
24. Wong MH, Huelsken J, Birchmeier W, et al.: Selection of multipotent stem cells during morphogenesis of small intestinal crypts of Lieberkuhn is perturbed by stimulation of Lef-1/beta-catenin signaling. J Biol Chem 2002, 277:15843-15850. Sustained expression of the Lef-1/β-catenin nuclear complex results in the deletion of intestinal epithelial stem cells during late embryonic intestinal development, suggesting that it plays a role in normal stem cell selection.
25. Wong MH, Rubinfeld B, Gordon JI: Effects of forced expression of an NH2-terminal truncated beta-catenin on mouse intestinal epithelial homeostasis. J Cell Biol 1998, 141:765-777.
26. Buzan J, Vidrich A, Skaar K, et al.: FGFR3 regulates epithelial stem cell numbers and crypt formation during murine intestinal development. Gastroenterology 2002, 122:A96. A first demonstration that FGFR-3 plays a role in the elaboration of the crypt stem cell compartment during intestinal development.
27. Vidrich A, Buzan J, Ilo C, et al.: Signaling through FGFR3 is necessary for expansion of the epithelial stem cell compartment during normal intestinal development. Gastroenterology 2003, 124:A22. Expression of FGFR-3 isoforms and ligands is examined in the developing murine intestine to determine which receptors and ligands are important during crypt morphogenesis. The clonogenic stem cell assay is used to determine whether stem cell repair capacity is decreased in the absence of FGFR-3, which may explain the reduced intestinal crypt content seen in FGFR-3-null mice.
28. Mariadason JM, Bordonaro M, Aslam F, et al.: Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res 2001, 61:3465-3471.
29. Nakamura M, Okano H, Blendy JA, et al.: Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 1994, 13:67-81.
30. Sakakibara S, Okano H: Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J Neurosci 1997, 17:8300-8312.
31. Kaneko Y, Sakakibara S, Imai T, et al.: Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 2000, 22:139-153.
32. Potten CS, Booth C, Tudor GL, et al.: Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 2003, 71:28-41. The expression pattern of Msi-1 in neonatal and adult intestine in regenerating crypts and in developing intestinal tumors is examined. Results support the thesis that Msi-1 may be a marker of intestinal stem cells and early progenitor cells.
33. Kayahara T, Sawada M, Takaishi S, et al.: Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine. FEBS Lett 2003, 535:131-135. Cellular expression patterns of Msi-1 and Hes1 in adult intestine and during intestinal development are examined. Hes1 is more broadly expressed than Msi-1.
34. Stappenbeck TS, Mills JC, Gordon JI: Molecular features of adult mouse small intestinal epithelial progenitors. Proc Natl Acad Sci U S A 2003, 100:1004-1009. Laser capture microdissection is used to capture crypt base cells for gene expression profiling to define those genes important for the regulation of intestinal stem cell function.
35. Yang Q, Bermingham NA, Finegold MJ, et al.: Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 2001, 294:2155-2158.
36. Skipper M, Lewis J: Getting to the guts of enteroendocrine differentiation. Nat Genet 2000, 24:3-4.
37. Jensen J, Pedersen EE, Galante P, et al.: Control of endodermal endocrine development by Hes-1. Nat Genet 2000, 24:36-44.
38. Jenny M, Uhl C, Roche C, et al.: Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J 2002, 21:6338-6347. The expression and function of ngn3 during intestinal development and in the adult intestine is examined. Data support the conclusion that ngn3 is required for the specification of a subset of enteroendocrine cells and that it operates downstream of Math1 but upstream of NeuroD.
39. Stappenbeck TS, Gordon JI: Rac1 mutations produce aberrant epithelial differentiation in the developing and adult mouse small intestine. Development 2000, 127:2629-2642.
40. Katz JP, Perreault N, Goldstein BG, et al.: The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon. Development 2002, 129:2619-2628. Using gene-targeting methodology to generate Klf4 mutant mice, in vivo evidence is obtained demonstrating that Klf4 is a goblet-specific terminal differentiation factor in both the adult and developing colon.
41. Mahatan CS, Kaestner KH, Geiman DE, et al.: Characterization of the structure and regulation of the murine gene encoding gut-enriched Kruppel-like factor (Kruppel-like factor 4). Nucleic Acids Res 1999, 27:4562-4569.
42. Suh E, Traber PG: An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol 1996, 16:619-625.
43. Silberg DG, Swain GP, Suh ER, et al.: Cdx1 and cdx2 expression during intestinal development. Gastroenterology 2000, 119:961-971.
44. Batlle E, Henderson JT, Beghtel H, et al.: Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002, 111:251-263. A comprehensive study examining the expression of EphB receptors and ephrin ligands and their role in controlling cell positioning along the crypt-to-villus axis of the intestine during development and in the adult. EphB receptor knockout mice are used to elucidate the role of these various receptors in directing the migration of specific subsets of intestinal epithelial cells along the crypt-to-villus axis.
45. Kullander K, Klein R: Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 2002, 3:475-486. This is a fairly comprehensive review of current data addressing the role of Eph and ephrin signaling during development and in adult tissues. Signaling mechanisms and topographic mapping are discussed and examples given.
46. Paris F, Fuks Z, Kang A, et al.: Endothelial apoptosis as the primary lesion initiating intestinal radiation damage in mice. Science 2001, 293:293-297.
47. Karlsson L, Lindahl P, Heath JK, et al.: Abnormal gastrointestinal development in PDGF-A and PDGFR-α deficient mice implicates a novel mesenchymal structure with putative instructive properties in villus morphogenesis. Development 2000, 127:3457-3466.
48. Kaestner KH, Silberg DG, Traber PG, et al.: The mesenchymal winged helix transcription factor Fkh6 is required for the control of gastrointestinal proliferation and differentiation. Genes Dev 1997, 11:1583-1595.
49. Pabst O, Zweigerdt R, Arnold HH: Targeted disruption of the homeobox transcription factor Nkx2·3 in mice results in postnatal lethality and abnormal development of small intestine and spleen. Development 1999, 126:2215-2225.
50. Beck F, Tata F, Chawengsaksophak K: Homeobox genes and gut development. Bioessays 2000, 22:431-441.
51. Ramalho-Santos M, Melton DA, et al.: Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 2000, 127:2763-2772.
52. Komano H, Fujiura Y, Kawaguchi M, et al.: Homeostatic regulation of intestinal epithelia by intraepithelial gamma delta T cells. Proc Natl Acad Sci U S A 1995, 92:6147-6151.
53. Bjerknes M, Cheng H: Modulation of specific intestinal epithelial progenitors by enteric neurons. Proc Natl Acad Sci U S A 2001, 98:12497-12502.
54. Fritsch C, Swietlicki EA, Lefebvre O, et al.: Epimorphin expression in intestinal myofibroblasts induces epithelial morphogenesis. J Clin Invest 2002, 110:1629-1641. The studies detailed in this article elegantly demonstrate, both in vivo and in vitro, that mesenchymally produced epimorphin directs the formation of the crypt-villus unit. Additionally, at least one mediator of the action of epimorphin is identified.
55. Hirai Y, Takebe K, Takashina M, et al.: Epimorphin: a mesenchymal protein essential for epithelial morphogenesis. Cell 1992, 69:471-481.
56. Hirai Y, Lochter A, Galosy S, et al.: Epimorphin functions as a key morphoregulator for mammary epithelial cells. J Cell Biol 1998, 140:159-169.
57. Plateroti M, Rubin DC, Duluc I, et al.: Subepithelial fibroblast cell lines from different levels of gut axis display regional characteristics. Am J Physiol 1998, 274:G945-G954.
58. Goyal A, Singh R, Swietlicki EA, et al.: Characterization of rat epimorphin/syntaxin 2 expression suggests a role in crypt-villus morphogenesis. Am J Physiol 1998, 275:G114-G124.
59. Bitgood MJ, McMahon AP: Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev Biol 1995, 172:126-138.