Wnt signalling and its role in stem cell-driven intestinal regeneration and hyperplasia

Acta Physiologica

Volumn 204, Issue 1, 2012, Pages 137-143

  Cordero, J B ^a   Sansom, O J ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

Intestine; Models; Regeneration; Transformation; Wnt signalling

Indexed keywords

BETA CATENIN; FRIZZLED PROTEIN; G PROTEIN COUPLED RECEPTOR KINASE 5; T CELL FACTOR PROTEIN; WNT PROTEIN;

ANIMAL TISSUE; CELL DIFFERENTIATION; CELL HYPERPLASIA; CELL PROLIFERATION; CELL REGENERATION; DROSOPHILA; GENETIC TRANSCRIPTION; INTESTINE CELL; INTESTINE EPITHELIUM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; HUMANS; HYPERPLASIA; INTESTINES; REGENERATION; STEM CELLS; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 83155181740     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2011.02288.x     Document Type: Review

References (67)

1. Amcheslavsky, A., Jiang, J. & Ip, Y.T. 2009. Tissue damage-induced intestinal stem cell division in Drosophila. Cell Stem Cell 4, 49-61.
2. Andreu, P., Colnot, S., Godard, C., Gad, S., Chafey, P., Niwa-Kawakita, M., Laurent-Puig, P., Kahn, A., Robine, S., Perret, C. & Romagnolo, B. 2005. Crypt-restricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development 132, 1443-1451.
3. Ashton, G.H., Morton, J.P., Myant, K., Phesse, T.J., Ridgway, R.A., Marsh, V., Wilkins, J.A., Athineos, D., Muncan, V., Kemp, R. et al. 2010. Focal adhesion kinase is required for intestinal regeneration and tumorigenesis downstream of Wnt/c-Myc signaling. Dev Cell 19, 259-269.
4. Bach, S.P., Chinery, R., O'Dwyer, S.T., Potten, C.S., Coffey, R.J. & Watson, A.J. 2000. Pyrrolidinedithiocarbamate increases the therapeutic index of 5-fluorouracil in a mouse model. Gastroenterology 118, 81-89.
5. 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. & Clevers, H. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007.
6. Barker, N., Ridgway, R.A., van Es, J.H., van de Wetering, M., Begthel, H., van den Born, M., Danenberg, E., Clarke, A.R., Sansom, O.J. & Clevers, H. 2009. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608-611.
7. 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.
8. Beebe, K., Lee, W.C. & Micchelli, C.A. 2010. JAK/STAT signaling coordinates stem cell proliferation and multilineage differentiation in the Drosophila intestinal stem cell lineage. Dev Biol 338, 28-37.
9. Bernal, N.P., Stehr, W., Zhang, Y., Profitt, S., Erwin, C.R. & Warner, B.W. 2005. Evidence for active Wnt signaling during postresection intestinal adaptation. J Pediatr Surg 40, 1025-1029; discussion 1029.
10. Bienz, M. & Clevers, H. 2003. Armadillo/beta-catenin signals in the nucleus-proof beyond a reasonable doubt? Nat Cell Biol 5, 179-182.
11. Biteau, B. & Jasper, H. 2011. EGF signaling regulates the proliferation of intestinal stem cells in Drosophila. Development 138, 1045-1055.
12. Biteau, B., Hochmuth, C.E. & Jasper, H. 2008. JNK activity in somatic stem cells causes loss of tissue homeostasis in the aging Drosophila gut. Cell Stem Cell 3, 442-455.
13. Bjerknes, M. & Cheng, H. 1999. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 116, 7-14.
14. Cai, J., Zhang, N., Zheng, Y., de Wilde, R.F., Maitra, A. & Pan, D. 2010. The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev 24, 2383-2388.
15. Casali, A. & Batlle, E. 2009. Intestinal stem cells in mammals and Drosophila. Cell Stem Cell 4, 124-127.
16. Chatterjee, M. & Ip, Y.T. 2009. Pathogenic stimulation of intestinal stem cell response in Drosophila. J Cell Physiol 220, 664-671.
17. Cordero, J., Vidal, M. & Sansom, O. 2009. APC as a master regulator of intestinal homeostasis and transformation: from flies to vertebrates. Cell Cycle 8, 2926-2931.
18. van der Flier, L.G., Haegebarth, A., Stange, D.E., van de Wetering, M. & Clevers, H. 2009a. OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 137, 15-17.
19. van der Flier, L.G., van Gijn, M.E., Hatzis, P., Kujala, P., Haegebarth, A., Stange, D.E., Begthel, H., van den Born, M., Guryev, V., Oving, I., van Es, J.H., Barker, N., Peters, P.J., van de Wetering, M. & Clevers, H. 2009b. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136, 903-912.
20. Fuchs, E., Tumbar, T. & Guasch, G. 2004. Socializing with the neighbors: stem cells and their niche. Cell 116, 769-778.
21. Gaspar, C. & Fodde, R. 2004. APC dosage effects in tumorigenesis and stem cell differentiation. Int J Dev Biol 48, 377-386.
22. Haegebarth, A. & Clevers, H. 2009. Wnt signaling, lgr5, and stem cells in the intestine and skin. Am J Pathol 174, 715-721.
23. Holstege, F.C. & Clevers, H. 2006. Transcription factor target practice. Cell 124, 21-23.
24. Hou, S.X. 2010. Intestinal stem cell asymmetric division in the Drosophila posterior midgut. J Cell Physiol 224, 581-584.
25. Ijiri, K. & Potten, C.S. 1986. Radiation-hypersensitive cells in small intestinal crypts; their relationships to clonogenic cells. Br J Cancer Suppl 7, 20-22.
26. Ireland, H., Kemp, R., Houghton, C., Howard, L., Clarke, A.R., Sansom, O.J. & Winton, D.J. 2004. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology 126, 1236-1246.
27. Jiang, H., Patel, P.H., Kohlmaier, A., Grenley, M.O., McEwen, D.G. & Edgar, B.A. 2009. Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137, 1343-1355.
28. Jiang, H., Grenley, M.O., Bravo, M.J., Blumhagen, R.Z. & Edgar, B.A. 2011. EGFR/Ras/MAPK Signaling Mediates Adult Midgut Epithelial Homeostasis and Regeneration in Drosophila. Cell Stem Cell 8, 84-95.
29. Jin, Z., Kirilly, D., Weng, C., Kawase, E., Song, X., Smith, S., Schwartz, J. & Xie, T. 2008. Differentiation-defective stem cells outcompete normal stem cells for niche occupancy in the Drosophila ovary. Cell Stem Cell 2, 39-49.
30. Karpowicz, P., Perez, J. & Perrimon, N. 2010. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137, 4135-4145.
31. Kinzler, K.W., Nilbert, M.C., Su, L.K., Vogelstein, B., Bryan, T.M., Levy, D.B., Smith, K.J., Preisinger, A.C., Hedge, P. & McKechnie, D. 1991. Identification of FAP locus genes from chromosome 5q21. Science 253, 661-665.
32. Kongkanuntn, R., Bubb, V.J., Sansom, O.J., Wyllie, A.H., Harrison, D.J. & Clarke, A.R. 1999. Dysregulated expression of beta-catenin marks early neoplastic change in Apc mutant mice, but not all lesions arising in Msh2 deficient mice. Oncogene 18, 7219-7225.
33. Korinek, V., Barker, N., Morin, P.J., van Wichen, D., de Weger, R., Kinzler, K.W., Vogelstein, B. & Clevers, H. 1997. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275, 1784-1787.
34. Korinek, V., Barker, N., Moerer, P., van Donselaar, E., Huls, G., Peters, P.J. & Clevers, H. 1998. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19, 379-383.
35. Lee, W.C., Beebe, K., Sudmeier, L. & Micchelli, C.A. 2009. Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation. Development 136, 2255-2264.
36. Lin, G., Xu, N. & Xi, R. 2008. Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455, 1119-1123.
37. Lin, G., Xu, N. & Xi, R. 2010. Paracrine unpaired signaling through the JAK/STAT pathway controls self-renewal and lineage differentiation of drosophila intestinal stem cells. J Mol Cell Biol 2, 37-49.
38. Liu, W., Singh, S.R. & Hou, S.X. 2010. JAK-STAT is restrained by Notch to control cell proliferation of the Drosophila intestinal stem cells. J Cell Biochem 109, 992-999.
39. Lopez-Garcia, C., Klein, A.M., Simons, B.D. & Winton, D.J. 2010. Intestinal stem cell replacement follows a pattern of neutral drift. Science 330, 822-825.
40. Micchelli, C.A. & Perrimon, N. 2006. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439, 475-479.
41. Muncan, V., Sansom, O.J., Tertoolen, L., Phesse, T.J., Begthel, H., Sancho, E., Cole, A.M., Gregorieff, A., de Alboran, I.M., Clevers, H. & Clarke, A.R. 2006. Rapid loss of intestinal crypts upon conditional deletion of the Wnt/Tcf-4 target gene c-Myc. Mol Cell Biol 26, 8418-8426.
42. Nystul, T.G. & Spradling, A.C. 2006. Breaking out of the mold: diversity within adult stem cells and their niches. Curr Opin Genet Dev 16, 463-468.
43. Ohlstein, B. & Spradling, A. 2006. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439, 470-474.
44. Ohlstein, B. & Spradling, A. 2007. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 315, 988-992.
45. Pickert, G., Neufert, C., Leppkes, M., Zheng, Y., Wittkopf, N., Warntjen, M., Lehr, H.A., Hirth, S., Weigmann, B., Wirtz, S., Ouyang, W., Neurath, M.F. & Becker, C. 2009. STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J Exp Med 206, 1465-1472.
46. Pinto, D., Gregorieff, A., Begthel, H. & Clevers, H. 2003. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev 17, 1709-1713.
47. Potten, C.S. 1998. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 353, 821-830.
48. Quyn, A.J., Appleton, P.L., Carey, F.A., Steele, R.J., Barker, N., Clevers, H., Ridgway, R.A., Sansom, O.J. & Näthke, I.S. 2010. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell 6, 175-181.
49. Radtke, F. & Clevers, H. 2005. Self-renewal and cancer of the gut: two sides of a coin. Science 307, 1904-1909.
50. Ren, F., Wang, B., Yue, T., Yun, E.Y., Ip, Y.T. & Jiang, J. 2010. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc Natl Acad Sci U S A 107, 21064-21069.
51. Sangiorgi, E. & Capecchi, M.R. 2008. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40, 915-920.
52. Sansom, O.J., Reed, K.R., Hayes, A.J., Ireland, H., Brinkmann, H., Newton, I.P., Batlle, E., Simon-Assmann, P., Clevers, H., Nathke, I.S., Clarke, A.R. & Winton, D.J. 2004. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18, 1385-1390.
53. Sansom, O.J., Meniel, V.S., Muncan, V., Phesse, T.J., Wilkins, J.A., Reed, K.R., Vass, J.K., Athineos, D., Clevers, H. & Clarke, A.R. 2007. Myc deletion rescues Apc deficiency in the small intestine. Nature 446, 676-679.
54. 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. & Clevers, H. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265.
55. Sato, T., van Es, J.H., Snippert, H.J., Stange, D.E., Vries, R.G., van den Born, M., Barker, N., Shroyer, N.F., van de Wetering, M. & Clevers, H. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418.
56. Schmidt, G.H., Winton, D.J. & Ponder, B.A. 1988. Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103, 785-790.
57. Seto, E.S. & Bellen, H.J. 2004. The ins and outs of Wingless signaling. Trends Cell Biol 14, 45-53.
58. Shaw, R.L., Kohlmaier, A., Polesello, C., Veelken, C., Edgar, B.A. & Tapon, N. 2010. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137, 4147-4158.
59. Snippert, H.J., van Es, J.H., van den Born, M., Begthel, H., Stange, D.E., Barker, N. & Clevers, H. 2009. Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine. Gastroenterology 136, 2187-2194 e1.
60. Snippert, H.J., van der Flier, L.G., Sato, T., van Es, J.H., van den Born, M., Kroon-Veenboer, C., Barker, N., Klein, A.M., van Rheenen, J., Simons, B.D. & Clevers, H. 2010. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143, 134-144.
61. Staley, B.K. & Irvine, K.D. 2010. Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr Biol 20, 1580-1587.
62. Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W.E., Rendl, M. & Fuchs, E. 2004. Defining the epithelial stem cell niche in skin. Science 303, 359-363.
63. Valentin-Vega, Y.A., Okano, H. & Lozano, G. 2008. The intestinal epithelium compensates for p53-mediated cell death and guarantees organismal survival. Cell Death Differ 15, 1772-1781.
64. Van der Flier, L.G., Sabates-Bellver, J., Oving, I., Haegebarth, A., De Palo, M., Anti, M., Van Gijn, M.E., Suijkerbuijkm, S., van de Wetering, M., Marra, G. & Clevers, H. 2007. The Intestinal Wnt/TCF Signature. Gastroenterology 132, 628-632.
65. Vermeulen, L., De Sousa, E.M.F., van der Heijden, M., Cameron, K., de Jong, J.H., Borovski, T., Tuynman, J.B., Todaro, M., Merz, C., Rodermond, H., Sprick, M.R., Kemper, K., Richel, D.J., Stassi, G. & Medema, J.P. 2010. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12, 468-476.
66. van de Wetering, M., Sancho, E., Verweij, C., de Lau, W., Oving, I., Hurlstone, A., van der Horn, K., Batlle, E., Coudreuse, D., Haramis, A.P. et al. 2002. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241-250.
67. Zhu, L., Gibson, P., Currle, D.S., Tong, Y., Richardson, R.J., Bayazitov, I.T., Poppleton, H., Zakharenko, S., Ellison, D.W. & Gilbertson, R.J. 2009. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457, 603-607.