JB Special Review - Wnt Signaling: Biological Functions and Its Implications in Diseases: Wnt-expressing cells in the intestines: Guides for tissue remodeling

Journal of Biochemistry

Volumn 161, Issue 1, 2017, Pages 19-25

  Miyoshi, Hiroyuki ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Fibroblast; Intestine; Stem cell niche; Wnt signaling wound healing

Indexed keywords

WNT PROTEIN;

ARTICLE; BIOCHEMICAL ANALYSIS; CELL REGENERATION; COLON BIOPSY; COLON INJURY; FIBROBLAST; HOMEOSTASIS; HUMAN; INTESTINE CELL; MESENCHYME CELL; NONHUMAN; PROTEIN EXPRESSION; WOUND HEALING; ANIMAL; CYTOLOGY; EPITHELIUM CELL; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; CELLULAR MICROENVIRONMENT; EPITHELIAL CELLS; HUMANS; INTESTINAL MUCOSA; WNT PROTEINS; WOUND HEALING;

EID: 85014515882     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvw070     Document Type: Article

References (59)

1. Brittan, M. and Wright, N.A. (2002) Gastrointestinal stem cells. J. Pathol. 197, 492-509
2. Park, H.S., Goodlad, R.A., Ahnen, D.J., Winnett, A., Sasieni, P., Lee, C.Y., and Wright, N.A. (1997) Effects of epidermal growth factor and dimethylhydrazine on crypt size, cell proliferation, and crypt fission in the rat colon. Cell proliferation and crypt fission are controlled independently. Am. J. Pathol. 151, 843-852
3. Seno, H., Miyoshi, H., Brown, S.L., Geske, M.J., Colonna, M., and Stappenbeck, T.S. (2009) Efficient colonic mucosal wound repair requires Trem2 signaling. Proc. Natl Acad. Sci. U. S. A. 106, 256-261
4. Smolich, B.D., McMahon, J.A., McMahon, A.P., and Papkoff, J. (1993) Wnt family proteins are secreted and associated with the cell surface. Mol. Biol. Cell 4, 1267-1275
5. Willert, K., Brown, J.D., Danenberg, E., Duncan, A.W., Weissman, I.L., Reya, T., Yates, J.R., and Nusse, R. (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452
6. Nile, A.H. and Hannoush, R.N. (2016) Fatty acylation of Wnt proteins. Nat. Chem. Biol. 12, 60-69
7. Hausmann, G, Banziger, C, and Basler, K. (2007) Helping Wingless take flight: how WNT proteins are secreted. Nat. Rev. Mol. Cell Biol. 8, 331-336
8. Janda, C.Y., Waghray, D., Levin, A.M., Thomas, C, and Garcia, K.C. (2012) Structural basis of Wnt recognition by Frizzled. Science 337, 59-64
9. Ai, X., Do, A.T., Lozynska, O., Kusche-Gullberg, M., Lindahl, U., and Emerson, C.P. Jr. (2003) QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling. J. Cell Biol. 162, 341-351
10. Gregorieff, A., Pinto, D., Begthel, H., Destree, O., Kielman, M., and Clevers, H. (2005) Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 129, 626-638
11. Clevers, H, Loh, K.M., and Nusse, R. (2014) An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346, 54
12. Fevr, T., Robine, S., Louvard, D., and Huelsken, J. (2007) Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol. Cell. Biol. 27, 7551-7559
13. Kuhnert, F., Davis, CR., Wang, H.T., Chu, P., Lee, M., Yuan, J., Nusse, R., and Kuo, C.J. (2004) Essential requirement for Wnt signaling in proliferation of adult small intestine and colon revealed by adenoviral expression of Dickkopf-1. Proc. Natl Acad. Sci. U. S. A. 101, 266-271
14. Kabiri, Z., Greicius, G, Madan, B., Biechele, S., Zhong, Z.D., Zaribafzadeh, H, Edison, Aliyev, J., Wu, Y.H., Bunte, R., Williams, B. O., Rossant, J., and Virshup, D. M. (2014) Stroma provides an intestinal stem cell niche in the absence of epithelial Wnts. Development 141, 2206-2215
15. Farin, H.F., Jordens, I., Mosa, M.H., Basak, O., Korving, J., Tauriello, D.V., de Punder, K., Angers, S., Peters, P.J., Maurice, M.M., and Clevers, H. (2016) Visualization of a short-range Wnt gradient in the intestinal stem-cell niche. Nature 530, 340-343
16. 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., and Clevers, H. (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418
17. Durand, A., Donahue, B., Peignon, G, Letourneur, F., Cagnard, N, Slomianny, C, Perret, C, Shroyer, N.F., and Romagnolo, B. (2012) Functional intestinal stem cells after Paneth cell ablation induced by the loss of transcription factor Math1 (Atoh1). Proc. Natl Acad. Sci. U.S.A. 109, 8965-8970
18. Farin, H.F., Van Es, J.H., and Clevers, H. (2012) Redundant sources of Wnt regulate intestinal stem cells and promote formation of paneth cells. Gastroenterology 143, 1518-1529
19. Tsukiyama, T. and Yamaguchi, T.P. (2012) Mice lacking Wnt2b are viable and display a postnatal olfactory bulb phenotype. Neurosci. Lett. 512, 48-52
20. de Lau, W., Barker, N, Low, T.Y., Koo, B.K., Li, V.S., Teunissen, H., Kujala, P., Haegebarth, A., Peters, P.J., van de Wetering, M., Stange, D.E., van Es, J.E., Guardavaccaro, D., Schasfoort, R.B., Mohri, Y., Nishimori, K., Mohammed, S., Heck, A.J., and Clevers, H. (2011) Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 476, 293-297
21. 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., and Clevers, H. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265
22. Miyoshi, H. and Stappenbeck, T.S. (2013) In vitro expansion and genetic modification of gastrointestinal stem cells in spheroid culture. Nat. Protoc. 8, 2471-2482
23. Miyoshi, H, Ajima, R., Luo, C.T., Yamaguchi, T.P., and Stappenbeck, T.S. (2012) Wnt5a potentiates TGF-beta signaling to promote colonic crypt regeneration after tissue injury. Science 338, 108-113
24. Kang, E., Yousefi, M., and Gruenheid, S. (2016) R-Spondins are expressed by the intestinal stroma and are differentially regulated during citrobacter rodentium-and DSS-Induced colitis in mice. PLoS One 11, e0152859
25. Kim, K.A., Kakitani, M., Zhao, J.S., Oshima, T., Tang, T., Binnerts, M., Liu, Y., Boyle, B., Park, E., Emtage, P., Funk, W.D., and Tomizuka, K. (2005) Mitogenic influence of human R-spondin1 on the intestinal epithelium. Science 309, 1256-1259
26. Sun, L., Miyoshi, H., Origanti, S., Nice, T.J., Barger, A.C., Manieri, N.A., Fogel, L.A., French, A.R., Piwnica-Worms, D., Piwnica-Worms, H., Virgin, H.W., Lenschow, D.J., and Stappenbeck, T.S. (2015) Type I interferons link viral infection to enhanced epithelial turnover and repair. Cell Host Microbe 17, 85-97
27. McDonald, S.L. and Silver, A. (2009) The opposing roles of Wnt-5a in cancer. Br. J. Cancer 101, 209-214
28. Mikels, A.J. and Nusse, R. (2006) Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol. 4, e115
29. Yamaguchi, T.P., Bradley, A., McMahon, A.P., and Jones, S. (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223
30. Cervantes, S., Yamaguchi, T.P., and Hebrok, M. (2009) Wnt5a is essential for intestinal elongation in mice. Dev. Biol. 326, 285-294
31. Ishikawa, T., Tamai, Y., Zorn, A.M., Yoshida, H., Seldin, M.F., Nishikawa, S., and Taketo, M.M. (2001) Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128, 25-33
32. Korn, C, Scholz, B., Hu, J., Srivastava, K., Wojtarowicz, J., Arnsperger, T., Adams, R.H., Boutros, M., Augustin, H.G., and Augustin, I. (2014) Endothelial cell-derived non-canonical Wnt ligands control vascular pruning in angiogenesis. Development 141, 1757-1766
33. Skinner, S.A. and O'Brien, P.E. (1996) The microvascular structure of the normal colon in rats and humans. J. Surg. Res. 61, 482-490
34. Tahara, T. and Yamamoto, T. (1988) Morphological changes of the villous microvascular architecture and intestinal growth in rats with streptozotocin-induced diabetes. Virchows Arch. 413, 151-158
35. Sato, A., Kayama, H., Shojima, K., Matsumoto, S., Koyama, H., Minami, Y., Nojima, S., Morii, E., Honda, H., Takeda, K., and Kikuchi, A. (2015) The Wnt5a-Ror2 axis promotes the signaling circuit between interleukin-12 and interferon-gamma in colitis. Sci. Rep. 5, 10536
36. Kawada, M., Arihiro, A., and Mizoguchi, E. (2007) Insights from advances in research of chemically induced experimental models of human inflammatory bowel disease. World J. Gastroenterol. 13, 5581-5593
37. Stappenbeck, T.S. and Miyoshi, H. (2009) The role of stromal stem cells in tissue regeneration and wound repair. Science 324, 1666-1669
38. Manieri, N.A., Drylewicz, M.R., Miyoshi, H., and Stappenbeck, T.S. (2012) Igf2bp1 is required for full induction of Ptgs2 mRNA in colonic mesenchymal stem cells in mice. Gastroenterology 143, 110-121
39. Philipp, I., Aufschnaiter, R., Ozbek, S., Pontasch, S., Jenewein, M., Watanabe, H., Rentzsch, F., Holstein, T.W., and Hobmayer, B. (2009) Wnt/beta-catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra. Proc. Natl Acad. Sci. U. S. A. 106, 4290-4295
40. Stoick-Cooper, C.L., Weidinger, G., Riehle, K.J., Hubbert, C., Major, M.B., Fausto, N., and Moon, R.T. (2007) Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 134, 479-489
41. Veeman, M.T., Axelrod, J.D., and Moon, R.T. (2003) A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5, 367-377
42. Matsuyama, M., Aizawa, S., and Shimono, A. (2009) Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genet. 5, e1000427
43. Buch, T., Heppner, F.L., Tertilt, C, Heinen, T.J., Kremer, M., Wunderlich, F.T., Jung, S., and Waisman, A. (2005) A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419-426
44. Powell, D.W., Mifflin, R.C., Valentich, J.D., Crowe, S.E., Saada, J.I., and West, A.B. (1999) Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am. J. Physiol. 277, C183-C201
45. San Roman, A.K., Jayewickreme, C.D., Murtaugh, L.C., and Shivdasani, R.A. (2014) Wnt secretion from epithelial cells and subepithelial myofibroblasts is not required in the mouse intestinal stem cell niche in vivo. Stem Cell Rep. 2, 127-134
46. Aoki, R., Shoshkes-Carmel, M., Gao, N., Shin, S., May, C.L., Golson, M.L., Zahm, A.M., Ray, M., Wiser, C.L., Wright, C.V., and Kaestner, K.H. (2016) Foxl1-expressing mesenchymal cells constitute the intestinal stem cell niche. Cell. Mol. Gastroenterol. Hepatol. 2, 175-188
47. Valenta, T., Degirmenci, B., Moor, A.E., Herr, P., Zimmerli, D., Moor, M.B., Hausmann, G, Cantu, C, Aguet, M., and Basler, K. (2016) Wnt Ligands Secreted by Subepithelial Mesenchymal Cells Are Essential for the Survival of Intestinal Stem Cells and Gut Homeostasis. Cell Rep. 15, 911-918
48. Kalluri, R. and Zeisberg, M. (2006) Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401
49. Rinn, J.L., Wang, J.K., Allen, N., Brugmann, S.A., Mikels, A.J., Liu, H., Ridky, T.W., Stadler, H.S., Nusse, R., Helms, J.A., and Chang, H.Y. (2008) A dermal HOX transcriptional program regulates site-specific epidermal fate. Genes Dev. 22, 303-307
50. Chang, H.Y., Chi, J.T., Dudoit, S., Bondre, C, van de Rijn, M., Botstein, D., and Brown, P.O. (2002) Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc. Natl Acad. Sci. U. S. A. 99, 12877-12882
51. Wilm, B., Ipenberg, A., Hastie, N.D., Burch, J.B., and Bader, D.M. (2005) The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 132, 5317-5328
52. Mutsaers, S.E., Birnie, K, Lansley, S., Herrick, S.E., Lim, C.B., and Prele, C.M. (2015) Mesothelial cells in tissue repair and fibrosis. Front. Pharmacol. 6, 113
53. Manieri, N.A., Mack, M.R., Himmelrich, M.D., Worthley, D.L., Hanson, E.M., Eckmann, L., Wang, T.C., and Stappenbeck, T.S. (2015) Mucosally transplanted mesenchymal stem cells stimulate intestinal healing by promoting angiogenesis. J. Clin. Invest. 125, 3606-3618
54. Walker, M.R., Brown, S.L., Riehl, T.E., Stenson, W.F., and Stappenbeck, T.S. (2010) Growth factor regulation of prostaglandin-endoperoxide synthase 2 (Ptgs2) expression in colonic mesenchymal stem cells. J. Biol. Chem. 285, 5026-5039
55. 2 promotes intestinal repair through an adaptive cellular response of the epithelium. EMBO J; doi: 10.15252/embj.201694660
56. Petersen, C.P. and Reddien, P.W. (2009) Wnt signaling and the polarity of the primary body axis. Cell 139, 1056-1068
57. Guder, C, Philipp, I., Lengfeld, T., Watanabe, H., Hobmayer, B., and Holstein, T.W. (2006) The Wnt code: cnidarians signal the way. Oncogene 25, 7450-7460
58. Ng, A.N., de Jong-Curtain, T.A., Mawdsley, D.J., White, S.J., Shin, J., Appel, B., Dong, P.D., Stainier, D.Y., and Heath, J.K. (2005) Formation of the digestive system in zebrafish: III. Intestinal epithelium morphogenesis. Dev. Biol. 286, 114-135
59. Kaiko, G.E., Ryu, S.H., Koues, O.I., Collins, P.L., Solnica-Krezel, L., Pearce, E.J., Pearce, E.L., Oltz, E.M., and Stappenbeck, T.S. (2016) The colonic crypt protects stem cells from microbiota-derived metabolites. Cell 165, 1708-1720