Wnt signaling and the regulation of stem cell function

Current Opinion in Cell Biology

Volumn 16, Issue 6, 2004, Pages 681-687

  Kléber, Maurice ^a   Sommer, Lukas ^a  

^a SWISS FEDERAL INSTITUTE OF TECHNOLOGY   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GROWTH FACTOR; WNT PROTEIN;

CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CELL TYPE; CENTRAL NERVOUS SYSTEM; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NEURAL CREST CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL LINEAGE; CELL PROLIFERATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS;

EID: 7744241519     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2004.08.006     Document Type: Review

References (54)

1. ••].
2. W.J. Nelson, and R. Nusse Convergence of Wnt, β-catenin, and cadherin pathways Science 303 2004 1483 1487
3. K.M. Cadigan, and R. Nusse Wnt signaling: a common theme in animal development Genes Dev 11 1997 3286 3305
4. B. De Strooper, and W. Annaert Where Notch and Wnt signaling meet. The presenilin hub J Cell Biol 152 2001 F17 F20
5. L. Haegele, B. Ingold, H. Naumann, G. Tabatabai, B. Ledermann, and S. Brandner Wnt signalling inhibits neural differentiation of embryonic stem cells by controlling bone morphogenetic protein expression Mol Cell Neurosci 24 2003 696 708
6. J. Aubert, H. Dunstan, I. Chambers, and A. Smith Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation Nat Biotechnol 20 2002 1240 1245
7. N. Sato, L. Meijer, L. Skaltsounis, P. Greengard, and A.H. Brivanlou Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor Nat Med 10 2004 55 63 In embryonic stem cells, activation of the canonical Wnt signaling pathway is sufficient to maintain self-renewal and suppress differentiation, as shown here by the use of a pharmacological inhibitor of GSK3β. The use of such GSK3β-inhibitors may be of practical value in regenerative medicine.
8. M.F. Kielman, M. Rindapaa, C. Gaspar, N. van Poppel, C. Breukel, S. van Leeuwen, M.M. Taketo, S. Roberts, R. Smits, and R. Fodde Apc modulates embryonic stem-cell differentiation by controlling the dosage of β-catenin signaling Nat Genet 32 2002 594 605
9. D. Pinto, A. Gregorieff, H. Begthel, and H. Clevers Canonical Wnt signals are essential for homeostasis of the intestinal epithelium Genes Dev 17 2003 1709 1713 This report establishes a direct role of Dkk, a Wnt inhibitor, in controlling proliferation of intestinal epithelial progenitor cells. Overexpression of Dkk results in hypoplastic crypts and, surprisingly, also in the loss of secretory cells.
10. M. van de Wetering, E. Sancho, C. Verweij, W. de Lau, I. Oving, A. Hurlstone, K. van der Horn, E. Batlle, D. Coudreuse, and A.P. Haramis The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells Cell 111 2002 241 250 Using DNA microarray analysis, Clevers and colleagues identified β-catenin/TCF as a major player in the genetic program of colorectal cancer cells. Inhibition of β-catenin/TCF in these cells leads to cell cycle arrest and to downregulation of the Wnt target gene c-myc. This in turn results in the activation of the cell cycle inhibitor p21, which is shown here to provide a molecular switch between cell cycle progression and differentiation.
11. L. Alonso, and E. Fuchs Stem cells in the skin: waste not, Wnt not Genes Dev 17 2003 1189 1200
12. T.W. Austin, G.P. Solar, F.C. Ziegler, L. Liem, and W. Matthews A role for the Wnt gene family in hematopoiesis: expansion of multilineage progenitor cells Blood 89 1997 3624 3635
13. T. Reya, A.W. Duncan, L. Ailles, J. Domen, D.C. Scherer, K. Willert, L. Hintz, R. Nusse, and I.L. Weissman A role for Wnt signalling in self-renewal of haematopoietic stem cells Nature 423 2003 409 414 This study establishes an important role of canonical Wnt signaling in self-renewal of haematopoietic stem cells. Overexpression of activated β-catenin maintains haematopoietic stem cells in long-term cultures and leads to expansion of stem cell function in vivo as demonstrated by transplantation experiments. Haematopoietic stem cells signal through the canonical Wnt pathway. This was also shown by the ectopic expression of axin or of a frizzled ligand-binding domain (both inhibitors of the Wnt signaling pathway), which results in the inhibition of haematopoietic stem cell growth in vitro and reduced reconstitution in vivo.
14. B. Varnum-Finney, L. Xu, C. Brashem-Stein, C. Nourigat, D. Flowers, S. Bakkour, W.S. Pear, and I.D. Bernstein Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling Nat Med 6 2000 1278 1281
15. J. Antonchuk, G. Sauvageau, and R.K. Humphries HOXB4-induced expansion of adult hematopoietic stem cells ex vivo Cell 109 2002 39 45
16. M. Cobas, A. Wilson, B. Ernst, S.J. Mancini, H.R. MacDonald, R. Kemler, and F. Radtke β-Catenin is dispensable for hematopoiesis and lymphopoiesis J Exp Med 199 2004 221 229
17. A.P. McMahon, and A. Bradley The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain Cell 62 1990 1073 1085
18. - mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum Cell 69 1992 581 595
19. M. Ikeya, S.M. Lee, J.E. Johnson, A.P. McMahon, and S. Takada Wnt signalling required for expansion of neural crest and CNS progenitors Nature 389 1997 966 970
20. S.M. Lee, S. Tole, E. Grove, and A.P. McMahon A local Wnt-3a signal is required for development of the mammalian hippocampus Development 127 2000 457 467
21. M.E. Dickinson, R. Krumlauf, and A.P. McMahon Evidence for a mitogenic effect of Wnt-1 in the developing mammalian central nervous system Development 120 1994 1453 1471
22. S.G. Megason, and A.P. McMahon A mitogen gradient of dorsal midline Wnts organizes growth in the CNS Development 129 2002 2087 2098 Activation of canonical Wnt signaling in the developing chicken spinal cord (achieved by in ovo electroporation) indicates a primary role of Wnt in cell cycle progression rather than in cell fate specification. Thereby, the cellular response is more pronounced in ventral than in dorsal portions of the spinal cord, prompting the authors to propose a 'mitogen gradient' of Wnt activity along the dorso-ventral axis.
23. A. Chenn, and C.A. Walsh Regulation of cerebral cortical size by control of cell cycle exit in neural precursors Science 297 2002 365 369 Forced expression of a constitutively active form of β-catenin in nestin-positive neural precursors results in enlarged brains and increased cerebral cortical surface area, pointing to a possible role of Wnt signaling in the growth of the cerebellar cortex in higher mammals. The authors nicely show that β-catenin regulates cell cycle progression and can thus function in the decision of precursors to proliferate or differentiate during CNS development.
24. D. Zechner, Y. Fujita, J. Hulsken, T. Muller, I. Walther, M.M. Taketo, E.B. Crenshaw III, W. Birchmeier, and C. Birchmeier β-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system Dev Biol 258 2003 406 418
25. •] (analyzing progenitors from the ganglionic eminence) report the modulation of Wnt signaling by FGF2 in neural progenitor proliferation, maturation and differentiation. However, Wnt-induced proliferation is not in both cases FGF2-dependent. Conceivably, cell-intrinsic differences between stem and progenitor cells from different brain areas could influence the output of signaling networks that include Wnt.
26. •].
27. N. Harada, Y. Tamai, T. Ishikawa, B. Sauer, K. Takaku, M. Oshima, and M.M. Taketo Intestinal polyposis in mice with a dominant stable mutation of the β-catenin gene EMBO J 18 1999 5931 5942
28. T.G. Oliver, and R.J. Wechsler-Reya Getting at the root and stem of brain tumors Neuron 42 2004 885 888
29. ••,24].
30. Y. Muroyama, H. Kondoh, and S. Takada Wnt proteins promote neuronal differentiation in neural stem cell culture Biochem Biophys Res Commun 313 2004 915 921
31. Y. Muroyama, M. Fujihara, M. Ikeya, H. Kondoh, and S. Takada Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord Genes Dev 16 2002 548 553
32. + adult stem cells during muscle regeneration Cell 113 2003 841 852 Muscle-derived progenitor cells display no myogenic potential in the uninjured tissue, while myogenic differentiation is greatly enhanced in regenerating muscle. This process is promoted by ectopic Wnt and inhibited by the application of a Wnt antagonist.
33. J. Huelsken, R. Vogel, B. Erdmann, G. Cotsarelis, and W. Birchmeier β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin Cell 105 2001 533 545
34. B.J. Merrill, U. Gat, R. DasGupta, and E. Fuchs Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin Genes Dev 15 2001 1688 1705
35. N.M. Le Douarin, and E. Dupin Multipotentiality of the neural crest Curr Opin Genet Dev 13 2003 529 536
36. M.I. Garcia-Castro, C. Marcelle, and M. Bronner-Fraser Ectodermal Wnt function as a neural crest inducer Science 297 2002 848 851 One of the many functions Wnts appear to fulfill in neural crest development is described in this paper: Wnt6 localized to the ectoderm promotes the formation of neural crest from neural plates. The various effects of Wnt on neural crest development are probably stage dependent [47].
37. R.I. Dorsky, R.T. Moon, and D.W. Raible Control of neural crest cell fate by the Wnt signalling pathway Nature 396 1998 370 373
38. E.J. Jin, C.A. Erickson, S. Takada, and L.W. Burrus Wnt and BMP signaling govern lineage segregation of melanocytes in the avian embryo Dev Biol 233 2001 22 37
39. K.J. Dunn, B.O. Williams, Y. Li, and W.J. Pavan Neural-crest-directed gene transfer demonstrates Wnt1 role in melanocyte expansion and differentiation during mouse development Proc Natl Acad Sci USA 97 2000 10050 10055
40. L. Hari, V. Brault, M. Kleber, H.Y. Lee, F. Ille, R. Leimeroth, C. Paratore, U. Suter, R. Kemler, and L. Sommer Lineage-specific requirements of β-catenin in neural crest development J Cell Biol 159 2002 867 880 NCSC-specific β-catenin gene ablation demonstrates that canonical Wnt signaling is required for sensory fate specification and melanocyte formation but not for stem cell proliferation. Moreover, at later stages, β-catenin might be involved in the aggregation of neural crest cells in dorsal root ganglia and the generation of late-born sensory neurons.
41. H.Y. Lee, M. Kléber, L. Hari, V. Brault, U. Suter, M.M. Taketo, R. Kemler, and L. Sommer Instructive role of Wnt/β-catenin in sensory fate specification in neural crest stem cells Science 303 2004 1020 1023 This study demonstrated that Wnt is not a general stem cell growth factor. Wnt/β-catenin signal activation in emigrating NCSCs regulates sensory fate decisions rather than stem cell expansion, as shown by conditional gene manipulation in vivo and by clonal cell culture analysis. In particular, sustained β-catenin activity in neural crest cells promotes the formation of sensory neural cells in vivo at the expense of virtually all other neural crest derivatives, while in culture Wnt1 instructs eNCSCs to adopt a sensory neuronal fate in a β-catenin-dependent manner.
42. G.M. Kruger, J.T. Mosher, S. Bixby, N. Joseph, T. Iwashita, and S.J. Morrison Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness Neuron 35 2002 657 669
43. S. Bixby, G.M. Kruger, J.T. Mosher, N.M. Joseph, and S.J. Morrison Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity Neuron 35 2002 643 656
44. C. Paratore, D.E. Goerich, U. Suter, M. Wegner, and L. Sommer Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling Development 128 2001 3949 3961
45. P.M. White, S.J. Morrison, K. Orimoto, C.J. Kubu, J.M. Verdi, and D.J. Anderson Neural crest stem cells undergo cell-intrinsic developmental changes in sensitivity to instructive differentiation signals Neuron 29 2001 57 71
46. C.J. Kubu, K. Orimoto, S.J. Morrison, G. Weinmaster, D.J. Anderson, and J.M. Verdi Developmental changes in Notch1 and numb expression mediated by local cell-cell interactions underlie progressively increasing δ sensitivity in neural crest stem cells Dev Biol 244 2002 199 214
47. M. Bronner-Fraser Development. Making sense of the sensory lineage Science 303 2004 966 968
48. D.P. Leone, S. Genoud, S. Atanasoski, R. Grausenburger, P. Berger, D. Metzger, W.B. Macklin, P. Chambon, and U. Suter Tamoxifen-inducible glia-specific Cre mice for somatic mutagenesis in oligodendrocytes and Schwann cells Mol Cell Neurosci 22 2003 430 440
49. D.R. Foltz, M.C. Santiago, B.E. Berechid, and J.S. Nye Glycogen synthase kinase-3β modulates notch signaling and stability Curr Biol 12 2002 1006 1011
50. S.M. Hussein, E.K. Duff, and C. Sirard Smad4 and β-catenin co-activators functionally interact with lymphoid-enhancing factor to regulate graded expression of Msx2 J Biol Chem 278 2003 48805 48814
51. E. Labbe, A. Letamendia, and L. Attisano Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-β and wnt pathways Proc Natl Acad Sci USA 97 2000 8358 8363
52. T. Theil, S. Aydin, S. Koch, L. Grotewold, and U. Ruther Wnt and Bmp signalling cooperatively regulate graded Emx2 expression in the dorsal telencephalon Development 129 2002 3045 3054
53. L. Gunhaga, M. Marklund, M. Sjodal, J.C. Hsieh, T.M. Jessell, and T. Edlund Specification of dorsal telencephalic character by sequential Wnt and FGF signaling Nat Neurosci 6 2003 701 707 In the developing telencephalon, Wnt provides a specification signal independent of cell proliferation. In particular, Wnt blocks ventral and induces, together with FGF, dorsal features. The paper provides an interesting model of telencephalon patterning occurring as a step-wise process.
54. M. Zirlinger, L. Lo, J. McMahon, A.P. McMahon, and D.J. Anderson Transient expression of the bHLH factor neurogenin-2 marks a subpopulation of neural crest cells biased for a sensory but not a neuronal fate Proc Natl Acad Sci USA 99 2002 8084 8089