Wnt/β-catenin signaling triggers neuron reprogramming and regeneration in the mouse retina

Cell Reports

Volumn 4, Issue 2, 2013, Pages 271-286

  Sanges, Daniela ^a   Romo, Neus ^a   Simonte, Giacoma ^a   Di Vicino, Umberto ^a   Tahoces, Ariadna Diaz ^c   Fernández, Eduardo ^c   Cosma, Maria Pia ^a,b  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^c MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CASEIN KINASE I; GLYCOGEN SYNTHASE; GLYCOPROTEIN; LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; NESTIN; SCAFFOLD PROTEIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUSION; CELL POLARITY; CELL PROLIFERATION; HEMATOPOIETIC STEM CELL; HYBRID CELL; IN VIVO STUDY; MOUSE; NERVE REGENERATION; NONHUMAN; PRIORITY JOURNAL; RETINA; RETINA INJURY; SIGNAL TRANSDUCTION; TISSUE REGENERATION;

MAMMALIA;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL FUSION; MICE; N-METHYLASPARTATE; NEURONS; REGENERATION; RETINA; RETINAL DEGENERATION; STEM CELLS; TRANSCRIPTOME; WNT PROTEINS; WNT SIGNALING PATHWAY;

EID: 84880769150     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.06.015     Document Type: Article

References (44)

1. Alvarez-Dolado M., Pardal R., Garcia-Verdugo J.M., Fike J.R., Lee H.O., Pfeffer K., Lois C., Morrison S.J., Alvarez-Buylla A. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 2003, 425:968-973.
2. Blau H.M., Chiu C.P., Webster C. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 1983, 32:1171-1180.
3. Blau H.M., Pavlath G.K., Hardeman E.C., Chiu C.P., Silberstein L., Webster S.G., Miller S.C., Webster C. Plasticity of the differentiated state. Science 1985, 230:758-766.
4. Cowan C.A., Atienza J., Melton D.A., Eggan K. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 2005, 309:1369-1373.
5. De Robertis E.M. Wnt signaling in axial patterning and regeneration: lessons from planaria. Sci. Signal. 2010, 3:pe21.
6. Fischer A.J. Neural regeneration in the chick retina. Prog. Retin. Eye Res. 2005, 24:161-182.
7. Frisén J. Stem cell plasticity?. Neuron 2002, 35:415-418.
8. Johansson C.B., Youssef S., Koleckar K., Holbrook C., Doyonnas R., Corbel S.Y., Steinman L., Rossi F.M., Blau H.M. Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat. Cell Biol. 2008, 10:575-583.
9. Kim K., Doi A., Wen B., Ng K., Zhao R., Cahan P., Kim J., Aryee M.J., Ji H., Ehrlich L.I., et al. Epigenetic memory in induced pluripotent stem cells. Nature 2010, 467:285-290.
10. Kuçi S., Kuçi Z., Latifi-Pupovci H., Niethammer D., Handgretinger R., Schumm M., Bruchelt G., Bader P., Klingebiel T. Adult stem cells as an alternative source of multipotential (pluripotential) cells in regenerative medicine. Curr. Stem Cell Res. Ther. 2009, 4:107-117.
11. Lengfeld T., Watanabe H., Simakov O., Lindgens D., Gee L., Law L., Schmidt H.A., Ozbek S., Bode H., Holstein T.W. Multiple Wnts are involved in Hydra organizer formation and regeneration. Dev. Biol. 2009, 330:186-199.
12. Li V.S., Ng S.S., Boersema P.J., Low T.Y., Karthaus W.R., Gerlach J.P., Mohammed S., Heck A.J., Maurice M.M., Mahmoudi T., Clevers H. Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 2012, 149:1245-1256.
13. Lin G., Slack J.M. Requirement for Wnt and FGF signaling in Xenopus tadpole tail regeneration. Dev. Biol. 2008, 316:323-335.
14. Lluis F., Cosma M.P. Somatic cell reprogramming control: signaling pathway modulation versus transcription factor activities. Cell Cycle 2009, 8:1138-1144.
15. Lluis F., Cosma M.P. Cell-fusion-mediated somatic-cell reprogramming: a mechanism for tissue regeneration. J. Cell. Physiol. 2010, 223:6-13.
16. Lluis F., Pedone E., Pepe S., Cosma M.P. Periodic activation of Wnt/beta-catenin signaling enhances somatic cell reprogramming mediated by cell fusion. Cell Stem Cell 2008, 3:493-507.
17. Lluis F., Pedone E., Pepe S., Cosma M.P. The Wnt/β-catenin signaling pathway tips the balance between apoptosis and reprograming of cell fusion hybrids. Stem Cells 2010, 28:1940-1949.
18. Lluis F., Ombrato L., Pedone E., Pepe S., Merrill B.J., Cosma M.P. T-cell factor 3 (Tcf3) deletion increases somatic cell reprogramming by inducing epigenome modifications. Proc. Natl. Acad. Sci. USA 2011, 108:11912-11917.
19. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 2004, 20:781-810.
20. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
21. Morillo S.M., Escoll P., de la Hera A., Frade J.M. Somatic tetraploidy in specific chick retinal ganglion cells induced by nerve growth factor. Proc. Natl. Acad. Sci. USA 2010, 107:109-114.
22. Niida A., Hiroko T., Kasai M., Furukawa Y., Nakamura Y., Suzuki Y., Sugano S., Akiyama T. DKK1, a negative regulator of Wnt signaling, is a target of the beta-catenin/TCF pathway. Oncogene 2004, 23:8520-8526.
23. Nirenberg S., Meister M. The light response of retinal ganglion cells is truncated by a displaced amacrine circuit. Neuron 1997, 18:637-650.
24. Nygren J.M., Liuba K., Breitbach M., Stott S., Thorén L., Roell W., Geisen C., Sasse P., Kirik D., Björklund A., et al. Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat. Cell Biol. 2008, 10:584-592.
25. Ogle B.M., Cascalho M., Platt J.L. Biological implications of cell fusion. Nat. Rev. Mol. Cell Biol. 2005, 6:567-575.
26. Osakada F., Ooto S., Akagi T., Mandai M., Akaike A., Takahashi M. Wnt signaling promotes regeneration in the retina of adult mammals. J.Neurosci. 2007, 27:4210-4219.
27. Otani A., Dorrell M.I., Kinder K., Moreno S.K., Nusinowitz S., Banin E., Heckenlively J., Friedlander M. Rescue of retinal degeneration by intravitreally injected adult bone marrow-derived lineage-negative hematopoietic stem cells. J.Clin. Invest. 2004, 114:765-774.
28. Polo J.M., Liu S., Figueroa M.E., Kulalert W., Eminli S., Tan K.Y., Apostolou E., Stadtfeld M., Li Y., Shioda T., et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 2010, 28:848-855.
29. Pomerantz J., Blau H.M. Nuclear reprogramming: a key to stem cell function in regenerative medicine. Nat. Cell Biol. 2004, 6:810-816.
30. Qian L., Huang Y., Spencer C.I., Foley A., Vedantham V., Liu L., Conway S.J., Fu J.D., Srivastava D. Invivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485:593-598.
31. Ramachandran R., Fausett B.V., Goldman D. Ascl1a regulates Müller glia dedifferentiation and retinal regeneration through a Lin-28-dependent, let-7 microRNA signalling pathway. Nat. Cell Biol. 2010, 12:1101-1107.
32. Sasahara M., Otani A., Oishi A., Kojima H., Yodoi Y., Kameda T., Nakamura H., Yoshimura N. Activation of bone marrow-derived microglia promotes photoreceptor survival in inherited retinal degeneration. Am. J. Pathol. 2008, 172:1693-1703.
33. Shin D.M., Liu R., Klich I., Ratajczak J., Kucia M., Ratajczak M.Z. Molecular characterization of isolated from murine adult tissues very small embryonic/epiblast like stem cells (VSELs). Mol. Cells 2010, 29:533-538.
34. Song K., Nam Y.J., Luo X., Qi X., Tan W., Huang G.N., Acharya A., Smith C.L., Tallquist M.D., Neilson E.G., et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012, 485:599-604.
35. Streilein J.W., Ma N., Wenkel H., Ng T.F., Zamiri P. Immunobiology and privilege of neuronal retina and pigment epithelium transplants. Vision Res. 2002, 42:487-495.
36. Sullivan S., Eggan K. The potential of cell fusion for human therapy. Stem Cell Rev. 2006, 2:341-349.
37. Tada M., Tada T., Lefebvre L., Barton S.C., Surani M.A. Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO J. 1997, 16:6510-6520.
38. Tada M., Takahama Y., Abe K., Nakatsuji N., Tada T. Nuclear reprogramming of somatic cells by invitro hybridization with ES cells. Curr. Biol. 2001, 11:1553-1558.
39. Terada N., Hamazaki T., Oka M., Hoki M., Mastalerz D.M., Nakano Y., Meyer E.M., Morel L., Petersen B.E., Scott E.W. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 2002, 416:542-545.
40. Timmers A.M., Zhang H., Squitieri A., Gonzalez-Pola C. Subretinal injections in rodent eyes: effects on electrophysiology and histology of rat retina. Mol. Vis. 2001, 7:131-137.
41. Vassilopoulos G., Russell D.W. Cell fusion: an alternative to stemcell plasticity and its therapeutic implications. Curr. Opin. Genet. Dev. 2003, 13:480-485.
42. Wang X., Willenbring H., Akkari Y., Torimaru Y., Foster M., Al-Dhalimy M., Lagasse E., Finegold M., Olson S., Grompe M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 2003, 422:897-901.
43. Weimann J.M., Charlton C.A., Brazelton T.R., Hackman R.C., Blau H.M. Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains. Proc. Natl. Acad. Sci. USA 2003, 100:2088-2093.
44. Ying Q.L., Nichols J., Evans E.P., Smith A.G. Changing potency by spontaneous fusion. Nature 2002, 416:545-548.