Sox2-mediated conversion of NG2 glia into induced neurons in the injured adult cerebral cortex

Stem Cell Reports

Volumn 3, Issue 6, 2014, Pages 1000-1014

  Heinrich, Christophe ^a,b   Bergami, Matteo ^a,g   Gascón, Sergio ^a,c   Lepier, Alexandra ^a   Viganò, Francesca ^a   Dimou, Leda ^a,c   Sutor, Bernd ^a   Berninger, Benedikt ^a,d,e   Götz, Magdalena ^a,c,f  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIV GRENOBLE ALPES   (France)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

^f Germany 3 Munich Cluster for Systems Neurology   (Germany)

^g UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLECORTIN; NEURON SPECIFIC NUCLEAR PROTEIN; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR SOX2; ASCL1 PROTEIN, MOUSE; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX;

ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL FATE; CELL PROLIFERATION; NERVE CELL; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROVIRUS; STAB WOUND; ANIMAL; CELL TRANSDIFFERENTIATION; CYTOLOGY; GENE EXPRESSION; GENETICS; GLIA; INJURIES; METABOLISM; MOUSE; NUCLEAR REPROGRAMMING; SYNAPTIC POTENTIAL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CELLULAR REPROGRAMMING; CEREBRAL CORTEX; GENE EXPRESSION; MICE; NEUROGLIA; NEURONS; SOXB1 TRANSCRIPTION FACTORS; SYNAPTIC POTENTIALS;

EID: 84922642870     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.10.007     Document Type: Article

References (39)

1. P. Arlotta, and B. Berninger Brains in metamorphosis: reprogramming cell identity within the central nervous system Curr. Opin. Neurobiol. 27C 2014 208 214
2. S. Bardehle, M. Kruger, F. Buggenthin, J. Schwausch, J. Ninkovic, H. Clevers, H.J. Snippert, F.J. Theis, M. Meyer-Luehmann, and I. Bechmann Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation Nat. Neurosci. 16 2013 580 586
3. M. Bergami, and B. Berninger A fight for survival: the challenges faced by a newborn neuron integrating in the adult hippocampus Dev. Neurobiol. 72 2012 1016 1031
4. D.E. Bergles, J.D. Roberts, P. Somogyi, and C.E. Jahr Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus Nature 405 2000 187 191
5. B. Berninger, M.R. Costa, U. Koch, T. Schroeder, B. Sutor, B. Grothe, and M. Götz Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia J. Neurosci. 27 2007 8654 8664
6. W.R. Beyer, M. Westphal, W. Ostertag, and D. von Laer Oncoretrovirus and lentivirus vectors pseudotyped with lymphocytic choriomeningitis virus glycoprotein: generation, concentration, and broad host range J. Virol. 76 2002 1488 1495
7. A. Buffo, M.R. Vosko, D. Erturk, G.F. Hamann, M. Jucker, D. Rowitch, and M. Götz Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair Proc. Natl. Acad. Sci. USA 102 2005 18183 18188
8. A. Buffo, I. Rite, P. Tripathi, A. Lepier, D. Colak, A.P. Horn, T. Mori, and M. Götz Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain Proc. Natl. Acad. Sci. USA 105 2008 3581 3586
9. A. Colin, M. Faideau, N. Dufour, G. Auregan, R. Hassig, T. Andrieu, E. Brouillet, P. Hantraye, G. Bonvento, and N. Deglon Engineered lentiviral vector targeting astrocytes in vivo Glia 57 2009 667 679
10. L. Dimou, and M. Götz Glial cells as progenitors and stem cells: new roles in the healthy and diseased brain Physiol. Rev. 94 2014 709 737
11. L. Dimou, C. Simon, F. Kirchhoff, H. Takebayashi, and M. Götz Progeny of Olig2-expressing progenitors in the gray and white matter of the adult mouse cerebral cortex J. Neurosci. 28 2008 10434 10442
12. F.H. Gage, and S. Temple Neural stem cells: generating and regenerating the brain Neuron 80 2013 588 601
13. W.P. Ge, W. Zhou, Q. Luo, L.Y. Jan, and Y.N. Jan Dividing glial cells maintain differentiated properties including complex morphology and functional synapses Proc. Natl. Acad. Sci. USA 106 2009 328 333
14. A. Giorgetti, M.C. Marchetto, M. Li, D. Yu, R. Fazzina, Y. Mu, A. Adamo, I. Paramonov, J.C. Cardoso, and M.B. Monasterio Cord blood-derived neuronal cells by ectopic expression of Sox2 and c-Myc Proc. Natl. Acad. Sci. USA 109 2012 12556 12561
15. V. Graham, J. Khudyakov, P. Ellis, and L. Pevny SOX2 functions to maintain neural progenitor identity Neuron 39 2003 749 765
16. A. Grande, K. Sumiyoshi, A. Lopez-Juarez, J. Howard, B. Sakthivel, B. Aronow, K. Campbell, and M. Nakafuku Environmental impact on direct neuronal reprogramming in vivo in the adult brain Nat. Commun. 4 2013 2373
17. Z. Guo, L. Zhang, Z. Wu, Y. Chen, F. Wang, and G. Chen In Vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer's disease model Cell Stem Cell 14 2014 188 202
18. C. Heinrich, R. Blum, S. Gascon, G. Masserdotti, P. Tripathi, R. Sanchez, S. Tiedt, T. Schroeder, M. Götz, and B. Berninger Directing astroglia from the cerebral cortex into subtype specific functional neurons PLoS Biol. 8 2010 e1000373
19. N. Heins, P. Malatesta, F. Cecconi, M. Nakafuku, K.L. Tucker, M.A. Hack, P. Chapouton, Y.A. Barde, and M. Götz Glial cells generate neurons: the role of the transcription factor Pax6 Nat. Neurosci. 5 2002 308 315
20. E.G. Hughes, S.H. Kang, M. Fukaya, and D.E. Bergles Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain Nat. Neurosci. 16 2013 668 676
21. M. Karow, R. Sanchez, C. Schichor, G. Masserdotti, F. Ortega, C. Heinrich, S. Gascon, M.A. Khan, D.C. Lie, and A. Dellavalle Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells Cell Stem Cell 11 2012 471 476
22. T. Kondo, and M. Raff Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells Science 289 2000 1754 1757
23. T. Kondo, and M. Raff Chromatin remodeling and histone modification in the conversion of oligodendrocyte precursors to neural stem cells Genes Dev. 18 2004 2963 2972
24. G. Kronenberg, K. Gertz, G. Cheung, A. Buffo, H. Kettenmann, M. Götz, and M. Endres Modulation of fate determinants Olig2 and Pax6 in resident glia evokes spiking neuroblasts in a model of mild brain ischemia Stroke 41 2010 2944 2949
25. J. Ladewig, J. Mertens, J. Kesavan, J. Doerr, D. Poppe, F. Glaue, S. Herms, P. Wernet, G. Kogler, and F.J. Muller Small molecules enable highly efficient neuronal conversion of human fibroblasts Nat. Methods 9 2012 575 578
26. S.C. Lin, and D.E. Bergles Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus Nat. Neurosci. 7 2004 24 32
27. E. Motori, J. Puyal, N. Toni, A. Ghanem, C. Angeloni, M. Malaguti, G. Cantelli-Forti, B. Berninger, K.K. Conzelmann, and M. Götz Inflammation-induced alteration of astrocyte mitochondrial dynamics requires autophagy for mitochondrial network maintenance Cell Metab. 18 2013 844 859
28. J. Ninkovic, A. Steiner-Mezzadri, M. Jawerka, U. Akinci, G. Masserdotti, S. Petricca, J. Fischer, A. von Holst, J. Beckers, and C.D. Lie The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network Cell Stem Cell 13 2013 403 418
29. W. Niu, T. Zang, Y. Zou, S. Fang, D.K. Smith, R. Bachoo, and C.L. Zhang In vivo reprogramming of astrocytes to neuroblasts in the adult brain Nat. Cell Biol. 15 2013 1164 1175
30. K. Ohira, T. Furuta, H. Hioki, K.C. Nakamura, E. Kuramoto, Y. Tanaka, N. Funatsu, K. Shimizu, T. Oishi, and M. Hayashi Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells Nat. Neurosci. 13 2010 173 179
31. A.A. Oliva Jr., M. Jiang, T. Lam, K.L. Smith, and J.W. Swann Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons J. Neurosci. 20 2000 3354 3368
32. L.H. Pevny, and S.K. Nicolis Sox2 roles in neural stem cells Int. J. Biochem. Cell Biol. 42 2010 421 424
33. K.L. Ring, L.M. Tong, M.E. Balestra, R. Javier, Y. Andrews-Zwilling, G. Li, D. Walker, W.R. Zhang, A.C. Kreitzer, and Y. Huang Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor Cell Stem Cell 11 2012 100 109
34. S. Robel, B. Berninger, and M. Götz The stem cell potential of glia: lessons from reactive gliosis Nat. Rev. Neurosci. 12 2011 88 104
35. C. Simon, H. Lickert, M. Götz, and L. Dimou Sox10-iCreERT2: a mouse line to inducibly trace the neural crest and oligodendrocyte lineage Genesis 50 2012 506 515
36. S. Sirko, G. Behrendt, P.A. Johansson, P. Tripathi, M. Costa, S. Bek, C. Heinrich, S. Tiedt, D. Colak, and M. Dichgans Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog glia Cell Stem Cell 12 2013 426 439
37. Z. Su, W. Niu, M.L. Liu, Y. Zou, and C.L. Zhang In vivo conversion of astrocytes to neurons in the injured adult spinal cord Nat. Commun. 5 2014 3338
38. O. Torper, U. Pfisterer, D.A. Wolf, M. Pereira, S. Lau, J. Jakobsson, A. Bjorklund, S. Grealish, and M. Parmar Generation of induced neurons via direct conversion in vivo Proc. Natl. Acad. Sci. USA 110 2013 7038 7043
39. T. Vierbuchen, A. Ostermeier, Z.P. Pang, Y. Kokubu, T.C. Sudhof, and M. Wernig Direct conversion of fibroblasts to functional neurons by defined factors Nature 463 2010 1035 1041