Reawakening the sleeping beauty in the adult brain: Neurogenesis from parenchymal glia

Current Opinion in Genetics and Development

Volumn 34, Issue , 2015, Pages 46-53

  Péron, Sophie ^a,b   Berninger, Benedikt ^a,b  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EXCITATORY AMINO ACID TRANSPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR; NOTCH RECEPTOR; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2;

ADULT; ASTROCYTE; BRAIN CORTEX; CELL PROLIFERATION; CELL REGENERATION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; CORPUS STRIATUM; EXCITOTOXICITY; GLIA CELL; HUMAN; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; ANIMAL; BRAIN INJURY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLIA; METABOLISM; NERVE CELL; REGENERATION;

MAMMALIA;

ANIMALS; ASTROCYTES; BRAIN INJURIES; CELLULAR REPROGRAMMING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEUROGENESIS; NEUROGLIA; NEURONS; REGENERATION;

EID: 84940203258     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2015.07.004     Document Type: Review

References (54)

1. Bonaguidi M.A., Wheeler M.A., Shapiro J.S., Stadel R.P., Sun G.J., Ming G.L., Song H. In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 2011, 145:1142-1155.
2. Mori T., Buffo A., Gotz M. The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol 2005, 69:67-99.
3. Ferretti P. Is there a relationship between adult neurogenesis and neuron generation following injury across evolution?. Eur J Neurosci 2011, 34:951-962.
4. Than-Trong E., Bally-Cuif L. Radial glia and neural progenitors in the adult zebrafish central nervous system. Glia 2015, 63:1406-1428.
5. Fuentealba L.C., Rompani S.B., Parraguez J.I., Obernier K., Romero R., Cepko C.L., Alvarez-Buylla A. Embryonic origin of postnatal neural stem cells. Cell 2015, 161:1644-1655.
6. Furutachi S., Miya H., Watanabe T., Kawai H., Yamasaki N., Harada Y., Imayoshi I., Nelson M., Nakayama K.I., Hirabayashi Y., et al. Slowly dividing neural progenitors are an embryonic origin of adult neural stem cells. Nat Neurosci 2015, 18:657-665.
7. Li G., Fang L., Fernandez G., Pleasure SJ: 1. The ventral hippocampus is the embryonic origin for adult neural stem cells in the dentate gyrus. Neuron 2013, 78:658-672.
8. Merkle F.T., Tramontin A.D., Garcia-Verdugo J.M., Alvarez-Buylla A. Radial glia give rise to adult neural stem cells in the subventricular zone. Proc Natl Acad Sci U S A 2004, 101:17528-17532.
9. Spassky N., Merkle F.T., Flames N., Tramontin A.D., Garcia-Verdugo J.M., Alvarez-Buylla A. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 2005, 25:10-18.
10. Kriegstein A., Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 2009, 32:149-184.
11. Dimou L., Gotz M. Glial cells as progenitors and stem cells: new roles in the healthy and diseased brain. Physiol Rev 2014, 94:709-737.
12. Robel S., Berninger B., Gotz M. The stem cell potential of glia: lessons from reactive gliosis. Nat Rev Neurosci 2011, 12:88-104.
13. Sharifi K., Morihiro Y., Maekawa M., Yasumoto Y., Hoshi H., Adachi Y., Sawada T., Tokuda N., Kondo H., Yoshikawa T., et al. FABP7 expression in normal and stab-injured brain cortex and its role in astrocyte proliferation. Histochem Cell Biol 2011, 136:501-513.
14. Sirko S., Behrendt G., Johansson P.A., Tripathi P., Costa M., Bek S., Heinrich C., Tiedt S., Colak D., Dichgans M., et al. Reactive glia in the injured brain acquire stem cell properties in response to sonic hedgehog [corrected]. Cell Stem Cell 2013, 12:426-439.
15. Buffo A., Rite I., Tripathi P., Lepier A., Colak D., Horn A.P., Mori T., Gotz M. Origin and progeny of reactive gliosis: a source of multipotent cells in the injured brain. Proc Natl Acad Sci U S A 2008, 105:3581-3586.
16. Magnusson J.P., Goritz C., Tatarishvili J., Dias D.O., Smith E.M., Lindvall O., Kokaia Z., Frisen J. A latent neurogenic program in astrocytes regulated by Notch signaling in the mouse. Science 2014, 346:237-241.
17. Duan C.L., Liu C.W., Shen S.W., Yu Z., Mo J.L., Chen X.H., Sun FY: 1. Striatal astrocytes transdifferentiate into functional mature neurons following ischemic brain injury. Glia 2015, 63:1660-1670.
18. Nato G., Caramello A., Trova S., Avataneo V., Rolando C., Taylor V., Buffo A., Peretto P., Luzzati F. Striatal astrocytes produce neuroblasts in an excitotoxic model of Huntington's disease. Development 2015, 142:840-845.
19. Andersen J., Urban N., Achimastou A., Ito A., Simic M., Ullom K., Martynoga B., Lebel M., Goritz C., Frisen J., et al. A transcriptional mechanism integrating inputs from extracellular signals to activate hippocampal stem cells. Neuron 2014, 83:1085-1097.
20. Castro D.S., Martynoga B., Parras C., Ramesh V., Pacary E., Johnston C., Drechsel D., Lebel-Potter M., Garcia L.G., Hunt C., et al. A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev 2011, 25:930-945.
21. Imayoshi I., Isomura A., Harima Y., Kawaguchi K., Kori H., Miyachi H., Fujiwara T., Ishidate F., Kageyama R. Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 2013, 342:1203-1208.
22. Vasconcelos F.F., Castro D.S. Transcriptional control of vertebrate neurogenesis by the proneural factor Ascl1. Front Cell Neurosci 2014, 8:412.
23. Caiazzo M., Dell'Anno M.T., Dvoretskova E., Lazarevic D., Taverna S., Leo D., Sotnikova T.D., Menegon A., Roncaglia P., Colciago G., et al. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 2011, 476:224-227.
24. Karow M., Sanchez R., Schichor C., Masserdotti G., Ortega F., Heinrich C., Gascon S., Khan M.A., Lie D.C., Dellavalle A., et al. Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells. Cell Stem Cell 2012, 11:471-476.
25. Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Sudhof T.C., Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
26. Berninger B., Guillemot F., Gotz M. Directing neurotransmitter identity of neurones derived from expanded adult neural stem cells. Eur J Neurosci 2007, 25:2581-2590.
27. Heinrich C., Blum R., Gascon S., Masserdotti G., Tripathi P., Sanchez R., Tiedt S., Schroeder T., Gotz M., Berninger B. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol 2010, 8:e1000373.
28. Nakatani H., Martin E., Hassani H., Clavairoly A., Maire C.L., Viadieu A., Kerninon C., Delmasure A., Frah M., Weber M., et al. Ascl1/Mash1 promotes brain oligodendrogenesis during myelination and remyelination. J Neurosci 2013, 33:9752-9768.
29. Parras C.M., Hunt C., Sugimori M., Nakafuku M., Rowitch D., Guillemot F. The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J Neurosci 2007, 27:4233-4242.
30. Braun S.M., Pilz G.A., Machado R.A., Moss J., Becher B., Toni N., Jessberger S. Programming hippocampal neural stem/progenitor cells into oligodendrocytes enhances remyelination in the adult brain after injury. Cell Rep 2015, 11:1679-1685.
31. Jessberger S., Toni N., Clemenson G.D., Ray J., Gage F.H. Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat Neurosci 2008, 11:888-893.
32. Kageyama R., Ohtsuka T., Hatakeyama J., Ohsawa R. Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 2005, 306:343-348.
33. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., Gotz M. Glial cells generate neurons: the role of the transcription factor Pax6. Nat Neurosci 2002, 5:308-315.
34. Buffo A., Vosko M.R., Erturk D., Hamann G.F., Jucker M., Rowitch D., Gotz M. Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc Natl Acad Sci U S A 2005, 102:18183-18188.
35. Torper O., Pfisterer U., Wolf D.A., Pereira M., Lau S., Jakobsson J., Bjorklund A., Grealish S., Parmar M. Generation of induced neurons via direct conversion in vivo. Proc Natl Acad Sci U S A 2013, 110:7038-7043.
36. Guo Z., Zhang L., Wu Z., Chen Y., Wang F., Chen G. In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer's disease model. Cell Stem Cell 2014, 14:188-202.
37. Heinrich C., Bergami M., Gascon S., Lepier A., Vigano F., Dimou L., Sutor B., Berninger B., Gotz M. Sox2-mediated conversion of NG2 glia into induced neurons in the injured adult cerebral cortex. Stem Cell Rep 2014, 3:1000-1014.
38. Niu W., Zang T., Smith D.K., Vue T.Y., Zou Y., Bachoo R., Johnson J.E., Zhang C.L. SOX2 reprograms resident astrocytes into neural progenitors in the adult brain. Stem Cell Rep 2015, 4:780-794.
39. Niu W., Zang T., Zou Y., Fang S., Smith D.K., Bachoo R., Zhang C.L. In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol 2013, 15:1164-1175.
40. Su Z., Niu W., Liu M.L., Zou Y., Zhang C.L. In vivo conversion of astrocytes to neurons in the injured adult spinal cord. Nat Commun 2014, 5:3338.
41. Sarkar A., Hochedlinger K. The sox family of transcription factors: versatile regulators of stem and progenitor cell fate. Cell Stem Cell 2013, 12:15-30.
42. Allan S.M., Rothwell N.J. Cytokines and acute neurodegeneration. Nat Rev Neurosci 2001, 2:734-744.
43. Amantea D., Nappi G., Bernardi G., Bagetta G., Corasaniti M.T. Post-ischemic brain damage: pathophysiology and role of inflammatory mediators. FEBS J 2009, 276:13-26.
44. Simon C., Gotz M., Dimou L. Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 2011, 59:869-881.
45. Bergles D.E., Roberts J.D., Somogyi P., Jahr C.E. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 2000, 405:187-191.
46. Lin S.C., Bergles D.E. Synaptic signaling between GABAergic interneurons and oligodendrocyte precursor cells in the hippocampus. Nat Neurosci 2004, 7:24-32.
47. Liu Y., Miao Q., Yuan J., Han S., Zhang P., Li S., Rao Z., Zhao W., Ye Q., Geng J., et al. Ascl1 converts dorsal midbrain astrocytes into functional neurons in vivo. J Neurosci 2015, 35:9336-9355.
48. Ring K.L., Tong L.M., Balestra M.E., Javier R., Andrews-Zwilling Y., Li G., Walker D., Zhang W.R., Kreitzer A.C., Huang Y. Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 2012, 11:100-109.
49. Giorgetti A., Marchetto M.C., Li M., Yu D., Fazzina R., Mu Y., Adamo A., Paramonov I., Cardoso J.C., Monasterio M.B., et al. Cord blood-derived neuronal cells by ectopic expression of Sox2 and c-Myc. Proc Natl Acad Sci U S A 2012, 109:12556-12561.
50. Amador-Arjona A., Cimadamore F., Huang C.T., Wright R., Lewis S., Gage F.H., Terskikh A.V. SOX2 primes the epigenetic landscape in neural precursors enabling proper gene activation during hippocampal neurogenesis. Proc Natl Acad Sci U S A 2015, 112:E1936-E1945.
51. Raposo A.A., Vasconcelos F.F., Drechsel D., Marie C., Johnston C., Dolle D., Bithell A., Gillotin S., van den Berg D.L., Ettwiller L., et al. Ascl1 coordinately regulates gene expression and the chromatin landscape during neurogenesis. Cell Rep 2015, 10:1544-1556.
52. Wapinski O.L., Vierbuchen T., Qu K., Lee Q.Y., Chanda S., Fuentes D.R., Giresi P.G., Ng Y.H., Marro S., Neff N.F., et al. Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 2013, 155:621-635.
53. Masserdotti G., Gillotin S., Sutor B., Drechsel D., Irmler M., Jorgensen H.F., Sass S., Theis F.J., Beckers J., Berninger B., et al. Transcriptional mechanisms of proneural factors and REST in regulating neuronal reprogramming of astrocytes. Cell Stem Cell 2015, 17:74-88.
54. Price J.D., Park K.Y., Chen J., Salinas R.D., Cho M.J., Kriegstein A.R., Lim D.A. The Ink4a/Arf locus is a barrier to direct neuronal transdifferentiation. J Neurosci 2014, 34:12560-12567.