Adult neural stem cells in distinct microdomains generate previously unknown interneuron types

Nature Neuroscience

Volumn 17, Issue 2, 2014, Pages 207-214

  Merkle, Florian T ^a,b,c,d,e   Fuentealba, Luis C ^a,b   Sanders, Timothy A ^a,b   Magno, Lorenza ^f,g   Kessaris, Nicoletta ^f,g   Alvarez Buylla, Arturo ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

^d HARVARD UNIVERSITY   (United States)

^e Harvard University   (United States)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NKX6.2; TRANSCRIPTION FACTOR ZIC; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BRAIN; INTERNEURON; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUBVENTRICULAR ZONE;

AGE FACTORS; ANIMALS; CEREBRAL VENTRICLES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; INTERNEURONS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MEMBRANE MICRODOMAINS; MICE; NEURAL STEM CELLS; NEUROGLIA; RNA, UNTRANSLATED; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 84893739389     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3610     Document Type: Article

References (49)

1. Alvarez-Buylla, A. & Garcia-Verdugo, J.M. Neurogenesis in adult subventricular zone. J. Neurosci. 22, 629-634 (2002).
2. Sakamoto, M. et al. Continuous neurogenesis in the adult forebrain is required for innate olfactory responses. Proc. Natl. Acad. Sci. USA 108, 8479-8484 (2011).
3. Imayoshi, I. et al. Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11, 1153-1161 (2008).
4. Kosaka, K. et al. Chemically defned neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci. Res. 23, 73-88 (1995).
5. Price, J.L. & Powell, T.P. The mitral and short axon cells of the olfactory bulb. J. Cell Sci. 7, 631-651 (1970).
6. Shepherd, G.M. The Synaptic Organization of the Brain (Oxford Univ. Press, 2004).
7. Doetsch, F., Caille, I., Lim, D.A., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716 (1999).
8. Alvarez-Buylla, A., Kohwi, M., Nguyen, T.M. & Merkle, F.T. The heterogeneity of adult neural stem cells and the emerging complexity of their niche. Cold Spring Harb. Symp. Quant. Biol. 73, 357-365 (2008).
9. Merkle, F.T., Mirzadeh, Z. & Alvarez-Buylla, A. Mosaic organization of neural stem cells in the adult brain. Science 317, 381-384 (2007).
10. Kelsch, W., Mosley, C.P., Lin, C.-W. & Lois, C. Distinct mammalian precursors are committed to generate neurons with defned dendritic projection patterns. PLoS Biol. 5, e300 (2007).
11. Ventura, R.E. & Goldman, J.E. Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J. Neurosci. 27, 4297-4302 (2007).
12. Young, K.M., Fogarty, M., Kessaris, N. & Richardson, W.D. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J. Neurosci. 27, 8286-8296 (2007).
13. Kriegstein, A. & Alvarez-Buylla, A. The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184 (2009).
14. Novak, A., Guo, C., Yang, W., Nagy, A. & Lobe, C.G. Z/EG, a double reporter mouse line that expresses enhanced green fuorescent protein upon Cre-mediated excision. Genesis 28, 147-155 (2000).
15. Seri, B. et al. Composition and organization of the SCZ: a large germinal layer containing neural stem cells in the adult mammalian brain. Cereb. Cortex 16 (suppl. 1), i103-i111 (2006).
16. Kohwi, M. et al. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1-and Dlx5/6-expressing progenitors. J. Neurosci. 27, 6878-6891 (2007).
17. Alonso, M. et al. Turning astrocytes from the rostral migratory stream into neurons: a role for the olfactory sensory organ. J. Neurosci. 28, 11089-11102 (2008).
18. Mirzadeh, Z., Merkle, F.T., Soriano-Navarro, M., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3, 265-278 (2008).
19. Shepherd, G., Chen, W., Willhite, D., Migliore, M. & Greer, C. The olfactory granule cell: from classical enigma to central role in olfactory processing. Brain Res. Brain Res. Rev. 55, 373-382 (2007).
20. Schneider, S.P. & Macrides, F. Laminar distributions of interneurons in main olfactory-bulb of adult hamster. Brain Res. Bull. 3, 73-82 (1978).
21. Mori, K., Kishi, K. & Ojima, H. Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory-bulb. J. Comp. Neurol. 219, 339-355 (1983).
22. Blanes, T. Sobre algunos puntos dudosos de la estrucutra del bulbo olfactario. Revista Trimestral Micrografca 3, 99-127 (1898).
23. Shepherd, G.M. Synaptic organization of the mammalian olfactory bulb. Physiol. Rev. 52, 864-917 (1972).
24. López-Mascaraque, L., De Carlos, J.A. & Valverde, F. Structure of the olfactory bulb of the hedgehog (Erinaceus europaeus): a Golgi study of the intrinsic organization of the superfcial layers. J. Comp. Neurol. 301, 243-261 (1990).
25. Larriva-Sahd, J. The accessory olfactory bulb in the adult rat: a cytological study of its cell types, neuropil, neuronal modules, and interactions with the main olfactory system. J. Comp. Neurol. 510, 309-350 (2008).
26. Van Gehuchten, A.I.M. Le bulbe olfactif chez quelques mammiferes. Cellule 5, 205-237 (1891).
27. Ihrie, R.A. et al. Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71, 250-262 (2011).
28. Ahn, S. & Joyner, A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 118, 505-516 (2004).
29. Danielian, P.S., Muccino, D., Rowitch, D.H., Michael, S.K. & McMahon, A.P. Modifcation of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8, 1323-1326 (1998).
30. Mao, J. et al. A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway. Cancer Res. 66, 10171-10178 (2006).
31. Price, M. Members of the Dlx-and Nkx2-gene families are regionally expressed in the developing forebrain. J. Neurobiol. 24, 1385-1399 (1993).
32. Sussel, L., Marin, O., Kimura, S. & Rubenstein, J.L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecifcation within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359-3370 (1999).
33. Marin, O., Anderson, S.A. & Rubenstein, J.L. Origin and molecular specifcation of striatal interneurons. J. Neurosci. 20, 6063-6076 (2000).
34. Flames, N. et al. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27, 9682-9695 (2007).
35. Taniguchi, H., Lu, J. & Huang, Z.J. The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339, 70-74 (2013).
36. Magno, L., Catanzariti, V., Nitsch, R., Krude, H. & Naumann, T. Ongoing expression of Nkx2.1 in the postnatal mouse forebrain: potential for understanding NKX2.1 haploinsuffciency in humans? Brain Res. 1304, 164-186 (2009).
37. Xu, Q., Tam, M. & Anderson, S.A. Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J. Comp. Neurol. 506, 16-29 (2008).
38. Tsai, H.-H. et al. Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science doi:10.1126/science.1222381 (2012).
39. Inan, M., Welagen, J. & Anderson, S.A. Spatial and temporal bias in the mitotic origins of somatostatin-and parvalbumin-expressing interneuron subgroups and the chandelier subtype in the medial ganglionic eminence. Cereb. Cortex 22, 820-827 (2012).
40. Moreno-Bravo, J.A., Perez-Balaguer, A., Martinez, S. & Puelles, E. Dynamic expression patterns of Nkx6.1 and Nkx6.2 in the developing mes-diencephalic basal plate. Dev. Dyn. 239, 2094-2101 (2010).
41. Inoue, T., Ota, M., Ogawa, M., Mikoshiba, K. & Aruga, J. Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors. J. Neurosci. 27, 5461-5473 (2007).
42. Aruga, J. et al. A novel zinc fnger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J. Neurochem. 63, 1880-1890 (1994).
43. Wataya, T. et al. Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation. Proc. Natl. Acad. Sci. USA 105, 11796-11801 (2008).
44. Borghesani, P.R. et al. BDNF stimulates migration of cerebellar granule cells. Development 129, 1435-1442 (2002).
45. Doetsch, F., Garcia-Verdugo, J.M. & Alvarez-Buylla, A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosci. 17, 5046-5061 (1997).
46. Puelles, L. et al. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J. Comp. Neurol. 424, 409-438 (2000).
47. Waclaw, R.R. et al. The zinc fnger transcription factor sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49, 503-516 (2006).
48. Fogarty, M. et al. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J. Neurosci. 27, 10935-10946 (2007).
49. Lee, E.C. et al. A highly effcient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65 (2001).