In vivo analysis of Ascl1 defined progenitors reveals distinct developmental dynamics during adult neurogenesis and gliogenesis

Journal of Neuroscience

Volumn 27, Issue 47, 2007, Pages 12764-12774

  Kim, Euiseok J ^a   Leung, Cheuk T ^b   Reed, Randall R ^b   Johnson, Jane E ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adult neurogenesis; bHLH transcription factor; Gliogenesis; Mash1; Neural stem cell; Oligodendrocyte precursor

Indexed keywords

CRE RECOMBINASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; TRANSCRIPTION FACTOR MASH1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GABAERGIC SYSTEM; GRAY MATTER; HIPPOCAMPUS; IN VIVO STUDY; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; WHITE MATTER;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOLOGICAL MARKERS; BRAIN; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, TRANSGENIC; NEUROGLIA; NEURONS; STEM CELLS;

EID: 36349022042     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3178-07.2007     Document Type: Article

References (56)

1. Ahn S, Joyner AL (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437:894-897.
2. Altman J (1969) Autoradiographic and histological studies of postnatal neurogenesis. IV. Cell proliferation and migration in the anterior forebrain, with special reference to persisting neurogenesis in the olfactory bulb. J Comp Neurol 137:433-457.
3. Alvarez-Buylla A, Lim DA (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41:683-686.
4. Battiste J, Helms AW, Kim EJ, Savage TK, Lagace DC, Mandyam CD, Eisch AJ, Miyoshi G, Johnson JE (2007) Ascl1 defines sequentially generated lineage-restricted neuronal and oligodendrocyte precursor cells in the spinal cord. Development 134:285-293.
5. Bertrand N, Castro DS, Guillemot F (2002) Proneural genes and the specification of neural cell types. Nat Rev Neuroscience 3:517-530.
6. Bull ND, Bartlett PF (2005) The adult mouse hippocampal progenitor is neurogenic but not a stem cell. J Neurosci 25:10815-10821.
7. Cameron HA, McKay RD (2001) Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. J Comp Neurol 435:406-417.
8. Chari DM, Blakemore WF (2002) Efficient recolonisation of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 37:307-313.
9. Dawson MR, Polito A, Levine JM, Reynolds R (2003) NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24:476-488.
10. Doetsch F (2003) The glial identity of neural stem cells. Nat Neurosci 6:1127-1134.
11. Farah MH, Olson JM, Sucic HB, Hume RI, Tapscott SJ, Turner DL (2000) Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127:693-702.
12. Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F (2000) A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67-80.
13. Gage FH (2000) Mammalian neural stem cells. Science 287:1433-1438.
14. Gensert JM, Goldman JE (1997) Endogenous progenitors remyelinate demyelinated axons in the adult CNS. Neuron 19:197-203.
15. Gokhan S, Marin-Husstege M, Yung SY, Fontanez D, Casaccia-Bonnefil P, Mehler MF (2005) Combinatorial profiles of oligodendrocyte-selective classes of transcriptional regulators differentially modulate myelin basic protein gene expression. J Neurosci 25:8311-8321.
16. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery-Padan R, Lledo PM, Gotz M (2005) Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8:865-872.
17. Helms AW, Battiste J, Henke RM, Nakada Y, Simplicio N, Guillemot F, Johnson JE (2005) Sequential roles for Mash1 and Ngn2 in the generation of dorsal spinal cord interneurons. Development 132:2709-2719.
18. Hevner RF, Hodge RD, Daza RA, Englund C (2006) Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res 55:223-233.
19. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
20. Kohwi M, Osumi N, Rubenstein JL, Alvarez-Buylla A (2005) Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J Neurosci 25:6997-7003.
21. Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, Alvarez-Buylla A (2007) A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci 27:6878-6891.
22. Kondo T, Raff M (2000) Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development 127:2989-2998.
23. Kosaka K, Aika Y, Toida K, Heizmann CW, Hunziker W, Jacobowitz DM, Nagatsu I, Streit P, Visser TJ, Kosaka T (1995) Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb. Neurosci Res 23:73-88.
24. Kosaka K, Toida K, Aika Y, Kosaka T (1998) How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells. Neurosci Res 30:101-110.
25. Kuo CT, Mirzadeh Z, Soriano-Navarro M, Rasin M, Wang D, Shen J, Sestan N, Garcia-Verdugo J, Alvarez-Buylla A, Jan LY, Jan YN (2006) Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 127:1253-1264.
26. Lagace DC, Whitman MC, Noonan MA, Ables JL, DeCarolis NA, Arguello AA, Donovan MH, Fischer SJ, Farnbauch LA, Beech RD, DiLeone RJ, Greer CA, Mandyam CD, Eisch AJ (2007) Dynamic contribution of nestin-expressing stem cells to adult neurogenesis. J Neurosci, in press.
27. Leung CT, Coulombe PA, Reed RR (2007) Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci 10:720-726.
28. Lie DC, Colamarino SA, Song HJ, Desire L, Mira H, Consiglio A, Lein ES, Jessberger S, Lansford H, Dearie AR, Gage FH (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437:1370-1375.
29. Liu S, Wang J, Zhu D, Fu Y, Lukowiak K, Lu YM (2003) Generation of functional inhibitory neurons in the adult rat hippocampus. J Neurosci 23:732-736.
30. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
31. Long JE, Garel S, Alvarez-Dolado M, Yoshikawa K, Osumi N, Alvarez-Buylla A, Rubenstein JL (2007) Dlx-dependent and -independent regulation of olfactory bulb interneuron differentiation. J Neurosci 27:3230-3243.
32. Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
33. Nakada Y, Hunsaker TL, Henke RM, Johnson JE (2004) Distinct domains within Mash1 and Math1 are required for function in neuronal differentiation versus cell-type specification. Development 131:1319-1330.
34. Ozen I, Galichet C, Watts C, Parras C, Guillemot F, Raineteau O (2007) Proliferating neuronal progenitors in the postnatal hippocampus transiently express the proneural gene Ngn2. Eur J Neurosci 25:2591-2603.
35. Parras CM, Schuurmans C, Scardigli R, Kim J, Anderson DJ, Guillemot F (2002) Divergent functions of the proneural genes Mash1 and Ngn2 in the specification of neuronal subtype identity. Genes and Development 16:324-338.
36. Parras CM, Galli R, Britz O, Soares S, Galichet C, Battiste J, Johnson JE, Nakafuku M, Vescovi A, Guillemot F (2004) Mash1 specifies neurons and oligodendrocytes in the postnatal brain. EMBO J 23:4495-4505.
37. Parras CM, Hunt C, Sugimori M, Nakafuku M, Rowitch D, Guillemot F (2007) The proneural gene Mash1 specifies an early population of telencephalic oligodendrocytes. J Neurosci 27:4233-4242.
38. Perez SE, Rebelo S, Anderson DJ (1999) Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126:1715-1728.
39. Pleasure SJ, Collins AE, Lowenstein DH (2000) Unique expression patterns of cell fate molecules delineate sequential stages of dentate gyrus development. J Neurosci 20:6095-6105.
40. Polito A, Reynolds R (2005) NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J Anat 207:707-716.
41. Reynolds R, Dawson M, Papadopoulos D, Polito A, Di Bello IC, Pham-Dinh D, Levine J (2002) The response of NG2-expressing oligodendrocyte progenitors to demyelination in MOG-EAE and MS. J Neurocytol 31:523-536.
42. Ridet JL, Malhotra SK, Privat A, Gage FH (1997) Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 20:570-577.
43. Rousseau A, Nutt CL, Betensky RA, Iafrate AJ, Han M, Ligon KL, Rowitch DH, Louis DN (2006) Expression of oligodendroglial and astrocytic lineage markers in diffuse gliomas: use of YKL-40, ApoE, ASCL1, and NKX2-2. J Neuropathol Exp Neurol 65:1149-1156.
44. Saghatelyan A, de Chevigny A, Schachner M, Lledo PM (2004) Tenascin-R mediates activity-dependent recruitment of neuroblasts in the adult mouse forebrain. Nat Neurosci 7:347-356.
45. Seki T, Namba T, Mochizuki H, Onodera M (2007) Clustering, migration, and neurite formation of neural precursor cells in the adult rat hippocampus. J Comp Neurol 502:275-290.
46. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153-7160.
47. Seri B, Garcia-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359-378.
48. Seri B, Herrera DG, Gritti A, Ferron S, Collado L, Vescovi A, Garcia-Verdugo JM, Alvarez-Buylla A (2006) Composition and organization of the SCZ: a large germinal layer containing neural stem cells in the adult mammalian brain. Cereb Cortex 16 [Suppl 1]:i103-111.
49. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
50. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, Kempermann G (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54:805-814.
51. Stump G, Durrer A, Klein AL, Lutolf S, Suter U, Taylor V (2002) Notch1 and its ligands Delta-like and Jagged are expressed and active in distinct cell populations in the postnatal mouse brain. Mech Dev 114:153-159.
52. Sugimori M, Nagao M, Bertrand N, Parras CM, Guillemot F, Nakafuku M (2007) Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development 134:1617-1629.
53. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
54. Wang S, Sdrulla A, Johnson JE, Yokota Y, Barres BA (2001) A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development. Neuron 29:603-614.
55. Woodruff RH, Tekki-Kessaris N, Stiles CD, Rowitch DH, Richardson WD (2001) Oligodendrocyte development in the spinal cord and telencephalon: common themes and new perspectives. Int J Dev Neurosci 19:379-385.
56. Woodruff RH, Fruttiger M, Richardson WD, Franklin RJ (2004) Platelet-derived growth factor regulates oligodendrocyte progenitor numbers in adult CNS and their response following CNS demyelination. Mol Cell Neurosci 25:252-262.