Dynamic contribution of nestin-expressing stem cells to adult neurogenesis

Journal of Neuroscience

Volumn 27, Issue 46, 2007, Pages 12623-12629

  Lagace, Diane C ^a   Whitman, Mary C ^b   Noonan, Michele A ^a   Ables, Jessica L ^a   DeCarolis, Nathan A ^a   Arguello, Amy A ^a   Donovan, Michael H ^a   Fischer, Stephanie J ^a   Farnbauch, Laure A ^a   Beech, Robert D ^b   DiLeone, Ralph J ^b   Greer, Charles A ^b   Mandyam, Chitra D ^c   Eisch, Amelia J ^a  

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

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Dentate gyrus; Olfactory bulb; Rostral migratory stream; Subgranular zone; Subventricular zone; Tamoxifen

Indexed keywords

BROXURIDINE; ESTROGEN; LIGAND; NESTIN; TAMOXIFEN; TRANSCRIPTION FACTOR SOX2; YELLOW FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL FATE; CONTROLLED STUDY; DENTATE GYRUS; GENETIC RECOMBINATION; GLIA; GRANULE CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; MORPHOLOGY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; STEM CELL; SUBVENTRICULAR ZONE;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DENTATE GYRUS; GENE TARGETING; INTERMEDIATE FILAMENT PROTEINS; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; OLFACTORY BULB; RECOMBINANT FUSION PROTEINS; RECOMBINATION, GENETIC; SELECTIVE ESTROGEN RECEPTOR MODULATORS; STEM CELLS; TAMOXIFEN;

EID: 36248958190     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3812-07.2007     Document Type: Article

References (45)

1. Abusaad I, MacKay D, Zhao J, Stanford P, Collier DA, Everall IP (1999) Stereological estimation of the total number of neurons in the murine hippocampus using the optical disector. J Comp Neurol 408:560-566.
2. 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.
3. Beech RD, Cleary MA, Treloar HB, Eisch AJ, Harrist AV, Zhong W, Greer CA, Duman RS, Picciotto MR (2004) Nestin promoter/enhancer directs transgene expression to precursors of adult generated periglomerular neurons. J Comp Neurol 475:128-141.
4. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
5. Burns KA, Ayoub AE, Breunig JJ, Adhami F, Weng WL, Colbert MC, Rakic P, Kuan CY (2007) Nestin-CreER mice reveal DNA synthesis by nonapoptotic neurons following cerebral ischemia-hypoxia. Cereb Cortex 17:2585-2592.
6. Carlen M, Meletis K, Barnabe-Heider F, Frisen J (2006) Genetic visualization of neurogenesis. Exp Cell Res 312:2851-2859.
7. Dayer AG, Ford AA, Cleaver KM, Yassaee M, Cameron HA (2003) Short-term and long-term survival of new neurons in the rat dentate gyrus. J Comp Neurol 460:563-572.
8. Doetsch F, Hen R (2005) Young and excitable: the function of new neurons in the adult mammalian brain. Curr Opin Neurobiol 15:121-128.
9. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-716.
10. Donovan MH, Yazdani U, Norris RD, Games D, German DC, Eisch AJ (2006) Decreased adult hippocampal neurogenesis in the PDAPP mouse model of Alzheimer's disease. J Comp Neurol 495:70-83.
11. Forni PE, Scuoppo C, Imayoshi I, Taulli R, Dastru W, Sala V, Betz UA, Muzzi P, Martinuzzi D, Vercelli AE, Kageyama R, Ponzetto C (2006) High levels of Cre expression in neuronal progenitors cause defects in brain development leading to microencephaly and hydrocephaly. J Neurosci 26:9593-9602.
12. Ganat YM, Silbereis J, Cave C, Ngu H, Anderson GM, Ohkubo Y, Ment LR, Vaccarino FM (2006) Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 26:8609-8621.
13. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7:1233-1241.
14. Graham V, Khudyakov J, Ellis P, Pevny L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749-765.
15. Harburg GC, Hall FS, Harrist AV, Sora I, Uhl GR, Eisch AJ (2007) Knockout of the mu opioid receptor enhances the survival of adult-generated hippocampal granule cell neurons. Neuroscience 144:77-87.
16. Hattiangady B, Shetty AK (2007) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging, in press.
17. Imayoshi I, Ohtsuka T, Metzger D, Chambon P, Kageyama R (2006) Temporal regulation of Cre recombinase activity in neural stem cells. Genesis 44:233-238.
18. Indra AK, Warot X, Brocard J, Bornert JM, Xiao JH, Chambon P, Metzger D (1999) Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res 27:4324-4327.
19. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391-399.
20. Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27:447-452.
21. Komitova M, Eriksson PS (2004) Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett 369:24-27.
22. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, Yamaguchi M, Kempermann G (2003) Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 467:455-463.
23. 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.
24. Lemasson M, Saghatelyan A, Olivo-Marin JC, Lledo PM (2005) Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J Neurosci 25:6816-6825.
25. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145-1148.
26. Mandairon N, Sacquet J, Jourdan F, Didier A (2006) Long-term fate and distribution of newborn cells in the adult mouse olfactory bulb: influences of olfactory deprivation. Neuroscience 141:443-451.
27. Mandyam CD, Norris RD, Eisch AJ (2004) Chronic morphine induces premature mitosis of proliferating cells in the adult mouse subgranular zone. J Neurosci Res 76:783-794.
28. Mandyam CD, Harburg GC, Eisch AJ (2007) Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone. Neuroscience 146:108-122.
29. Merson TD, Dixon MP, Collin C, Rietze RL, Bartlett PF, Thomas T, Voss AK (2006) The transcriptional coactivator Querkopf controls adult neurogenesis. J Neurosci 26:11359-11370.
30. Ming GL, Song H (2005) Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250.
31. Mirich JM, Williams NC, Berlau DJ, Brunjes PC (2002) Comparative study of aging in the mouse olfactory bulb. J Comp Neurol 454:361-372.
32. Mori T, Tanaka K, Buffo A, Wurst W, Kuhn R, Gotz M (2006) Inducible gene deletion in astroglia and radial glia - a valuable tool for functional and lineage analysis. Glia 54:21-34.
33. Ninkovic J, Mori T, Gotz M (2007) Distinct modes of neuron addition in adult mouse neurogenesis. J Neurosci 27:10906-10911.
34. Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G, Puche AC (2007) Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825-836.
35. Pevny L, Rao MS (2003) The stem-cell menagerie. Trends Neurosci 26:351-359.
36. Rao MS, Hattiangady B, Shetty AK (2006) The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5:545-558.
37. 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.
38. 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.
39. 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.
40. Soriano P (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 21:70-71.
41. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-1034.
42. Wiese C, Rolletschek A, Kania G, Blyszczuk P, Tarasov KV, Tarasova Y, Wersto RP, Boheler KR, Wobus AM (2004) Nestin expression-a property of multi-lineage progenitor cells? Cell Mol Life Sci 61:2510-2522.
43. Yamaguchi M, Saito H, Suzuki M, Mori K (2000) Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. NeuroReport 11:1991-1996.
44. Yu TS, Dandekar M, Monteggia LM, Parada LF, Kernie SG (2005) Temporally regulated expression of Cre recombinase in neural stem cells. Genesis 41:147-153.
45. Zimmerman L, Parr B, Lendahl U, Cunningham M, McKay R, Gavin B, Mann J, Vassileva G, McMahon A (1994) Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 12:11-24.