Gsx2 controls region-specific activation of neural stem cells and injury-induced neurogenesis in the adult subventricular zone

Genes and Development

Volumn 27, Issue 11, 2013, Pages 1272-1287

  López Juárez, Alejandro ^a   Howard, Jennifer ^a   Ullom, Kristy ^a   Howard, Lindsey ^a   Grande, Andrew ^a,b,c   Pardo, Andrea ^a,d   Waclaw, Ronald ^a,b   Sun, Yu Yo ^a,e   Yang, Dianer ^a,e   Kuan, Chia Yi ^a,b,e   Campbell, Kenneth ^a,b   Nakafuku, Masato ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adult neurogenesis; Injury; Regional identity; Stem cell; Stroke

Indexed keywords

DLX2 PROTEIN; DOUBLECORTIN; GSX2 PROTEIN; KI 67 ANTIGEN; NKX2.1 PROTEIN; PBX3 PROTEIN; SP8 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CELL ACTIVATION; CELL PROLIFERATION; DENTATE GYRUS; GAIN OF FUNCTION MUTATION; HIPPOCAMPUS; LOSS OF FUNCTION MUTATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL NICHE; SUBVENTRICULAR ZONE;

EID: 84878883225     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.217539.113     Document Type: Article

References (59)

1. Adhami F, Liao G, Morozov YM, Schloemer A, Schmithorst VJ, Lorenz JN, Dunn RS, Vorhees CV, Wills-Karp M, Degen JL, et al. 2006. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am J Pathol 169: 566-583.
2. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL. 2002. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129: 4753-4761.
3. Balordi F, Fishell G. 2007. Mosaic removal of hedgehog signaling in the adult SVZ reveals that the residual wild-type stem cells have a limited capacity for self-renewal. J Neurosci 27: 14248-14259.
4. Basak O, Giachino C, Fiorini E, Macdonald HR, Taylor V. 2012. Neurogenic subventricular zone stem/progenitor cells are Notch1-dependent in their active but not quiescent state. J Neurosci 32: 5654-5666.
5. Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie DC, et al. 2010. In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7: 744-758.
6. Bonaguidi MA, Wheeler MA, Shapiro JS, Stadel RP, Sun GJ, Ming GL, Song H. 2011. In vivo clonal analysis reveals selfrenewing and multipotent adult neural stem cell characteristics. Cell 145: 1142-1155.
7. Brill MS, Snapyan M, Wohlfrom H, Ninkovic J, Jawerka M, Mastick GS, Ashery-Padan R, Saghatelyan A, Berninger B, Götz M. 2008. A dlx2- and pax6-dependent transcriptional code for periglomerular neuron specification in the adult olfactory bulb. J Neurosci 28: 6439-6452.
8. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascon S, Erdelyi F, Szabo G, et al. 2009. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12: 1524-1533.
9. Briñón JG, Martinez-Guijarro FJ, Bravo IG, Arevalo R, Crespo C, Okazaki K, Hidaka H, Aijon J, Alonso JR. 1999. Coexpression of neurocalcin with other calcium-binding proteins in the rat main olfactory bulb. J Comp Neurol 407: 404-414.
10. 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.
11. Fuentealba LC, Obernier K, Alvarez-Buylla A. 2012. Adult neural stem cells bridge their niche. Cell Stem Cell 10: 698-708.
12. Giachino C, Taylor V. 2009. Lineage analysis of quiescent regenerative stem cells in the adult brain by genetic labelling reveals spatially restricted neurogenic niches in the olfactory bulb. Eur J Neurosci 30: 9-24.
13. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, et al. 2003. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925.
14. Gritti A, Bonfanti L, Doetsch F, Caille I, Alvarez-Buylla A, Lim DA, Galli R, Verdugo JM, Herrera DG, Vescovi AL. 2002. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 22: 437-445.
15. Hack MA, Saghatelyan A, de Chevigny A, Pfeifer A, Ashery- Padan R, Lledo PM, Götz M. 2005. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 8: 865-872.
16. Hansson O, Petersen A, Leist M, Nicotera P, Castilho RF, Brundin P. 1999. Transgenic mice expressing a Huntington's disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity. Proc Natl Acad Sci 96: 8727-8732.
17. Ihrie RA, Shah JK, Harwell CC, Levine JH, Guinto CD, Lezameta M, Kriegstein AR, Alvarez-Buylla A. 2011. Persistent sonic hedgehog signaling in adult brain determines neural stem cell positional identity. Neuron 71: 250-262.
18. Kaslin J, Ganz J, Brand M. 2008. Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363: 101-122.
19. Kim EJ, Ables JL, Dickel LK, Eisch AJ, Johnson JE. 2011. Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS ONE 6: e18472.
20. Kizil C, Kyritsis N, Dudczig S, Kroehne V, Freudenreich D, Kaslin J, Brand M. 2012. Regenerative neurogenesis from neural progenitor cells requires injury-induced expression of gata3. Dev Cell 23: 1230-1237.
21. 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.
22. Kokovay E, Wang Y, Kusek G, Wurster R, Lederman P, Lowry N, Shen Q, Temple S. 2012. VCAM1 is essential to maintain the structure of the SVZ niche and acts as an environmental sensor to regulate SVZ lineage progression. Cell Stem Cell 11: 220-230.
23. Kriks S, Lanuza GM, Mizuguchi R, Nakafuku M, Goulding M. 2005. Gsh2 is required for the repression of Ngn1 and specification of dorsal interneuron fate in the spinal cord. Development 132: 2991-3002.
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. Lledo PM, Merkle FT, Alvarez-Buylla A. 2008. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31: 392-400.
26. Lyons GE, Micales BK, Schwarz J, Martin JF, Olson EN. 1995. Expression of mef2 genes in the mouse central nervous system suggests a role in neuronal maturation. J Neurosci 15: 5727-5738.
27. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC. 2004. Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24: 1726-1733.
28. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317: 381-384.
29. Ming GL, Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28: 223-250.
30. Mirzadeh Z, Merkle FT, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2008. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 3: 265-278.
31. Mirzadeh Z, Doetsch F, Sawamoto K, Wichterle H, Alvarez-Buylla A. 2010. The subventricular zone en-face: Wholemount staining and ependymal flow. J Vis Exp 39: e1938.
32. Mori T, Tanaka K, Buffo A, Wurst W, Kuhn R, Götz M. 2006. Inducible gene deletion in astroglia and radial glia-a valuable tool for functional and lineage analysis. Glia 54: 21-34.
33. Morshead CM, Reynolds BA, Craig CG, McBurney MW, Staines WA, Morassutti D, Weiss S, van der Kooy D. 1994. Neural stem cells in the adult mammalian forebrain: A relatively quiescent subpopulation of subependymal cells. Neuron 13: 1071-1082.
34. Nakafuku M, Grande A. 2013. Neurogenesis in the damaged mammalian brain. In Patterning and cell type specification in the developing CNS and PNS: comprehensive developmental neuroscience (ed. Rubenstein JLR, Rakic P). Elsevier, Maryland Heights, MO (in press).
35. Nakamura T, Colbert MC, Robbins J. 2006. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res 98: 1547-1554.
36. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M. 2002. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110: 429-441.
37. Ninkovic J, Götz M. 2007. Signaling in adult neurogenesis: From stem cell niche to neuronal networks. Curr Opin Neurobiol 17: 338-344.
38. 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.
39. Pastrana E, Cheng LC, Doetsch F. 2009. Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci 106: 6387-6392.
40. Pei Z, Wang B, Chen G, Nagao M, Nakafuku M, Campbell K. 2011. Homeobox genes Gsx1 and Gsx2 differentially regulate telencephalic progenitor maturation. Proc Natl Acad Sci 108: 1675-1680.
41. Ponti G, Obernier K, Guinto C, Jose L, Bonfanti L, Alvarez- Buylla A. 2013. Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc Natl Acad Sci 110: E1045-E1054.
42. Puelles L, Rubenstein JL. 2003. Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26: 469-476.
43. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. 2008. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3: 289-300.
44. Shook BA, Manz DH, Peters JJ, Kang S, Conover JC. 2012. Spatiotemporal changes to the subventricular zone stem cell pool through aging. J Neurosci 32: 6947-6956.
45. Simons BD, Clevers H. 2011. Strategies for homeostatic stem cell self-renewal in adult tissues. Cell 145: 851-862.
46. Song J, Zhong C, Bonaguidi MA, Sun GJ, Hsu D, Gu Y, Meletis K, Huang ZJ, Ge S, Enikolopov G, et al. 2012. Neuronal circuitry mechanism regulating adult quiescent neural stemcell fate decision. Nature 489: 150-154.
47. Stenman J, Toresson H, Campbell K. 2003. Identification of two distinct progenitor populations in the lateral ganglionic eminence: Implications for striatal and olfactory bulb neurogenesis. J Neurosci 23: 167-174.
48. Szucsik JC, Witte DP, Li H, Pixley SK, Small KM, Potter SS. 1997. Altered forebrain and hindbrain development in mice mutant for the Gsh-2 homeobox gene. Dev Biol 191: 230-242.
49. Tavazoie M, Van der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3: 279-288.
50. Toresson H, Campbell K. 2001. A role for Gsh1 in the developing striatum and olfactory bulb of Gsh2 mutant mice. Development 128: 4769-4780.
51. Toresson H, Potter SS, Campbell K. 2000. Genetic control of dorsal-ventral identity in the telencephalon: Opposing roles for Pax6 and Gsh2. Development 127: 4361-4371.
52. Waclaw RR, Allen ZJ 2nd, Bell SM, Erdelyi F, Szabo G, Potter SS, Campbell K. 2006. The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49: 503-516.
53. Waclaw RR, Wang B, Pei Z, Ehrman LA, Campbell K. 2009. Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 63: 451-465.
54. Wang L, Sharma K, Deng HX, Siddique T, Grisotti G, Liu E, Roos RP. 2008. Restricted expression of mutant SOD1 in spinal motor neurons and interneurons induces motor neuron pathology. Neurobiol Dis 29: 400-408.
55. Wang B, Waclaw RR, Allen ZJ 2nd, Guillemot F, Campbell K. 2009. Ascl1 is a required downstream effector of Gsx gene function in the embryonic mouse telencephalon. Neural Dev 4: 5.
56. Young KM, Fogarty M, Kessaris N, Richardson WD. 2007. 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.
57. Yun K, Potter S, Rubenstein JL. 2001. Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 128: 193-205.
58. Yun K, Garel S, Fischman S, Rubenstein JL. 2003. Patterning of the lateral ganglionic eminence by the Gsh1 and Gsh2 homeobox genes regulates striatal and olfactory bulb histogenesis and the growth of axons through the basal ganglia. J Comp Neurol 461: 151-165.
59. Zhao C, Deng W, Gage FH. 2008. Mechanisms and functional implications of adult neurogenesis. Cell 132: 645-660.