Conditional ablation of Tbr2 results in abnormal development of the olfactory bulbs and subventricular zone-rostral migratory stream

Developmental Dynamics

Volumn 243, Issue 3, 2014, Pages 440-450

  Kahoud, Robert J ^a,b,d   Elsen, Gina E ^b,e   Hevner, Robert F ^b,c   Hodge, Rebecca D ^b,c  

^a SEATTLE CHILDREN S HOSPITAL   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d MAYO CLINIC   (United States)

^e UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Neural development; Olfactory bulbs; Rostral migratory stream; Subventricular zone; Tbr2

Indexed keywords

NEURAL DEVELOPMENT; OLFACTORY BULBS; ROSTRAL MIGRATORY STREAM; SUBVENTRICULAR ZONE; TBR2;

ANIMALS; GENE DELETION; MICE; MICE, MUTANT STRAINS; MORPHOGENESIS; NEURAL STEM CELLS; OLFACTORY BULB; OLFACTORY RECEPTOR NEURONS; T-BOX DOMAIN PROTEINS;

EID: 84894280069     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.24090     Document Type: Article

References (42)

1. Allen ZJ, Waclaw RR, Colbert MC, Campbell K. 2007. Molecular identity of olfactory bulb interneurons: transcriptional codes of periglomerular neuron subtypes. J Mol Hist 38:517-525.
2. Arnold SJ, Huang G-J, Cheung AF, Era T, Nishikawa S-I, Bikoff EK, Molnar Z, Robertson EJ, Groszer M. 2008. The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev 22:2479-2484.
3. Batista-Brito R, Close J, Machold R, Fishell G. 2008. The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 28:3966-3975.
4. Blanchart A, De Carlos JA, López-Mascaraque L. 2006. Time frame of mitral cell development in the mice olfactory bulb. J Comp Neurol 496:529-543.
5. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, Yang R, Lepier A, Gascón S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner RF, Raineteau O, Götz M. 2009. Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12:1524-1533.
6. Bulfone A, Martinez S, Marigo V, Campanella M, Basile A, Quaderi N, Gattuso C, Rubenstein JL, Ballabio A. 1999. Expression pattern of the Tbr2 (Eomesodermin) gene during mouse and chick brain development. Mech Dev 84:133-138.
7. Couillard-Despres S, Winner B, Schaubeck S, Aigner R, Vroemen M, Weidner N, Bogdahn U, Winkler J, Kuhn H-G, Aigner L. 2005. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21:1-14.
8. De Marchis S, Bovetti S, Carletti B, Hsieh Y-C, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F. 2007. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657-664.
9. Elsen GE, Hodge RD, Bedogni F, Daza RAM, Nelson BR, Shiba N, Reiner SL, Hevner RF. 2013. The protomap is propagated to cortical plate neurons through an Eomes-dependent intermediate map. Proc Natl Acad Sci USA 110:4081-4086.
10. Englund C, Fink A, Lau C, Pham D, Daza RAM, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25:247-251.
11. Faedo A, Ficara F, Ghiani M, Aiuti A, Rubenstein JLR, Bulfone A. 2002. Developmental expression of the T-box transcription factor T-bet/Tbx21 during mouse embryogenesis. Mech Dev 116:157-160.
12. Gong Q, Shipley MT. 1995. Evidence that pioneer olfactory axons regulate telencephalon cell cycle kinetics to induce the formation of the olfactory bulb. Neuron 14:91-101.
13. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L. 1988. The new stereological tools - disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
14. Hack I, Bancila M, Loulier K, Carroll P, Cremer H. 2002. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat Neurosci 5:939-945.
15. Hellwig S, Hack I, Zucker B, Brunne B, Junghans D. 2012. Reelin together with ApoER2 regulates interneuron migration in the olfactory bulb. PLoS ONE 7:e50646.
16. Hodge RD, Hevner RF. 2011 Expression and actions of transcription factors in adult hippocampal neurogenesis. Dev Neurobiol 71:680-689.
17. Hodge RD, Kowalczyk TD, Wolf S, Encinas J, Rippey C, Enikolopov G, Kempermann G, Hevner RF. 2008. Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J Neurosci 28:3707-3717.
18. Hodge RD, Kahoud RJ, Hevner RF. 2012a. Transcriptional control of glutamatergic differentiation during adult neurogenesis. Cell Mol Life Sci 69:2125-2134.
19. Hodge RD, Nelson BR, Kahoud RJ, Yang R, Mussar KE, Reiner SL, Hevner RF. 2012b. Tbr2 Is essential for hippocampal lineage progression from neural stem cells to intermediate progenitors and neurons. J Neurosci 32:6275-6287.
20. Hodge RD, Garcia AJ, Elsen GE, Nelson BR, Mussar KE, Reiner SL, Ramirez J-M, Hevner RF. 2013. Tbr2 expression in Cajal-Retzius cells and intermediate neuronal progenitors is required for morphogenesis of the Dentate Gyrus. J Neurosci 33:4165-4180.
21. Hsieh J. 2012. Orchestrating transcriptional control of adult neurogenesis. Genes Dev 26:1010-1021.
22. Imamura F, Ayoub AE, Rakic P, Greer CA. 2011. Timing of neurogenesis is a determinant of olfactory circuitry. Nat Neurosci 14:331-337.
23. 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.
24. Intlekofer AM, Banerjee A, Takemoto N, Gordon SM, DeJong CS, Shin H, Hunter CA, Wherry EJ, Lindsten T, Reiner SL. 2008. Anomalous type 17 response to viral infection by CD8+ T Cells lacking T-bet and Eomesodermin. Science 321:408-411.
25. Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JLR, 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.
26. Lledo P-M, Saghatelyan A. 2005. Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience. Trends Neurosci 28:248-254.
27. Lledo P, Merkle F, Alvarezbuylla A. 2008. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 31:392-400.
28. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317:381-384.
29. Mizuguchi R, Naritsuka H, Mori K, Yoshihara Y. 2012. Tbr2 deficiency in mitral and tufted cells disrupts excitatory-inhibitory balance of neural circuitry in the mouse olfactory bulb. J Neurosci 32:8831-8844.
30. Pencea V, Luskin MB. 2003. Prenatal development of the rodent rostral migratory stream. J Comp Neurol 463:402-418.
31. Peretto P, Giachino C, Aimar P, Fasolo A, Bonfanti L. 2005. Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 487:407-427.
32. Roybon L, Deierborg T, Brundin P, Li J-Y. 2009. Involvement of Ngn2, Tbr and NeuroD proteins during postnatal olfactory bulb neurogenesis. Eur J Neurosci 29:232-243.
33. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ. 2000. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:95-99.
34. Seri B, García-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.
35. Sessa A, Mao C, Hadjantonakis A, Klein W, Broccoli V. 2008. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60:56-69.
36. Sessa A, Mao C-A, Colasante G, Nini A, Klein WH, Broccoli V. 2010. Tbr2-positive intermediate (basal) neuronal progenitors safeguard cerebral cortex expansion by controlling amplification of pallial glutamatergic neurons and attraction of subpallial GABAergic interneurons. Genes Dev 24:1816-1826.
37. Shaker T, Dennis D, Kurrasch DM, Schuurmans C. 2012. Neurog1 and Neurog2 coordinately regulate development of the olfactory system. Neural Dev 7:28.
38. Takashima Y, Era T, Nakao K, Kondo S, Kasuga M, Smith AG, Nishikawa S-I. 2007. Neuroepithelial cells supply an initial transient wave of MSC differentiation. Cell 129:1377-1388.
39. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schütz G. 1999. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99-103.
40. Walker TL, Yasuda T, Adams DJ, Bartlett PF. 2007. The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 27:3734-3742.
41. Whitman MC, Greer CA. 2009. Adult neurogenesis and the olfactory system. Prog Neurobiol 2:162-175.
42. Winpenny E, Lebel-Potter M, Fernandez ME, Brill MS, Gotz M, Guillemot F, Raineteau O. 2011. Sequential generation of olfactory bulb Glutamatergic neurons by Neurog2-expressing precursor cells. Neural Dev 6:12.