Brain-derived neurotrophic factor participates in determination of neuronal laminar fate in the developing mouse cerebral cortex

Journal of Neuroscience

Volumn 26, Issue 51, 2006, Pages 13218-13230

  Fukumitsu, Hidefumi ^a   Ohtsuka, Masanari ^a   Murai, Rina ^a   Nakamura, Hiroyuki ^b   Itoh, Kazuo ^b   Furukawa, Shoei ^a  

^a GIFU PHARMACEUTICAL UNIVERSITY   (Japan)

^b GIFU UNIVERSITY   (Japan)

Author keywords

Brain derived neurotrophic factor (BDNF); Interkinetic migration; Laminar fate; Neocortex; Neurotrophin; Precocious neurogenesis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR ANTIBODY; PROTEIN ANTIBODY; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN VENTRICLE; CELL CYCLE S PHASE; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; STEM CELL; TELENCEPHALON;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL MOVEMENT; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INJECTIONS, INTRAVENTRICULAR; MICE; NEURONS; PREGNANCY; STEM CELLS;

EID: 33845770755     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4251-06.2006     Document Type: Article

References (55)

1. Angenvine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766-768.
2. Baquet ZC, Gorski JA, Jones KR (2004) Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J Neurosci 24:4250-4258.
3. Barnabe-Heider F, Miller FD (2003) Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J Neurosci 23:5149-5160.
4. Bayer SA, Altman J (1991) Neocortical development. New York: Raven.
5. Becker-Andre M, Wiesenberg I, Schaeren-Wiemers N, Andre E, Missbach M, Saurat JH, Carlberg C (1994) Pineal gland hormone melatonin binds and activates an orphan of the nuclear receptor superfamily. J Biol Chem 269:28531-28534.
6. Behar TN, Dugich-Djordjevic MM, Li Y-X, Ma W, Somogyi R, Wen X, Brown E, Scott C, McKay RDG, Barker JL (1997) Neurotrophins stimulate chemotaxis of embryonic cortical neurons. Eur J Neurosci 9:2561-2570.
7. Bohner AP, Akers RM, McConnell SK (1997) Induction of deep layer cortical neurons in vitro. Development 124:915-923.
8. Brunstrom JE, Gray-Swain MR, Osborne PA, Pearlman AL (1997) Neuronal heterotopias in the developing cerebral cortex produced by neurotrophin-4. Neuron 18:505-517.
9. Caviness Jr VS, Takahashi T, Nowakowski RS (1995) Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci 18:379-383.
10. Caviness Jr VS, Goto T, Tarui T, Takahashi T, Bhide PG, Nowakowski RS (2003) Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. Cereb Cortex 13:592-598.
11. Desai AR, McConnell SK (2000) Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127:2863-2872.
12. Dyer MA, Cepko CL (2001) Regulating proliferation during retinal development. Nat Rev Neurosci 2:333-342.
13. Ferland RJ, Cherry TJ, Preware PO, Morrisey EE, Walsh CA (2003) Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J Comp Neurol 460:266-279.
14. Frantz GD, McConnell SK (1996) Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17:55-61.
15. Fujita S (1963) The matrix cell and cytogenesis in the developing central nervous system. J Comp Neurol 120:37-42.
16. Fukumitsu H, Furukawa Y, Tsusaka M, Kinukawa H, Nitta A, Nomoto H, Mima T, Furukawa S (1998) Simultaneous expression of brain-derived neurotrophic factor and neurotrophin-3 in Cajal-Retzius, subplate and ventricular progenitor cells during early development stages of the rat cerebral cortex. Neuroscience 84:115-127.
17. Gilbert CD, Kelly JP (1975) The projections of cells in different layers of the cat's visual cortex. J Comp Neurol 163:81-105.
18. Gilbert CD, Wiesell TN (1985) Intrinsic connectivity and receptive field properties in visual cortex. Vision Res 25:365-374.
19. Gorski JA, Zeiler SR, Tamowski S, Jones KR (2003) Brain-derived neurotrophic factor is required for maintenance of cortical dendrites. J Neurosci 23:6856-6865.
20. Goto T, Mitsuhashi T, Takahashi T (2004) Altered patterns of neuron production in the p27kip knockout mouse. Dev Neurosci 26:208-217.
21. Gotz M, Stoykova A, Gruss P (1998) Pax6 controls radial glia differentiation in the cerebral cortex Neuron 21:1031-1044.
22. Hatta T, Morishima K, Nabeshima K, Taga T, Otani H (2002) The role of gp130 in cerebral cortical development: in vivo functional analysis in a mouse exo utero system. J Neurosci 22:5516-5524.
23. Hermans-Borgmeyer I, Hampe W, Schinke B, Methner A, Nykjaer A, Susens U, Fenger U, Herbarth B, Schaller HC (1998) Unique expression pattern of a novel mosaic receptor in the developing cerebral cortex. Mech Dev 70:65-76.
24. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353-366.
25. Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C (2003) Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25:139-151.
26. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24:677-736.
27. Ito H, Nakajima A, Nomoto H, Furukawa S (2003) Neurotrophins facilitate neuronal differentiation of cultured neural stem cells via induction of mRNA expression of basic helix-loop-helix transcription factors Mash1 and Math1. J Neurosci Res 71:648-658.
28. Jones KR, Farinas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
29. Kanegae Y, Lee G, Sato Y, Tanaka M, Nakai M, Sakaki T, Sugano S, Saito I (1995) Efficient gene activation in mammalian cells by using recombinant adenovirus expressing site-specific Cre recombinase. Nucleic Acid Res 23:3816-3821.
30. Lu B (2003) BDNF and activity-dependent synaptic function. Learn Mem 10:86-98.
31. Lukaszewicz A, Savatier P, Cortay V, Kennedy H, Dehay C (2002) Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J Neurosci 22:6610-6622.
32. Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD (1990) NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 5:501-509.
33. McConnell SK, Kaznowski CE (1991) Cell cycle dependence of laminar determination in developing neocortex. Science 254:282-285.
34. McEvilly RJ, de Diaz MO, Schonemann MD, Hooshmand F, Rosenfeld MG (2002) Transcriptional regulation of cortical neuron migration by POU domain factors. Science 295:1528-1532.
35. Medina DL, Sciarretta C, Calella AM, Von Bohlen Und Halbach O, Unsicker K, Minichiello L (2004) TrkB regulates neocortex formation through the Shc/PLCγ-mediated control of neuronal migration. EMBO J 23:3803-3814.
36. Miyama S, Takahashi T, Nowakowski RS, Caviness Jr VS (1997) A gradient in the duration of the G1 phase in the murine neocortical proliferative epithelium. Cereb Cortex 7:678-689.
37. Morrison SJ (2001) Neuronal potential and lineage determination by neural stem cells. Curr Opin Cell Biol 13:666-672.
38. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479:168-180.
39. Nitta A, Ohmiya M, Jin-nouchi T, Sometani A, Asami T, Kinukawa H, Fukumitsu H, Nomoto H, Furukawa S (1999) Endogenous neurotrophin-3 is retrogradely transported in the rat sciatic nerve. Neuroscience 88:679-685.
40. Nowakowski RS, Lewin SB, Miller MW (1989) Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 18:311-318.
41. Ohmiya M, Shudai T, Nitta A, Nomoto H, Furukawa Y, Furukawa S (2002) Brain-derived neurotrophic factor alters cell migration of particular progenitors in the developing mouse cerebral cortex. Neurosci Lett 317:21-24.
42. Paxinos G, Franklin K (2001) The mouse brain in stereotaxic coordinates, Ed 2. London: Academic.
43. Polleux F, Dehay C, Kennedy H (1998) Neurogenesis and commitment of corticospinal neurons in reeler. J Neurosci 18:9910-9923.
44. Rakic P (1974) Neuron in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425-427.
45. Rice DS, Curran T (1999) Mutant mice with scrambled brains: understanding the signaling pathways that control cell positioning in the CNS. Genes Dev 13:2758-2773.
46. Ringstedt T, Linnarsson S, Wagner J, Lendahl U, Kokaia Z, Arenas E, Ernfors P, Ibanez CF (1998) BDNFregulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron 21:305-315.
47. Ross SE, Greenberg ME, Stiles CD (2003) Basic helix-loop-helix factors in cortical development. Neuron 39:13-25.
48. Roy K, Kuznicki K, Wu Q, Sun Z, Bock D, Schutz G, Vranich N, Monaghan AP (2004) The Tlx gene regulates the timing of neurogenesis in the cortex. J Neurosci 24:8333-8345.
49. Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, Klenin N, Brown C, Langevin LM, Seibt J, Tang H, Cunningham JM, Dyck R, Walsh C, Campbell K, Polleux F, Guillemot F (2004) Sequential phases of cortical specification involve neurogenin-dependent and -independent pathways. EMBO J 23:2892-2902.
50. Soriano E, del Rio JA (2005) The cells of Cajal-Retzius: still a mystery one century after. Neuron 46:389-394.
51. Takahashi T, Nowakowski RS, Caviness Jr VS (1995) The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 15:6046-6057.
52. Takahashi T, Nowakowski RS, Caviness Jr VS (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16:6183-6196.
53. Tarabykin V, Stoykova A, Usman N, Gruss P (2001) Cortical upper layer neurons derived from subventricular zone as indicated by Svet1 gene expression. Development 128:1983-1993.
54. Tole S, Chirstian C, Grove EA (1997) Early specification and autonomous development of cortical fields in the mouse hippocampus. Development 124:4959-4970.
55. Warren N, Price DJ (1997) Roles of Pax-6 in murine diencephalic development. Development 124:1573-1582.