Foxg1 haploinsufficiency reduces the population of cortical intermediate progenitor cells: effect of increased p21 expression

Cerebral Cortex

Volumn 18, Issue 8, 2008, Pages 1865-1875

  Siegenthaler, Julie A ^a,b,c   Tremper Wells, Barbara A ^a,b,c   Miller, Michael W ^a,b,c,d  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b BINGHAMTON UNIVERSITY   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

^d SYRACUSE VA MEDICAL CENTER   (United States)

Author keywords

Cell cycle; Ki 67; p27; Progenitor cells; Subventricular zone; Ventricular zone

Indexed keywords

FOXG1 PROTEIN; KI 67 ANTIGEN; PROTEIN P21; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CYCLE; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FETUS; FOREBRAIN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INTERMEDIATE PROGENITOR CELL; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEM CELL; SUBVENTRICULAR ZONE; WILD TYPE;

ANIMALS; CELL CYCLE; CELL PROLIFERATION; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH INHIBITORS; HAPLOTYPES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PREGNANCY; STEM CELLS; UP-REGULATION;

EID: 47649086901     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhm209     Document Type: Article

References (56)

1. Al-Ghoul WM, Miller MW. 1989. Transient expression of Alz-50-immunoreactivity in developing rat neocortex: a marker for naturally occurring neuronal death? Brain Res. 481:361-367.
2. Alvarez-Buylla A, Garcia-Verdugo JM. 2002. Neurogenesis in adult subventricular zone. J Neurosci. 3:629-634.
3. Angevine JB Jr, Sidman RL. 1961. Autoradiographic study of cell migration during histiogenesis of cerebral cortex in the mouse. Nature. 192:766-768.
4. Brückner G, Marěs V, Biesold D. 1976. Neurogenesis in the visual system of the rat. An autoradiographic investigation. J Comp Neurol. 166:245-255.
5. Calegari F, Haubensak W, Haffner C, Huttner WB. 2005. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci. 25:6533-6538.
6. 3H]thymidine autoradiography. Brain Res. 256:293-302.
7. Caviness VS Jr, 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.
8. Caviness VS Jr, Takahashi T, Nowakowski RS. 1995. Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. Trends Neurosci. 18:379-383.
9. Delalle I, Takahashi T, Nowakowski RS, Tsai LH, Caviness VS Jr. 1999. Cyclin E-p27 opposition and regulation of the G1 phase of the cell cycle in the murine neocortical PVE: a quantitative analysis of mRNA in situ hybridization. Cereb Cortex. 9:824-832.
10. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1997. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 13:5046-5061.
11. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. 1999. Regeneration of a germinal layer in the adult mammalian brain. Proc Natl Acad Sci USA. 20:11619-11624.
12. Dou C, Lee J, Liu B, Liu F, Massagué J, Xuan S, Lai E. 2000. BF-1 interferes with transforming growth factor β signaling by associating with Smad partners. Mol Cell Biol. 20:6201-6211.
13. Dou CL, Li S, Lai E. 1999. Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres. Cereb Cortex. 9:543-550.
14. Eagleson KL, Schlueter McFadyen-Ketchum LJ, Ahrens ET, Mills PH, Does MD, Nickols J, Levitt P. 2007. Disruption of Foxg1 expression by knock-in of Cre recombinase: effects on the development of the mouse telencephalon. Neuroscience. 148:385-399.
15. Englund C, Fink A, Lau C, Pham D, Daza RA, 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.
16. Ferrere A, Vitalis T, Gingras H, Gaspar P, Cases O. 2006. Expression of Cux-1 and Cux-2 in the developing somatosensory cortex of normal and barrel-defective mice. Anat Rec A Discov Mol Cell Evol Biol. 288:158-165.
17. Forni PE, Scuoppo C, Imayoshi I, Taulli R, Dastrù W, Sala V, Betz UA, Muzzi P, Martinuzzi D, Vercelli AE, et al. 2006. High levels of Cre expression in neuronal progenitors cause defects in brain development leading to microencephaly and hydrocephaly. J Neurosci. 26:9593-9602.
18. Gomes WA, Mehler MF, Kessler JA. 2003. Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglia lineage commitment. Dev Biol. 255:164-177.
19. Goto T, Mitsuhashi T, Takahashi T. 2004. Altered patterns of neuron production in the p27 knockout mouse. Dev Neurosci. 26:208-217.
20. Hanashima C, Li SC, Shen L, Lai E, Fishell G. 2004. Foxg1 suppresses early cortical cell fate. Science. 303:56-59.
21. Hanashima C, Shen L, Li SC, Lai E. 2002. Brain factor-1 controls the proliferation and differentiation of neocortical progenitor cells through independent mechanisms. J Neurosci. 22:6526-6536.
22. Haubensak W, Attardo A, Denk W, Huttner WB. 2004. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA. 101:3196-3201.
23. Hebert JM, McConnell SK. 2000. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev Biol. 222:296-306.
24. Iacopetti P, Michelini M, Stuckman I, Oback B, Aaku-Saraste E, Huttner WB. 1999. Expression of the antiproliferative gene Tis21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc Natl Acad Sci USA. 96:4639-4644.
25. Malatesta P, Hartfuss E, Gotz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development. 127:5253-5263.
26. Martens DJ, Tropepe V, van Der Kooy D. 2000. Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J Neurosci. 20:1085-1095.
27. Martinez-Cerdeno V, Noctor SC, Kriegstein AR. 2006. The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb Cortex. 16 (Suppl 1):i152-i161.
28. Martynoga B, Morrison H, Price DJ, Mason JO. 2005. Foxg1 is required for specification of ventral telencephalon and region-specific regulation of dorsal telencephalic precursor proliferation and apoptosis. Dev Biol. 283:113-127.
29. Miller MW. 1985. Co-generation of projection and local circuit neurons in neocortex. Dev Brain Res. 23:187-192.
30. Miller MW. 1988a. Effect of prenatal exposure to ethanol on the development of cerebral cortex: 1. Neuronal generation. Alcohol Clin Exp Res. 12:440-449.
31. Miller MW. 1988b. Development of projection and local circuit neurons in cerebral cortex. In: Peters A, Jones EG, editors. Cerebral Cortex. Vol. 7. Development and Maturation of Cerebral Cortex. New York: Plenum. p. 133-175.
32. Miller MW. 1989. Effects of prenatal exposure to ethanol on neocortical development: II. Cell proliferation in the ventricular and subventricular zones of the rat. J Comp Neurol. 287:326-338.
33. Miller MW. 1992. Effects of prenatal exposure to ethanol on cell proliferation and neuronal migration. In: Miller MW, editor. Development of the central nervous system: effects of alcohol and opiates. New York: Wiley-Liss. p. 47-69.
34. Miller MW. 1996. Limited ethanol exposure selectively alters the proliferation of precursor cells in the cerebral cortex. Alcohol Clin Exp Res. 20:139-143.
35. Miller MW, Kuhn PE. 1995. Cell cycle kinetics in fetal rat cerebral cortex: effects of prenatal treatment with ethanol assessed by a cumulative labeling technique with flow cytometry. Alcohol Clin Exp Res. 19:233-237.
36. Miller MW, Nowakowski RS. 1991. Effect of prenatal exposure t ethanol on the cell cycle kinetics and growth fraction in the proliferative zones of fetal rat cerebral cortex. Alcohol Clin Exp Res. 15:229-232.
37. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M. 2004. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development. 131:3133-3145.
38. Muzio L, Mallamaci A. 2005. Foxg1 confines Cajal-Retzius neuronogenesis and hippocampal morphogenesis to the dorsomedial pallium. J Neurosci. 25:4435-4441.
39. kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20:1511-1524.
40. Nguyen L, Besson A, Roberts J, Guillemot F. 2006. Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle. 5:2314-2318.
41. 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.
42. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kreigstein AR. 2001. Neurons derived from radial glial cells establish radial units in the neocortex. Nature. 409:714-720.
43. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 7:136-144.
44. Rodriguez C, Huang LJ, Son JK, McKee A, Xiao Z, Lodish HF. 2001. Functional cloning of the proto-oncogene brain factor-1 (BF-1) as a Smad-binding antagonist of transforming growth factor-β signaling. J Biol Chem. 276:30224-30230.
45. Samuelsen GB, Larsen KB, Bogdanovic N, Laursen H, Graem N, Larsen JF, Pakkenberg B. 2003. The changing number of cells in the human fetal forebrain and its subdivisions: a stereologic analysis. Cereb Cortex. 13:115-122.
46. Seoane J, Le HV, Shen L, Anderson SA, Massagué J. 2004. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell. 117:211-223.
47. Shen L, Nam HS, Song P, Moore H, Anderson SA. 2006. FoxG1 haploinsufficiency results in impaired neurogenesis in the postnatal hippocampus and contextual memory deficits. Hippocampus. 16:875-890.
48. Sherr CJ, Roberts JM. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501-1512.
49. Siegenthaler JA, Miller MW. 2005. Transforming growth factor β1 promotes cell cycle exit through the cyclin-dependent kinase inhibitor p21 in the developing cerebral cortex. J Neurosci. 25:8627-8636.
50. Siegenthaler JA, Miller MW. 2007. Generation of Cajal-Retzius neurons in the mouse forebrain is regulated by transforming growth factor β1-Fox signaling. Dev Biol. doi:10.1016/j.ydbio.2007.09.036.
51. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr. 1999. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci. 19:10357-10371.
52. Tao W, Lai E. 1992. Telencephalon-restricted expression of BF-1, a new member of the HNF-3/fork head gene family, in the developing rat brain. Neuron. 8:957-966.
53. Tarabykin V, Stoykova A, Usman N, Gruss P. 2001. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development. 128:1983-1993.
54. Kip1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb Cortex. 15:1343-1355.
55. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, Lai E. 1995. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron. 14:1141-1152.
56. Zimmer C, Tiveron MC, Bodmer R, Cremer H. 2004. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex. 14:1408-1420.