Sox1 maintains the undifferentiated state of cortical neural progenitor cells via the suppression of Prox1-mediated cell cycle exit and neurogenesis

Stem Cells

Volumn 29, Issue 1, 2011, Pages 89-98

  Elkouris, Maximilianos ^a   Balaskas, Nikos ^a   Poulou, Maria ^a   Politis, Panagiotis K ^b   Panayiotou, Elena ^c   Malas, Stavros ^c   Thomaidou, Dimitra ^d   Remboutsika, Eumorphia ^a  

^a BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^c CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^d HELLENIC PASTEUR INSTITUTE   (Greece)

Author keywords

Cell division; Cortex; Neural stem cells; Neurogenesis; Sox genes

Indexed keywords

TRANSCRIPTION FACTOR CDX1; TRANSCRIPTION FACTOR SOX1;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL ELONGATION; CELL PROLIFERATION; CHICK; CONTROLLED STUDY; EMBRYO; MOUSE; MOUSE EMBRYO; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; SELF CONCEPT; STEM CELL; WILD TYPE;

ANIMALS; BROMODEOXYURIDINE; CELL CYCLE; CELL DIVISION; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE KNOCK-IN TECHNIQUES; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; MICE; MICE, MUTANT STRAINS; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; SOXB1 TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

PROSPERO;

EID: 79951839166     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.554     Document Type: Article

References (66)

1. Edlund T, Jessell TM. Progression from extrinsic to intrinsic signaling in cell fate specification: a view from the nervous system. Cell 1999;96:211-224. (Pubitemid 29059351)
2. Gotz M, Huttner WB. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005;6:777-788. (Pubitemid 41726116)
3. Louvi A, Artavanis-Tsakonas S. Notch signalling in vertebrate neural development. Nat Rev Neurosci 2006;7:93-102. (Pubitemid 43151596)
4. Bertrand N, Castro DS, Guillemot F. Proneural genes and the specification of neural cell types. Nat Rev Neurosci 2002;3:517-530. (Pubitemid 135706662)
5. Dyer MA. Regulation of proliferation, cell fate specification and differentiation by the homeodomain proteins Prox1, Six3, And Chx10 in the developing retina. Cell Cycle 2003;2:350-357.
6. Dyer MA, Livesey FJ, Cepko CL et al. Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat Genet 2003;34:53-58. (Pubitemid 36548790)
7. Begley CG, Lipkowitz S, Gobel V et al. Molecular characterization of NSCL, a gene encoding a helix-loop-helix protein expressed in the developing nervous system. Proc Natl Acad Sci USA 1992;89:38-42.
8. Roztocil T, Matter-Sadzinski L, Alliod C et al. NeuroM, a neural helix-loop-helix transcription factor, defines a new transition stage in neurogenesis. Development 1997;124:3263-3272. (Pubitemid 27440441)
9. Misra K, Gui H, Matise MP. Prox1 regulates a transitory state for interneuron neurogenesis in the spinal cord. Dev Dyn 2008;237:393-402. (Pubitemid 351312111)
10. Schepers GE, Teasdale RD, Koopman P. Twenty pairs of sox: Extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 2002;3:167-170.
11. Malas S, Duthie S, Deloukas P et al. The isolation and high-resolution chromosomal mapping of human SOX14 and SOX21; two members of the SOX gene family related to SOX1, SOX2, And SOX3 Mamm Genome 1999;10:934-937. (Pubitemid 29445387)
12. Uchikawa M, Kamachi Y, Kondoh H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: Their expression during embryonic organogenesis of the chicken. Mech Dev 1999;84:103-120. (Pubitemid 29331657)
13. Bylund M, Andersson E, Novitch BG et al. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 2003;6:1162-1168. (Pubitemid 37346036)
14. Holmberg J, Hansson E, Malewicz M et al. SoxB1 transcription factors and Notch signaling use distinct mechanisms to regulate proneural gene function and neural progenitor differentiation. Development 2008;135:1843-1851.
15. Sandberg M, Kallstrom M, Muhr J. Sox21 promotes the progression of vertebrate neurogenesis. Nat Neurosci 2005;8:995-1001. (Pubitemid 41061509)
16. Nishiguchi S, Wood H, Kondoh H et al. Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev 1998;12:776-781. (Pubitemid 28150879)
17. Malas S, Postlethwaite M, Ekonomou A et al. Sox1-deficient mice suffer from epilepsy associated with abnormal ventral forebrain development and olfactory cortex hyperexcitability. Neuroscience 2003;119:421-432. (Pubitemid 36588820)
18. Zappone MV, Galli R, Catena R et al. Sox2 regulatory sequences direct expression of a (beta)-geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 2000;127:2367-2382. (Pubitemid 30386576)
19. Alexiades MR, Cepko C. Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn 1996;205:293-307. (Pubitemid 26074006)
20. Nowakowski RS, Lewin SB, Miller MW. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 1989;18:311-318. (Pubitemid 19147398)
21. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45, 1-6.
22. Wegner M, Stolt CC. From stem cells to neurons and glia: A Soxist's view of neural development. Trends Neurosci 2005;28:583-588. (Pubitemid 41476688)
23. Pevny L, Placzek M. SOX genes and neural progenitor identity. Curr Opin Neurobiol 2005;15:7-13. (Pubitemid 40249955)
24. Kiefer JC. Back to basics: Sox genes. Dev Dyn 2007;236:2356-2366.
25. Barraud P, Thompson L, Kirik D et al. Isolation and characterization of neural precursor cells from the Sox1-GFP reporter mouse. Eur J Neurosci 2005;22:1555-1569. (Pubitemid 41482944)
26. Kan L, Israsena N, Zhang Z et al. Sox1 acts through multiple independent pathways to promote neurogenesis. Dev Biol 2004;269:580-594. (Pubitemid 38521119)
27. Kan L, Jalali A, Zhao LR et al. Dual function of Sox1 in telencephalic progenitor cells. Dev Biol 2007;310:85-98. (Pubitemid 47445493)
28. Ekonomou A, Kazanis I, Malas S et al. Neuronal migration and ventral subtype identity in the telencephalon depend on SOX1. Plos Biol 2005;3:e186, 1111-1199.
29. Deleyrolle LP, Rietze RL, Reynorlds BA. The neurosphere assay, a method under scrutiny. Acta Neuropsychiatrica 2007;20:2-8. (Pubitemid 351160815)
30. Falk S, Wurdak H, Ittner LM et al. Brain area-specific effect of TGFbeta signaling on Wnt-dependent neural stem cell expansion. Cell Stem Cell 2008;2:472-483. (Pubitemid 351598080)
31. Lukaszewicz A, Savatier P, Cortay V et al. Contrasting effects of basic fibroblast growth factor and neurotrophin 3 on cell cycle kinetics of mouse cortical stem cells. J Neurosci 2002;22:6610-6622. (Pubitemid 35386417)
32. Calegari F, Haubensak W, Haffner C et al. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J Neurosci 2005;25:6533-6538. (Pubitemid 40995285)
33. Calegari F, Huttner WB. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J Cell Sci 2003;116:4947-4955. (Pubitemid 38016701)
34. Ohnuma S, Harris WA. Neurogenesis and the cell cycle. Neuron 2003;40:199-208. (Pubitemid 37244092)
35. Bally-Cuif L, Hammerschmidt M. Induction and patterning of neuronal development, and its connection to cell cycle control. Curr Opin Neurobiol 2003;13:16-25. (Pubitemid 36197924)
36. Takahashi T, Nowakowski RS, Caviness VS,Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 1995;15:6046-6057.
37. Martens DJ, Tropepe V, van Der Kooy D. Separate proliferation kinetics of fibroblast growth factor-responsive and epidermal growth factor-responsive neural stem cells within the embryonic forebrain germinal zone. J Neurosci 2000;20:1085-1095. (Pubitemid 30220466)
38. Toyoshima H, Hunter T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 1994;78:67-74. (Pubitemid 24228301)
39. Durand B, Fero ML, Roberts JM et al. p27Kip1 alters the response of cells to mitogen and is part of a cell-intrinsic timer that arrests the cell cycle and initiates differentiation. Curr Biol 1998;8:431-440. (Pubitemid 28181120)
40. Durand B, Gao FB, Raff M. Accumulation of the cyclin-dependent kinase inhibitor p27/Kip1 and the timing of oligodendrocyte differentiation. EMBO J 1997;16:306-317. (Pubitemid 27049388)
41. Durand B, Raff M. A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 2000;22:64-71. (Pubitemid 30057135)
42. Gao FB, Durand B, Raff M. Oligodendrocyte precursor cells count time but not cell divisions before differentiation. Curr Biol 1997;7:152-155. (Pubitemid 27155625)
43. Hirata J, Nakagoshi H, Nabeshima Y et al. Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 1995;377:627-630.
44. Knoblich JA, Jan LY, Jan YN. Asymmetric segregation of Numb and Prospero during cell division. Nature 1995;377:624-627.
45. Spana EP, Doe CQ. The prospero transcription factor is asymmetrically localized to the cell cortex during neuroblast mitosis in Drosophila. Development 1995;121:3187-3195.
46. Tomarev SI, Zinovieva RD, Chang B et al. Characterization of the mouse Prox1 gene. Biochem Biophys Res Commun 1998;248:684-689. (Pubitemid 28404482)
47. Sosa-Pineda B, Wigle JT, Oliver G. Hepatocyte migration during liver development requires Prox1. Nat Genet 2000;25:254-255. (Pubitemid 30437306)
48. Wang J, Kilic G, Aydin M et al. Prox1 activity controls pancreas morphogenesis and participates in the production of "secondary transition" pancreatic endocrine cells. Dev Biol 2005;286:182-194.
49. Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999;98:769-778. (Pubitemid 29446894)
50. Bermingham-McDonogh O, Oesterle EC, Stone JS et al. Expression of Prox1 during mouse cochlear development. J Comp Neurol 2006;496:172-186.
51. Lavado A, Oliver G. Prox1 expression patterns in the developing and adult murine brain. Dev Dyn 2007;236:518-524. (Pubitemid 46233295)
52. Wigle JT, Chowdhury K, Gruss P et al. Prox1 function is crucial for mouse lens-fibre elongation. Nat Genet 1999;21:318-322. (Pubitemid 29124943)
53. Yamamoto S, Nagao M, Sugimori M et al. Transcription factor expression and Notch-dependent regulation of neural progenitors in the adult rat spinal cord. J Neurosci 2001;21:9814-9823. (Pubitemid 34184066)
54. Miura H, Kusakabe Y, Kato H et al. Co-expression pattern of Shh with Prox1 and that of Nkx2.2 with Mash1 in mouse taste bud. Gene Expr Patterns 2003;3:427-430. (Pubitemid 36950415)
55. Francois M, Caprini A, Hosking B et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008;456:643-647.
56. Gui H, Li S, Matise MP. A cell-autonomous requirement for Cip/Kip cyclin-kinase inhibitors in regulating neuronal cell cycle exit but not differentiation in the developing spinal cord. Dev Biol 2007;301:14-26. (Pubitemid 44958402)
57. Garcia-Dominguez M, Poquet C, Garel S et al. Ebf gene function is required for coupling neuronal differentiation and cell cycle exit. Development 2003;130:6013-6025. (Pubitemid 38008804)
58. Pevny LH, Lovell-Badge R. Sox genes find their feet. Curr Opin Genet Dev 1997;7:338-344. (Pubitemid 27292285)
59. Pevny LH, Sockanathan S, Placzek M et al. A role for SOX1 in neural determination. Development 1998;125:1967-1978. (Pubitemid 28274383)
60. Suter DM, Tirefort D, Julien S et al. A Sox1 to Pax6 switch drives neuroectoderm to radial glia progression during differentiation of mouse embryonic stem cells. Stem Cells 2009;27:49-58.
61. Genethliou N, Panayiotou E, Panayi H et al. SOX1 links the function of neural patterning and Notch signalling in the ventral spinal cord during the neuron-glial fate switch. Biochem Biophys Res Commun 2009;390:1114-1120.
62. Mouthon MA, Fouchet P, Mathieu C et al. Neural stem cells from mouse forebrain are contained in a population distinct from the 'side population'. J Neurochem 2006;99:807-817.
63. Kim M, Morshead CM. Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J Neurosci 2003;23:10703-10709. (Pubitemid 37485284)
64. Corti S, Nizzardo M, Nardini M et al. Isolation and characterization of murine neural stem/progenitor cells based on Prominin-1 expression. Exp Neurol 2007;205:547-562. (Pubitemid 46778917)
65. Gabay L, Lowell S, Rubin LL et al. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 2003;40:485-499. (Pubitemid 37494699)
66. Dromard C, Bartolami S, Deleyrolle L et al. NG2 and Olig2 expression provides evidence for phenotypic deregulation of cultured central nervous system and peripheral nervous system neural precursor cells. Stem Cells 2007;25:340-353. (Pubitemid 46232788)