Beta-catenin signaling negatively regulates intermediate progenitor population numbers in the developing cortex

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Mutch, Christopher A ^a   Schulte, Jessica D ^a   Olson, Eric ^b   Chenn, Anjen ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; AXIN2; BETA CATENIN; CELL MARKER; EOMESODERMIN; UNCLASSIFIED DRUG; WNT PROTEIN; EOMES PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL COUNT; CELL KINETICS; CELL MATURATION; CELL POPULATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE DELETION; GLIA CELL; INTRACELLULAR SIGNALING; MITOSIS RATE; MOUSE; NEGATIVE FEEDBACK; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSGENIC MOUSE; ANIMAL; BRAIN CORTEX; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR IMAGING; PROTEIN STABILITY; SIGNAL TRANSDUCTION; STEM CELL;

MAMMALIA;

ANIMALS; BETA CATENIN; CELL COUNT; CEREBRAL CORTEX; GENE EXPRESSION REGULATION; MICE; MOLECULAR IMAGING; PROTEIN STABILITY; SIGNAL TRANSDUCTION; STEM CELLS; T-BOX DOMAIN PROTEINS;

EID: 77957875747     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012376     Document Type: Article

References (69)

1. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409: 714-720.
2. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, et al. (2002) Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 22: 3161-3173.
3. Rakic P (1988) Specification of cerebral cortical areas. Science 241: 170-176.
4. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, et al. (2004) Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131: 3133-3145.
5. 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 U S A 101: 3196-3201.
6. 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.
7. Kriegstein A, Noctor S, Martinez-Cerdeno V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7: 883-890.
8. Takahashi T, Nowakowski RS, Caviness VS Jr (1995) Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci 15: 6058-6068.
9. Attardo A, Calegari F, Haubensak W, Wilsch-Brauninger M, Huttner WB (2008) Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLoS One 3: e2388.
10. Pontious A, Kowalczyk T, Englund C, Hevner RF (2008) Role of intermediate progenitor cells in cerebral cortex development. Dev Neurosci 30: 24-32.
11. Smart IH (1973) Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures. J Anat 116: 67-91.
12. Kowalczyk T, Pontious A, Englund C, Daza RAM, Bedogni F, et al. (2009) Intermediate Neuronal Progenitors (Basal Progenitors) Produce Pyramidal-Projection Neurons for All Layers of Cerebral Cortex. Cereb Cortex bhn260.
13. 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, 152-161.
14. Smart IHM, Dehay C, Giroud P, Berland M, Kennedy H (2002) Unique Morphological Features of the Proliferative Zones and Postmitotic Compartments of the Neural Epithelium Giving Rise to Striate and Extrastriate Cortex in the Monkey. Cereb Cortex 12: 37-53.
15. Hansen DV, Lui JH, Parker PRL, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464: 554-561.
16. Sessa A, Mao C-a, Hadjantonakis A-K, Klein WH, 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.
17. Arnold SJ, Huang GJ, Cheung AF, Era T, Nishikawa S, et al. (2008) The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev 22: 2479-2484.
18. Britz O, Mattar P, Nguyen L, Langevin L-M, Zimmer C, et al. (2006) A Role for Proneural Genes in the Maturation of Cortical Progenitor Cells. Cereb Cortex 16: i138-151.
19. Castro DS, Skowronska-Krawczyk D, Armant O, Donaldson IJ, Parras C, et al. (2006) Proneural bHLH and Brn Proteins Coregulate a Neurogenic Program through Cooperative Binding to a Conserved DNA Motif. Developmental Cell 11: 831-844.
20. Farkas LM, Haffner C, Giger T, Khaitovich P, Nowick K, et al. (2008) Insulinoma-Associated 1 Has a Panneurogenic Role and Promotes the Generation and Expansion of Basal Progenitors in the Developing Mouse Neocortex. Neuron 60: 40-55.
21. Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297: 365-369.
22. Woodhead GJ, Mutch CA, Olson EC, Chenn A (2006) Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J Neurosci 26: 12620-12630.
23. Wrobel CN, Mutch CA, Swaminathan S, Taketo MM, Chenn A (2007) Persistent expression of stabilized beta-catenin delays maturation of radial glial cells into intermediate progenitors. Dev Biol 309: 285-297.
24. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, et al. (2002) Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22: 1172-1183.
25. Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, et al. (2002) Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22: 1184-1193.
26. Yan D, Wiesmann M, Rohan M, Chan V, Jefferson AB, et al. (2001) Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta -catenin signaling is activated in human colon tumors. Proc Natl Acad Sci U S A 98: 14973-14978.
27. Teissedre B, Pinderhughes A, Incassati A, Hatsell SJ, Hiremath M, et al. (2009) MMTV-Wnt1 and -DeltaN89beta-catenin induce canonical signaling in distinct progenitors and differentially activate Hedgehog signaling within mammary tumors. PLoS One 4: e4537.
28. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, et al. (2007) Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25: 2827-2836.
29. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125: 2315-2325.
30. Backman M, Machon O, Mygland L, van den Bout CJ, Zhong W, et al. (2005) Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol 279: 155-168.
31. Machon O, Backman M, Machonova O, Kozmik Z, Vacik T, et al. (2007) A dynamic gradient of Wnt signaling controls initiation of neurogenesis in the mammalian cortex and cellular specification in the hippocampus. Dev Biol 311: 223-237.
32. Englund C, Fink A, Lau C, Pham D, Daza RA, et al. (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.
33. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, et al. (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.
34. 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.
35. Yoon K-J, Koo B-K, Im S-K, Jeong H-W, Ghim J, et al. (2008) Mind Bomb 1-Expressing Intermediate Progenitors Generate Notch Signaling to Maintain Radial Glial Cells. Neuron 58: 519-531.
36. Quinn JC, Molinek M, Martynoga BS, Zaki PA, Faedo A, et al. (2007) Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev Biol 302: 50-65.
37. Bulfone A, Martinez S, Marigo V, Campanella M, Basile A, et al. (1999) Expression pattern of the Tbr2 (Eomesodermin) gene during mouse and chick brain development. Mech Devel 84: 133-138.
38. Bayatti N, Sarma S, Shaw C, Eyre JA, Vouyiouklis DA, et al. (2008) Progressive loss of PAX6, TBR2, NEUROD and TBR1 mRNA gradients correlates with translocation of EMX2 to the cortical plate during human cortical development. European Journal of Neuroscience 28: 1449-1456.
39. Brill MS, Ninkovic J, Winpenny E, Hodge RD, Ozen I, et al. (2009) Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci 12: 1524-1533.
40. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, et al. (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925.
41. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, et al. (2001) Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253-1264.
42. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, et al. (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23: 99-103.
43. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, et al. (1997) Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275: 1784-1787.
44. Tetsu O, McCormick F (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398: 422-426.
45. Barth AI, Pollack AL, Altschuler Y, Mostov KE, Nelson WJ (1997) NH2-terminal deletion of beta-catenin results in stable colocalization of mutant beta-catenin with adenomatous polyposis coli protein and altered MDCK cell adhesion. J Cell Biol 136: 693-706.
46. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, et al. (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. Embo J 18: 5931-5942.
47. Zechner D, Fujita Y, Hulsken J, Muller T, Walther I, et al. (2003) beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev Biol 258: 406-418.
48. Dorsky RI, Sheldahl LC, Moon RT (2002) A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev Biol 241: 229-237.
49. Barolo S (2006) Transgenic Wnt//TCF pathway reporters: all you need is Lef? Oncogene 25: 7505-7511.
50. Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, et al. (2003) Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci U S A 100: 3299-3304.
51. Holm PC, Mader MT, Haubst N, Wizenmann A, Sigvardsson M, et al. (2007) Loss- and gain-of-function analyses reveal targets of Pax6 in the developing mouse telencephalon. Molecular and Cellular Neuroscience 34: 99-119.
52. Siegenthaler JA, Tremper-Wells BA, Miller MW (2008) Foxg1 Haploinsufficiency Reduces the Population of Cortical Intermediate Progenitor Cells: Effect of Increased p21 Expression. Cereb Cortex 18: 1865-1875.
53. Mutch CA, Funatsu N, Monuki ES, Chenn A (2009) Beta-catenin signaling levels in progenitors influence the laminar cell fates of projection neurons. J Neurosci 29: 13710-13719.
54. Kuwahara A, Hirabayashi Y, Knoepfler PS, Taketo MM, Sakai J, et al. Wnt signaling and its downstream target N-myc regulate basal progenitors in the developing neocortex. Development 137: 1035-1044.
55. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, et al. (2004) The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131: 2791-2801.
56. Hanashima C, Li SC, Shen L, Lai E, Fishell G (2004) Foxg1 suppresses early cortical cell fate. Science 303: 56-59.
57. Liu Q, Dwyer ND, O'Leary DDM (2000) Differential Expression of COUP-TFI, CHL1, and Two Novel Genes in Developing Neocortex Identified by Differential Display PCR. J Neurosci 20: 7682-7690.
58. Faedo A, Tomassy GS, Ruan Y, Teichmann H, Krauss S, et al. (2008) COUP-TFI Coordinates Cortical Patterning, Neurogenesis, and Laminar Fate and Modulates MAPK/ERK, AKT, and ss-Catenin Signaling. Cereb Cortex 18: 2117-2131.
59. Zhang J, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER, et al. (2010) Cortical Neural Precursors Inhibit Their Own Differentiation via N-Cadherin Maintenance of [beta]-Catenin Signaling. Developmental Cell 18: 472-479.
60. Weimer JM, Yokota Y, Stanco A, Stumpo DJ, Blackshear PJ, et al. (2009) MARCKS modulates radial progenitor placement, proliferation and organization in the developing cerebral cortex. Development 136: 2965-2975.
61. Yokota Y, Kim WY, Chen Y, Wang X, Stanco A, et al. (2009) The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 61: 42-56.
62. Huttner WB, Brand M (1997) Asymmetric division and polarity of neuroepithelial cells. Current Opinion in Neurobiology 7: 29-39.
63. Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82: 631-641.
64. Kormish JD, Sinner D, Zorn AM (2009) Interactions between SOX factors and Wnt/beta-catenin signaling in development and disease. Developmental Dynamics 239: 56-68.
65. Kan L, Israsena N, Zhang Z, Hu M, Zhao L-R, et al. (2004) Sox1 acts through multiple independent pathways to promote neurogenesis. Developmental Biology 269: 580-594.
66. Martinez-Morales PL, Quiroga AC, Barbas JA, Morales AV (2010) SOX5 controls cell cycle progression in neural progenitors by interfering with the WNT-[beta]-catenin pathway. EMBO Rep 11: 466-472.
67. Sinner D, Kordich JJ, Spence JR, Opoka R, Rankin S, et al. (2007) Sox17 and Sox4 Differentially Regulate {beta}-Catenin/T-Cell Factor Activity and Proliferation of Colon Carcinoma Cells. Mol Cell Biol 27: 7802-7815.
68. Sinner D, Rankin S, Lee M, Zorn AM (2004) Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 131: 3069-3080.
69. Chen Y, Shi L, Zhang L, Li R, Liang J, et al. (2008) The Molecular Mechanism Governing the Oncogenic Potential of SOX2 in Breast Cancer. JBC 283: 17969-17978.