BDNF/MAPK/ERK-induced BMP7 expression in the developing cerebral cortex induces premature radial glia differentiation and impairs neuronal migration

Cerebral Cortex

Volumn 20, Issue 9, 2010, Pages 2132-2144

  Ortega, Juan Alberto ^a   Alcántara, Soledad ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

astrocytogenesis; cortical development; neurotrophins

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; OSTEOGENIC PROTEIN 1; PROTEIN; PROTEIN P53; PROTEIN P73; PROTEIN SC1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL DIFFERENTIATION; CELL MATURATION; CELL MIGRATION; EMBRYO; FEMALE; GENE EXPRESSION; GLIA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL;

ANIMALS; ASTROCYTES; BONE MORPHOGENETIC PROTEIN 7; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL MOVEMENT; CELLS, CULTURED; CEREBRAL CORTEX; DNA-BINDING PROTEINS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MAP KINASE SIGNALING SYSTEM; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; NEURONS; NUCLEAR PROTEINS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 77955936385     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhp275     Document Type: Article

References (70)

1. Aakalu G, Smith WB, Nguyen N, Jiang C, Schuman EM. 2001. Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron. 30:489-502.
2. Aguado F, Carmona MA, Pozas E, Aguilo A, Martinez-Guijarro FJ, Alcantara S, Borrell V, Yuste R, Ibanez CF, Soriano E. 2003. BDNF regulates spontaneous correlated activity at early developmental stages by increasing synaptogenesis and expression of the K+/Cl-co-transporter KCC2. Development. 130:1267-1280.
3. Alcantara S, Frisen J, del Rio JA, Soriano E, Barbacid M, Silos-Santiago I. 1997. TrkB signaling is required for postnatal survival of CNS neurons and protects hippocampal and motor neurons from axotomy-induced cell death. J Neurosci. 17:3623-3633.
4. Alcantara S, Pozas E, Ibanez CF, Soriano E. 2006. BDNF-modulated spatial organization of Cajal-Retzius and GABAergic neurons in the marginal zone plays a role in the development of cortical organization. Cereb Cortex. 16:487-499.
5. Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL. 2001. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development. 128:353-363.
6. Ang ES, Jr, Haydar TF, Gluncic V, Rakic P. 2003. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci. 23:5805-5815.
7. Barnabe-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD. 2005. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron. 48:253-265.
8. Bonhoeffer T. 1996. Neurotrophins and activity-dependent development of the neocortex. Curr Opin Neurobiol. 6:119-126.
9. 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.
10. Cooper JA. 2008. A mechanism for inside-out lamination in the neocortex. Trends Neurosci. 31:113-119.
11. Chang F, Steelman LS, Lee JT, Shelton JG, Navolanic PM, Blalock WL, Franklin RA, McCubrey JA. 2003. Signal transduction mediated by the Ras/Raf/MEK/ERK pathway from cytokine receptors to transcription factors: potential targeting for therapeutic intervention. Leukemia. 17:1263-1293.
12. Chang Q, Khare G, Dani V, Nelson S, Jaenisch R. 2006. The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron. 49:341-348.
13. Chao MV. 2003. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci. 4:299-309.
14. Cheng A, Coksaygan T, Tang H, Khatri R, Balice-Gordon RJ, Rao MS, Mattson MP. 2007. Truncated tyrosine kinase B brain-derived neuro-trophic factor receptor directs cortical neural stem cells to a glial cell fate by a novel signaling mechanism. J Neurochem. 100:1515-1530.
15. D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T. 1995. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature. 374:719-723.
16. Davidson W, Ren Q, Kari G, Kashi O, Dicker AP, Rodeck U. 2008. Inhibition of p73 function by Pifithrin-alpha as revealed by studies in zebrafish embryos. Cell Cycle. 7:1224-1230.
17. 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.
18. Feng L, Hatten ME, Heintz N. 1994. Brain lipid-binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron. 12:895-908.
19. Feng L, Heintz N. 1995. Differentiating neurons activate transcription of the brain lipid-binding protein gene in radial glia through a novel regulatory element. Development. 121:1719-1730.
20. Fox K, Wong RO. 2005. A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron. 48:465-477.
21. Fukumitsu H, Ohtsuka M, Murai R, Nakamura H, Itoh K, Furukawa S. 2006. Brain-derived neurotrophic factor participates in determination of neuronal laminar fate in the developing mouse cerebral cortex. J Neurosci. 26:13218-13230.
22. Gongidi V, Ring C, Moody M, Brekken R, Sage EH, Rakic P, Anton ES. 2004. SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron. 41:57-69.
23. Gorski JA, Zeiler SR, Tamowski S, Jones KR. 2003. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J Neurosci. 23:6856-6865.
24. Gotz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol. 6:777-788.
25. Guillemot F. 2005. Cellular and molecular control of neurogenesis in the mammalian telencephalon. Curr Opin Cell Biol. 17:639-647.
26. Guo S, Kim WJ, Lok J, Lee SR, Besancon E, Luo BH, Stins MF, Wang X, Dedhar S, Lo EH. 2008. Neuroprotection via matrix-trophic coupling between cerebral endothelial cells and neurons. Proc Natl Acad Sci\USA. 105:7582-7587.
27. Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Gotz M. 2003. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development. 130:4597-4609.
28. Hartfuss E, Galli R, Heins N, Gotz M. 2001. Characterization of CNS precursor subtypes and radial glia. Dev Biol. 229:15-30.
29. Hatten ME. 1985. Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol. 100:384-396.
30. Hong EJ, McCord AE, Greenberg ME. 2008. A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron. 60:610-624.
31. Huang EJ, Reichardt LF. 2001. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci. 24:677-736.
32. Hughes PE, Alexi T, Walton M, Williams CE, Dragunow M, Clark RG, Gluckman PD. 1999. Activity and injury-dependent expression of inducible transcription factors, growth factors and apoptosis-related genes within the central nervous system. Prog Neurobiol. 57:421-450.
33. Hunter KE, Hatten ME. 1995. Radial glial cell transformation to astrocytes is bidirectional: regulation by a diffusible factor in embryonic forebrain. Proc Natl Acad Sci\USA. 92:2061-2065.
34. Ihrie RA, Alvarez-Buylla A. 2008. Cells in the astroglial lineage are neural stem cells. Cell Tissue Res. 331:179-191.
35. Imura T, Tane K, Toyoda N, Fushiki S. 2008. Endothelial cell-derived bone morphogenetic proteins regulate glial differentiation of cortical progenitors. Eur J Neurosci. 27:1596-1606.
36. Kohara K, Yasuda H, Huang Y, Adachi N, Sohya K, Tsumoto T. 2007. A local reduction in cortical GABAergic synapses after a loss of endogenous brain-derived neurotrophic factor, as revealed by single-cell gene knock-out method. J Neurosci. 27:7234-7244.
37. Kriegstein AR, Noctor SC. 2004. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27:392-399.
38. Laurikkala J, Mikkola ML, James M, Tummers M, Mills AA, Thesleff I. 2006. p63 regulates multiple signalling pathways required for ectodermal organogenesis and differentiation. Development. 133:1553-1563.
39. Lively S, Brown IR. 2007. Analysis of the extracellular matrix protein SC1 during reactive gliosis in the rat lithium-pilocarpine seizure model. Brain Res. 1163:1-9.
40. Lu B. 2003. BDNF and activity-dependent synaptic modulation. Learn Mem. 10:86-98.
41. Lu B, Martinowich K. 2008. Cell biology of BDNF and its relevance to schizophrenia. Novartis Found Symp. 289:119-129; discussion 129-135, 193-195.
42. Lu B, Pang PT, Woo NH. 2005. The yin and yang of neurotrophin action. Nat Rev Neurosci. 6:603-614.
43. Malatesta P, Appolloni I, Calzolari F. 2008. Radial glia and neural stem cells. Cell Tissue Res. 331:165-178.
44. Malatesta P, Hack MA, Hartfuss E, Kettenmann H, Klinkert W, Kirchhoff F, Gotz M. 2003. Neuronal or glial progeny: regional differences in radial glia fate. Neuron. 37:751-764.
45. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, Chang F, Lehmann B, Terrian DM, Milella M, Tafuri A, et al. 2007. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 1773:1263-1284.
46. 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.
47. Mendis DB, Ivy GO, Brown IR. 1996. SC1, a brain extracellular matrix glycoprotein related to SPARC and follistatin, is expressed by rat cerebellar astrocytes following injury and during development. Brain Res. 730:95-106.
48. Miller FD, Gauthier AS. 2007. Timing is everything: making neurons versus glia in the developing cortex. Neuron. 54:357-369.
49. Miller FD, Kaplan DR. 2007. To die or not to die: neurons and p63. Cell Cycle. 6:312-317.
50. Nadarajah B, Parnavelas JG. 2002. Modes of neuronal migration in the developing cerebral cortex. Nat Rev Neurosci. 3:423-432.
51. Nagappan G, Lu B. 2005. Activity-dependent modulation of the BDNF receptor TrkB: mechanisms and implications. Trends Neurosci. 28:464-471.
52. Namihira M, Kohyama J, Semi K, Sanosaka T, Deneen B, Taga T, Nakashima K. 2009. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev Cell. 16:245-255.
53. 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.
54. Pattabiraman PP, Tropea D, Chiaruttini C, Tongiorgi E, Cattaneo A, Domenici L. 2005. Neuronal activity regulates the developmental expression and subcellular localization of cortical BDNF mRNA isoforms in vivo. Mol Cell Neurosci. 28:556-570.
55. Pozniak CD, Radinovic S, Yang A, McKeon F, Kaplan DR, Miller FD. 2000. An anti-apoptotic role for the p53 family member, p73, during developmental neuron death. Science. 289:304-306.
56. Rakic P. 1990. Principles of neural cell migration. Experientia. 46:882-891.
57. Reichardt LF. 2006. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci. 361:1545-1564.
58. Ringstedt T, Linnarsson S, Wagner J, Lendahl U, Kokaia Z, Arenas E, Ernfors P, Ibanez CF. 1998. BDNF regulates reelin expression and Cajal-Retzius cell development in the cerebral cortex. Neuron. 21:305-315.
59. Sancho-Tello M, Valles S, Montoliu C, Renau-Piqueras J, Guerri C. 1995. Developmental pattern of GFAP and vimentin gene expression in rat brain and in radial glial cultures. Glia. 15:157-166.
60. Scharfman HE. 2005. Brain-derived neurotrophic factor and epilepsy-a missing link? Epilepsy Curr. 5:83-88.
61. Scholzen T, Gerdes J. 2000. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 182:311-322.
62. Spitzer NC. 2006. Electrical activity in early neuronal development. Nature. 444:707-712.
63. Tabata H, Nakajima K. 2001. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuro-nal migration in the developing cortex. Neuroscience. 103:865-872.
64. Tsai SJ. 2005. Is autism caused by early hyperactivity of brain-derived neurotrophic factor? Med Hypotheses. 65:79-82.
65. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, et al. 2004. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science. 303:844-848.
66. Wade SB, Oommen P, Conner WC, Earnest DJ, Miranda RC. 1999. Overlapping and divergent actions of estrogen and the neuro-trophins on cell fate and p53-dependent signal transduction in conditionally immortalized cerebral cortical neuroblasts. J Neurosci. 19:6994-7006.
67. Wu GS. 2004. The functional interactions between the p53 and MAPK signaling pathways. Cancer Biol Ther. 3:156-161.
68. Yan W, Chen X. 2007. Targeted repression of bone morphogenetic protein 7, a novel target of the p53 family, triggers proliferative defect in p53-deficient breast cancer cells. Cancer Res. 67: 9117-9124.
69. Yanagisawa M, Takizawa T, Ochiai W, Uemura A, Nakashima K, Taga T. 2001. Fate alteration of neuroepithelial cells from neurogenesis to astrocytogenesis by bone morphogenetic proteins. Neurosci Res. 41:3. 1-396.
70. Zhang LI, Poo MM. 2001. Electrical activity and development of neural circuits. Nat Neurosci. (4 Suppl):1207-1214.