Activation of MAPK/PI3K/SMAD pathways by TGF-β1 controls differentiation of radial glia into astrocytes in vitro

Developmental Neuroscience

Volumn 34, Issue 1, 2012, Pages 68-81

  Stipursky, Joice ^a   Francis, Daniel ^a   Gomes, Flávia Carvalho Alcantara ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Astrocytes; Cerebral cortex; MAPK; PI3K; Radial glia; SMADs; TGF 1

Indexed keywords

BETA TUBULIN; EOMESODERMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NESTIN; OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CELL FATE; CELL POPULATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; GLIA; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; ASTROCYTES; BENZAMIDES; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; DIOXOLES; FLAVONOIDS; IMMUNOHISTOCHEMISTRY; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; NEURONS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84864280768     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000338108     Document Type: Article

References (80)

1. Hunter KE, Hatten ME: Radial glial cell transformation to astrocytes is bidirectional: regulation by a diffusible factor in embryon-ic forebrain. Proc Natl Acad Sci USA 1995; 92: 2061-2065.
2. Bentivoglio M, Mazzarello P: The history of radial glia. Brain Res Bull 1999; 49: 305-315.
3. Munoz-Garcia D, Ludwin SK: Gllogenesis in organotypic tissue culture of the spinal cord of the embryonic mouse. I. Immunocyto-chemical and ultrastructural studies. J Neu-rocytol 1986; 15: 273-290. (Pubitemid 16065162)
4. Stipursky J, de Sampaio e Spohr TCL, Romão L, Gomes FCA: Neuron-astrocyte interac-tion in cell fate commitment in the central nervous system; in Stem Cells: From Tools for Studying Mechanism of Neuronal Differ-entiation towards Therapy. Berlin, Springer, 2009, pp 145-170.
5. Voigt T: Development of glial cells in the ce-rebral wall of ferrets: direct tracing of their transformation from radial glia into astro-cytes. J Comp Neurol 1989; 289: 74-88. (Pubitemid 19263991)
6. Culican SM, Baumrind NL, Yamamoto M, Pearlman AL: Cortical radial glia: identifica-tion in tissue culture and evidence for their transformation to astrocytes. J Neurosci 1990; 10: 684-692. (Pubitemid 20089088)
7. Noctor SC, Flint AC, Weissman TA, Dam-merman RS, Kriegstein AR: Neurons de-rived from radial glial cells establish radial units in neocortex. Nature 2001; 409: 714-720. (Pubitemid 32144516)
8. Miyata T, Kawaguchi A, Okano H, Ogawa M: Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001; 13: 727-741. (Pubitemid 32907370)
9. Götz M, Hartfuss E, Malatesta R: Radial glia as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res Bull 2002; 57: 777-788. (Pubitemid 34522153)
10. Noctor SC, Flint AC, Weissman TA, Wong WS, Clinton BK, Kriegstein AR: Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 2002; 22: 3161-3173. (Pubitemid 35379204)
11. Malatesta P, Hack MA, Hartfuss E, Ketten-mann H, Klinkert W, Kirchhoff F, Götz M: Neuronal or glial progeny: regional differ-ences in radial glia fate. Neuron 2003; 37: 751-764. (Pubitemid 36288548)
12. de Azevedo LC, Fallet C, Moura-Neto V, Daumas-Duport C, Hedin-Pereira C, Lent R: Cortical radial glial cells in human fetuses: depth-correlated transformation into astro-cytes. J Neurobiol 2003; 55: 288-298. (Pubitemid 36566148)
13. Anthony TE, Klein C, Fishell G, Heintz N: Radial glia serves as neuronal progenitors in all regions of the central nervous system. Neuron 2004; 25: 881-890. (Pubitemid 38429732)
14. Anton ES, Marchionni MA, Lee KF, Rakic P: Role of GGF/neuregulin signaling in interac-tions between migrating neurons and radial glia in the developing cerebral cortex. Devel-opment 1997; 124: 3501-3510. (Pubitemid 27470034)
15. Stipursky J, Romão L, Tortelli V, Neto VM, Gomes FC: Neuron-glia signaling: implica-tions for astrocyte differentiation and syn-apse formation. Life Sci 2011; 89: 524-531.
16. Schmid RS, McGrath B, Berechid BE, Boyles B, Marchionni M, Sestan N, Anton ES: Neu-regulin1-erbB2 signaling is required for the establishment of radial glia and their trans-formation into astrocytes in cerebral cortex. Neuroscience 2003; 100: 4251-4256. (Pubitemid 36418189)
17. Patten BA, Peyrin JM, Weinmaster G, Corfas G: Sequential signaling through Notch1 and erbB receptors mediates radial glia differen-tiation. J Neurosci 2003; 23: 6132-6140. (Pubitemid 36859451)
18. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME: Regulation of gliogene-sis in the central nervous system by the JAK-STAT signaling pathway. Science 1997; 278: 477-483. (Pubitemid 27454434)
19. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miya-zono K, Taga T: Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 1999; 284: 479-482. (Pubitemid 29289619)
20. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T: DNA methylation is a critical cell-intrinsic determinant of astro-cyte differentiation in the fetal brain. Dev Cell 2001; 1: 749-758. (Pubitemid 33586130)
21. Mi H, Haeberle H, Barres BA: Induction of astrocyte differentiation by endothelial cells. J Neurosci 2001; 21: 1538-1547 (Pubitemid 32182194)
22. Uemura A, Takizawa T, Ochiai W, Yanagi-sawa M, Nakashima K, Taga T: Cardiotro-phin-like cytokine induces astrocyte differ-entiation of fetal neuroepithelial cells via ac-tivation of STAT3. Cytokine 2002; 18: 1-7. (Pubitemid 34762072)
23. Nishino J, Yamashita K, Hashiguchi H, Fujii H, Shimazaki T, Hamada H: Meteorin: a se-creted protein that regulates glial cell differ-entiation and promotes axonal extension. EMBO J 2004; 23: 1998-2008. (Pubitemid 38902078)
24. He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guil-lemot F, Fan G, de Vellis J, Sun Y: A positive autoregulatory loop of Jak-STAT signaling controls the onset of astroGllogenesis. Na-ture Neurosci 2005; 8: 616-625. (Pubitemid 40594203)
25. Barnabé-Heider F, Wasylnka JA, Fernandes KJL, Porsche MS, Kaplan DR, Miller FD: Ev-idence that embryonic neurons regulate the onset of cortical Gllogenesis via cardiotro-phin-1. Neuron 2005; 48: 253-265. (Pubitemid 41476359)
26. Stipursky J, Gomes FCA: TGF-ß1/SMAD signaling induces astrocyte fate commit-ment in vitro: implications for radial glia de-velopment. Glia 2007; 55: 1023-1033. (Pubitemid 47066742)
27. Massagué J: TGF-ß1 signal transduction. Annu Rev Biochem 1998; 67: 753-791.
28. Gomes FCA, Sousa VO, Romão L: Emerging roles for TGF-ß1 in nervous system develop-ment. Int J Dev Neurosci 2005; 23: 413-424. (Pubitemid 40981867)
29. Massagué J, Gomis RR: The logic of TGFß signaling. FEBS Lett 2006; 580: 2811-2820.
30. Javelaud D, Mauviel A: Crosstalk mecha-nisms between the mitogen-activated pro-tein kinase pathways and Smad signaling downstream of TGF-ß: implications for car-cinogenesis. Oncogene 2005; 24: 5742-5750. (Pubitemid 43086134)
31. Moustakas A, Heldin CH: Non-Smad TGF-ß signals. J Cell Sci 2005; 118: 3573-3584.
32. Zhang YE: Non-Smad pathways in TGF-ß signaling. Cell Res 2009; 19: 128-139.
33. Miller MW, Luo J: Effects of ethanol and transforming growth factor beta (TGF beta) on neuronal proliferation and nCAM ex-pression. Alcohol Clin Exp Res 2003; 26: 1281-1285.
34. Sousa VO, Romão L, Moura Neto V, Gomes FCA: Glial fibrillary acidic protein gene pro-moter is differently modulated by trans-forming growth factor-beta 1 in astrocytes from distinct brain regions. Eur J Neurosci 2004; 19: 1721-1730. (Pubitemid 38482560)
35. Sousa VO, Almeida JC, Eller CM, Gomes FC: Characterization of TGF-beta 1 type II receptor in cultured cortical astrocytes. In Vitro Cell Dev Biol Anim 2006; 42: 171-175. (Pubitemid 44744151)
36. Mecha M, Rabadán MA, Peña-Melián A, Va-lencia M, Mondéjar T, Blanco MJ: Expression of TGF-ßs in the embryonic nervous system: analysis of interbalance between isoforms. Dev Dyn 2008; 237: 1709-1717 (Pubitemid 351813068)
37. Romão LF, Sousa V de O, Neto VM, Gomes FC: Glutamate activates GFAP gene promot-er from cultured astrocytes through TGF-beta1 pathways. J Neurochem 2008; 2: 746-756.
38. Englund C, Fink A, Lau C, Pham D, Daza RAM, Bulfone A, Kowalczyk T, Hevner RF: Pax6, Tbr2, and Tbr1 are expressed sequen-tially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 2005; 25: 247-251. (Pubitemid 40110787)
39. Shi Y, Massagué J: Mechanisms of TGF-ß signaling from cell membrane to the nucleus. Cell 2003; 113: 685-700. (Pubitemid 36724933)
40. Jinnin M, Ihn M, Tamaki K: Characteriza-tion of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor-ß1- induced extracellular ma-trix expression. Mol Pharmacol 2006; 69: 597-607. (Pubitemid 43121957)
41. Campbell K, Götz M: Radial glia: multi-pur-pose cells for vertebrate brain development. Trends Neurosci 2002; 25: 235-238. (Pubitemid 34327796)
42. Hartfuss E, Galli R, Heins N, Götz M: Char-acterization of CNS precursor subtypes and radial glia. Dev Biol 2001; 229: 15-30. (Pubitemid 32061711)
43. Pinto L, Götz M: Radial glial cell heterogene-ity - the source of diverse progeny in the CNS. Prog Neurobiol 2007; 83: 2-23. (Pubitemid 47241312)
44. Kriegstein A, Alvarez-Buylla A: The glial na-ture of embryonic and adult neural stem cells. Annu Rev Neurosci 2009; 32: 149-184.
45. Ortega JA, Alcántara S: BDNF/MAPK/ERK-induced BMP7 expression in the developing cerebral cortex induces premature radial glia differentiation and impairs neuronal migra-tion. Cereb Cortex 2010; 20: 2132-2144.
46. Ciceroni C, Mosillo P, Mastrantoni E, Sale P, Ricci-Vitiani L, Biagioni F, Stocchi F, Nico-letti F, Melchiorri D: mGLU3 metabotropic glutamate receptors modulate the differen-tiation of SVZ-derived neural stem cells to-wards the astrocytic lineage. Glia 2010; 58: 813-822.
47. Ebner S, Dunbar M, McKinnon RD: Distinct roles for PI 3K in proliferation and survival of oligodendrocyte progenitor cells. J Neurosci Res 2001; 62: 336-345.
48. Broughton SK, Chen H, Riddle A, Kuhn SE, Nagalla S, Roberts CT Jr, Back SA: Large-scale generation of highly enriched neural stem-cell-derived oligodendroglial cultures: maturation-dependent differences in insu-lin-like growth factor-mediated signal trans-duction. J Neurochem 2007; 100: 628-638. (Pubitemid 46095614)
49. Birling MC, Price J: A study of the potential of the embryonic rat telencephalon to gener-ate oligodendrocytes. Dev Biol 1998; 193: 100-113. (Pubitemid 28096584)
50. Rogister B, Ben-Hur T, Dubois-Dalcq M: From neural stem cells to myelinating oligo-dendrocytes. Mol Cell Neurosci 1999; 14: 287-300. (Pubitemid 29506160)
51. Kriegstein AR, Götz M: Radial glia diversity: a matter of cell fate. Glia 2003; 43: 37-43. (Pubitemid 36781695)
52. Sessa A, Mao CA, Colasante G, Nini A, Klein WH, Broccoli V: Tbr2-positive intermediate (basal) neuronal progenitors safeguard cere-bral cortex expansion by controlling ampli-fication of pallial glutamatergic neurons and attraction of subpallial GABAergic inter-neurons. Genes Dev 2010; 24: 1816-1826.
53. Kang W, Wong LC, Shi SH, Hébert JM: The transition from radial glial to intermediate progenitor cell is inhibited by FGF signaling during corticogenesis. J Neurosci 2009; 146: 14571-14580.
54. Munji RN, Choe Y, Li G, Siegenthaler JA, Pleasure SJ: Wnt signaling regulates neuro-nal differentiation of cortical intermediate progenitors. J Neurosci 2011; 31: 1676-1687
55. Zhang M, Wang M, Tang X, Li T-F, Zhang Y, Chen D: Smad3 prevents ß-catenin degrada-tion and facilitates ß-catenin nuclear trans-location in chondrocytes. J Biol Chem 2010; 12: 8703-8710.
56. Zhang J, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER, Pisarek AJ, Stocker AM, Mutch CA, Funatsu N, Chenn A: Corti-cal neural precursors inhibit their own dif-ferentiation via N-cadherin maintenance of beta-catenin signaling. Dev Cell 2010; 18: 472-479.
57. Varea O, Arevalo MA, Garrido JJ, Garcia-Segura LM, Wandosell F, Mendez P: Interac-tion of estrogen receptors with insulin-like growth factor-I and Wnt signaling in the nervous system. Steroids 2010; 75: 565-569.
58. Pu P, Zhang Z, Kang C, Jiang R, Jia Z, Wang G, Jiang H: Downregulation of Wnt2 and ß-catenin by siRNA suppresses malignant gli-oma cell growthWnt2/ß-catenin in glioma. Cancer Gene Ther 2009; 16: 351-361.
59. Rappl A, Piontek G, Schlegel J: EGFR-depen-dent migration of glial cells is mediated by reorganisation of N-cadherin. J Cell Sci 2008; 24: 4089-4097
60. Chung H, Seo S, Moon M, Park S: Phos-phatidylinositol-3 -kinase/Akt/glycogen syn-thase kinase-3 b and ERK1/2 pathways medi-ate protective effects of acylated and un-acylated ghrelin against oxygen-glucose de-privation-induced apoptosis in primary rat cortical neuronal cells. J Endocrinol 2008; 198: 511-521.
61. Wachs FP, Winner B, Couillard-Despres S, Schiller T, Aigner R, Winkler J, Bogdahn U, Aigner L: Transforming growth factor-beta1 is a negative modulator of adult neurogene-sis. J Neuropathol Exp Neurol 2006; 65: 358-370. (Pubitemid 44264833)
62. Yanagisawa M, Takizawa T, Ochiai W, Ue-mura A, Nakashima K, Taga T: Fate altera-tion of neuroepithelial cells from neurogen-esis to astrocytogenesis by bone morphoge-netic proteins. Neurosci Res 2001; 41: 391-396. (Pubitemid 33733758)
63. Vogel T, Ahrens S, Buttner N, Krieglstein K: Transforming growth factor ß promotes neuronal cell fate of mouse cortical and hip-pocampal progenitors in vitro and in vivo: identification of Nedd9 as an essential sig-naling component. Cereb Cortex 2010; 3: 661-671.
64. Wang Y, Symes AJ: Smad3 deficiency reduc-es neurogenesis in adult mice. J Mol Neuro-sci 2010; 41: 383-396.
65. Powrozek TA, Miller MW: Ethanol affects transforming growth factor beta1-initiated signals: cross-talking pathways in the devel-oping rat cerebral wall. J Neurosci 2009; 29: 9521-9533.
66. Lesné S, Docagne F, Gabriel C, Liot G, Lahiri DK, Buee L, Plawinski L, Delacourte A, MacKenzie ET, Buisson A, Vivien D: Trans-forming growth factor-ß 1 potentiates amy-loid-beta generation in astrocytes and in transgenic mice. J Biol Chem 2003; 278: 18408-18418. (Pubitemid 36799463)
67. Law AKT, Gupta D, Levy S, Wallace DC, McKeon RJ, Buck CR: TGF-ß1 induction of the adenine nucleotide translocator 1 in as-trocytes occurs through Smads and Sp1 transcription factors. BMC Neurosci 2004; 5: 1.
68. Li H, Grumet M: BMP and LIF signaling co-ordinately regulate lineage restriction of ra-dial glia in the developing forebrain. Glia 2007; 55: 24-35. (Pubitemid 44845506)
69. Derynck R, Zhang YE: Smad-dependent and Smad-independent pathways in TGF-ß fam-ily signaling. Nature 2003; 425: 577-584. (Pubitemid 37280136)
70. Wrana JL: Crossing Smads. Sci STKE 2000; 23: re1.
71. Conery AR, Cao Y, Thompson EA, Townsend CM Jr, Ko TC, Luo K: Akt interacts directly with Smad3 to regulate the sensitivity to TGF-beta induced apoptosis. Nat Cell Biol 2004; 6: 366-372. (Pubitemid 38584827)
72. Remy I, Montmarquette A, Michnick SW: PKB/Akt modulates TGF-beta signaling through a direct interaction with Smad3. Nat Cell Biol 2004; 6: 358-365. (Pubitemid 38584826)
73. Gaiano N, Fishell G: The role of Notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 2002; 25: 471-490. (Pubitemid 34748025)
74. Zhou CJ, Zhao C, Pleasure SJ: Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding ab-normalities. J Neurosci 2004; 24: 121-126. (Pubitemid 38181677)
75. Patten BA, Sardi SP, Koirala S, Nakafuku M, Corfas G: Notch1 signaling regulates radial glia differentiation through multiple tran-scriptional mechanisms. J Neurosci 2006; 26: 3102-3108.
76. Yoon K, Nery S, Rutlin ML, Radtke F, Fishell G, Gaiano N Fibroblast growth factor recep-tor signaling promotes radial glial identity and interacts with Notch1 signaling in telen-cephalic progenitors. J Neurosci 2004; 24: 9497-9506. (Pubitemid 39441503)
77. Gierdalski M, Sardi SD, Corfas G, Juliano SL: Endogenous neuregulin restores radial glia in a (ferret) model of cortical dysplasia. J Neurosci 2005; 25: 8498-8504. (Pubitemid 41324735)
78. Das AV, Mallya KB, Zhao X, Ahmad F, Bhat-tacharya S, Thoreson WB, Hegde GV, Ah-mad I: Neural stem cell properties of Müller glia in the mammalian retina: regulation by Notch and Wnt signaling. Dev Biol 2006; 299: 283-302. (Pubitemid 44550105)
79. Ghashghaei HT, Weimer JM, Schmid RS, Yo-kota Y, McCarthy KD, Popko B, Anton ES: Reinduction of ErbB2 in astrocytes promotes radial glial progenitor identity in adult cere-bral cortex. Genes Dev 2007; 21: 3258-3271. (Pubitemid 350277753)
80. de Sampaio e Spohr TCL, Martinez R, Fe-derowicz ES, Moura-Neto V, Gomes FCA: Neuron-glia interaction effects on GFAP gene: a novel role for transforming growth factor-ß1. Eur J Neurosci 2002; 16: 2059-2069.