Opposing effects of retinoid signaling on astrogliogenesis in embryonic day 13 and 17 cortical progenitor cells

Journal of Neurochemistry

Volumn 106, Issue 4, 2008, Pages 1681-1698

  Faigle, Roland ^a,b,c   Liu, Lidong ^a,b   Cundiff, Paige ^b   Funa, Keiko ^c   Xia, Zhengui ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

CNTF; Glial differentiation; Gliogenesis; Neural stem cell; Neurogenesis; Retinoic acid

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; RETINOID;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CELL LINE; CONTROLLED STUDY; EMBRYO; GROWTH REGULATION; MACROGLIA; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STEM CELL;

AGE FACTORS; ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RETINOIDS; SIGNAL TRANSDUCTION; STEM CELLS; TRETINOIN;

RATTUS;

EID: 48749131941     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05525.x     Document Type: Article

References (71)

1. Abematsu M., Kagawa T., Fukuda S., Inoue T., Takebayashi H., Komiya S. Taga T. (2006) Basic fibroblast growth factor endows dorsal telencephalic neural progenitors with the ability to differentiate into oligodendrocytes but not gamma-aminobutyric acidergic neurons. J. Neurosci. Res. 83, 731 743.
2. Aggarwal S., Kim S. W., Cheon K., Tabassam F. H., Yoon J. H. Koo J. S. (2006) Nonclassical action of retinoic acid on the activation of the cAMP response element-binding protein in normal human bronchial epithelial cells. Mol. Biol. Cell 17, 566 575.
3. Barnabe-Heider F., Wasylnka J. A., Fernandes K. J., Porsche C., Sendtner M., Kaplan D. R. Miller F. D. (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48, 253 265.
4. Bonni A., Frank D. A., Schindler C. Greenberg M. E. (1993) Characterization of a pathway for ciliary neurotrophic factor signaling to the nucleus. Science (New York, N.Y.) 262, 1575 1579.
5. Bonni A., Sun Y., Nadal-Vicens M., Bhatt A., Frank D. A., Rozovsky I., Stahl N., Yancopoulos G. D. Greenberg M. E. (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science (New York, N.Y.) 278, 477 483.
6. Brooks III S. C., Kazmer S., Levin A. A. Yen A. (1996) Myeloid differentiation and retinoblastoma phosphorylation changes in HL-60 cells induced by retinoic acid receptor- and retinoid X receptor-selective retinoic acid analogs. Blood 87, 227 237.
7. Burrows R. C., Wancio D., Levitt P. Lillien L. (1997) Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19, 251 267.
8. Chapellier B., Mark M., Messaddeq N. et al. (2002) Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled. EMBO J. 21, 3402 3413.
9. Davis A. A. Temple S. (1994) A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372, 263 266.
10. Deneen B., Ho R., Lukaszewicz A., Hochstim C. J., Gronostajski R. M. Anderson D. J. (2006) The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52, 953 968.
11. Derouet D., Rousseau F., Alfonsi F. et al. (2004) Neuropoietin, a new IL-6-related cytokine signaling through the ciliary neurotrophic factor receptor. Proc. Natl Acad. Sci. USA 101, 4827 4832.
12. Eagleson K. L., Ferri R. T. Levitt P. (1996) Complementary distribution of collagen type IV and the epidermal growth factor receptor in the rat embryonic telencephalon. Cereb. Cortex 6, 540 549.
13. Faigle R., Brederlau A., Elmi M., Arvidsson Y., Hamazaki T. S., Uramoto H. Funa K. (2004) ASK1 inhibits astroglial development via p38 mitogen-activated protein kinase and promotes neuronal differentiation in adult hippocampus-derived progenitor cells. Mol. Cell. Biol. 24, 280 293.
14. Fan G., Martinowich K., Chin M. H. et al. (2005) DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development (Cambridge, England) 132, 3345 3356.
15. Fukuda S., Kondo T., Takebayashi H. Taga T. (2004) Negative regulatory effect of an oligodendrocytic bHLH factor OLIG2 on the astrocytic differentiation pathway. Cell Death Differ. 11, 196 202.
16. Gabay L., Lowell S., Rubin L. L. Anderson D. J. (2003) Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron 40, 485 499.
17. Gehin M., Vivat V., Wurtz J. M., Losson R., Chambon P., Moras D. Gronemeyer H. (1999) Structural basis for engineering of retinoic acid receptor isotype-selective agonists and antagonists. Chem. Biol. 6, 519 529.
18. Goncalves M. B., Boyle J., Webber D. J., Hall S., Minger S. L. Corcoran J. P. (2005) Timing of the retinoid-signalling pathway determines the expression of neuronal markers in neural progenitor cells. Dev. Biol. 278, 60 70.
19. Gross R. E., Mehler M. F., Mabie P. C., Zang Z., Santschi L. Kessler J. A. (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595 606.
20. Hack M. A., Sugimori M., Lundberg C., Nakafuku M. Gotz M. (2004) Regionalization and fate specification in neurospheres: the role of Olig2 and Pax6. Mol. Cell. Neurosci. 25, 664 678.
21. Henion P. D. Weston J. A. (1994) Retinoic acid selectively promotes the survival and proliferation of neurogenic precursors in cultured neural crest cell populations. Dev. Biol. 161, 243 250.
22. Jang Y. K., Park J. J., Lee M. C., Yoon B. H., Yang Y. S., Yang S. E. Kim S. U. (2004) Retinoic acid-mediated induction of neurons and glial cells from human umbilical cord-derived hematopoietic stem cells. J. Neurosci. Res. 75, 573 584.
23. Koubova J., Menke D. B., Zhou Q., Capel B., Griswold M. D. Page D. C. (2006) Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl Acad. Sci. USA 103, 2474 2479.
24. Lane M. A. Bailey S. J. (2005) Role of retinoid signalling in the adult brain. Prog. Neurobiol. 75, 275 293.
25. Li W., Cogswell C. A. LoTurco J. J. (1998) Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP. J. Neurosci. 18, 8853 8862.
26. Li Y., Hashimoto Y., Agadir A., Kagechika H. Zhang X. (1999) Identification of a novel class of retinoic acid receptor beta-selective retinoid antagonists and their inhibitory effects on AP-1 activity and retinoic acid-induced apoptosis in human breast cancer cells. J. Biol. Chem. 274, 15360 15366.
27. Lillien L. E., Sendtner M., Rohrer H., Hughes S. M. Raff M. C. (1988) Type-2 astrocyte development in rat brain cultures is initiated by a CNTF-like protein produced by type-1 astrocytes. Neuron 1, 485 494.
28. Liu L., Cavanaugh J. E., Wang Y., Sakagami H., Mao Z. Xia Z. (2003) ERK5 activation of MEF2-mediated gene expression plays a critical role in BDNF-promoted survival of developing but not mature cortical neurons. Proc. Natl Acad. Sci. USA 100, 8532 8537.
29. Liu L., Cundiff P., Abel G., Wang Y., Faigle R., Sakagami H., Xu M. Xia Z. (2006) Extracellular signal-regulated kinase (ERK) 5 is necessary and sufficient to specify cortical neuronal fate. Proc. Natl Acad. Sci. USA 103, 9697 9702.
30. Luskin M. B., Pearlman A. L. Sanes J. R. (1988) Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1, 635 647.
31. Mabie P. C., Mehler M. F., Marmur R., Papavasiliou A., Song Q. Kessler J. A. (1997) Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 17, 4112 4120.
32. Maden M. (2001) Role and distribution of retinoic acid during CNS development. Int. Rev. Cytol. 209, 1 77.
33. Mark M., Ghyselinck N. B. Chambon P. (2006) Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 46, 451 480.
34. Martin B., Bernardon J. M., Cavey M. T., Bernard B., Carlavan I., Charpentier B., Pilgrim W. R., Shroot B. Reichert U. (1992) Selective synthetic ligands for human nuclear retinoic acid receptors. Skin Pharmacol. 5, 57 65.
35. Matt N., Ghyselinck N. B., Wendling O., Chambon P. Mark M. (2003) Retinoic acid-induced developmental defects are mediated by RARbeta/RXR heterodimers in the pharyngeal endoderm. Development (Cambridge, England) 130, 2083 2093.
36. Mehler M. F., Mabie P. C., Zhu G., Gokhan S. Kessler J. A. (2000) Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate. Dev. Neurosci. 22, 74 85.
37. Mey J. McCaffery P. (2004) Retinoic acid signaling in the nervous system of adult vertebrates. Neuroscientist 10, 409 421.
38. Miller F. D. Gauthier A. S. (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54, 357 369.
39. Molne M., Studer L., Tabar V., Ting Y. T., Eiden M. V. McKay R. D. (2000) Early cortical precursors do not undergo LIF-mediated astrocytic differentiation. J. Neurosci. Res. 59, 301 311.
40. Morrow T., Song M. R. Ghosh A. (2001) Sequential specification of neurons and glia by developmentally regulated extracellular factors. Development (Cambridge, England) 128, 3585 3594.
41. Nakajima K., Yamanaka Y., Nakae K. et al. (1996) A central role for Stat3 in IL-6-induced regulation of growth and differentiation in M1 leukemia cells. EMBO J. 15, 3651 3658.
42. Nakashima K., Yanagisawa M., Arakawa H., Kimura N., Hisatsune T., Kawabata M., Miyazono K. Taga T. (1999) Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science (New York, N.Y.) 284, 479 482.
43. Niederreither K., Vermot J., Schuhbaur B., Chambon P. Dolle P. (2000) Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development (Cambridge, England) 127, 75 85.
44. Noll E. Miller R. H. (1994) Regulation of oligodendrocyte differentiation: a role for retinoic acid in the spinal cord. Development (Cambridge, England) 120, 649 660.
45. Ochiai W., Yanagisawa M., Takizawa T., Nakashima K. Taga T. (2001) Astrocyte differentiation of fetal neuroepithelial cells involving cardiotrophin-1-induced activation of STAT3. Cytokine 14, 264 271.
46. Poser S., Impey S., Xia Z. Storm D. R. (2003) Brain-derived neurotrophic factor protection of cortical neurons from serum withdrawal-induced apoptosis is inhibited by cAMP. J. Neurosci. 23, 4420 4427.
47. Radominska-Pandya A., Chen G., Czernik P. J., Little J. M., Samokyszyn V. M., Carter C. A. Nowak G. (2000) Direct interaction of all-trans-retinoic acid with protein kinase C (PKC). Implications for PKC signaling and cancer therapy. J. Biol. Chem. 275, 22324 22330.
48. Reynolds B. A. Weiss S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science (New York, N.Y.) 255, 1707 1710.
49. Ross S. E., Greenberg M. E. Stiles C. D. (2003) Basic helix-loop-helix factors in cortical development. Neuron 39, 13 25.
50. Santa-Olalla J., Baizabal J. M., Fregoso M., del Carmen Cardenas M. Covarrubias L. (2003) The in vivo positional identity gene expression code is not preserved in neural stem cells grown in culture. Eur. J. Neurosci. 18, 1073 1084.
51. Sauvageot C. M. Stiles C. D. (2002) Molecular mechanisms controlling cortical gliogenesis. Curr. Opin. Neurobiol. 12, 244 249.
52. Schoenermark M. P., Mitchell T. I., Rutter J. L., Reczek P. R. Brinckerhoff C. E. (1999) Retinoid-mediated suppression of tumor invasion and matrix metalloproteinase synthesis. Ann. N. Y. Acad. Sci. 878, 466 486.
53. Schulze G. E., Clay R. J., Mezza L. E., Bregman C. L., Buroker R. A. Frantz J. D. (2001) BMS-189453, a novel retinoid receptor antagonist, is a potent testicular toxin. Toxicol. Sci. 59, 297 308.
54. Setoguchi T. Kondo T. (2004) Nuclear export of OLIG2 in neural stem cells is essential for ciliary neurotrophic factor-induced astrocyte differentiation. J. Cell Biol. 166, 963 968.
55. Sheikh M. S., Shao Z. M., Li X. S. et al. (1994) Retinoid-resistant estrogen receptor-negative human breast carcinoma cells transfected with retinoic acid receptor-alpha acquire sensitivity to growth inhibition by retinoids. J. Biol. Chem. 269, 21440 21447.
56. Staines W. A., Craig J., Reuhl K. McBurney M. W. (1996) Retinoic acid treated P19 embryonal carcinoma cells differentiate into oligodendrocytes capable of myelination. Neuroscience 71, 845 853.
57. Stockli K. A., Lillien L. E., Naher-Noe M., Breitfeld G., Hughes R. A., Raff M. C., Thoenen H. Sendtner M. (1991) Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain. J. Cell Biol. 115, 447 459.
58. Sugimori M., Nagao M., Bertrand N., Parras C. M., Guillemot F. Nakafuku M. (2007) Combinatorial actions of patterning and HLH transcription factors in the spatiotemporal control of neurogenesis and gliogenesis in the developing spinal cord. Development (Cambridge, England) 134, 1617 1629.
59. Sun Y., Nadal-Vicens M., Misono S., Lin M. Z., Zubiaga A., Hua X., Fan G. Greenberg M. E. (2001) Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104, 365 376.
60. Takahashi T., Goto T., Miyama S., Nowakowski R. S. Caviness Jr V. S. (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.
61. Takizawa T., Nakashima K., Namihira M., Ochiai W., Uemura A., Yanagisawa M., Fujita N., Nakao M. Taga T. (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. cell 1, 749 758.
62. Tanigaki K., Nogaki F., Takahashi J., Tashiro K., Kurooka H. Honjo T. (2001) Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29, 45 55.
63. Tsai S., Bartelmez S., Heyman R., Damm K., Evans R. Collins S. J. (1992) A mutated retinoic acid receptor-alpha exhibiting dominant-negative activity alters the lineage development of a multipotent hematopoietic cell line. Genes Dev. 6, 2258 2269.
64. Uemura A., Takizawa T., Ochiai W., Yanagisawa M., Nakashima K. Taga T. (2002) Cardiotrophin-like cytokine induces astrocyte differentiation of fetal neuroepithelial cells via activation of STAT3. Cytokine 18, 1 7.
65. Viti J., Feathers A., Phillips J. Lillien L. (2003) Epidermal growth factor receptors control competence to interpret leukemia inhibitory factor as an astrocyte inducer in developing cortex. J. Neurosci. 23, 3385 3393.
66. Vivat-Hannah V., You D., Rizzo C., Daris J. P., Lapointe P., Zusi F. C., Marinier A., Lorenzi M. V. Gottardis M. M. (2001) Synergistic cytotoxicity exhibited by combination treatment of selective retinoid ligands with taxol (Paclitaxel). Cancer Res. 61, 8703 8711.
67. Wendling O., Ghyselinck N. B., Chambon P. Mark M. (2001) Roles of retinoic acid receptors in early embryonic morphogenesis and hindbrain patterning. Development (Cambridge, England) 128, 2031 2038.
68. White J. C., Shankar V. N., Highland M., Epstein M. L., DeLuca H. F. Clagett-Dame M. (1998) Defects in embryonic hindbrain development and fetal resorption resulting from vitamin A deficiency in the rat are prevented by feeding pharmacological levels of all-trans-retinoic acid. Proc. Natl Acad. Sci. USA 95, 13459 13464.
69. Wilson J. G., Roth C. B. Warkany J. (1953) An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am. J. Anat. 92, 189 217.
70. Wuarin L., Sidell N. de Vellis J. (1990) Retinoids increase perinatal spinal cord neuronal survival and astroglial differentiation. Int. J. Dev. Neurosci. 8, 317 326.
71. Yanagisawa M., Nakashima K. Taga T. (1999) STAT3-mediated astrocyte differentiation from mouse fetal neuroepithelial cells by mouse oncostatin M. Neurosci. Lett. 269, 169 172.