Astroglia-derived retinoic acid is a key factor in glia-induced neurogenesis

FASEB Journal

Volumn 21, Issue 10, 2007, Pages 2496-2509

  Kornyei Z ^a,e   Gocza E ^b   Ruhl R ^c   Orsolits, B ^a   Voros E ^a   Szabo B ^d   Vagovits B ^a   Madarasz E ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

^c UNIVERSITY OF DEBRECEN   (Hungary)

^d EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Astrocyte; Neuronal differentiation; RA; Stem cell

Indexed keywords

4 [2 [5,6 DIHYDRO 5,5 DIMETHYL 8 (4 METHYLPHENYL) 2 NAPHTHYL]ETHYNYL]BENZOIC ACID; RETINOIC ACID;

ANIMAL CELL; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; MACROGLIA; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AGING; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BRAIN; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; GENES, REPORTER; MICE; MICE, TRANSGENIC; MORPHOGENESIS; NEUROGLIA; NEURONS; STEM CELLS; TRETINOIN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 34547807203     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7756com     Document Type: Article

References (50)

1. Ma, D. K., Ming, G. L., and Song, H. (2005) Glial influences on neural stem cell development: cellular niches for adult neurogenesis. Curr. Opin. Neurobiol. 15, 514-520
2. Nicole, O., Ali, C., Docagne, F., Plawinski, L., MacKenzie, E. T., Vivien, D., and Buisson, A. (2001) Neuroprotection mediated by glial cell line-derived neurotrophic factor: involvement of a reduction of NMDA-induced calcium influx by the mitogen-activated protein kinase pathway. J. Neurosci. 21, 3024-3033
3. Chen, Y., Ai, Y., Slevin, J. R., Maley, B. E., and Gash, D. M. (2005) Progenitor proliferation in the adult hippocampus and substantia nigra induced by glial cell line-derived neurotrophic factor. Exp. Neurol. 196, 87-95
4. Ueki, T., Tanaka, M.,Yamashita, K., Mikawa, S., Fu Qiu, Z., Maragakis, N. J., Hevner, R. F., Miura, N., Sugimura, H., and Sato, K. (2003) A novel secretory factor, neurogenesin-1, provides neurogenic environmental cues for neural stem cells in the adult hippocampus. J. Neurosci. 23,11732-11740
5. Wagner, J., Akerud, P., Castro, D. S., Holm, P. C., Canals, J. M., Snyder, E. Y., Perlmann, T., and Arenas, E. (1999) Induction of a midbrain dopaminergic phenotype in Nurr1-overexpressing neural stem cells by type 1 astrocytes. Nat. Biotechnol. 17, 653-659
6. Hall, A. C., Mira, H., Wagner, J., and Arenas, E. (2003) Region-specific effects of glia on neuronal induction and differentiation with a focus on dopaminergic neurons. Glia 43, 47-51
7. Castelo-Branco, G., Sousa, K. M., Bryja, V., Pinto, L., Wagner, J., and Arenas, E. (2006) Ventral midbrain glia express region-specific transcription factors and regulate dopaminergic neurogenesis through Wnt-5a secretion. Mol. Cell. Neurosci. 31, 251-262
8. Lie, D. C., Colamarino, S. A., Song, H. J., Desire, L., Mira, H., Consiglio, A., Lein, E. S., Jessberger, S., Lansford, H., Dearie, A. R., and Gage, F. H. (2005) Wnt signalling regulates adult hippocampal neurogenesis. Nature 437, 1370-1375
9. Mey, J., and McCaffery, P. (2004) Retinoic acid signaling in the nervous system of adult vertebrates. Neuroscientist 10, 409-421
10. Lane, M., and Bailey, S. J. (2005) Role of retinoid signalling in the adult brain. Prog. Neurobiol. 75, 275-293
11. Denisenko-Nehrbass, N. I., Jarvis, E., Scharff, C., Nottebohm, F., and Mello, C. V. (2000) Site-specific retinoic acid production in the brain of adult songbirds. Neuron 27, 359-370
12. Crandall, J., Sakai, Y., Zhang, J., Koul, O., Mineur, Y., Crusio, W. E., and McCaffery, P. (2004) 13-cis-retinoic acid suppresses hippocampal cell division and hippocampal-dependent learning in mice. Proc. Natl. Acad. Sci. U. S. A. 101, 5111-5116
13. Wang, T. W., Zhang, H., and Parent, J. M. (2005) Retinoic acid regulates postnatal neurogenesis in the murine subventricular zone-olfactory bulb pathway. Development 132, 2721-2732
14. Haskell, G. T., and LaMantia, A. S. (2005) Retinoic acid signaling identifies a distinct precursor population in the developing and adult forebrain. J. Neurosci. 25, 7636-7647
15. Asson-Batres, M. A., and Smith, W. B. (2006) Localization of retinaldehyde dehydrogenases and retinoid binding proteins to sustentacular cells, glia, Bowman's gland cells, and stroma: potential sites of retinoic acid synthesis in the postnatal rat olfactory organ. J. Comp. Neurol. 496, 149-171
16. Jacobs, S., Lie, D. C., DeCicco, K. L., Shi, Y., DeLuca, L. M., Gage, F. H., and Evans, R. M. (2006) Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 103, 3902-3907
17. McCaffery, P., Zhang, J., and Crandall, J. E. (2006) Retinoic acid signaling and function in the adult hippocampus. J. Neurobiol. 66, 780-791
18. Rossant, J., Zirngibl, R., Cado, D., Shago, M., and Giguere, V. (1991) Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5, 1333-1344
19. Chattopadhyay, N., and Brown, E. M. (2001) Retinoic acid receptors are expressed in human primary astrocytes and their agonists inhibit parathyroid hormone-related peptide expression and secretion. Brain Res. Mol. Brain Res. 92,172-176
20. Esfandiari, A., Gagelin, C., Gavaret, J. M., Pavelka, S., Lennon, A. M., Pierre, M., and Courtin, F. (1994) Induction of type III-deiodinase activity in astroglial cells by retinoids. Glia 11, 255-261
21. Cedazo-Mínguez, A., Hamker, U., Meske, V., Veh, R W., Hellweg, R., Jacobi, C., Albert, F., Cowburn, R. F., and Ohm, T. G. (2001) Regulation of apolipoprotein E secretion in rat primary hippocampal astrocyte cultures. Neuroscience 105, 651-661
22. Choi, W. H., Ji, K. A., Jeon, S. B., Yang, M. S., Kim, H., Min, K., Shong, M., Jou, I., and Joe, E. H. (2005) Anti-inflammatory roles of retinoic acid in rat brain astrocytes: Suppression of interferon-gamma-induced JAK/STAT phosphorylation. Biochem. Biophys. Res. Commun. 329, 125-131
23. Wuarin, L., Sidell N., and de Vellis J. (1990) Retinoids increase perinatal spinal cord neuronal survival and astroglial differentiation. Int. J. Dev. Neurosci. 8(3):317-326
24. McCaffery P., Koul O., Smith D., Napoli, J. L., Chen N., and Ullman M. D. (2004) Ethanol increases retinoic acid production in astrocytes and in cerebellum. Brain Res. Dev. Brain Res. 153, 233-241
25. Környei, Z., Szlavik, V., Szabo, B., Gocza, E., Czirok, A., and Madarasz, E. (2005) Humoral and contact interactions in astroglia/stem cell co-cultures in the course of glia-induced neurogenesis. Glia 49, 430-444
26. Nolte, C., Matyash, M., Pivneva, T., Schipke, C. G., Ohlemeyer, C., Hanisch, U. K., Kirchhoff, F., and Kettenmann, H. (2001) GFAP promoter-controlled EGFP-expressing transgenic mice: a tool to visualize astrocytes and astrogliosis in living brain tissue. Glia 33, 72-86
27. Schlett, K., and Madarasz, E. (1997) Retinoic acid induced neural differentiation in a neuroectodermal cell line immortalized by p53 deficiency. J. Neurosci. Res. 47, 405-415
28. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J. (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 90, 8424-8428
29. Hadjantonakis, A. K., Gertsenstein, M., Ikawa, M., Okabe, M., and Nagy, A. (1998) Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev. 76, 79-90
30. Nagy, A., Gerstensten, M., Vintersten, K., and Behringer, R. (2003) Manipulating the Mouse Embryo, pp. 453-506, Cold Spring Harbor Press, Cold Spring Harbor, New York
31. Rühl, R. (2006) Method to determine 4-oxo-retinoic acids, retinoic acids and retinol in serum and cell extracts by liquid chromatography/diode- array detection atmospheric pressure chemical ionisation tandem mass spectrometry. Rapid Commun. Mass. Spectrom. 20, 2497-2504
32. Romand, R., Kondo, T., Fraulob, V., Petkovich, M., Dolle, P., and Hashino, E. (2006) Dynamic expression of retinoic acid-synthesizing and -metabolizing enzymes in the developing mouse inner ear. J. Comp. Neurol. 496, 643-654
33. Sonneveld, E., van den Brink, C. E., van der Leede, B. J., Maden, M., and van der Saag, P. T. (1999) Embryonal carcinoma cell lines stably transfected with mRARbeta2-lacZ: sensitive system for measuring levels of active retinoids. Exp. Cell Res. 250, 284-297
34. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
35. Johnson, A. T., Klein, E. S., Gillett, S. J., Wang, L., Song, T. K., Pino, M. E., and Chandraratna, R. A. (1995) Synthesis and characterization of a highly potent and effective antagonist of retinoic acid receptors. J. Med. Chem. 38, 4764-4767
36. Schmidt, C. K., Brouwer, A., and Nau, H. (2003) Chromatographic analysis of endogenous retinoids in tissues and serum. Anal. Biochem. 315, 36-48
37. Kane, M. A., Chen, N., Sparks, S., and Napoli, J. L. (2005) Quantification of endogenous retinoic acid in limited biological samples by LC/MS/MS. Biochem. J. 388, 363-369
38. Napoli, J. L. (1999) Retinoic acid: its biosynthesis and metabolism. Prog. Nucleic Acids Res. Mol. Biol. 63, 139-188
39. Tárnok, K., Pataki, A, Kovacs, J., Schlett, K., and Madarasz, E. (2002) Stage dependent effects of cell to cell contacts on in vitro induced neurogenesis by immortalised neuroectodermal progenitors. Eur. J. Cell Biol. 81, 403-412
40. Schlett, K., Czirok, A., Tárnok, K., Vicsek, T., and Madarasz, E. (2000) Dynamics of cell aggregation during in vitro neurogenesis by immortalized neuroectodermal progenitors. J. Neurosci. Res. 60, 184-194
41. Lim, D. A., and Alvarez-Buylla, A. (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 96, 7526-7531
42. Song, H., Stevens, C. F., and Gage, F. H. (2002) Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44
43. Nakayama, T., Momoki-Soga, T., and Inoue, N. (2003) Astrocyte-derived factors instruct differentiation of embryonic stem cells into neurons. Neurosci. Res. 46, 241-249
44. Luo, T., Wagner, E., Grun, F., and Drager, U. C. (2004) Retinoic acid signaling in the brain marks formation of optic projections, maturation of the dorsal telencephalon, and function of limbic sites. J. Comp. Neurol. 470, 297-316
45. Demeter, K., Herberth, B., Duda, E., Domonkos, A., Jaffredo, T., Herman, J. P., and Madarasz, E. (2004) Fate of cloned embryonic neuroectodermal cells implanted into the adult, newborn and embryonic forebrain. Exp. Neurol. 188, 254-267
46. Chadashvili, T., and Peterson, D. A. (2006) Cytoarchitecture of fibroblast growth factor receptor 2 (FGFR-2) immunoreactivity in astrocytes of neurogenic and non-neurogenic regions of the young adult and aged rat brain. J. Comp. Neurol. 498, 1-15
47. Aloisi, F., Rosa, S., Testa, U., Bonsi, P., Russo, G., Peschle, C., and Levi, G. (1994) Regulation of leukemia inhibitory factor synthesis in cultured human astrocytes. J. Immunol. 152, 5022-5031
48. Wobus, A. M., and Boheler, K. R. (2005) Embryonic stem cells: prospects for developmental biology and cell therapy. Physiol. Rev. 85, 635-678
49. Aouadi, M., Bost, F., Caron, L., Laurent, K., Le Marchand Brustel, Y., and Binetruy, B. (2006) p38 mitogen-activated protein kinase activity commits embryonic stem cells to either neurogenesis or cardiomyogenesis. Stem Cells 24, 1399-1406
50. Keegan, B. R., Feldman, J. L., Begemann, G., Ingham, P. W., and Yelon, D. (2005) Retinoic acid signaling restricts the cardiac progenitor pool. Science 307, 247-249