Orphan nuclear receptor TLX regulates astrogenesis by modulating BMP signaling

Frontiers in Neuroscience

Volumn , Issue 8 APR, 2014, Pages

  Qin, Song ^a,b   Niu, Wenze ^b   Iqbal, Nida ^b   Smith, Derek K ^b   Zhang, Chun Li ^b  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Astrogenesis; BMP SMAD signaling; Neural stem cells; Neurogenesis; Nuclear receptor; Tlx

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; GLIAL FIBRILLARY ACIDIC PROTEIN; INHIBITOR OF DIFFERENTIATION 3; ORPHAN NUCLEAR RECEPTOR; ORPHAN NUCLEAR RECEPTOR TLX; PROTEIN S100B; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROGENESIS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENHANCER REGION; GEL MOBILITY SHIFT ASSAY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84904911049     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00074     Document Type: Article

References (44)

1. Attisano, L., and Wrana, J. L. (2000). Smads as transcriptional co-modulators. Curr. Opin. Cell Biol. 12, 235-243. doi: 10.1016/S0955-0674(99)00081-2
2. Bonaguidi, M. A., Peng, C. Y., McGuire, T., Falciglia, G., Gobeske, K. T., Czeisler, C., et al. (2008). Noggin expands neural stem cells in the adult hippocampus. J. Neurosci. 28, 9194-9204. doi: 10.1523/JNEUROSCI.3314-07.2008
3. Bond, A. M., Bhalala, O. G., and Kessler, J. A. (2012). The dynamic role of bone morphogenetic proteins in neural stem cell fate and maturation. Dev. Neurobiol. 72, 1068-1084. doi: 10.1002/dneu.22022
4. Bonni, A., Sun, Y., Nadal-Vicens, M., Bhatt, A., Frank, D. A., Rozovsky, I., et al. (1997). Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278, 477-483. doi: 10.1126/science.278.5337.477
5. Colak, D., Mori, T., Brill, M. S., Pfeifer, A., Falk, S., Deng, C., et al. (2008). Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J. Neurosci. 28, 434-446. doi: 10.1523/JNEUROSCI.4374-07.2008
6. Dahlqvist, C., Blokzijl, A., Chapman, G., Falk, A., Dannaeus, K., Ibanez, C. F., et al. (2003). Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130, 6089-6099. doi: 10.1242/dev.00834
7. Doetsch, F. (2003). The glial identity of neural stem cells. Nat. Neurosci. 6, 1127-1134. doi: 10.1038/nn1144
8. Gomes, W. A., Mehler, M. F., and Kessler, J. A. (2003). Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev. Biol. 255, 164-177. doi: 10.1016/S0012-1606(02)00037-4
9. Gross, R. E., Mehler, M. F., Mabie, P. C., Zang, Z., Santschi, L., and Kessler, J. A. (1996). Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595-606. doi: 10.1016/S0896-6273(00)80193-2
10. Guillemot, F. (2007). Cell fate specification in the mammalian telencephalon. Prog. Neurobiol. 83, 37-52. doi: 10.1016/j.pneurobio.2007.02.009
11. He, F., Ge, W., Martinowich, K., Becker-Catania, S., Coskun, V., Zhu, W., et al. (2005). A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat. Neurosci. 8, 616-625. doi: 10.1038/nn1440
12. Itasaki, N., and Hoppler, S. (2010). Crosstalk between Wnt and bone morphogenic protein signaling: a turbulent relationship. Dev. Dyn. 239, 16-33. doi: 10.1002/dvdy.22009
13. Kriegstein, A., and Alvarez-Buylla, A. (2009). The glial nature of embryonic and adult neural stem cells. Annu. Rev. Neurosci. 32, 149-184. doi: 10.1146/annurev.neuro.051508.135600
14. Land, P. W., and Monaghan, A. P. (2003). Expression of the transcription factor, tailless, is required for formation of superficial cortical layers. Cereb. Cortex 13, 921-931. doi: 10.1093/cercor/13.9.921
15. Liu, H. K., Belz, T., Bock, D., Takacs, A., Wu, H., Lichter, P., et al. (2008). The nuclear receptor tailless is required for neurogenesis in the adult subventricular zone. Genes Dev. 22, 2473-2478. doi: 10.1101/gad.479308
16. Li, W., Sun, G., Yang, S., Qu, Q., Nakashima, K., and Shi, Y. (2008). Nuclear receptor TLX regulates cell cycle progression in neural stem cells of the developing brain. Mol. Endocrinol. 22, 56-64. doi: 10.1210/me.2007-0290
17. Miller, F. D., and Gauthier, A. S. (2007). Timing is everything: making neurons versus glia in the developing cortex. Neuron 54, 357-369. doi: 10.1016/j.neuron.2007.04.019
18. Mira, H., Andreu, Z., Suh, H., Lie, D. C., Jessberger, S., Consiglio, A., et al. (2010). Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell 7, 78-89. doi: 10.1016/j.stem.2010.04.016
19. Miyawaki, T., Uemura, A., Dezawa, M., Yu, R. T., Ide, C., Nishikawa, S., et al. (2004). Tlx, an orphan nuclear receptor, regulates cell numbers and astrocyte development in the developing retina. J. Neurosci. 24, 8124-8134. doi: 10.1523/JNEUROSCI.2235-04.2004
20. Monaghan, A. P., Bock, D., Gass, P., Schwager, A., Wolfer, D. P., Lipp, H. P., et al. (1997). Defective limbic system in mice lacking the tailless gene. Nature 390, 515-517. doi: 10.1038/37364
21. Monaghan, A. P., Grau, E., Bock, D., and Schutz, G. (1995). The mouse homolog of the orphan nuclear receptor tailless is expressed in the developing forebrain. Development 121, 839-853.
22. Morrison, S. J., Perez, S. E., Qiao, Z., Verdi, J. M., Hicks, C., Weinmaster, G., et al. (2000). Transient notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101, 499-510. doi: 10.1016/S0092-8674(00)80860-0
23. Nakashima, K., Takizawa, T., Ochiai, W., Yanagisawa, M., Hisatsune, T., Nakafuku, M., et al. (2001). BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc. Natl. Acad. Sci. U.S.A. 98, 5868-5873. doi: 10.1073/pnas.101109698
24. Nakashima, K., Yanagisawa, M., Arakawa, H., Kimura, N., Hisatsune, T., Kawabata, M., et al. (1999). Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284, 479-482. doi: 10.1126/science.284.5413.479
25. Niu, W., Zou, Y., Shen, C., and Zhang, C. L. (2011). Activation of postnatal neural stem cells requires nuclear receptor TLX. J. Neurosci. 31, 13816-13828. doi: 10.1523/JNEUROSCI.1038-11.2011
26. Obernier, K., Simeonova, I., Fila, T., Mandl, C., Holzl-Wenig, G., Monaghan-Nichols, P., et al. (2011). Expression of Tlx in both stem cells and transit amplifying progenitors regulates stem cell activation and differentiation in the neonatal lateral subependymal zone. Stem Cells 29, 1415-1426. doi: 10.1002/stem.682
27. Qin, S., Liu, M., Niu, W., and Zhang, C. L. (2011). Dysregulation of Kruppel-like factor 4 during brain development leads to hydrocephalus in mice. Proc. Natl. Acad. Sci. U.S.A. 108, 21117-21121. doi: 10.1073/pnas.1112351109
28. Qin, S., and Zhang, C. L. (2012). Role of Kruppel-like factor 4 in neurogenesis and radial neuronal migration in the developing cerebral cortex. Mol. Cell. Biol. 32, 4297-4305. doi: 10.1128/MCB.00838-12
29. Qin, S., Zou, Y., and Zhang, C. L. (2013). Cross-talk between KLF4 and STAT3 regulates axon regeneration. Nat. Commun. 4, 2633. doi: 10.1038/ncomms3633
30. Qu, Q., Sun, G., Li, W., Yang, S., Ye, P., Zhao, C., et al. (2010). Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat. Cell Biol. 12, 31-40. doi: 10.1038/ncb2001
31. Roy, K., Kuznicki, K., Wu, Q., Sun, Z., Bock, D., Schutz, G., et al. (2004). The Tlx gene regulates the timing of neurogenesis in the cortex. J. Neurosci. 24, 8333-8345. doi: 10.1523/JNEUROSCI.1148-04.2004
32. Sehgal, R., Sheibani, N., Rhodes, S. J., and Belecky Adams, T. L. (2009). BMP7 and SHH regulate Pax2 in mouse retinal astrocytes by relieving TLX repression. Dev. Biol. 332, 429-443. doi: 10.1016/j.ydbio.2009.05.579
33. Shi, Y., Chichung Lie, D., Taupin, P., Nakashima, K., Ray, J., Yu, R. T., et al. (2004). Expression and function of orphan nuclear receptor TLX in adult neural stem cells. Nature 427, 78-83. doi: 10.1038/nature02211
34. Sun, G., Yu, R. T., Evans, R. M., and Shi, Y. (2007). Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 104, 15282-15287. doi: 10.1073/pnas.0704089104
35. Temple, S. (2001). The development of neural stem cells. Nature 414, 112-117. doi: 10.1038/35102174
36. Ullian, E. M., Sapperstein, S. K., Christopherson, K. S., and Barres, B. A. (2001). Control of synapse number by glia. Science 291, 657-661. doi: 10.1126/science.291.5504.657
37. Wrana, J. L. (2000). Regulation of smad activity. Cell 100, 189-192. doi: 10.1016/S0092-8674(00)81556-1
38. Yamaguchi, M., Saito, H., Suzuki, M., and Mori, K. (2000). Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport 11, 1991-1996. doi: 10.1097/00001756-200006260-00037
39. Yokoyama, A., Takezawa, S., Schule, R., Kitagawa, H., and Kato, S. (2008). Transrepressive function of TLX requires the histone demethylase LSD1. Mol. Cell. Biol. 28, 3995-4003. doi: 10.1128/MCB.02030-07
40. Yu, R. T., Chiang, M. Y., Tanabe, T., Kobayashi, M., Yasuda, K., Evans, R. M., et al. (2000). The orphan nuclear receptor Tlx regulates Pax2 and is essential for vision. Proc. Natl. Acad. Sci. U.S.A. 97, 2621-2625. doi: 10.1073/pnas.050566897
41. Yu, R. T., McKeown, M., Evans, R. M., and Umesono, K. (1994). Relationship between Drosophila gap gene tailless and a vertebrate nuclear receptor Tlx. Nature 370, 375-379. doi: 10.1038/370375a0
42. Zhang, C. L., Zou, Y., He, W., Gage, F. H., and Evans, R. M. (2008). A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451, 1004-1007. doi: 10.1038/nature06562
43. Zhang, C. L., Zou, Y., Yu, R. T., Gage, F. H., and Evans, R. M. (2006). Nuclear receptor TLX prevents retinal dystrophy and recruits the corepressor atrophin1. Genes Dev. 20, 1308-1320. doi: 10.1101/gad.1413606
44. Zou, Y., Niu, W., Qin, S., Downes, M., Burns, D. K., and Zhang, C. L. (2012). The nuclear receptor TLX is required for gliomagenesis within the adult neurogenic niche. Mol. Cell. Biol. 32, 4811-4820. doi: 10.1128/MCB.01122-12