Quetiapine promotes oligodendroglial process outgrowth and membrane expansion by orchestrating the effects of Olig1.
GPR17
OPC differentiation
Olig1
process outgrowth
quetiapine
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
18
02
2021
received:
11
06
2020
accepted:
18
02
2021
pubmed:
5
3
2021
medline:
11
3
2022
entrez:
4
3
2021
Statut:
ppublish
Résumé
Oligodendroglial lineage cells go through a series of morphological changes before myelination. Prior to myelination, cell processes and membrane structures enlarge by approximately 7,000 times, which is required to support axonal wrapping and myelin segment formation. Failure of these processes leads to maldevelopment and impaired myelination. Quetiapine, an atypical antipsychotic drug, was proved to promote oligodendroglial differentiation and (re)myelination, pending detailed effects and regulatory mechanism. In this study, we showed that quetiapine promotes morphological maturation of oligodendroglial lineage cells and myelin segment formation, and a short-term quetiapine treatment is sufficient to induce these changes. To uncover the underlying mechanism, we examined the effect of quetiapine on the Oligodendrocyte transcription factor 1 (Olig1). We found that quetiapine upregulates Olig1 expression level and promotes nuclear Olig1 translocation to the cytosol, where it functions not as a transcription modulator, but in a way that highly correlates with oligodendrocyte morphological transformation. In addition, quetiapine treatment reverses the negative regulatory effect of the Olig1-regulated G protein-coupled receptor 17 (GPR17) on oligodendroglial morphological maturation. Our results demonstrate that quetiapine enhances oligodendroglial differentiation and myelination by promoting cell morphological transformation. This would shed light on the orchestration of oligodendroglia developmental mechanisms, and provides new targets for further therapeutic research.
Substances chimiques
Basic Helix-Loop-Helix Transcription Factors
0
Quetiapine Fumarate
2S3PL1B6UJ
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1709-1722Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Arnett, H. A., Fancy, S. P., Alberta, J. A., Zhao, C., Plant, S. R., Kaing, S., … Stiles, C. D. (2004). bHLH transcription factor Olig1 is required to repair demyelinated lesions in the CNS. Science, 306(5704), 2111-2115. https://doi.org/10.1126/science.1103709
Barateiro, A., Brites, D., & Fernandes, A. (2016). Oligodendrocyte development and myelination in neurodevelopment: Molecular mechanisms in health and disease. Current Pharmaceutical Design, 22(6), 656-679. https://doi.org/10.2174/1381612822666151204000636
Baron, W., & Hoekstra, D. (2010). On the biogenesis of myelin membranes: Sorting, trafficking and cell polarity. FEBS Letters, 584(9), 1760-1770. https://doi.org/10.1016/j.febslet.2009.10.085
Baumann, N., & Pham-Dinh, D. (2001). Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiological Reviews, 81(2), 871-927. https://doi.org/10.1152/physrev.2001.81.2.871
Bergles, D. E., & Richardson, W. D. (2015). Oligodendrocyte development and plasticity. Cold Spring Harbor Perspectives in Biology, 8(2), a020453. https://doi.org/10.1101/cshperspect.a020453
Boccazzi, M., Lecca, D., Marangon, D., Guagnini, F., Abbracchio, M. P., & Ceruti, S. (2016). A new role for the P2Y-like GPR17 receptor in the modulation of multipotency of oligodendrocyte precursor cells in vitro. Purinergic Signal, 12(4), 661-672. https://doi.org/10.1007/s11302-016-9530-7
Boda, E., Vigano, F., Rosa, P., Fumagalli, M., Labat-Gest, V., Tempia, F., … Buffo, A. (2011). The GPR17 receptor in NG2 expressing cells: Focus on in vivo cell maturation and participation in acute trauma and chronic damage. Glia, 59(12), 1958-1973. https://doi.org/10.1002/glia.21237
Bonfanti, E., Bonifacino, T., Raffaele, S., Milanese, M., Morgante, E., Bonanno, G., … Fumagalli, M. (2020). Abnormal upregulation of GPR17 receptor contributes to oligodendrocyte dysfunction in SOD1 G93A mice. International Journal of Molecular Sciences, 21(7), 2395. https://doi.org/10.3390/ijms21072395
Chen, X., Liu, H., Gan, J., Wang, X., Yu, G., Li, T., … Xiao, L. (2019). Quetiapine modulates histone methylation status in oligodendroglia and rescues adolescent behavioral alterations of socially isolated mice. Frontiers in Psychiatry, 10, 984. https://doi.org/10.3389/fpsyt.2019.00984
Chen, Y., Wu, H., Wang, S., Koito, H., Li, J., Ye, F., … Lu, Q. R. (2009). The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nature Neuroscience, 12(11), 1398-1406. https://doi.org/10.1038/nn.2410
Coppolino, G. T., Marangon, D., Negri, C., Menichetti, G., Fumagalli, M., Gelosa, P., … Abbracchio, M. P. (2018). Differential local tissue permissiveness influences the final fate of GPR17-expressing oligodendrocyte precursors in two distinct models of demyelination. Glia, 66(5), 1118-1130. https://doi.org/10.1002/glia.23305
Dai, J., Bercury, K. K., Jin, W., & Macklin, W. B. (2015). Olig1 acetylation and nuclear export mediate oligodendrocyte development. The Journal of Neuroscience, 35(48), 15875-15893. https://doi.org/10.1523/jneurosci.0882-15.2015
Emery, B. (2010). Regulation of oligodendrocyte differentiation and myelination. Science, 330(6005), 779-782. https://doi.org/10.1126/science.1190927
Emery, B., Agalliu, D., Cahoy, J. D., Watkins, T. A., Dugas, J. C., Mulinyawe, S. B., … Barres, B. A. (2009). Myelin gene regulatory factor is a critical transcriptional regulator required for CNS myelination. Cell, 138(1), 172-185. https://doi.org/10.1016/j.cell.2009.04.031
Fang, F., Zhang, H., Zhang, Y., Xu, H., Huang, Q., Adilijiang, A., … Li, X. M. (2013). Antipsychotics promote the differentiation of oligodendrocyte progenitor cells by regulating oligodendrocyte lineage transcription factors 1 and 2. Life Sciences, 93(12-14), 429-434. https://doi.org/10.1016/j.lfs.2013.08.004
Fumagalli, M., Daniele, S., Lecca, D., Lee, P. R., Parravicini, C., Fields, R. D., … Abbracchio, M. P. (2011). Phenotypic changes, signaling pathway, and functional correlates of GPR17-expressing neural precursor cells during oligodendrocyte differentiation. The Journal of Biological Chemistry, 286(12), 10593-10604. https://doi.org/10.1074/jbc.M110.162867
Fumagalli, M., Lecca, D., & Abbracchio, M. P. (2016). CNS remyelination as a novel reparative approach to neurodegenerative diseases: The roles of purinergic signaling and the P2Y-like receptor GPR17. Neuropharmacology, 104, 82-93. https://doi.org/10.1016/j.neuropharm.2015.10.005
Gonzalez Cardona, J., Smith, M. D., Wang, J., Kirby, L., Schott, J. T., Davidson, T., … Calabresi, P. A. (2019). Quetiapine has an additive effect to triiodothyronine in inducing differentiation of oligodendrocyte precursor cells through induction of cholesterol biosynthesis. PLoS One, 14(9), e0221747. https://doi.org/10.1371/journal.pone.0221747
Hennen, S., Wang, H., Peters, L., Merten, N., Simon, K., Spinrath, A., … Kostenis, E. (2013). Decoding signaling and function of the orphan G protein-coupled receptor GPR17 with a small-molecule agonist. Science Signaling, 6(298), ra93. https://doi.org/10.1126/scisignal.2004350
Ishii, A., Fyffe-Maricich, S. L., Furusho, M., Miller, R. H., & Bansal, R. (2012). ERK1/ERK2 MAPK signaling is required to increase myelin thickness independent of oligodendrocyte differentiation and initiation of myelination. The Journal of Neuroscience, 32(26), 8855-8864. https://doi.org/10.1523/jneurosci.0137-12.2012
Jain, R., Watson, U., Vasudevan, L., & Saini, D. K. (2018). ERK activation pathways downstream of GPCRs. International Review of Cell and Molecular Biology, 338, 79-109. https://doi.org/10.1016/bs.ircmb.2018.02.003
Jeffries, M. A., Urbanek, K., Torres, L., Wendell, S. G., Rubio, M. E., & Fyffe-Maricich, S. L. (2016). ERK1/2 activation in preexisting oligodendrocytes of adult mice drives new myelin synthesis and enhanced CNS function. The Journal of Neuroscience, 36(35), 9186-9200. https://doi.org/10.1523/JNEUROSCI.1444-16.2016
Lecca, D., Trincavelli, M. L., Gelosa, P., Sironi, L., Ciana, P., Fumagalli, M., … Abbracchio, M. P. (2008). The recently identified P2Y-like receptor GPR17 is a sensor of brain damage and a new target for brain repair. PLoS One, 3(10), e3579. https://doi.org/10.1371/journal.pone.0003579
Lee, S., Chong, S. Y., Tuck, S. J., Corey, J. M., & Chan, J. R. (2013). A rapid and reproducible assay for modeling myelination by oligodendrocytes using engineered nanofibers. Nature Protocols, 8(4), 771-782. https://doi.org/10.1038/nprot.2013.039
Li, H., Lu, Y., Smith, H. K., & Richardson, W. D. (2007). Olig1 and Sox10 interact synergistically to drive myelin basic protein transcription in oligodendrocytes. The Journal of Neuroscience, 27(52), 14375-14382. https://doi.org/10.1523/JNEUROSCI.4456-07.2007
Lu, C., Dong, L., Zhou, H., Li, Q., Huang, G., Bai, S. J., & Liao, L. (2018). G-protein-coupled receptor Gpr17 regulates oligodendrocyte differentiation in response to lysolecithin-induced demyelination. Scientific Reports, 8(1), 4502. https://doi.org/10.1038/s41598-018-22452-0
Lu, Q. R., Sun, T., Zhu, Z., Ma, N., Garcia, M., Stiles, C. D., & Rowitch, D. H. (2002). Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell, 109(1), 75-86. https://doi.org/10.1016/s0092-8674(02)00678-5
Ma, L., Yang, F., Zhao, R., Li, L., Kang, X., Xiao, L., & Jiang, W. (2015). Quetiapine attenuates cognitive impairment and decreases seizure susceptibility possibly through promoting myelin development in a rat model of malformations of cortical development. Brain Research, 1622, 443-451. https://doi.org/10.1016/j.brainres.2015.07.012
McIntyre, R. S., Soczynska, J. K., Woldeyohannes, H. O., Alsuwaidan, M., & Konarski, J. Z. (2007). A preclinical and clinical rationale for quetiapine in mood syndromes. Expert Opinion on Pharmacotherapy, 8(9), 1211-1219. https://doi.org/10.1517/14656566.8.9.1211
Mei, F., Fancy, S. P. J., Shen, Y. A., Niu, J., Zhao, C., Presley, B., … Chan, J. R. (2014). Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis. Nature Medicine, 20(8), 954-960. https://doi.org/10.1038/nm.3618
Mei, F., Guo, S., He, Y., Wang, L., Wang, H., Niu, J., … Xiao, L. (2012). Quetiapine, an atypical antipsychotic, is protective against autoimmune-mediated demyelination by inhibiting effector T cell proliferation. PLoS One, 7(8), e42746. https://doi.org/10.1371/journal.pone.0042746
Mi, G., Wang, Y., Ye, E., Gao, Y., Liu, Q., Chen, P., … Yang, Z. (2018). The antipsychotic drug quetiapine stimulates oligodendrocyte differentiation by modulating the cell cycle. Neurochemistry International, 118, 242-251. https://doi.org/10.1016/j.neuint.2018.04.001
Nasrallah, H. A. (2008). Atypical antipsychotic-induced metabolic side effects: Insights from receptor-binding profiles. Molecular Psychiatry, 13(1), 27-35. https://doi.org/10.1038/sj.mp.4002066
Niu, J., Mei, F., Wang, L., Liu, S., Tian, Y., Mo, W., … Xiao, L. (2012). Phosphorylated olig1 localizes to the cytosol of oligodendrocytes and promotes membrane expansion and maturation. Glia, 60(9), 1427-1436. https://doi.org/10.1002/glia.22364
Niu, J., Wang, L., Liu, S., Li, C., Kong, J., Shen, H. Y., & Xiao, L. (2012). An efficient and economical culture approach for the enrichment of purified oligodendrocyte progenitor cells. Journal of Neuroscience Methods, 209(1), 241-249. https://doi.org/10.1016/j.jneumeth.2012.05.032
Othman, A., Frim, D. M., Polak, P., Vujicic, S., Arnason, B. G., & Boullerne, A. I. (2011). Olig1 is expressed in human oligodendrocytes during maturation and regeneration. Glia, 59(6), 914-926. https://doi.org/10.1002/glia.21163
Ou, Z., Sun, Y., Lin, L., You, N., Liu, X., Li, H., … Chen, Y. (2016). Olig2-targeted G-protein-coupled receptor Gpr17 regulates oligodendrocyte survival in response to lysolecithin-induced demyelination. The Journal of Neuroscience, 36(41), 10560-10573. https://doi.org/10.1523/JNEUROSCI.0898-16.2016
Saher, G., & Stumpf, S. K. (2015). Cholesterol in myelin biogenesis and hypomyelinating disorders. Biochimica et Biophysica Acta, 1851(8), 1083-1094. https://doi.org/10.1016/j.bbalip.2015.02.010
Simon, K., Hennen, S., Merten, N., Blättermann, S., Gillard, M., Kostenis, E., & Gomeza, J. (2016). The orphan G protein-coupled receptor GPR17 negatively regulates oligodendrocyte differentiation via Gαi/o and its downstream effector molecules. The Journal of Biological Chemistry, 291(2), 705-718. https://doi.org/10.1074/jbc.M115.683953
Spiegelberg, B. D. (2013). G protein coupled-receptor signaling and reversible lysine acetylation. Journal of Receptor and Signal Transduction Research, 33(5), 261-266. https://doi.org/10.3109/10799893.2013.822889
Wang, H., Liu, S., Tian, Y., Wu, X., He, Y., Li, C., … Xiao, L. (2015). Quetiapine inhibits microglial activation by neutralizing abnormal STIM1-mediated intercellular calcium homeostasis and promotes myelin repair in a cuprizone-induced mouse model of demyelination. Frontiers in Cellular Neuroscience, 9, 492. https://doi.org/10.3389/fncel.2015.00492
Wang, H. N., Liu, G. H., Zhang, R. G., Xue, F., Wu, D., Chen, Y. C., … Tan, Q. R. (2015). Quetiapine ameliorates schizophrenia-like behaviors and protects myelin integrity in cuprizone intoxicated mice: The involvement of notch signaling pathway. The International Journal of Neuropsychopharmacology, 19(2), pyv088. https://doi.org/10.1093/ijnp/pyv088
Webster, H. D. (1971). The geometry of peripheral myelin sheaths during their formation and growth in rat sciatic nerves. The Journal of Cell Biology, 48(2), 348-367. https://doi.org/10.1083/jcb.48.2.348
Xiao, L., Xu, H., Zhang, Y., Wei, Z., He, J., Jiang, W., … Li, X. M. (2008). Quetiapine facilitates oligodendrocyte development and prevents mice from myelin breakdown and behavioral changes. Molecular Psychiatry, 13(7), 697-708. https://doi.org/10.1038/sj.mp.4002064
Xin, M., Yue, T., Ma, Z., Wu, F. F., Gow, A., & Lu, Q. R. (2005). Myelinogenesis and axonal recognition by oligodendrocytes in brain are uncoupled in Olig1-null mice. The Journal of Neuroscience, 25(6), 1354-1365. https://doi.org/10.1523/JNEUROSCI.3034-04.2005
Young, K. M., Psachoulia, K., Tripathi, R. B., Dunn, S. J., Cossell, L., Attwell, D., … Richardson, W. D. (2013). Oligodendrocyte dynamics in the healthy adult CNS: Evidence for myelin remodeling. Neuron, 77(5), 873-885. https://doi.org/10.1016/j.neuron.2013.01.006
Zhang, Y., Zhang, H. D., Fang, F., Xu, H. Y., Kong, L., Zhang, Z. J., … Li, X. M. (2014). EPA-1046-Antipsychotics promote the differentiation of oligodendrocyte progenitor cells by regulating oligodendrocyte lineage transcription factors 1 and 2. European Psychiatry, 29, 1. https://doi.org/10.1016/S0924-9338(14)78333-6
Zhao, H., Gao, X. Y., Liu, Z. H., Lin, J. W., Wang, S. P., Wang, D. X., & Zhang, Y. B. (2019). Effects of the transcription factor Olig1 on the differentiation and remyelination of oligodendrocyte precursor cells after focal cerebral ischemia in rats. Molecular Medicine Reports, 20(5), 4603-4611. https://doi.org/10.3892/mmr.2019.10713
Zhou, Q., & Anderson, D. J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell, 109(1), 61-73. https://doi.org/10.1016/s0092-8674(02)00677-3
Zuchero, J. B., & Barres, B. A. (2013). Intrinsic and extrinsic control of oligodendrocyte development. Current Opinion in Neurobiology, 23(6), 914-920. https://doi.org/10.1016/j.conb.2013.06.005