Abstract
White matter injury (WMI) prevents the normal development of myelination, leading to central nervous system myelination disorders and the production of chronic sequelae associated with WMI, such as chronic dyskinesia, cognitive impairment and cerebral palsy. This results in a large emotional and socioeconomic burden. Decreased myelination in preterm infant WMI is associated with the delayed development or destruction of oligodendrocyte (OL) lineage cells, particularly oligodendrocyte precursor cells (OPCs). The development of cells from the OL lineage involves the migration, proliferation and different stages of OL differentiation, finally leading to myelination. A series of complex intrinsic, extrinsic and epigenetic factors regulate the OPC cell cycle withdrawal, OL lineage progression and myelination. We focus on the inhibitor of DNA binding 2 (ID2), because it is widely involved in the different stages of OL differentiation and genesis. ID2 is a key transcription factor for the normal development of OL lineage cells, and the pathogenesis of WMI is closely linked with OL developmental disorders. ID4, another family member of the IDs protein, also plays a similar role in OL differentiation and genesis. ID2 and ID4 belong to the helix-loop-helix family; they lack the DNA-binding sequences and inhibit oligodendrogenesis and OPC differentiation. In this review, we mainly discuss the roles of ID2 in OL development, especially during OPC differentiation, and summarize the ID2-mediated intracellular and extracellular signaling pathways that regulate these processes. We also discuss ID4 in relation to bone morphogenetic protein signaling and oligodendrogenesis. It is likely that these developmental mechanisms are also involved in the myelin repair or remyelination in human neurological diseases.
Funding source: National Science Foundation of China
Award Identifier / Grant number: 81330016
Award Identifier / Grant number: 81630038
Award Identifier / Grant number: 81771634
Funding source: National Key Research and Development Program of China
Award Identifier / Grant number: 2017YFA0104200
Funding source: Ministry of Education of China
Award Identifier / Grant number: IRT0935
Funding source: Science and Technology Bureau of Sichuan Province
Award Identifier / Grant number: 2016TD0002
Funding source: Ministry of Health of China
Award Identifier / Grant number: 1311200003303
Funding statement: This work was supported by the National Science Foundation of China (Nos. 81330016, 81630038 and 81771634), the National Key Research and Development Program of China (No. 2017YFA0104200), the Ministry of Education of China (No. IRT0935), the Science and Technology Bureau of Sichuan Province (No. 2016TD0002) and by a grant of the clinical discipline program (Neonatology) from the Ministry of Health of China (1311200003303).
References
Araujo, F.M., Meola, J., Rosa, E.S.J.C., Paz, C.C.P., Ferriani, R.A., and Nogueira, A.A. (2017). Increased expression of ID2, PRELP and SMOC2 genes in patients with endometriosis. Braz. J. Med. Biol. Res. 50, e5782.10.1590/1414-431x20175782Suche in Google Scholar
Azim, K. and Butt, A.M. (2011). GSK3 beta negatively regulates oligodendrocyte differentiation and myelination in vivo. Glia 59, 540–553.10.1002/glia.21122Suche in Google Scholar PubMed
Azim, K., Fischer, B., Hurtado-Chong, A., Draganova, K., Cantu, C., Zemke, M., Sommer, L., Butt, A., and Raineteau, O. (2014). Persistent Wnt/beta-catenin signaling determines dorsalization of the postnatal subventricular zone and neural stem cell specification into oligodendrocytes and glutamatergic neurons. Stem Cells 32, 1301–1312.10.1002/stem.1639Suche in Google Scholar PubMed
Back, S.A. (2017). White matter injury in the preterm infant: pathology and mechanisms. Acta Neuropathol. 134, 331–349.10.1007/s00401-017-1718-6Suche in Google Scholar PubMed PubMed Central
Back, S.A. and Miller, S.P. (2014). Brain injury in premature neonates: a primary cerebral dysmaturation disorder? Ann. Neurol. 75, 469–486.10.1002/ana.24132Suche in Google Scholar PubMed PubMed Central
Back, S.A. and Rosenberg, P.A. (2014). Pathophysiology of glia in perinatal white matter injury. Glia 62, 1790–1815.10.1002/glia.22658Suche in Google Scholar PubMed PubMed Central
Back, S.A., Luo, N.L., Borenstein, N.S., Levine, J.M., Volpe, J.J., and Kinney, H.C. (2001). Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J. Neurosci. 21, 1302–1312.10.1523/JNEUROSCI.21-04-01302.2001Suche in Google Scholar PubMed PubMed Central
Back, S.A., Kroenke, C.D., Sherman, L.S., Lawrence, G., Gong, X., Taber, E.N., Sonnen, J.A., Larson, E.B., and Montine, T.J. (2011). White matter lesions defined by diffusion tensor imaging in older adults. Ann. Neurol. 70, 465–476.10.1002/ana.22484Suche in Google Scholar PubMed PubMed Central
Benezra, R., Davis, R.L., Lockshon, D., Turner, D.L., and Weintraub, H. (1990). The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61, 49–59.10.1016/0092-8674(90)90214-YSuche in Google Scholar
Bercury, K.K. and Macklin, W.B. (2015). Dynamics and mechanisms of CNS myelination. Dev. Cell. 32, 447–458.10.1016/j.devcel.2015.01.016Suche in Google Scholar PubMed PubMed Central
Blauwkamp, T.A., Chang, M.V., and Cadigan, K.M. (2008). Novel TCF-binding sites specify transcriptional repression by Wnt signalling. EMBO J. 27, 1436–1446.10.1038/emboj.2008.80Suche in Google Scholar
Buser, J.R., Maire, J., Riddle, A., Gong, X., Nguyen, T., Nelson, K., Luo, N.L., Ren, J., Struve, J., Sherman, L.S., et al. (2012). Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 71, 93–109.10.1002/ana.22627Suche in Google Scholar
Butt, A.M. and Berry, M. (2000). Oligodendrocytes and the control of myelination in vivo: new insights from the rat anterior medullary velum. J. Neurosci. Res. 59, 477–488.10.1002/(SICI)1097-4547(20000215)59:4<477::AID-JNR2>3.0.CO;2-JSuche in Google Scholar
Cate, H.S., Sabo, J.K., Merlo, D., Kemper, D., Aumann, T.D., Robinson, J., Merson, T.D., Emery, B., Perreau, V.M., and Kilpatrick, T.J. (2010). Modulation of bone morphogenic protein signalling alters numbers of astrocytes and oligodendroglia in the subventricular zone during cuprizone-induced demyelination. J. Neurochem. 115, 11–22.10.1111/j.1471-4159.2010.06660.xSuche in Google Scholar
Cavallo, R.A., Cox, R.T., Moline, M.M., Roose, J., Polevoy, G.A., Clevers, H., Peifer, M., and Bejsovec, A. (1998). Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395, 604–608.10.1038/26982Suche in Google Scholar
Chang, A., Nishiyama, A., Peterson, J., Prineas, J., and Trapp, B.D. (2000). NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J. Neurosci. 20, 6404–6412.10.1523/JNEUROSCI.20-17-06404.2000Suche in Google Scholar
Chen, X.S., Zhou, D.S., and Yao, Z.X. (2007). The inhibitor of DNA binding 2 is mainly expressed in oligodendrocyte lineage cells in adult rat brain. Neurosci. Lett. 428, 93–98.10.1016/j.neulet.2007.09.044Suche in Google Scholar
Chen, Y., Wu, H., Wang, S., Koito, H., Li, J., Ye, F., Hoang, J., Escobar, S.S., Gow, A., Arnett, H.A., et al. (2009). The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat. Neurosci. 12, 1398–1406.10.1038/nn.2410Suche in Google Scholar
Cheng, X., Wang, Y., He, Q., Qiu, M., Whittemore, S.R., and Cao, Q. (2007). Bone morphogenetic protein signaling and olig1/2 interact to regulate the differentiation and maturation of adult oligodendrocyte precursor cells. Stem Cells 25, 3204–3214.10.1634/stemcells.2007-0284Suche in Google Scholar
Chien, A.J., Conrad, W.H., and Moon, R.T. (2009). A Wnt survival guide: from flies to human disease. J. Invest. Dermatol. 129, 1614–1627.10.1038/jid.2008.445Suche in Google Scholar
Chong, S.W., Nguyen, T.T., Chu, L.T., Jiang, Y.J., and Korzh, V. (2005). Zebrafish id2 developmental expression pattern contains evolutionary conserved and species-specific characteristics. Dev. Dyn. 234, 1055–1063.10.1002/dvdy.20625Suche in Google Scholar PubMed
Coppolino, G.T., Marangon, D., Negri, C., Menichetti, G., Fumagalli, M., Gelosa, P., Dimou, L., Furlan, R., Lecca, D., and 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, 1118–1130.10.1002/glia.23305Suche in Google Scholar PubMed PubMed Central
Czepiel, M., Boddeke, E., and Copray, S. (2015). Human oligodendrocytes in remyelination research. Glia 63, 513–530.10.1002/glia.22769Suche in Google Scholar PubMed
Dai, Z.-M., Sun, S., Wang, C., Huang, H., Hu, X., Zhang, Z., Lu, Q.R., and Qiu, M. (2014). Stage-specific regulation of oligodendrocyte development by Wnt/beta-catenin signaling. J. Neurosci. 34, 8467–8473.10.1523/JNEUROSCI.0311-14.2014Suche in Google Scholar PubMed PubMed Central
Delconte, R.B., Shi, W., Sathe, P., Ushiki, T., Seillet, C., Minnich, M., Kolesnik, T.B., Rankin, L.C., Mielke, L.A., Zhang, J.G., et al. (2016). The helix-loop-helix protein ID2 governs NK cell fate by tuning their sensitivity to interleukin-15. Immunity 44, 103–115.10.1016/j.immuni.2015.12.007Suche in Google Scholar PubMed
Deshmukh, V.A., Tardif, V., Lyssiotis, C.A., Green, C.C., Kerman, B., Kim, H.J., Padmanabhan, K., Swoboda, J.G., Ahmad, I., Kondo, T., et al. (2013). A regenerative approach to the treatment of multiple sclerosis. Nature 502, 327–332.10.1038/nature12647Suche in Google Scholar PubMed PubMed Central
Dettman, R.W., Birch, D., Fernando, A., Kessler, J.A., and Dizon, M.L.V. (2018). Targeted knockdown of bone morphogenetic protein signaling within neural progenitors protects the brain and improves motor function following postnatal hypoxia-ischemia. Dev. Neurosci. 40, 23–38.10.1159/000485379Suche in Google Scholar PubMed PubMed Central
Dizon, M.L.V., Maa, T., and Kessler, J.A. (2011). The bone morphogenetic protein antagonist noggin protects white matter after perinatal hypoxia-ischemia. Neurobiol. Dis. 42, 318–326.10.1016/j.nbd.2011.01.023Suche in Google Scholar PubMed PubMed Central
Emery, B. (2010). Regulation of oligodendrocyte differentiation and myelination. Science 330, 779–782.10.1126/science.1190927Suche in Google Scholar PubMed
Fabbrizio, E., El Messaoudi, S., Polanowska, J., Paul, C., Cook, J.R., Lee, J.H., Negre, V., Rousset, M., Pestka, S., Le Cam, A., et al. (2002). Negative regulation of transcription by the type II arginine methyltransferase PRMT5. EMBO Rep. 3, 641–645.10.1093/embo-reports/kvf136Suche in Google Scholar PubMed PubMed Central
Fancy, S.P.J., Baranzini, S.E., Zhao, C., Yuk, D.-I., Irvine, K.-A., Kaing, S., Sanai, N., Franklin, R.J.M., and Rowitch, D.H. (2009). Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes Dev. 23, 1571–1585.10.1101/gad.1806309Suche in Google Scholar PubMed PubMed Central
Fancy, S.P.J., Harrington, E.P., Yuen, T.J., Silbereis, J.C., Zhao, C., Baranzini, S.E., Bruce, C.C., Otero, J.J., Huang, E.J., Nusse, R., et al. (2011). Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat. Neurosci. 14, 1009–1016.10.1038/nn.2855Suche in Google Scholar PubMed PubMed Central
Fancy, S.P.J., Harrington, E.P., Baranzini, S.E., Silbereis, J.C., Shiow, L.R., Yuen, T.J., Huang, E.J., Lomvardas, S., and Rowitch, D.H. (2014). Parallel states of pathological Wnt signaling in neonatal brain injury and colon cancer. Nat. Neurosci. 17, 506.10.1038/nn.3676Suche in Google Scholar PubMed PubMed Central
Franklin, R.J. (2015). Regenerative medicines for remyelination: from aspiration to reality. Cell Stem Cell 16, 576–577.10.1016/j.stem.2015.05.010Suche in Google Scholar PubMed
Freese, J.L., Pino, D., and Pleasure, S.J. (2010). Wnt signaling in development and disease. Neurobiol. Dis. 38, 148–153.10.1016/j.nbd.2009.09.003Suche in Google Scholar PubMed PubMed Central
Fukuda, S., Kondo, T., Takebayashi, H., and Taga, T. (2004). Negative regulatory effect of an oligodendrocytic bHLH factor OLIG2 on the astrocytic differentiation pathway. Cell Death Differ. 11, 196–202.10.1038/sj.cdd.4401332Suche in Google Scholar PubMed
Fumagalli, M., Lecca, D., and 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, 82–93.10.1016/j.neuropharm.2015.10.005Suche in Google Scholar PubMed
Gano, D., Andersen, S.K., Partridge, J.C., Bonifacio, S.L., Xu, D., Glidden, D.V., Ferriero, D.M., Barkovich, A.J., and Glass, H.C. (2015). Diminished white matter injury over time in a cohort of premature newborns. J. Pediatr. 166, 39–43.10.1016/j.jpeds.2014.09.009Suche in Google Scholar PubMed PubMed Central
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, 164–177.10.1016/S0012-1606(02)00037-4Suche in Google Scholar
Guillemot, F. (1999). Vertebrate bHLH genes and the determination of neuronal fates. Exp. Cell Res. 253, 357–364.10.1006/excr.1999.4717Suche in Google Scholar PubMed
Hara, E., Hall, M., and Peters, G. (1997). Cdk2-dependent phosphorylation of Id2 modulates activity of E2A-related transcription factors. EMBO J. 16, 332–342.10.1093/emboj/16.2.332Suche in Google Scholar PubMed PubMed Central
Harbour, J.W., Luo, R.X., Santi, A.D., Postigo, A.A., and Dean, D.C. (1999). Cdk phosphorylation triggers sequential intramolecular interactions that progressively block Rb functions as cells move through G1. Cell 98, 859–869.10.1016/S0092-8674(00)81519-6Suche in Google Scholar
Havrda, M.C., Paolella, B.R., Ran, C., Jering, K.S., Wray, C.M., Sullivan, J.M., Nailor, A., Hitoshi, Y., and Israel, M.A. (2014). Id2 mediates oligodendrocyte precursor cell maturation arrest and is tumorigenic in a PDGF-rich microenvironment. Cancer Res. 74, 1822–1832.10.1158/0008-5472.CAN-13-1839Suche in Google Scholar PubMed PubMed Central
Hecht, A. and Kemler, R. (2000). Curbing the nuclear activities of beta-catenin – control over Wnt target gene expression. EMBO Rep. 1, 24–28.10.1093/embo-reports/kvd012Suche in Google Scholar PubMed PubMed Central
Huang, J., Vogel, G., Yu, Z., Almazan, G., and Richard, S. (2011). Type II arginine methyltransferase PRMT5 regulates gene expression of inhibitors of differentiation/DNA binding Id2 and Id4 during glial cell differentiation. J. Biol. Chem. 286, 44424–44432.10.1074/jbc.M111.277046Suche in Google Scholar PubMed PubMed Central
Huang, Y., Rajappa, P., Hu, W., Hoffman, C., Cisse, B., Kim, J.H., Gorge, E., Yanowitch, R., Cope, W., Vartanian, E., et al. (2017). A proangiogenic signaling axis in myeloid cells promotes malignant progression of glioma. J. Clin. Invest. 127, 1826–1838.10.1172/JCI86443Suche in Google Scholar PubMed PubMed Central
Huddleston, J.E. (2011). Development a new move for PRMT5. Nat. Rev. Mol. Cell Biol. 12, 76.10.1038/nrm3056Suche in Google Scholar PubMed
Hughes, E.G., Kang, S.H., Fukaya, M., and Bergles, D.E. (2013). Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat. Neurosci. 16, 668–676.10.1038/nn.3390Suche in Google Scholar PubMed PubMed Central
Iavarone, A., Garg, P., Lasorella, A., Hsu, J., and Israel, M.A. (1994). The helix-loop-helix protein Id-2 enhances cell proliferation and binds to the retinoblastoma protein. Genes Dev. 8, 1270–1284.10.1101/gad.8.11.1270Suche in Google Scholar PubMed
Karkhanis, V., Hu, Y.-J., Baiocchi, R.A., Imbalzano, A.N., and Sif, S. (2011). Versatility of PRMT5-induced methylation in growth control and development. Trends Biochem. Sci. 36, 633–641.10.1016/j.tibs.2011.09.001Suche in Google Scholar PubMed PubMed Central
Keunen, K., Benders, M.J., Leemans, A., Fieret-Van Stam, P.C., Scholtens, L.H., Viergever, M.A., Kahn, R.S., Groenendaal, F., de Vries, L.S., and Van den Heuvel, M.P. (2017). White matter maturation in the neonatal brain is predictive of school age cognitive capacities in children born very preterm. Dev. Med. Child Neurol. 59, 939–946.10.1111/dmcn.13487Suche in Google Scholar PubMed
Khurana, T., Khurana, B., and Noegel, A.A. (2002). LIM proteins: association with the actin cytoskeleton. Protoplasma 219, 1–12.10.1007/s007090200000Suche in Google Scholar PubMed
Khwaja, O. and Volpe, J.J. (2008). Pathogenesis of cerebral white matter injury of prematurity. Arch. Dis. Child-Fetal. 93, F153–F161.10.1136/adc.2006.108837Suche in Google Scholar PubMed PubMed Central
Kitajima, K., Takahashi, R., and Yokota, Y. (2006). Localization of Id2 mRNA in the adult mouse brain. Brain Res. 1073–1074, 93–102.10.1016/j.brainres.2005.12.048Suche in Google Scholar PubMed
Kondo, T. and Raff, M. (2000). Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development 127, 2989–2998.10.1242/dev.127.14.2989Suche in Google Scholar PubMed
Kotter, M.R., Li, W.W., Zhao, C., and Franklin, R.J.M. (2006). Myelin impairs CNS remyelination by inhibiting oligodendrocyte precursor cell differentiation. J. Neurosci. 26, 328–332.10.1523/JNEUROSCI.2615-05.2006Suche in Google Scholar PubMed PubMed Central
Kremer, D., Aktas, O., Hartung, H.-P., and Kuery, P. (2011). The complex world of oligodendroglial differentiation inhibitors. Ann. Neurol. 69, 602–618.10.1002/ana.22415Suche in Google Scholar PubMed
Kurooka, H. and Yokota, Y. (2005). Nucleo-cytoplasmic shuttling of Id2, a negative regulator of basic helix-loop-helix transcription factors. J. Biol. Chem. 280, 4313–4320.10.1074/jbc.M412614200Suche in Google Scholar PubMed
Lasorella, A. and Iavarone, A. (2006). The protein ENH is a cytoplasmic sequestration factor for Id2 in normal and tumor cells from the nervous system. Proc. Natl. Acad. Sci. USA 103, 4976–4981.10.1073/pnas.0600168103Suche in Google Scholar PubMed PubMed Central
Lasorella, A., Iavarone, A., and Israel, M.A. (1996). Id2 specifically alters regulation of the cell cycle by tumor suppressor proteins. Mol. Cell Biol. 16, 2570–2578.10.1128/MCB.16.6.2570Suche in Google Scholar PubMed PubMed Central
Lasorella, A., Noseda, M., Beyna, M., Yokota, Y., and Iavarone, A. (2000). Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407, 592–598.10.1038/35036504Suche in Google Scholar PubMed
Lasorella, A., Stegmuller, J., Guardavaccaro, D., Liu, G., Carro, M.S., Rothschild, G., de la Torre-Ubieta, L., Pagano, M., Bonni, A., and Iavarone, A. (2006). Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442, 471–474.10.1038/nature04895Suche in Google Scholar PubMed
Lecca, D., Trincavelli, M.L., Gelosa, P., Sironi, L., Ciana, P., Fumagalli, M., Villa, G., Verderio, C., Grumelli, C., Guerrini, U., et al. (2008). The recently identified P2Y-like receptor GPR17 is a sensor of brain damage and a new target for brain repair. PLoS One 3, e3579.10.1371/journal.pone.0003579Suche in Google Scholar PubMed PubMed Central
Lee, D.K., George, S.R., Evans, J.F., Lynch, K.R., and O’Dowd, B.F. (2001). Orphan G protein-coupled receptors in the CNS. Curr. Opin. Pharmacol. 1, 31–39.10.1016/S1471-4892(01)00003-0Suche in Google Scholar
Levine, J.M. and Reynolds, R. (1999). Activation and proliferation of endogenous oligodendrocyte precursor cells during ethidium bromide-induced demyelination. Exp. Neurol. 160, 333–347.10.1006/exnr.1999.7224Suche in Google Scholar PubMed
Levine, J.M., Stincone, F., and Lee, Y.S. (1993). Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7, 307–321.10.1002/glia.440070406Suche in Google Scholar PubMed
Liu, L., Oza, S., Hogan, D., Chu, Y., Perin, J., Zhu, J., Lawn, J.E., Cousens, S., Mathers, C., and Black, R.E. (2016). Global, regional, and national causes of under-5 mortality in 2000–15: an updated systematic analysis with implications for the Sustainable Development Goals. Lancet 388, 3027–3035.10.1016/S0140-6736(16)31593-8Suche in Google Scholar PubMed PubMed Central
Mabie, P.C., Mehler, M.F., Marmur, R., Papavasiliou, A., Song, Q., and Kessler, J.A. (1997). Bone morphogenetic proteins induce astroglial differentiation of oligodendroglial-astroglial progenitor cells. J. Neurosci. 17, 4112–4120.10.1523/JNEUROSCI.17-11-04112.1997Suche in Google Scholar PubMed PubMed Central
Macara, I.G. (2001). Transport into and out of the nucleus. Microbiol. Mol. Biol. Rev. 65, 570–594.10.1128/MMBR.65.4.570-594.2001Suche in Google Scholar PubMed PubMed Central
Martinez-Biarge, M., Madero, R., Gonzalez, A., Quero, J., and Garcia-Alix, A. (2012). Perinatal morbidity and risk of hypoxic-ischemic encephalopathy associated with intrapartum sentinel events. Am. J. Obstet. Gynecol. 206, 148.e1–148.e7.10.1016/j.ajog.2011.09.031Suche in Google Scholar PubMed
Mekki-Dauriac, S., Agius, E., Kan, P., and Cochard, P. (2002). Bone morphogenetic proteins negatively control oligodendrocyte precursor specification in the chick spinal cord. Development 129, 5117–5130.10.1242/dev.129.22.5117Suche in Google Scholar
Memezawa, A., Takada, I., Takeyama, K., Igarashi, M., Ito, S., Aiba, S., Kato, S., and Kouzmenko, A.P. (2007). Id2 gene-targeted crosstalk between Wnt and retinoid signaling regulates proliferation in human keratinocytes. Oncogene 26, 5038–5045.10.1038/sj.onc.1210320Suche in Google Scholar
Mitew, S., Hay, C.M., Peckham, H., Xiao, J., Koenning, M., and Emery, B. (2014). Mechanisms regulating the development of oligodendrocytes and central nervous system myelin. Neuroscience 276, 29–47.10.1016/j.neuroscience.2013.11.029Suche in Google Scholar
Miyagi, M., Mikawa, S., Hasegawa, T., Sho, K., Matsuyama, Y., and Sato, K. (2011). Bone morphogenetic protein receptor expressions in the adult rat brain. Neuroscience 176, 93–109.10.1016/j.neuroscience.2010.12.027Suche in Google Scholar
Morgan, D.O. (1997). Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261–291.10.1146/annurev.cellbio.13.1.261Suche in Google Scholar
Nakashima, K., Yanagisawa, M., Arakawa, H., Kimura, N., Hisatsune, T., Kawabata, M., Miyazono, K., and Taga, T. (1999). Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284, 479–482.10.1126/science.284.5413.479Suche in Google Scholar
Nawaz, S., Sanchez, P., Schmitt, S., Snaidero, N., Mitkovski, M., Velte, C., Bruckner, B.R., Alexopoulos, I., Czopka, T., Jung, S.Y., et al. (2015). Actin filament turnover drives leading edge growth during myelin sheath formation in the central nervous system. Dev. Cell. 34, 139–151.10.1016/j.devcel.2015.05.013Suche in Google Scholar
Nishiyama, A., Lin, X.H., Giese, N., Heldin, C.H., and Stallcup, W.B. (1996). Interaction between NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells is required for optimal response to PDGF. J. Neurosci. Res. 43, 315–330.10.1002/(SICI)1097-4547(19960201)43:3<315::AID-JNR6>3.0.CO;2-MSuche in Google Scholar
Pierson, C.R., Folkerth, R.D., Billiards, S.S., Trachtenberg, F.L., Drinkwater, M.E., Volpe, J.J., and Kinney, H.C. (2007). Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol. 114, 619–631.10.1007/s00401-007-0295-5Suche in Google Scholar
Plemel, J.R., Manesh, S.B., Sparling, J.S., and Tetzlaff, W. (2013). Myelin inhibits oligodendroglial maturation and regulates oligodendrocytic transcription factor expression. Glia 61, 1471–1487.10.1002/glia.22535Suche in Google Scholar
Preston, M., Gong, X., Su, W., Matsumoto, S.G., Banine, F., Winkler, C., Foster, S., Xing, R., Struve, J., Dean, J., et al. (2013). Digestion products of the PH20 hyaluronidase inhibit remyelination. Ann. Neurol. 73, 266–280.10.1002/ana.23788Suche in Google Scholar PubMed PubMed Central
Reid, M.V., Murray, K.A., Marsh, E.D., Golden, J.A., Simmons, R.A., and Grinspan, J.B. (2012). Delayed myelination in an intrauterine growth retardation model is mediated by oxidative stress upregulating bone morphogenetic protein 4. J. Neuropathol. Exp. Neurol. 71, 640–653.10.1097/NEN.0b013e31825cfa81Suche in Google Scholar PubMed PubMed Central
Riddle, A., Dean, J., Buser, J.R., Gong, X., Maire, J., Chen, K., Ahmad, T., Cai, V., Nguyen, T., Kroenke, C.D., et al. (2011). Histopathological correlates of magnetic resonance imaging-defined chronic perinatal white matter injury. Ann. Neurol. 70, 493–507.10.1002/ana.22501Suche in Google Scholar PubMed PubMed Central
Riddle, A., Maire, J., Gong, X., Chen, K.X., Kroenke, C.D., Hohimer, A.R., and Back, S.A. (2012). Differential susceptibility to axonopathy in necrotic and non-necrotic perinatal white matter injury. Stroke 43, 178–184.10.1161/STROKEAHA.111.632265Suche in Google Scholar PubMed PubMed Central
Rockman, S.P., Currie, S.A., Ciavarella, M., Vincan, E., Dow, C., Thomas, R.J.S., and Phillips, W.A. (2001). Id2 is a target of the beta-catenin/T cell factor pathway in colon carcinoma. J. Biol. Chem. 276, 45113–45119.10.1074/jbc.M107742200Suche in Google Scholar PubMed
Roschger, C. and Cabrele, C. (2017). The Id-protein family in developmental and cancer-associated pathways. Cell Commun. Signal. 15, 7.10.1186/s12964-016-0161-ySuche in Google Scholar PubMed PubMed Central
Sabo, J.K., Heine, V., Silbereis, J.C., Schirmer, L., Levison, S.W., and Rowitch, D.H. (2017). Olig1 is required for noggin-induced neonatal myelin repair. Ann. Neurol. 81, 560–571.10.1002/ana.24907Suche in Google Scholar PubMed PubMed Central
Samanta, J. and Kessler, J.A. (2004). Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131, 4131–4142.10.1242/dev.01273Suche in Google Scholar PubMed
Sanchez, S.E., Petrillo, E., Beckwith, E.J., Zhang, X., Rugnone, M.L., Hernando, C.E., Cuevas, J.C., Herz, M.A.G., Depetris-Chauvin, A., Simpson, C.G., et al. (2010). A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468, 112–116.10.1038/nature09470Suche in Google Scholar PubMed
Scaglione, A., Patzig, J., Liang, J., Frawley, R., Bok, J., Mela, A., Yattah, C., Zhang, J., Teo, S.X., Zhou, T., et al. (2018). PRMT5-mediated regulation of developmental myelination. Nat. Commun. 9, 2840.10.1038/s41467-018-04863-9Suche in Google Scholar PubMed PubMed Central
See, J., Mamontov, P., Ahn, K., Wine-Lee, L., Crenshaw, E.B., III, and Grinspan, J.B. (2007). BMP signaling mutant mice exhibit glial cell maturation defects. Mol. Cell Neurosci. 35, 171–182.10.1016/j.mcn.2007.02.012Suche in Google Scholar PubMed PubMed Central
Selesniemi, K., Albers, R.E., and Brown, T.L. (2016). Id2 mediates differentiation of labyrinthine placental progenitor cell line, SM10. Stem Cells Dev. 25, 959–974.10.1089/scd.2016.0010Suche in Google Scholar PubMed PubMed Central
Sharma, P., Chinaranagari, S., and Chaudhary, J. (2015). Inhibitor of differentiation 4 (ID4) acts as an inhibitor of ID-1, -2 and -3 and promotes basic helix loop helix (bHLH) E47 DNA binding and transcriptional activity. Biochimie 112, 139–150.10.1016/j.biochi.2015.03.006Suche in Google Scholar PubMed PubMed Central
Shen, S.M., Li, J.D., and Casaccia-Bonnefil, P. (2005). Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J. Cell Biol. 169, 577–589.10.1083/jcb.200412101Suche in Google Scholar PubMed PubMed Central
Shen, S., Sandoval, J., Swiss, V.A., Li, J., Dupree, J., Franklin, R.J.M., and Casaccia-Bonnefil, P. (2008). Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci. 11, 1024–1034.10.1038/nn.2172Suche in Google Scholar PubMed PubMed Central
Sherr, C.J. and Roberts, J.M. (1999). CDK inhibitors: positive and negative regulators of G(1)-phase progression. Genes Dev. 13, 1501–1512.10.1101/gad.13.12.1501Suche in Google Scholar PubMed
Sullivan, J.M., Havrda, M.C., Kettenbach, A.N., Paolella, B.R., Zhang, Z., Gerber, S.A., and Israel, M.A. (2016). Phosphorylation regulates Id2 degradation and mediates the proliferation of neural precursor cells. Stem Cells 34, 1321–1331.10.1002/stem.2291Suche in Google Scholar PubMed PubMed Central
Sumida, T., Ishikawa, A., Nakano, H., Yamada, T., Mori, Y., and Desprez, P.Y. (2016). Targeting ID2 expression triggers a more differentiated phenotype and reduces aggressiveness in human salivary gland cancer cells. Genes Cells 21, 915–920.10.1111/gtc.12389Suche in Google Scholar PubMed
Sussman, C.R., Davies, J.E., and Miller, R.H. (2002). Extracellular and intracellular regulation of oligodendrocyte development: roles of sonic hedgehog and expression of E proteins. Glia 40, 55–64.10.1002/glia.10114Suche in Google Scholar PubMed
Tawk, M., Makoukji, J., Belle, M., Fonte, C., Trousson, A., Hawkins, T., Li, H., Ghandour, S., Schumacher, M., and Massaad, C. (2011). Wnt/beta-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J. Neurosci. 31, 3729–3742.10.1523/JNEUROSCI.4270-10.2011Suche in Google Scholar PubMed PubMed Central
Toma, J.G., El-Bizri, H., Barnabe-Heider, F., Aloyz, R., and Miller, F.D. (2000). Evidence that helix-loop-helix proteins collaborate with retinoblastoma tumor suppressor protein to regulate cortical neurogenesis. J. Neurosci. 20, 7648–7656.10.1523/JNEUROSCI.20-20-07648.2000Suche in Google Scholar PubMed PubMed Central
van Haastert, I.C., Groenendaal, F., Uiterwaal, C.S.P.M., Termote, J.U.M., van der Heide-Jalving, M., Eijsermans, M.J.C., Gorter, J.W., Helders, P.J.M., Jongmans, M.J., and de Vries, L.S. (2011). Decreasing incidence and severity of cerebral palsy in prematurely born children. J. Pediatr. 159, 86–U112.10.1016/j.jpeds.2010.12.053Suche in Google Scholar PubMed
van Tilborg, E., Heijnen, C.J., Benders, M.J., van Bel, F., Fleiss, B., Gressens, P., and Nijboer, C.H. (2016). Impaired oligodendrocyte maturation in preterm infants: potential therapeutic targets. Prog. Neurobiol. 136, 28–49.10.1016/j.pneurobio.2015.11.002Suche in Google Scholar PubMed
van Tilborg, E., de Theije, C.G.M., van Hal, M., Wagenaar, N., de Vries, L.S., Benders, M.J., Rowitch, D.H., and Nijboer, C.H. (2018). Origin and dynamics of oligodendrocytes in the developing brain: Implications for perinatal white matter injury. Glia 66, 221–238.10.1002/glia.23256Suche in Google Scholar PubMed PubMed Central
Volpe, J.J. (2009). Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 8, 110–124.10.1016/S1474-4422(08)70294-1Suche in Google Scholar PubMed PubMed Central
Volpe, J.J., Kinney, H.C., Jensen, F.E., and Rosenberg, P.A. (2011). The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int. J. Dev. Neurosci. 29, 423–440.10.1016/j.ijdevneu.2011.02.012Suche in Google Scholar PubMed PubMed Central
Wang, S.L., Sdrulla, A., Johnson, J.E., Yokota, Y., and Barres, B.A. (2001). A role for the helix-loop-helix protein Id2 in the control of oligodendrocyte development. Neuron 29, 603–614.10.1016/S0896-6273(01)00237-9Suche in Google Scholar PubMed
Wegner, M. and Stolt, C.C. (2005). From stem cells to neurons and glia: a Soxist’s view of neural development. Trends Neurosci. 28, 583–588.10.1016/j.tins.2005.08.008Suche in Google Scholar PubMed
Weinberg, R.A. (1995). The retinoblastoma protein and cell-cycle control. Cell 81, 323–330.10.1016/0092-8674(95)90385-2Suche in Google Scholar PubMed
Weintraub, H. (1993). The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241–1244.10.1016/0092-8674(93)90610-3Suche in Google Scholar PubMed
Wu, Y., Liu, Y., Levine, E.M., and Rao, M.S. (2003). Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors. Dev. Dyn. 226, 675–689.10.1002/dvdy.10278Suche in Google Scholar PubMed
Wu, M., Hernandez, M., Shen, S., Sabo, J.K., Kelkar, D., Wang, J., O’Leary, R., Phillips, G.R., Cate, H.S., and Casaccia, P. (2012). Differential modulation of the oligodendrocyte transcriptome by sonic hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation. J. Neurosci. 32, 6651–6664.10.1523/JNEUROSCI.4876-11.2012Suche in Google Scholar PubMed PubMed Central
Xiao, D., Qu, Y., Pan, L., Li, X., and Mu, D. (2018). MicroRNAs participate in the regulation of oligodendrocytes development in white matter injury. Rev. Neurosci. 29, 151–160.10.1515/revneuro-2017-0019Suche in Google Scholar PubMed
Yates, P.R., Atherton, G.T., Deed, R.W., Norton, J.D., and Sharrocks, A.D. (1999). Id helix-loop-helix proteins inhibit nucleoprotein complex formation by the TCF ETS-domain transcription factors. EMBO J. 18, 968–976.10.1093/emboj/18.4.968Suche in Google Scholar PubMed PubMed Central
Ye, F., Chen, Y., Hoang, T., Montgomery, R.L., Zhao, X.-h., Bu, H., Hu, T., Taketo, M.M., van Es, J.H., Clevers, H., et al. (2009). HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat. Neurosci. 12, 829–838.10.1038/nn.2333Suche in Google Scholar PubMed PubMed Central
Yokota, Y. (2001). Id and development. Oncogene 20, 8290–8298.10.1038/sj.onc.1205090Suche in Google Scholar PubMed
Yu, L., Liu, C.H., Vandeusen, J., Becknell, B., Dai, Z.Y., Wu, Y.Z., Raval, A., Liu, T.H., Ding, W., Mao, C., et al. (2005). Global assessment of promoter methylation in a mouse model of cancer identifies ID4 as a putative tumor-suppressor gene in human leukemia. Nat. Genet. 37, 265–274.10.1038/ng1521Suche in Google Scholar PubMed
Yu, Y., Casaccia, P., and Lu, Q.R. (2010). Shaping the oligodendrocyte identity by epigenetic control. Epigenetics 5, 124–128.10.4161/epi.5.2.11160Suche in Google Scholar PubMed PubMed Central
Yuen, T.J., Silbereis, J.C., Griveau, A., Chang, S.M., Daneman, R., Fancy, S.P.J., Zahed, H., Maltepe, E., and Rowitch, D.H. (2014). Oligodendrocyte-encoded HIF function couples postnatal myelination and white matter angiogenesis. Cell 158, 383–396.10.1016/j.cell.2014.04.052Suche in Google Scholar PubMed PubMed Central
Zhang, C., Zhang, Z., Shu, H., Liu, S., Song, Y., Qiu, K., and Yang, H. (2010). The modulatory effects of bHLH transcription factors with the Wnt/beta-catenin pathway on differentiation of neural progenitor cells derived from neonatal mouse anterior subventricular zone. Brain Res. 1315, 1–10.10.1016/j.brainres.2009.12.013Suche in Google Scholar PubMed
Zhang, Z., Rahme, G.J., Chatterjee, P.D., Havrda, M.C., and Israel, M.A. (2017). ID2 promotes survival of glioblastoma cells during metabolic stress by regulating mitochondrial function. Cell Death Dis. 8, e2615.10.1038/cddis.2017.14Suche in Google Scholar PubMed PubMed Central
Zhong, C. and Zhu, J. (2017). Transcriptional regulators dictate innate lymphoid cell fates. Protein Cell 8, 242–254.10.1007/s13238-017-0369-7Suche in Google Scholar PubMed PubMed Central
Zhou, Q. and Anderson, D.J. (2002). The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109, 61–73.10.1016/S0092-8674(02)00677-3Suche in Google Scholar
Zhou, Q., Wang, S.L., and Anderson, D.J. (2000). Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25, 331–343.10.1016/S0896-6273(00)80898-3Suche in Google Scholar PubMed
Zimmerman, L.B., DeJesusEscobar, J.M., and Harland, R.M. (1996). The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599–606.10.1016/S0092-8674(00)80133-6Suche in Google Scholar
Zuchero, J.B. and Barres, B.A. (2013). Intrinsic and extrinsic control of oligodendrocyte development. Curr. Opin. Neurobiol. 23, 914–920.10.1016/j.conb.2013.06.005Suche in Google Scholar PubMed PubMed Central
©2019 Walter de Gruyter GmbH, Berlin/Boston
Artikel in diesem Heft
- Frontmatter
- Neurogenesis and brain aging
- The effects of dietary methionine restriction on the function and metabolic reprogramming in the liver and brain – implications for longevity
- Epigenetic mechanisms, trauma, and psychopathology: targeting chromatin remodeling complexes
- Dynamics of brain connectivity after stroke
- Could the inhibitor of DNA binding 2 and 4 play a role in white matter injury?
- Hyperpolarization-activated and cyclic nucleotide-gated channel proteins as emerging new targets in neuropathic pain
- Classic psychedelics: the special role of the visual system
- Plant-derived medicines for neuropathies: a comprehensive review of clinical evidence
Artikel in diesem Heft
- Frontmatter
- Neurogenesis and brain aging
- The effects of dietary methionine restriction on the function and metabolic reprogramming in the liver and brain – implications for longevity
- Epigenetic mechanisms, trauma, and psychopathology: targeting chromatin remodeling complexes
- Dynamics of brain connectivity after stroke
- Could the inhibitor of DNA binding 2 and 4 play a role in white matter injury?
- Hyperpolarization-activated and cyclic nucleotide-gated channel proteins as emerging new targets in neuropathic pain
- Classic psychedelics: the special role of the visual system
- Plant-derived medicines for neuropathies: a comprehensive review of clinical evidence