Cited by 28Neurogenesis and neuroplasticity mechanismsDown syndrome and intellectual disability researchGenetics and Neurodevelopmental Disorders

Aberrant Oligodendrogenesis in Down Syndrome: Shift in Gliogenesis?

Open access
Reiche, Laura, Küry, Patrick, Göttle, Peter·2019·Cells

Abstract

Down syndrome (DS), or trisomy 21, is the most prevalent chromosomal anomaly accounting for cognitive impairment and intellectual disability (ID). Neuropathological changes of DS brains are characterized by a reduction in the number of neurons and oligodendrocytes, accompanied by hypomyelination and astrogliosis. Recent studies mainly focused on neuronal development in DS, but underestimated the role of glial cells as pathogenic players. Aberrant or impaired differentiation within the oligodendroglial lineage and altered white matter functionality are thought to contribute to central nervous system (CNS) malformations. Given that white matter, comprised of oligodendrocytes and their myelin sheaths, is vital for higher brain function, gathering knowledge about pathways and modulators challenging oligodendrogenesis and cell lineages within DS is essential. This review article discusses to what degree DS-related effects on oligodendroglial cells have been described and presents collected evidence regarding induced cell-fate switches, thereby resulting in an enhanced generation of astrocytes. Moreover, alterations in white matter formation observed in mouse and human post-mortem brains are described. Finally, the rationale for a better understanding of pathways and modulators responsible for the glial cell imbalance as a possible source for future therapeutic interventions is given based on current experience on pro-oligodendroglial treatment approaches developed for demyelinating diseases, such as multiple sclerosis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3390/cells8121591

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Studies using transcriptomics and new analytical tools have suggested that neurogenesis, gliogenesis and myelination may be temporally altered in Down syndrome.

    “Indeed, studies using transcriptomics and new analytical tools have suggested that neurogenesis, gliogenesis and myelination may be temporally altered in DS39,106,107.”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 169 · Cited by 28

Research works printed but not linked: 153

  1. [1]Baburamani A.A. Patkee P.A. Arichi T. Rutherford M.A. New approaches to studying early brain development in Down syndrome Dev. Med. Child Neurol. 2019 61 867 879 10.1111/dmcn.14260 31102269 PMC6618001 · DOI · Paper page
  2. [2]Chapman R.S. Hesketh L.J. Behavioral phenotype of individuals with Down syndrome Ment. Retard. Dev. Disabil. Res. Rev. 2000 6 84 95 10.1002/1098-2779(2000)6:2<84::AID-MRDD2>3.0.CO;2-P 10899801 · DOI
  3. [3]Dossi E. Vasile F. Rouach N. Human astrocytes in the diseased brain Brain Res. Bull. 2017 10.1016/j.brainresbull.2017.02.001 28212850 PMC5766741 · DOI · Paper page
  4. [4]Haydar T.F. Reeves R.H. Trisomy 21 and early brain development Trends Neurosci. 2012 35 81 91 10.1016/j.tins.2011.11.001 22169531 PMC3273608 · DOI · Paper page
  5. [5]Gardiner K.J. Pharmacological approaches to improving cognitive function in Down syndrome: Current status and considerations Drug Des. Dev. Ther. 2015 9 103 125 10.2147/DDDT.S51476 PMC4277121 25552901 · DOI
  6. [6]Stagni F. Giacomini A. Emili M. Guidi S. Bartesaghi R. Neurogenesis impairment: An early developmental defect in Down syndrome Free Radic. Biol. Med. 2017 10.1016/j.freeradbiomed.2017.07.026 28756311 · DOI · Paper page
  7. [7]Antonarakis S.E. Down syndrome and the complexity of genome dosage imbalance Nat. Rev. Genet. 2017 18 147 163 10.1038/nrg.2016.154 28029161 · DOI
  8. [9]Kremer D. Göttle P. Hartung H.-P. Küry P. Pushing Forward: Remyelination as the New Frontier in CNS Diseases Trends Neurosci. 2016 39 246 263 10.1016/j.tins.2016.02.004 26964504 · DOI
  9. [10]Kanaumi T. Milenkovic I. Adle-Biassette H. Aronica E. Kovacs G.G. Non-neuronal cell responses differ between normal and Down syndrome developing brains Int. J. Dev. Neurosci. 2013 31 796 803 10.1016/j.ijdevneu.2013.09.011 24113258 · DOI
  10. [12]Zdaniuk G. Wierzba-Bobrowicz T. Szpak G.M. Stepien T. Astroglia disturbances during development of the central nervous system in fetuses with Down’s syndrome Folia Neuropathol. 2011 49 109 114 21845539
  11. [13]Mito T. Becker L.E. Developmental changes of S-100 protein and glial fibrillary acidic protein in the brain in Down syndrome Exp. Neurol. 1993 120 170 176 10.1006/exnr.1993.1052 8491278 · DOI · Paper page
  12. [14]Murphy G.M. Jr. Ellis W.G. Lee Y.L. Stultz K.E. Shrivastava R. Tinklenberg J.R. Eng L.F. Astrocytic gliosis in the amygdala in Down’s syndrome and Alzheimer’s disease Prog. Brain Res. 1992 94 475 483 1287731
  13. [15]Takashima S. Becker L.E. Basal ganglia calcification in Down’s syndrome J. Neurol. Neurosurg. Psychiatry 1985 48 61 64 10.1136/jnnp.48.1.61 3156213 PMC1028184 · DOI
  14. [16]Karlsen A.S. Pakkenberg B. Total numbers of neurons and glial cells in cortex and basal ganglia of aged brains with Down syndrome—A stereological study Cereb. Cortex 2011 21 2519 2524 10.1093/cercor/bhr033 21427166 · DOI · Paper page
  15. [17]Wisniewski K.E. Schmidt-Sidor B. Postnatal delay of myelin formation in brains from Down syndrome infants and children Clin. Neuropathol. 1989 8 55 62 2524302
  16. [18]Abraham H. Vincze A. Veszpremi B. Kravjak A. Gomori E. Kovacs G.G. Seress L. Impaired myelination of the human hippocampal formation in Down syndrome Int. J. Dev. Neurosci. 2012 30 147 158 10.1016/j.ijdevneu.2011.11.005 22155002 · DOI · Paper page
  17. [19]Koo B.K. Blaser S. Harwood-Nash D. Becker L.E. Murphy E.G. Magnetic resonance imaging evaluation of delayed myelination in Down syndrome: A case report and review of the literature J. Child Neurol. 1992 7 417 421 10.1177/088307389200700417 1469252 · DOI · Paper page
  18. [20]Fenoll R. Pujol J. Esteba-Castillo S. de Sola S. Ribas-Vidal N. Garcia-Alba J. Sanchez-Benavides G. Martinez-Vilavella G. Deus J. Dierssen M. Anomalous White Matter Structure and the Effect of Age in Down Syndrome Patients J. Alzheimers Dis. 2017 57 61 70 10.3233/JAD-161112 28222523 · DOI
  19. [21]Romano A. Moraschi M. Cornia R. Bozzao A. Rossi-Espagnet M.C. Giove F. Albertini G. Pierallini A. White matter involvement in young non-demented Down’s syndrome subjects: A tract-based spatial statistic analysis Neuroradiology 2018 60 1335 1341 10.1007/s00234-018-2102-5 30264168 · DOI
  20. [22]Gunbey H.P. Bilgici M.C. Aslan K. Has A.C. Ogur M.G. Alhan A. Incesu L. Structural brain alterations of Down’s syndrome in early childhood evaluation by DTI and volumetric analyses Eur. Radiol. 2017 27 3013 3021 10.1007/s00330-016-4626-6 27798752 · DOI
  21. [23]Powell D. Caban-Holt A. Jicha G. Robertson W. Davis R. Gold B.T. Schmitt F.A. Head E. Frontal white matter integrity in adults with Down syndrome with and without dementia Neurobiol. Aging 2014 35 1562 1569 10.1016/j.neurobiolaging.2014.01.137 24582640 PMC3992921 · DOI
  22. [25]Liu J. Dietz K. DeLoyht J.M. Pedre X. Kelkar D. Kaur J. Vialou V. Lobo M.K. Dietz D.M. Nestler E.J. Impaired adult myelination in the prefrontal cortex of socially isolated mice Nat. Neurosci. 2012 15 1621 1623 10.1038/nn.3263 23143512 PMC3729624 · DOI · Paper page
  23. [27]Baddeley A. Jarrold C. Working memory and Down syndrome J. Intellect. Disabil. Res. 2007 51 925 931 10.1111/j.1365-2788.2007.00979.x 17990999 · DOI
  24. [28]Rowe J. Lavender A. Turk V. Cognitive executive function in Down’s syndrome Br. J. Clin. Psychol. 2006 45 5 17 10.1348/014466505X29594 16480563 · DOI
  25. [29]Nelson L. Johnson J.K. Freedman M. Lott I. Groot J. Chang M. Milgram N.W. Head E. Learning and memory as a function of age in Down syndrome: A study using animal-based tasks Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2005 29 443 453 10.1016/j.pnpbp.2004.12.009 15795053 · DOI
  26. [30]Pennington B.F. Moon J. Edgin J. Stedron J. Nadel L. The neuropsychology of Down syndrome: Evidence for hippocampal dysfunction Child Dev. 2003 74 75 93 10.1111/1467-8624.00522 12625437 · DOI · Paper page
  27. [31]Lanfranchi S. Carretti B. Spano G. Cornoldi C. A specific deficit in visuospatial simultaneous working memory in Down syndrome J. Intellect. Disabil. Res. 2009 53 474 483 10.1111/j.1365-2788.2009.01165.x 19396941 · DOI
  28. [32]Lanfranchi S. Cornoldi C. Vianello R. Verbal and Visuospatial Working Memory Deficits in Children With Down Syndrome Am. J. Ment. Retard. 2004 109 456 466 10.1352/0895-8017(2004)109<456:VAVWMD>2.0.CO;2 15471512 · DOI
  29. [33]Lanfranchi S. Jerman O. Vianello R. Working Memory and Cognitive Skills in Individuals with Down Syndrome Child Neuropsychol. 2009 15 397 416 10.1080/09297040902740652 19274603 · DOI
  30. [34]Fields R.D. White matter in learning, cognition and psychiatric disorders Trends Neurosci. 2008 31 361 370 10.1016/j.tins.2008.04.001 18538868 PMC2486416 · DOI · Paper page
  31. [35]Simon K. Hennen S. Merten N. Blattermann S. Gillard M. Kostenis E. Gomeza J. The Orphan G Protein-coupled Receptor GPR17 Negatively Regulates Oligodendrocyte Differentiation via Galphai/o and Its Downstream Effector Molecules J. Biol. Chem. 2016 291 705 718 10.1074/jbc.M115.683953 26620557 PMC4705391 · DOI
  32. [36]Wang X. Zhao Y. Zhang X. Badie H. Zhou Y. Mu Y. Loo L.S. Cai L. Thompson R.C. Yang B. Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down’s syndrome Nat. Med. 2013 19 473 480 10.1038/nm.3117 23524343 PMC3911880 · DOI
  33. [37]Meraviglia V. Ulivi A.F. Boccazzi M. Valenza F. Fratangeli A. Passafaro M. Lecca D. Stagni F. Giacomini A. Bartesaghi R. SNX27, a protein involved in down syndrome, regulates GPR17 trafficking and oligodendrocyte differentiation Glia 2016 64 1437 1460 10.1002/glia.23015 27270750 · DOI
  34. [38]Rowitch D.H. Kriegstein A.R. Developmental genetics of vertebrate glial-cell specification Nature 2010 468 214 222 10.1038/nature09611 21068830 · DOI
  35. [39]Casano A.M. Peri F. Microglia: Multitasking specialists of the brain Dev. Cell. 2015 32 469 477 10.1016/j.devcel.2015.01.018 25710533 · DOI · Paper page
  36. [40]Michell-Robinson M.A. Touil H. Healy L.M. Owen D.R. Durafourt B.A. Bar-Or A. Antel J.P. Moore C.S. Roles of microglia in brain development, tissue maintenance and repair Brain 2015 138 1138 1159 10.1093/brain/awv066 25823474 PMC5963417 · DOI
  37. [41]Peters A. A fourth type of neuroglial cell in the adult central nervous system J. Neurocytol. 2004 33 345 357 10.1023/B:NEUR.0000044195.64009.27 15475689 · DOI
  38. [42]Kriegstein A. Alvarez-Buylla A. The glial nature of embryonic and adult neural stem cells Annu. Rev. Neurosci. 2009 32 149 184 10.1146/annurev.neuro.051508.135600 19555289 PMC3086722 · DOI · Paper page
  39. [44]Raff M.C. Miller R.H. Noble M. A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium Nature 1983 303 390 396 10.1038/303390a0 6304520 · DOI
  40. [45]Dimou L. Gotz M. Glial cells as progenitors and stem cells: New roles in the healthy and diseased brain Physiol. Rev. 2014 94 709 737 10.1152/physrev.00036.2013 24987003 · DOI
  41. [46]Nishiyama A. Boshans L. Goncalves C.M. Wegrzyn J. Patel K.D. Lineage, fate, and fate potential of NG2-glia Brain Res. 2016 1638 116 128 10.1016/j.brainres.2015.08.013 26301825 PMC4761528 · DOI
  42. [47]Tanner D.C. Cherry J.D. Mayer-Pröschel M. Oligodendrocyte Progenitors Reversibly Exit the Cell Cycle and Give Rise to Astrocytes in Response to Interferon-γ J. Neurosci. 2011 31 6235 10.1523/JNEUROSCI.5905-10.2011 21508246 PMC3104669 · DOI
  43. [48]Menn B. Garcia-Verdugo J.M. Yaschine C. Gonzalez-Perez O. Rowitch D. Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain J. Neurosci. 2006 26 7907 7918 10.1523/JNEUROSCI.1299-06.2006 16870736 PMC6674207 · DOI · Paper page
  44. [50]Snaidero N. Simons M. Myelination at a glance J. Cell Sci. 2014 127 2999 3004 10.1242/jcs.151043 25024457 · DOI
  45. [51]Snaidero N. Simons M. The logistics of myelin biogenesis in the central nervous system Glia 2017 65 1021 1031 10.1002/glia.23116 28168748 · DOI
  46. [52]Miron V.E. Kuhlmann T. Antel J.P. Cells of the oligodendroglial lineage, myelination, and remyelination Biochim. Biophys. Acta 2011 1812 184 193 10.1016/j.bbadis.2010.09.010 20887785 · DOI
  47. [53]Lu Q.R. Sun T. Zhu Z. Ma N. Garcia M. Stiles C.D. Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection Cell 2002 109 75 86 10.1016/S0092-8674(02)00678-5 11955448 · DOI
  48. [54]El Waly B. Macchi M. Cayre M. Durbec P. Oligodendrogenesis in the normal and pathological central nervous system Front. Neurosci. 2014 8 145 10.3389/fnins.2014.00145 24971048 PMC4054666 · DOI
  49. [56]Zhang L. He X. Liu L. Jiang M. Zhao C. Wang H. He D. Zheng T. Zhou X. Hassan A. Hdac3 Interaction with p300 Histone Acetyltransferase Regulates the Oligodendrocyte and Astrocyte Lineage Fate Switch Dev. Cell 2016 37 582 10.1016/j.devcel.2016.06.004 27326936 · DOI
  50. [57]Golden J.A. Hyman B.T. Development of the superior temporal neocortex is anomalous in trisomy 21 J. Neuropathol. Exp. Neurol. 1994 53 513 520 10.1097/00005072-199409000-00011 8083693 · DOI · Paper page
  51. [58]Winter T.C. Ostrovsky A.A. Komarniski C.A. Uhrich S.B. Cerebellar and frontal lobe hypoplasia in fetuses with trisomy 21: Usefulness as combined US markers Radiology 2000 214 533 538 10.1148/radiology.214.2.r00fe40533 10671607 · DOI
  52. [60]Schmidt-Sidor B. Wisniewski K.E. Shepard T.H. Sersen E.A. Brain growth in Down syndrome subjects 15 to 22 weeks of gestational age and birth to 60 months Clin. Neuropathol. 1990 9 181 190 2146054
  53. [61]Liu B. Filippi S. Roy A. Roberts I. Stem and progenitor cell dysfunction in human trisomies EMBO Rep. 2015 16 44 62 10.15252/embr.201439583 25520324 PMC4304728 · DOI
  54. [62]Guidi S. Bonasoni P. Ceccarelli C. Santini D. Gualtieri F. Ciani E. Bartesaghi R. Neurogenesis impairment and increased cell death reduce total neuron number in the hippocampal region of fetuses with Down syndrome Brain Pathol. 2008 18 180 197 10.1111/j.1750-3639.2007.00113.x 18093248 PMC8095525 · DOI · Paper page
  55. [63]Lu J. Lian G. Zhou H. Esposito G. Steardo L. Delli-Bovi L.C. Hecht J.L. Lu Q.R. Sheen V. OLIG2 over-expression impairs proliferation of human Down syndrome neural progenitors Hum. Mol. Genet. 2012 21 2330 2340 10.1093/hmg/dds052 22343408 PMC3335315 · DOI · Paper page
  56. [64]Chakrabarti L. Best T.K. Cramer N.P. Carney R.S. Isaac J.T. Galdzicki Z. Haydar T.F. Olig1 and Olig2 triplication causes developmental brain defects in Down syndrome Nat. Neurosci. 2010 13 927 934 10.1038/nn.2600 20639873 PMC3249618 · DOI · Paper page
  57. [65]Lockrow J. Fortress A. Granholm A.-C. Age-Related Neurodegeneration and Memory Loss in Down Syndrome Curr. Gerontol. Geriatr. Res. 2012 2012 463909 10.1155/2012/463909 22545043 PMC3318235 · DOI
  58. [66]Bonni A. Sun Y. Nadal-Vicens M. Bhatt A. Frank D.A. Rozovsky I. Stahl N. Yancopoulos G.D. Greenberg M.E. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway Science 1997 278 477 483 10.1126/science.278.5337.477 9334309 · DOI
  59. [67]Hong S. Song M.-R. STAT3 but not STAT1 is required for astrocyte differentiation PLoS ONE 2014 9 e86851 10.1371/journal.pone.0086851 24466267 PMC3900679 · DOI
  60. [68]Kurabayashi N. Nguyen M.D. Sanada K. DYRK1A overexpression enhances STAT activity and astrogliogenesis in a Down syndrome mouse model EMBO Rep. 2015 16 1548 1562 10.15252/embr.201540374 26373433 PMC4641506 · DOI
  61. [69]Cao F. Hata R. Zhu P. Nakashiro K. Sakanaka M. Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells Biochem. Biophys. Res. Commun. 2010 394 843 847 10.1016/j.bbrc.2010.03.092 20303333 · DOI
  62. [70]Corsi M.M. Dogliotti G. Pedroni F. Palazzi E. Magni P. Chiappelli M. Licastro F. Plasma nerve growth factor (NGF) and inflammatory cytokines (IL-6 and MCP-1) in young and adult subjects with Down syndrome: An interesting pathway Neuro Endocrinol. Lett. 2006 27 773 778 17187019
  63. [71]Hallam D.M. Capps N.L. Travelstead A.L. Brewer G.J. Maroun L.E. Evidence for an interferon-related inflammatory reaction in the trisomy 16 mouse brain leading to caspase-1-mediated neuronal apoptosis J. Neuroimmunol. 2000 110 66 75 10.1016/S0165-5728(00)00289-7 11024535 · DOI
  64. [72]Lee H.C. Tan K.L. Cheah P.S. Ling K.H. Potential Role of JAK-STAT Signaling Pathway in the Neurogenic-to-Gliogenic Shift in Down Syndrome Brain Neural Plasticity 2016 2016 7434191 10.1155/2016/7434191 26881131 PMC4737457 · DOI
  65. [73]Trazzi S. Fuchs C. Valli E. Perini G. Bartesaghi R. Ciani E. The amyloid precursor protein (APP) triplicated gene impairs neuronal precursor differentiation and neurite development through two different domains in the Ts65Dn mouse model for Down syndrome J. Biol. Chem. 2013 288 20817 20829 10.1074/jbc.M113.451088 23740250 PMC3774353 · DOI
  66. [75]Wilcock D.M. Neuroinflammation in the aging down syndrome brain; lessons from Alzheimer’s disease Curr. Gerontol. Geriatr. Res. 2012 2012 170276 10.1155/2012/170276 22454637 PMC3290800 · DOI · Paper page
  67. [76]Ferrando-Miguel R. Shim K.S. Cheon M.S. Gimona M. Furuse M. Lubec G. Overexpression of Interferon α/β Receptor β Chain in Fetal Down Syndrome Brain Neuroembryol. Aging 2003 2 147 155 10.1159/000079401 · DOI
  68. [77]Guimera J. Casas C. Estivill X. Pritchard M. Human minibrain homologue (MNBH/DYRK1): Characterization, alternative splicing, differential tissue expression, and overexpression in Down syndrome Genomics 1999 57 407 418 10.1006/geno.1999.5775 10329007 · DOI · Paper page
  69. [78]Sun Y. Lehmbecker A. Kalkuhl A. Deschl U. Sun W. Rohn K. Tzvetanova I.D. Nave K.A. Baumgartner W. Ulrich R. STAT3 represents a molecular switch possibly inducing astroglial instead of oligodendroglial differentiation of oligodendroglial progenitor cells in Theiler’s murine encephalomyelitis Neuropathol. Appl. Neurobiol. 2015 41 347 370 10.1111/nan.12133 24606160 · DOI
  70. [79]Corbin J.G. Kelly D. Rath E.M. Baerwald K.D. Suzuki K. Popko B. Targeted CNS expression of interferon-gamma in transgenic mice leads to hypomyelination, reactive gliosis, and abnormal cerebellar development Mol. Cell. Neurosci. 1996 7 354 370 10.1006/mcne.1996.0026 8812062 · DOI
  71. [80]Martí E. Bovolenta P. Sonic hedgehog in CNS development: One signal, multiple outputs Trends Neurosci. 2002 25 89 96 10.1016/S0166-2236(02)02062-3 11814561 · DOI
  72. [81]Alberta J.A. Park S.-K. Mora J. Yuk D.-i. Pawlitzky I. Iannarelli P. Vartanian T. Stiles C.D. Rowitch D.H. Sonic Hedgehog Is Required during an Early Phase of Oligodendrocyte Development in Mammalian Brain Mol. Cell. Neurosci. 2001 18 434 441 10.1006/mcne.2001.1026 11640898 · DOI
  73. [82]Danesin C. Agius E. Escalas N. Ai X. Emerson C. Cochard P. Soula C. Ventral Neural Progenitors Switch toward an Oligodendroglial Fate in Response to Increased Sonic Hedgehog (Shh) Activity: Involvement of Sulfatase 1 in Modulating Shh Signaling in the Ventral Spinal Cord J. Neurosci. 2006 26 5037 10.1523/JNEUROSCI.0715-06.2006 16687495 PMC6674256 · DOI
  74. [83]Loulier K. Ruat M. Traiffort E. Increase of proliferating oligodendroglial progenitors in the adult mouse brain upon Sonic hedgehog delivery in the lateral ventricle J. Neurochem. 2006 98 530 542 10.1111/j.1471-4159.2006.03896.x 16805844 · DOI
  75. [84]Ferent J. Zimmer C. Durbec P. Ruat M. Traiffort E. Sonic Hedgehog Signaling Is a Positive Oligodendrocyte Regulator during Demyelination J. Neurosci. 2013 33 1759 10.1523/JNEUROSCI.3334-12.2013 23365216 PMC6619133 · DOI
  76. [86]Laouarem Y. Traiffort E. Developmental and Repairing Production of Myelin: The Role of Hedgehog Signaling Front. Cell. Neurosci. 2018 12 10.3389/fncel.2018.00305 30237763 PMC6135882 · DOI
  77. [87]Oh S. Huang X. Chiang C. Specific requirements of sonic hedgehog signaling during oligodendrocyte development Dev. Dyn. 2005 234 489 496 10.1002/dvdy.20422 15880651 · DOI
  78. [88]Yu K. McGlynn S. Matise M.P. Floor plate-derived sonic hedgehog regulates glial and ependymal cell fates in the developing spinal cord Development 2013 140 1594 1604 10.1242/dev.090845 23482494 PMC3596997 · DOI
  79. [89]Trazzi S. Mitrugno V.M. Valli E. Fuchs C. Rizzi S. Guidi S. Perini G. Bartesaghi R. Ciani E. APP-dependent up-regulation of Ptch1 underlies proliferation impairment of neural precursors in Down syndrome Hum. Mol. Genet. 2011 20 1560 1573 10.1093/hmg/ddr033 21266456 · DOI
  80. [90]Samanta J. Grund E.M. Silva H.M. Lafaille J.J. Fishell G. Salzer J.L. Inhibition of Gli1 mobilizes endogenous neural stem cells for remyelination Nature 2015 526 448 452 10.1038/nature14957 26416758 PMC4970518 · DOI
  81. [91]Tan M. Hu X. Qi Y. Park J. Cai J. Qiu M. Gli3 mutation rescues the generation, but not the differentiation, of oligodendrocytes in Shh mutants Brain Res. 2006 1067 158 163 10.1016/j.brainres.2005.10.041 16336945 · DOI
  82. [92]Wang L.C. Almazan G. Role of Sonic Hedgehog Signaling in Oligodendrocyte Differentiation Neurochem. Res. 2016 41 3289 3299 10.1007/s11064-016-2061-3 27639396 · DOI
  83. [93]Ravanelli A.M. Kearns C.A. Powers R.K. Wang Y. Hines J.H. Donaldson M.J. Appel B. Sequential specification of oligodendrocyte lineage cells by distinct levels of Hedgehog and Notch signaling Dev. Biol. 2018 444 93 106 10.1016/j.ydbio.2018.10.004 30347186 PMC6263812 · DOI
  84. [94]Fischer D.F. van Dijk R. Sluijs J.A. Nair S.M. Racchi M. Levelt C.N. van Leeuwen F.W. Hol E.M. Activation of the Notch pathway in Down syndrome: Cross-talk of Notch and APP FASEB J. 2005 19 1451 1458 10.1096/fj.04-3395com 16126912 · DOI
  85. [95]Kamakura S. Oishi K. Yoshimatsu T. Nakafuku M. Masuyama N. Gotoh Y. Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling Nat. Cell Biol. 2004 6 547 554 10.1038/ncb1138 15156153 · DOI
  86. [96]Wu Y. Liu Y. Levine E.M. Rao M.S. Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors Dev. Dyn. 2003 226 675 689 10.1002/dvdy.10278 12666205 · DOI
  87. [97]Logan C.Y. Nusse R. The Wnt signaling pathway in development and disease Annu. Rev. Cell Dev. Biol. 2004 20 781 810 10.1146/annurev.cellbio.20.010403.113126 15473860 · DOI · Paper page
  88. [98]Soomro S. Jie J. Fu H. Oligodendrocytes Development and Wnt Signaling Pathway Int. J. Hum. Anat. 2018 1 17 35 10.14302/issn.2577-2279.ijha-18-2407 · DOI
  89. [99]Granno S. Nixon-Abell J. Berwick D.C. Tosh J. Heaton G. Almudimeegh S. Nagda Z. Rain J.C. Zanda M. Plagnol V. Downregulated Wnt/beta-catenin signalling in the Down syndrome hippocampus Sci. Rep. 2019 9 7322 10.1038/s41598-019-43820-4 31086297 PMC6513850 · DOI
  90. [101]Fancy S.P. Baranzini S.E. Zhao C. Yuk D.I. Irvine K.A. Kaing S. Sanai N. Franklin R.J. Rowitch D.H. Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS Genes Dev. 2009 23 1571 1585 10.1101/gad.1806309 19515974 PMC2704469 · DOI
  91. [102]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. HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction Nat. Neurosci. 2009 12 829 838 10.1038/nn.2333 19503085 PMC2701973 · DOI · Paper page
  92. [103]Fu H. Qi Y. Tan M. Cai J. Takebayashi H. Nakafuku M. Richardson W. Qiu M. Dual origin of spinal oligodendrocyte progenitors and evidence for the cooperative role of Olig2 and Nkx2.2 in the control of oligodendrocyte differentiation Development 2002 129 681 693 11830569
  93. [104]Sun S. Zhu X.-J. Huang H. Guo W. Tang T. Xie B. Xu X. Zhang Z. Shen Y. Dai Z.-M. WNT signaling represses astrogliogenesis via Ngn2-dependent direct suppression of astrocyte gene expression Glia 2019 67 1333 1343 10.1002/glia.23608 30889310 · DOI
  94. [105]Li S.S. Qu Z.D. Haas M. Ngo L. Heo Y.J. Kang H.J. Britto J.M. Cullen H.D. Vanyai H.K. Tan S.S. The HSA21 gene EURL/C21ORF91 controls neurogenesis within the cerebral cortex and is implicated in the pathogenesis of Down Syndrome Sci. Rep. 2016 6 14 10.1038/srep29514 27404227 PMC4941730 · DOI
  95. [106]Serrano-Pérez M.C. Fernández M. Neria F. Berjón-Otero M. Doncel-Pérez E. Cano E. Tranque P. NFAT transcription factors regulate survival, proliferation, migration, and differentiation of neural precursor cells Glia 2015 63 987 1004 10.1002/glia.22797 25731131 · DOI
  96. [107]Kurabayashi N. Sanada K. Increased dosage of DYRK1A and DSCR1 delays neuronal differentiation in neocortical progenitor cells Genes Dev. 2013 27 2708 2721 10.1101/gad.226381.113 24352425 PMC3877759 · DOI
  97. [108]Baek K.H. Zaslavsky A. Lynch R.C. Britt C. Okada Y. Siarey R.J. Lensch M.W. Park I.H. Yoon S.S. Minami T. Down’s syndrome suppression of tumour growth and the role of the calcineurin inhibitor DSCR1 Nature 2009 459 1126 1130 10.1038/nature08062 19458618 PMC2724004 · DOI
  98. [109]Arron J.R. Winslow M.M. Polleri A. Chang C.P. Wu H. Gao X. Neilson J.R. Chen L. Heit J.J. Kim S.K. NFAT dysregulation by increased dosage of DSCR1 and DYRK1A on chromosome 21 Nature 2006 441 595 600 10.1038/nature04678 16554754 · DOI · Paper page
  99. [110]Jung M.S. Park J.H. Ryu Y.S. Choi S.H. Yoon S.H. Kwen M.Y. Oh J.Y. Song W.J. Chung S.H. Regulation of RCAN1 protein activity by Dyrk1A protein-mediated phosphorylation J. Biol. Chem. 2011 286 40401 40412 10.1074/jbc.M111.253971 21965663 PMC3220559 · DOI
  100. [111]Weider M. Starost L.J. Groll K. Kuspert M. Sock E. Wedel M. Frob F. Schmitt C. Baroti T. Hartwig A.C. Nfat/calcineurin signaling promotes oligodendrocyte differentiation and myelination by transcription factor network tuning Nat. Commun. 2018 9 899 10.1038/s41467-018-03336-3 29500351 PMC5834605 · DOI
  101. [112]Nalivaeva N.N. Turner A.J. The amyloid precursor protein: A biochemical enigma in brain development, function and disease FEBS Lett. 2013 587 2046 2054 10.1016/j.febslet.2013.05.010 23684647 · DOI
  102. [113]Zhou Z.D. Chan C.H. Ma Q.H. Xu X.H. Xiao Z.C. Tan E.K. The roles of amyloid precursor protein (APP) in neurogenesis: Implications to pathogenesis and therapy of Alzheimer disease Cell Adhes. Migr. 2011 5 280 292 10.4161/cam.5.4.16986 21785276 PMC3210295 · DOI
  103. [114]Guidi S. Emili M. Giacomini A. Stagni F. Bartesaghi R. Neuroanatomical alterations in the temporal cortex of human fetuses with Down syndrome Proceedings of the 2nd International Conference of the Trisomy 21 Research Society Chicago, IL, USA 7–11 June 2017 79
  104. [115]Hof P.R. Bouras C. Perl D.P. Sparks D.L. Mehta N. Morrison J.H. Age-related distribution of neuropathologic changes in the cerebral cortex of patients with Down’s syndrome. Quantitative regional analysis and comparison with Alzheimer’s disease Arch. Neurol. 1995 52 379 391 10.1001/archneur.1995.00540280065020 7710374 · DOI
  105. [116]Hyman B.T. West H.L. Rebeck G.W. Lai F. Mann D.M. Neuropathological changes in Down’s syndrome hippocampal formation. Effect of age and apolipoprotein E genotype Arch. Neurol. 1995 52 373 378 10.1001/archneur.1995.00540280059019 7710373 · DOI
  106. [117]Leverenz J.B. Raskind M.A. Early amyloid deposition in the medial temporal lobe of young Down syndrome patients: A regional quantitative analysis Exp. Neurol. 1998 150 296 304 10.1006/exnr.1997.6777 9527899 · DOI · Paper page
  107. [118]Trazzi S. Fuchs C. De Franceschi M. Mitrugno V.M. Bartesaghi R. Ciani E. APP-dependent alteration of GSK3β activity impairs neurogenesis in the Ts65Dn mouse model of Down syndrome Neurobiol. Dis. 2014 67 24 36 10.1016/j.nbd.2014.03.003 24636797 · DOI
  108. [119]Ballabh P. Intraventricular hemorrhage in premature infants: Mechanism of disease Pediatr. Res. 2010 67 1 8 10.1203/PDR.0b013e3181c1b176 19816235 PMC2799187 · DOI
  109. [120]Dummula K. Vinukonda G. Chu P. Xing Y. Hu F. Mailk S. Csiszar A. Chua C. Mouton P. Kayton R.J. Bone morphogenetic protein inhibition promotes neurological recovery after intraventricular hemorrhage J. Neurosci. 2011 31 12068 12082 10.1523/JNEUROSCI.0013-11.2011 21865450 PMC3167068 · DOI
  110. [121]Dohare P. Cheng B. Ahmed E. Yadala V. Singla P. Thomas S. Kayton R. Ungvari Z. Ballabh P. Glycogen synthase kinase-3β inhibition enhances myelination in preterm newborns with intraventricular hemorrhage, but not recombinant Wnt3A Neurobiol. Dis. 2018 118 22 39 10.1016/j.nbd.2018.06.015 29940337 PMC6673662 · DOI
  111. [122]Sugaya K. Mechanism of glial differentiation of neural progenitor cells by amyloid precursor protein Neurodegener. Dis. 2008 5 170 172 10.1159/000113693 18322381 · DOI
  112. [123]Roth A.D. Ramirez G. Alarcon R. Von Bernhardi R. Oligodendrocytes damage in Alzheimer’s disease: Beta amyloid toxicity and inflammation Biol. Res. 2005 38 381 387 10.4067/S0716-97602005000400011 16579521 · DOI
  113. [124]Kremer D. Akkermann R. Küry P. Dutta R. Current advancements in promoting remyelination in multiple sclerosis Mult. Scler. 2019 25 7 14 10.1177/1352458518800827 30270725 PMC6389436 · DOI
  114. [125]Küry P. Kremer D. Göttle P. Drug repurposing for neuroregeneration in multiple sclerosis Neural Regen. Res. 2018 13 1366 1367 10.4103/1673-5374.235242 30106047 PMC6108191 · DOI
  115. [126]Azim K. Angonin D. Marcy G. Pieropan F. Rivera A. Donega V. Cantu C. Williams G. Berninger B. Butt A.M. Pharmacogenomic identification of small molecules for lineage specific manipulation of subventricular zone germinal activity PLoS Biol. 2017 15 e2000698 10.1371/journal.pbio.2000698 28350803 PMC5370089 · DOI
  116. [127]Preisner A. Albrecht S. Cui Q.L. Hucke S. Ghelman J. Hartmann C. Taketo M.M. Antel J. Klotz L. Kuhlmann T. Non-steroidal anti-inflammatory drug indometacin enhances endogenous remyelination Acta Neuropathol. 2015 130 247 261 10.1007/s00401-015-1426-z 25943886 · DOI
  117. [128]Najm F.J. Madhavan M. Zaremba A. Shick E. Karl R.T. Factor D.C. Miller T.E. Nevin Z.S. Kantor C. Sargent A. Drug-based modulation of endogenous stem cells promotes functional remyelination in vivo Nature 2015 522 216 220 10.1038/nature14335 25896324 PMC4528969 · DOI · Paper page
  118. [129]Chen Y. Zhen W. Guo T. Zhao Y. Liu A. Rubio J.P. Krull D. Richardson J.C. Lu H. Wang R. Histamine Receptor 3 negatively regulates oligodendrocyte differentiation and remyelination PLoS ONE 2017 12 e0189380 10.1371/journal.pone.0189380 29253893 PMC5734789 · DOI
  119. [130]Schwartzbach C.J. Grove R.A. Brown R. Tompson D. Then Bergh F. Arnold D.L. Lesion remyelinating activity of GSK239512 versus placebo in patients with relapsing-remitting multiple sclerosis: A randomised, single-blind, phase II study J. Neurol. 2017 264 304 315 10.1007/s00415-016-8341-7 27888416 PMC5306088 · DOI
  120. [131]Mei F. Fancy S.P.J. Shen Y.A. Niu J. Zhao C. Presley B. Miao E. Lee S. Mayoral S.R. Redmond S.A. Micropillar arrays as a high-throughput screening platform for therapeutics in multiple sclerosis Nature Med. 2014 20 954 960 10.1038/nm.3618 24997607 PMC4830134 · DOI
  121. [132]Green A.J. Gelfand J.M. Cree B.A. Bevan C. Boscardin W.J. Mei F. Inman J. Arnow S. Devereux M. Abounasr A. Clemastine fumarate as a remyelinating therapy for multiple sclerosis (ReBUILD): A randomised, controlled, double-blind, crossover trial Lancet 2017 390 2481 2489 10.1016/S0140-6736(17)32346-2 29029896 · DOI · Paper page
  122. [133]Hammond T.R. McEllin B. Morton P.D. Raymond M. Dupree J. Gallo V. Endothelin-B Receptor Activation in Astrocytes Regulates the Rate of Oligodendrocyte Regeneration during Remyelination Cell Rep. 2015 13 2090 2097 10.1016/j.celrep.2015.11.002 26628380 · DOI
  123. [134]Wu X. Qu X. Zhang Q. Dong F. Yu H. Yan C. Qi D. Wang M. Liu X. Yao R. Quercetin promotes proliferation and differentiation of oligodendrocyte precursor cells after oxygen/glucose deprivation-induced injury Cell Mol. Neurobiol. 2014 34 463 471 10.1007/s10571-014-0030-4 24519463 PMC11488863 · DOI
  124. [136]Rafalski V.A. Ho P.P. Brett J.O. Ucar D. Dugas J.C. Pollina E.A. Chow L.M. Ibrahim A. Baker S.J. Barres B.A. Expansion of oligodendrocyte progenitor cells following SIRT1 inactivation in the adult brain Nat. Cell Biol. 2013 15 614 624 10.1038/ncb2735 23644469 PMC4026158 · DOI
  125. [137]Prozorovski T. Ingwersen J. Lukas D. Göttle P. Koop B. Graf J. Schneider R. Franke K. Schumacher S. Britsch S. Regulation of sirtuin expression in autoimmune neuroinflammation: Induction of SIRT1 in oligodendrocyte progenitor cells Neurosci. Lett. 2019 704 116 125 10.1016/j.neulet.2019.04.007 30953735 · DOI
  126. [138]Kang W. Nguyen K.C.Q. Hebert J.M. Transient Redirection of SVZ Stem Cells to Oligodendrogenesis by FGFR3 Activation Promotes Remyelination Stem Cell Rep. 2019 12 1223 1231 10.1016/j.stemcr.2019.05.006 PMC6565886 31189094 · DOI
  127. [139]Kuro-o M. Klotho Pflug. Arch. 2010 459 333 343 10.1007/s00424-009-0722-7 19730882 · DOI
  128. [140]Torbus-Paluszczak M. Bartman W. Adamczyk-Sowa M. Klotho protein in neurodegenerative disorders Neurol. Sci. 2018 39 1677 1682 10.1007/s10072-018-3496-x 30062646 PMC6154120 · DOI
  129. [141]Zare L. Baharvand H. Javan M. In vivo conversion of astrocytes to oligodendrocyte lineage cells using chemicals: Targeting gliosis for myelin repair Regen. Med. 2018 13 803 819 10.2217/rme-2017-0155 30284949 · DOI
  130. [142]Khalaj A.J. Hasselmann J. Augello C. Moore S. Tiwari-Woodruff S.K. Nudging oligodendrocyte intrinsic signaling to remyelinate and repair: Estrogen receptor ligand effects J. Steroid Biochem. Mol. Biol. 2016 160 43 52 10.1016/j.jsbmb.2016.01.006 26776441 PMC5233753 · DOI
  131. [143]Li W.J. Mao F.X. Chen H.J. Qian L.H. Buzby J.S. Treatment with UDP-glucose, GDNF, and memantine promotes SVZ and white matter self-repair by endogenous glial progenitor cells in neonatal rats with ischemic PVL Neuroscience 2015 284 444 458 10.1016/j.neuroscience.2014.10.012 25453769 · DOI
  132. [144]Rajkowska G. Mahajan G. Maciag D. Sathyanesan M. Iyo A.H. Moulana M. Kyle P.B. Woolverton W.L. Miguel-Hidalgo J.J. Stockmeier C.A. Oligodendrocyte morphometry and expression of myelin—Related mRNA in ventral prefrontal white matter in major depressive disorder J. Psychiatr. Res. 2015 65 53 62 10.1016/j.jpsychires.2015.04.010 25930075 PMC4836860 · DOI
  133. [145]Meffre D. Massaad C. Grenier J. Lithium chloride stimulates PLP and MBP expression in oligodendrocytes via Wnt/beta-catenin and Akt/CREB pathways Neuroscience 2015 284 962 971 10.1016/j.neuroscience.2014.10.064 25451297 · DOI
  134. [146]Ghareghani M. Sadeghi H. Zibara K. Danaei N. Azari H. Ghanbari A. Melatonin Increases Oligodendrocyte Differentiation in Cultured Neural Stem Cells Cell. Mol. Neurobiol. 2017 37 1319 1324 10.1007/s10571-016-0450-4 27987059 PMC11482234 · DOI
  135. [147]Blanchard B. Heurtaux T. Garcia C. Moll N.M. Caillava C. Grandbarbe L. Klosptein A. Kerninon C. Frah M. Coowar D. Tocopherol derivative TFA-12 promotes myelin repair in experimental models of multiple sclerosis J. Neurosci. 2013 33 11633 11642 10.1523/JNEUROSCI.0774-13.2013 23843531 PMC6618682 · DOI
  136. [148]Das I. Park J.-M. Shin J.H. Jeon S.K. Lorenzi H. Linden D.J. Worley P.F. Reeves R.H. Hedgehog agonist therapy corrects structural and cognitive deficits in a Down syndrome mouse model Sci. Transl. Med. 2013 5 201ra120 10.1126/scitranslmed.3005983 PMC4006719 24005160 · DOI
  137. [149]Wang J. Ye Z. Zheng S. Chen L. Wan Y. Deng Y. Yang R. Lingo-1 shRNA and Notch signaling inhibitor DAPT promote differentiation of neural stem/progenitor cells into neurons Brain Res. 2016 1634 34 44 10.1016/j.brainres.2015.11.029 26607252 · DOI
  138. [150]Imamura O. Arai M. Dateki M. Takishima K. Donepezil promotes differentiation of neural stem cells into mature oligodendrocytes at the expense of astrogenesis J. Neurochem. 2017 140 231 244 10.1111/jnc.13856 27664791 · DOI
  139. [151]Cui X. Guo Y.E. Fang J.H. Shi C.J. Suo N. Zhang R. Xie X. Donepezil, a drug for Alzheimer’s disease, promotes oligodendrocyte generation and remyelination Acta Pharmacol. Sin 2019 10.1038/s41401-018-0206-4 PMC6888883 30918344 · DOI
  140. [152]Kang M.L. Kwon J.S. Kim M.S. Induction of neuronal differentiation of rat muscle-derived stem cells in vitro using basic fibroblast growth factor and ethosuximide Int. J. Mol. Sci. 2013 14 6614 6623 10.3390/ijms14046614 23528890 PMC3645657 · DOI
  141. [153]Setoguchi T. Kondo T. Nuclear export of OLIG2 in neural stem cells is essential for ciliary neurotrophic factor-induced astrocyte differentiation J. Cell Biol. 2004 166 963 968 10.1083/jcb.200404104 15452140 PMC2172021 · DOI
  142. [154]Zare L. Baharvand H. Javan M. Trichostatin A Promotes the Conversion of Astrocytes to Oligodendrocyte Progenitors in a Defined Culture Medium Iran J. Pharm. Res. 2019 18 286 295 31089363 PMC6487402
  143. [155]Ghasemi-Kasman M. Zare L. Baharvand H. Javan M. In vivo conversion of astrocytes to myelinating cells by miR-302/367 and valproate to enhance myelin repair J. Tissue Eng. Regen. Med. 2018 12 e462 e472 10.1002/term.2276 28127945 · DOI
  144. [156]Farhangi S. Dehghan S. Totonchi M. Javan M. In vivo conversion of astrocytes to oligodendrocyte lineage cells in adult mice demyelinated brains by Sox2 Mult. Scler. Relat. Disord. 2019 28 263 272 10.1016/j.msard.2018.12.041 30639828 · DOI
  145. [157]Hack M.A. Saghatelyan A. de Chevigny A. Pfeifer A. Ashery-Padan R. Lledo P.M. Gotz M. Neuronal fate determinants of adult olfactory bulb neurogenesis Nat. Neurosci. 2005 8 865 872 10.1038/nn1479 15951811 · DOI
  146. [158]Maire C.L. Wegener A. Kerninon C. Nait Oumesmar B. Gain-of-function of Olig transcription factors enhances oligodendrogenesis and myelination Stem Cells 2010 28 1611 1622 10.1002/stem.480 20672298 · DOI
  147. [159]Jessberger S. Toni N. Clemenson G.D. Jr. Ray J. Gage F.H. Directed differentiation of hippocampal stem/progenitor cells in the adult brain Nat. Neurosci. 2008 11 888 893 10.1038/nn.2148 18587391 PMC2795354 · DOI
  148. [160]Braun S.M. Pilz G.A. Machado R.A. Moss J. Becher B. Toni N. Jessberger S. Programming Hippocampal Neural Stem/Progenitor Cells into Oligodendrocytes Enhances Remyelination in the Adult Brain after Injury Cell Rep. 2015 11 1679 1685 10.1016/j.celrep.2015.05.024 26074082 · DOI
  149. [161]Gardiner K. Costa A.C. The proteins of human chromosome 21 Am. J. Med. Genet C Semin Med. Genet. 2006 142C 196 205 10.1002/ajmg.c.30098 17048356 PMC3299406 · DOI
  150. [162]Wiseman F.K. Alford K.A. Tybulewicz V.L.J. Fisher E.M.C. Down syndrome-recent progress and future prospects Hum. Mol. Genet. 2009 18 R75 R83 10.1093/hmg/ddp010 19297404 PMC2657943 · DOI
  151. [163]Kang H.J. Kawasawa Y.I. Cheng F. Zhu Y. Xu X. Li M. Sousa A.M. Pletikos M. Meyer K.A. Sedmak G. Spatio-temporal transcriptome of the human brain Nature 2011 478 483 489 10.1038/nature10523 22031440 PMC3566780 · DOI · Paper page
  152. [165]Herault Y. Delabar J.M. Fisher E.M.C. Tybulewicz V.L.J. Yu E. Brault V. Rodent models in Down syndrome research: Impact and future opportunities Dis. Model. Mech. 2017 10 1165 1186 10.1242/dmm.029728 28993310 PMC5665454 · DOI
  153. [166]Gupta M. Dhanasekaran A.R. Gardiner K.J. Mouse models of Down syndrome: Gene content and consequences Mamm. Genome 2016 27 538 555 10.1007/s00335-016-9661-8 27538963 PMC5471624 · DOI

Authors
Reiche, L., Küry, P., & Göttle, P.
Affiliations
Heinrich Heine University Düsseldorf (DE)
Corresponding author
Göttle, Peter
Venue
Cells
Publisher
MDPI AG
Published
2019-12-07
Volume
8
Issue
12
Pages
1591
ISSN
2073-4409 (ISSN-L)
OpenAlex
W2994323406
Cited by
28
References
169
Citations by year
2026: 1 · 2025: 5 · 2024: 3 · 2023: 5 · 2022: 4 · 2021: 7 · 2020: 3
FWCI
0.44
Type
journal article
Language
en
Open access
Locations
  • Cells (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Down syndrome and intellectual disability research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords
Down syndrome, oligodendrogenesis, oligodendrocytes, astrocytes, gliogenesis, cell fate transitions, white matter, hypomyelination, astrocyte activation, intellectual disability, oligodendroglial lineage, demyelinating disease, multiple sclerosis
MeSH terms
Animals, Down Syndrome, Humans, Neuroglia, Receptors, Notch, White Matter

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review