Maturation and electrophysiological properties of human pluripotent stem cell-derived oligodendrocytes

Stem Cells

Volumn 34, Issue 4, 2016, Pages 1040-1053

  Livesey, Matthew R ^a   Magnani, Dario ^a,b,c   Cleary, Elaine M ^b,c   Vasistha, Navneet A ^a   James, Owain T ^a,d   Selvaraj, Bhuvaneish T ^a,b   Burr, Karen ^a,b   Story, David ^a,b,c   Shaw, Christopher E ^e   Kind, Peter C ^a,d   Hardingham, Giles E ^a   Wyllie, David J A ^a,d   Chandran, Siddharthan ^a,b,c,d  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d Institute for Stem Cell Biology and Regenerative Medicine   (India)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Amyotrophic lateral sclerosis; Electrophysiology; Human; Oligodendrocyte; oligodendrocyte precursor cell; Stem cell

Indexed keywords

AMPA RECEPTOR; CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; LIGAND GATED ION CHANNEL; NEUROTRANSMITTER; POTASSIUM CHANNEL; SODIUM CHANNEL; TETRODOTOXIN; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL POPULATION; CELL VIABILITY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; MALE; MEMBRANE CURRENT; MULTIPLE SCLEROSIS; OLIGODENDROCYTE PRECURSOR CELL; SPECIES CONSERVATION; ANIMAL; GENETICS; MUTATION; NERVOUS SYSTEM DEVELOPMENT; OLIGODENDROGLIA; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLURIPOTENT STEM CELL;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL DIFFERENTIATION; ELECTROPHYSIOLOGICAL PHENOMENA; FEMALE; HUMANS; MALE; MULTIPLE SCLEROSIS; MUTATION; NEUROGENESIS; OLIGODENDROGLIA; PLURIPOTENT STEM CELLS; POTASSIUM CHANNELS, VOLTAGE-GATED; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84954289552     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2273     Document Type: Article

References (69)

1. Saab AS, Tzvetanova ID, Nave KA,. The role of myelin and oligodendrocytes in axonal energy metabolism. Curr Opin Neurobiol 2013; 23: 1065-1072.
2. Crawford AH, Stockley JH, Tripathi RB, et al., Oligodendrocyte progenitors: Adult stem cells of the central nervous system? Exp Neurol 2014; 260: 50-55.
3. Kang SH, Li Y, Fukaya M, et al., Degeneration and impaired regeneration of gray matter oligodendrocytes in amyotrophic lateral sclerosis. Nat Neurosci 2013; 16: 571-579.
4. Lee Y, Morrison BM, Li Y, et al., Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012; 487: 443-448.
5. Philips T, Bento-Abreu A, Nonneman A, et al., Oligodendrocyte dysfunction in the pathogenesis of amyotrophic lateral sclerosis. Brain 2013; 136: 471-482.
6. Gijselinck I, Van Langenhove T, van der Zee J, et al., A C9orf72 promoter repeat expansion in a Flanders-Belgian cohort with disorders of the frontotemporal lobar degeneration-amyotrophic lateral sclerosis spectrum: A gene identification study. Lancet Neurol 2012; 11: 54-65.
7. Majounie E, Renton AE, Mok K, et al., Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: A cross-sectional study. Lancet Neurol 2012; 11: 323-330.
8. Smith BN, Newhouse S, Shatunov A, et al., The C9ORF72 expansion mutation is a common cause of ALS+/-FTD in Europe and has a single founder. Eur J Hum Genet 2013; 21: 102-108.
9. Oberheim NA, Takano T, Han X, et al., Uniquely hominid features of adult human astrocytes. J Neurosci 2009; 29: 3276-3287.
10. Dermitzakis ET, Clark AG,. Evolution of transcription factor binding sites in Mammalian gene regulatory regions: Conservation and turnover. Mol Biol Evol 2002; 19: 1114-1121.
11. Janke C, Beck M, Stahl T, et al., Phylogenetic diversity of the expression of the microtubule-associated protein tau: Implications for neurodegenerative disorders. Brain Res Mol Brain Res 1999; 68: 119-128.
12. Wilson MD, Barbosa-Morais NL, Schmidt D, et al., Species-specific transcription in mice carrying human chromosome 21. Science 2008; 322: 434-438.
13. Odom DT, Dowell RD, Jacobsen ES, et al., Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 2007; 39: 730-732.
14. Bradl M, Lassmann H,. Oligodendrocytes: Biology and pathology. Acta Neuropathol 2010; 119: 37-53.
15. Hu BY, Du ZW, Zhang SC,. Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc 2009; 4: 1614-1622.
16. Wang S, Bates J, Li X, et al., Human iPSC-derived oligodendrocyte progenitor cells can myelinate and rescue a mouse model of congenital hypomyelination. Cell Stem Cell 2013; 12: 252-264.
17. Douvaras P, Wang J, Zimmer M, et al., Efficient generation of myelinating oligodendrocytes from primary progressive multiple sclerosis patients by induced pluripotent stem cells. Stem Cell Reports 2014; 3: 250-259.
18. Bilican B, Serio A, Barmada SJ, et al., Mutant induced pluripotent stem cell lines recapitulate aspects of TDP-43 proteinopathies and reveal cell-specific vulnerability. Proc Natl Acad Sci USA 2012; 109: 5803-5808.
19. Chambers SM, Fasano CA, Papapetrou EP, et al., Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 2009; 27: 275-280.
20. Bilican B, Livesey MR, Haghi G, et al., Physiological normoxia and absence of EGF is required for the long-term propagation of anterior neural precursors from human pluripotent cells. Plos One 2014; 9: e85932.
21. AR reversal potential in hPSC-derived cortical neurons. J Neurosci 2014; 34: 4070-4075.
22. Sim FJ, McClain CR, Schanz SJ, et al., CD140a identifies a population of highly myelinogenic, migration-competent and efficiently engrafting human oligodendrocyte progenitor cells. Nat Biotechnol 2011; 29: 934-941.
23. Tripathi RB, Clarke LE, Burzomato V, et al., Dorsally and ventrally derived oligodendrocytes have similar electrical properties but myelinate preferred tracts. J Neurosci 2011; 31: 6809-6819.
24. Sontheimer H, Trotter J, Schachner M, et al., Channel expression correlates with differentiation stage during the development of oligodendrocytes from their precursor cells in culture. Neuron 1989; 2: 1135-1145.
25. Barres BA, Koroshetz WJ, Swartz KJ, et al., Ion channel expression by white matter glia: The O-2A glial progenitor cell. Neuron 1990; 4: 507-524.
26. De Biase LM, Nishiyama A, Bergles DE,. Excitability and synaptic communication within the oligodendrocyte lineage. J Neurosci 2010; 30: 3600-3611.
27. Karadottir R, Hamilton NB, Bakiri Y, et al., Spiking and nonspiking classes of oligodendrocyte precursor glia in CNS white matter. Nat Neurosci 2008; 11: 450-456.
28. Clarke LE, Young KM, Hamilton NB, et al., Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J Neurosci 2012; 32: 8173-8185.
29. Neusch C, Rozengurt N, Jacobs RE, et al., Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J Neurosci 2001; 21: 5429-5438.
30. Maldonado PP, Velez-Fort M, Levavasseur F, et al., Oligodendrocyte precursor cells are accurate sensors of local K + in mature gray matter. J Neurosci 2013; 33: 2432-2442.
31. Karadottir R, Attwell D,. Neurotransmitter receptors in the life and death of oligodendrocytes. Neuroscience 2007; 145: 1426-1438.
32. Follett PL, Deng W, Dai W, et al., Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: A protective role for topiramate. J Neurosci 2004; 24: 4412-4420.
33. Fannon J, Tarmier W, Fulton D,. Neuronal activity and AMPA-type glutamate receptor activation regulates the morphological development of oligodendrocyte precursor cells. Glia 2015.
34. Wosik K, Ruffini F, Almazan G, et al., Resistance of human adult oligodendrocytes to AMPA/kainate receptor-mediated glutamate injury. Brain 2004; 127: 2636-2648.
35. Traynelis SF, Wollmuth LP, McBain CJ, et al., Glutamate receptor ion channels: Structure, regulation, and function. Pharmacol Rev 2010; 62: 405-496.
36. Koike M, Iino M, Ozawa S,. Blocking effect of 1-naphthyl acetyl spermine on Ca(2+)-permeable AMPA receptors in cultured rat hippocampal neurons. Neurosci Res 1997; 29: 27-36.
37. DeJesus-Hernandez M, Mackenzie IR, Boeve BF, et al., Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011; 72: 245-256.
38. Renton AE, Majounie E, Waite A, et al., A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011; 72: 257-268.
39. Devlin AC, Burr K, Borooah S, et al., Human iPSC-derived motoneurons harbouring TARDBP or C9ORF72 ALS mutations are dysfunctional despite maintaining viability. Nat Commun 2015; 6: 5999.
40. Fratta P, Poulter M, Lashley T, et al., Homozygosity for the C9orf72 GGGGCC repeat expansion in frontotemporal dementia. Acta Neuropathol 2013; 126: 401-409.
41. Donnelly CJ, Zhang PW, Pham JT, et al., RNA toxicity from the ALS/FTD C9ORF72 expansion is mitigated by antisense intervention. Neuron 2013; 80: 415-428.
42. Belzil VV, Bauer PO, Prudencio M, et al., Reduced C9orf72 gene expression in c9FTD/ALS is caused by histone trimethylation, an epigenetic event detectable in blood. Acta Neuropathol 2013; 126: 895-905.
43. Suzuki N, Maroof AM, Merkle FT, et al., The mouse C9ORF72 ortholog is enriched in neurons known to degenerate in ALS and FTD. Nat Neurosci 2013; 16: 1725-1727.
44. Fratta P, Mizielinska S, Nicoll AJ, et al., C9orf72 hexanucleotide repeat associated with amyotrophic lateral sclerosis and frontotemporal dementia forms RNA G-quadruplexes. Sci Rep 2012; 2: 1016.
45. Reddy K, Zamiri B, Stanley SY, et al., The disease-associated r(GGGGCC)n repeat from the C9orf72 gene forms tract length-dependent uni- and multimolecular RNA G-quadruplex structures. J Biol Chem 2013; 288: 9860-9866.
46. Zamiri B, Reddy K, Macgregor RB, Jr., et al., TMPyP4 porphyrin distorts RNA G-quadruplex structures of the disease-associated r(GGGGCC)n repeat of the C9orf72 gene and blocks interaction of RNA-binding proteins. J Biol Chem 2014; 289: 4653-4659.
47. Sareen D, O'Rourke JG, Meera P, et al., Targeting RNA foci in iPSC-derived motor neurons from ALS patients with a C9ORF72 repeat expansion. Sci Transl Med 2013; 5: 208ra149.
48. Jiang P, Chen C, Liu XB, et al., Generation and characterization of spiking and nonspiking oligodendroglial progenitor cells from embryonic stem cells. Stem Cells 2013; 31: 2620-2631.
49. Scheffler B, Schmandt T, Schroder W, et al., Functional network integration of embryonic stem cell-derived astrocytes in hippocampal slice cultures. Development 2003; 130: 5533-5541.
50. Husseini L, Schmandt T, Scheffler B, et al., Functional analysis of embryonic stem cell-derived glial cells after integration into hippocampal slice cultures. Stem Cells Dev 2008; 17: 1141-1152.
51. Kukley M, Nishiyama A, Dietrich D,. The fate of synaptic input to NG2 glial cells: Neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells. J Neurosci 2010; 30: 8320-8331.
52. Stacpoole SR, Spitzer S, Bilican B, et al., High yields of oligodendrocyte lineage cells from human embryonic stem cells at physiological oxygen tensions for evaluation of translational biology. Stem Cell Reports 2013; 1: 437-450.
53. Chittajallu R, Aguirre A, Gallo V,. NG2-positive cells in the mouse white and grey matter display distinct physiological properties. J Physiol 2004; 561: 109-122.
54. Van den Eynden J, Ali SS, Horwood N, et al., Glycine and glycine receptor signalling in non-neuronal cells. Front Mol Neurosci 2009; 2: 9.
55. 2+-permeable AMPA receptors in cortical glia. J Neurosci 1996; 16: 519-530.
56. Swanson GT, Kamboj SK, Cull-Candy SG,. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 1997; 17: 58-69.
57. Zonouzi M, Renzi M, Farrant M, et al., Bidirectional plasticity of calcium-permeable AMPA receptors in oligodendrocyte lineage cells. Nat Neurosci 2011; 14: 1430-1438.
58. Patneau DK, Wright PW, Winters C, et al., Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 1994; 12: 357-371.
59. Itoh T, Beesley J, Itoh A, et al., AMPA glutamate receptor-mediated calcium signaling is transiently enhanced during development of oligodendrocytes. J Neurochem 2002; 81: 390-402.
60. Butts BD, Houde C, Mehmet H,. Maturation-dependent sensitivity of oligodendrocyte lineage cells to apoptosis: Implications for normal development and disease. Cell Death Differ 2008; 15: 1178-1186.
61. Brettschneider J, Arai K, Del Tredici K, et al., TDP-43 pathology and neuronal loss in amyotrophic lateral sclerosis spinal cord. Acta Neuropathol 2014; 128: 423-437.
62. Freibaum BD, Lu Y, Lopez-Gonzalez R, et al., GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature 2015; 525: 129-133.
63. Zhang K, Donnelly CJ, Haeusler AR, et al., The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature 2015; 525: 56-61.
64. Koppers M, Blokhuis AM, Westeneng HJ, et al., C9orf72 ablation in mice does not cause motor neuron degeneration or motor deficits. Ann Neurol 2015; 78: 426-438.
65. Mizielinska S, Lashley T, Norona FE, et al., C9orf72 frontotemporal lobar degeneration is characterised by frequent neuronal sense and antisense RNA foci. Acta Neuropathol 2013; 126: 845-857.
66. Murray ME, DeJesus-Hernandez M, Rutherford NJ, et al., Clinical and neuropathologic heterogeneity of c9FTD/ALS associated with hexanucleotide repeat expansion in C9ORF72. Acta Neuropathol 2011; 122: 673-690.
67. Al-Sarraj S, King A, Troakes C, et al., p62 positive, TDP-43 negative, neuronal cytoplasmic and intranuclear inclusions in the cerebellum and hippocampus define the pathology of C9orf72-linked FTLD and MND/ALS. Acta Neuropathol 2011; 122: 691-702.
68. Brettschneider J, Van Deerlin VM, Robinson JL, et al., Pattern of ubiquilin pathology in ALS and FTLD indicates presence of C9ORF72 hexanucleotide expansion. Acta Neuropathol 2012; 123: 825-839.
69. Meyer K, Ferraiuolo L, Miranda CJ, et al., Direct conversion of patient fibroblasts demonstrates non-cell autonomous toxicity of astrocytes to motor neurons in familial and sporadic ALS. Proc Natl Acad Sci U S A 2014; 111: 829-832.