Human Stem Cell-Derived Spinal Cord Astrocytes with Defined Mature or Reactive Phenotypes

Abbott, 1988, Developmental neurobiology. The milieu is the message, Nature, 332, 490, 10.1038/332490a0 Allaman, 2011, Astrocyte-neuron metabolic relationships: for better and for worse, Trends Neurosci., 34, 76, 10.1016/j.tins.2010.12.001 Amoroso, 2013, Accelerated high-yield generation of limb-innervating motor neurons from human stem cells, J. Neurosci., 33, 574, 10.1523/JNEUROSCI.0906-12.2013 Anthony, 2007, The folate metabolic enzyme ALDH1L1 is restricted to the midline of the early CNS, suggesting a role in human neural tube defects, J. Comp. Neurol., 500, 368, 10.1002/cne.21179 Bernardinelli, 2011, Astrocytes display complex and localized calcium responses to single-neuron stimulation in the hippocampus, J. Neurosci., 31, 8905, 10.1523/JNEUROSCI.6341-10.2011 Bi, 2013, Reactive astrocytes secrete lcn2 to promote neuron death, Proc. Natl. Acad. Sci. USA, 110, 4069, 10.1073/pnas.1218497110 Bock, 2011, Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines, Cell, 144, 439, 10.1016/j.cell.2010.12.032 Boulting, 2011, A functionally characterized test set of human induced pluripotent stem cells, Nat. Biotechnol., 29, 279, 10.1038/nbt.1783 Brederlau, 2006, Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson’s disease: effect of in vitro differentiation on graft survival and teratoma formation, Stem Cells, 24, 1433, 10.1634/stemcells.2005-0393 Caldwell, 2001, Growth factors regulate the survival and fate of cells derived from human neurospheres, Nat. Biotechnol., 19, 475, 10.1038/88158 Cassina, 2005, Astrocyte activation by fibroblast growth factor-1 and motor neuron apoptosis: implications for amyotrophic lateral sclerosis, J. Neurochem., 93, 38, 10.1111/j.1471-4159.2004.02984.x Chambers, 2009, Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling, Nat. Biotechnol., 27, 275, 10.1038/nbt.1529 Chao, 2010, The role of excitatory amino acid transporters in cerebral ischemia, Neurochem. Res., 35, 1224, 10.1007/s11064-010-0178-3 Chen, 2011, The physical basis of FGFR3 response to fgf1 and fgf2, Biochemistry, 50, 8576, 10.1021/bi200986f Croitoru-Lamoury, 2003, Expression of chemokines and their receptors in human and simian astrocytes: evidence for a central role of TNF alpha and IFN gamma in CXCR4 and CCR5 modulation, Glia, 41, 354, 10.1002/glia.10181 Cui, 2011, FOXO3a inhibits TNF-α- and IL-1β-induced astrocyte proliferation:Implication for reactive astrogliosis, Glia, 59, 641, 10.1002/glia.21134 Dermietzel, 1989, Differential expression of three gap junction proteins in developing and mature brain tissues, Proc. Natl. Acad. Sci. USA, 86, 10148, 10.1073/pnas.86.24.10148 Di Giorgio, 2007, Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model, Nat. Neurosci., 10, 608, 10.1038/nn1885 Elde, 1991, Prominent expression of acidic fibroblast growth factor in motor and sensory neurons, Neuron, 7, 349, 10.1016/0896-6273(91)90288-B Emdad, 2012, Efficient differentiation of human embryonic and induced pluripotent stem cells into functional astrocytes, Stem Cells Dev., 21, 404, 10.1089/scd.2010.0560 Faideau, 2010, In vivo expression of polyglutamine-expanded huntingtin by mouse striatal astrocytes impairs glutamate transport: a correlation with Huntington’s disease subjects, Hum. Mol. Genet., 19, 3053, 10.1093/hmg/ddq212 Filous, 2010, Immature astrocytes promote CNS axonal regeneration when combined with chondroitinase ABC, Dev. Neurobiol., 70, 826, 10.1002/dneu.20820 Fine, 1996, Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia, J. Biol. Chem., 271, 15303, 10.1074/jbc.271.26.15303 Garré, 2010, FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels, Proc. Natl. Acad. Sci. USA, 107, 22659, 10.1073/pnas.1013793107 Glass, 2010, Mechanisms underlying inflammation in neurodegeneration, Cell, 140, 918, 10.1016/j.cell.2010.02.016 Goldshmit, 2012, Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish, J. Neurosci., 32, 7477, 10.1523/JNEUROSCI.0758-12.2012 Gupta, 2013, Glial molecular alterations with mouse brain development and aging: up-regulation of the Kir4.1 and aquaporin-4, Age (Dordr), 35, 59, 10.1007/s11357-011-9330-5 Gwak, 2012, Spatial and temporal activation of spinal glial cells: role of gliopathy in central neuropathic pain following spinal cord injury in rats, Exp. Neurol., 234, 362, 10.1016/j.expneurol.2011.10.010 Haidet-Phillips, 2011, Astrocytes from familial and sporadic ALS patients are toxic to motor neurons, Nat. Biotechnol., 29, 824, 10.1038/nbt.1957 Hirano, 1988, Gliogenesis in rat spinal cord: evidence for origin of astrocytes and oligodendrocytes from radial precursors, J. Neurosci. Res., 21, 155, 10.1002/jnr.490210208 Hu, 2010, Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency, Proc. Natl. Acad. Sci. USA, 107, 4335, 10.1073/pnas.0910012107 Huang, 2004, Glutamate transporters bring competition to the synapse, Curr. Opin. Neurobiol., 14, 346, 10.1016/j.conb.2004.05.007 Imura, 2006, Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes, Glia, 53, 277, 10.1002/glia.20281 Irmady, 2011, Fibroblast growth factor 2 regulates astrocyte differentiation in a region-specific manner in the hindbrain, Glia, 59, 708, 10.1002/glia.21141 James, 2006, Contribution of human embryonic stem cells to mouse blastocysts, Dev. Biol., 295, 90, 10.1016/j.ydbio.2006.03.026 Juopperi, 2012, Astrocytes generated from patient induced pluripotent stem cells recapitulate features of Huntington’s disease patient cells, Mol. Brain, 5, 17, 10.1186/1756-6606-5-17 Kamo, 1987, A distinctive distribution of reactive astroglia in the precentral cortex in amyotrophic lateral sclerosis, Acta Neuropathol., 74, 33, 10.1007/BF00688335 Karumbayaram, 2009, Directed differentiation of human-induced pluripotent stem cells generates active motor neurons, Stem Cells, 27, 806, 10.1002/stem.31 Krencik, 2011, Directed differentiation of functional astroglial subtypes from human pluripotent stem cells, Nat. Protoc., 6, 1710, 10.1038/nprot.2011.405 Krencik, 2011, Specification of transplantable astroglial subtypes from human pluripotent stem cells, Nat. Biotechnol., 29, 528, 10.1038/nbt.1877 Kriks, 2011, Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease, Nature, 480, 547, 10.1038/nature10648 Kuegler, 2012, GFAP-independent inflammatory competence and trophic functions of astrocytes generated from murine embryonic stem cells, Glia, 60, 218, 10.1002/glia.21257 Lafaille, 2012, Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells, Nature, 491, 769, 10.1038/nature11583 Lee, 1993, Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta, J. Immunol., 150, 2659, 10.4049/jimmunol.150.7.2659 Li, 2005, Specification of motoneurons from human embryonic stem cells, Nat. Biotechnol., 23, 215, 10.1038/nbt1063 Lie, 2005, Wnt signalling regulates adult hippocampal neurogenesis, Nature, 437, 1370, 10.1038/nature04108 Lin, 2009, An FGF-responsive astrocyte precursor isolated from the neonatal forebrain, Glia, 57, 592, 10.1002/glia.20788 McCarthy, 1980, Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue, J. Cell Biol., 85, 890, 10.1083/jcb.85.3.890 Meeuwsen, 2003, Cytokine, chemokine and growth factor gene profiling of cultured human astrocytes after exposure to proinflammatory stimuli, Glia, 43, 243, 10.1002/glia.10259 Mitani, 2003, Functional changes of glial glutamate transporter GLT-1 during ischemia: an in vivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1, J. Neurosci., 23, 7176, 10.1523/JNEUROSCI.23-18-07176.2003 Morrow, 2001, Sequential specification of neurons and glia by developmentally regulated extracellular factors, Development, 128, 3585, 10.1242/dev.128.18.3585 Murayama, 1991, A unique pattern of astrocytosis in the primary motor area in amyotrophic lateral sclerosis, Acta Neuropathol., 82, 456, 10.1007/BF00293379 Nagai, 2007, Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons, Nat. Neurosci., 10, 615, 10.1038/nn1876 Okamoto, 2011, Reduction in paracrine Wnt3 factors during aging causes impaired adult neurogenesis, FASEB J., 25, 3570, 10.1096/fj.11-184697 Ornitz, 1996, Receptor specificity of the fibroblast growth factor family, J. Biol. Chem., 271, 15292, 10.1074/jbc.271.25.15292 Panatier, 2011, Astrocytes are endogenous regulators of basal transmission at central synapses, Cell, 146, 785, 10.1016/j.cell.2011.07.022 Pringle, 2003, Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains, Development, 130, 93, 10.1242/dev.00184 Reilly, 1998, Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2, Glia, 22, 202, 10.1002/(SICI)1098-1136(199802)22:2<202::AID-GLIA11>3.0.CO;2-1 Rothstein, 1995, Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis, Ann. Neurol., 38, 73, 10.1002/ana.410380114 Rothstein, 1996, Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate, Neuron, 16, 675, 10.1016/S0896-6273(00)80086-0 Schiffer, 1996, Reactive astrogliosis of the spinal cord in amyotrophic lateral sclerosis, J. Neurol. Sci., 139, 27, 10.1016/0022-510X(96)00073-1 Serio, 2013, Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy, Proc. Natl. Acad. Sci. USA, 110, 4697, 10.1073/pnas.1300398110 Shaltouki, 2013, Efficient generation of astrocytes from human pluripotent stem cells in defined conditions, Stem Cells, 31, 941, 10.1002/stem.1334 Sofroniew, 2009, Molecular dissection of reactive astrogliosis and glial scar formation, Trends Neurosci., 32, 638, 10.1016/j.tins.2009.08.002 Sokolova, 2012, Expression of protease-activated receptor (PAR)-2, but not other PARs, is regulated by inflammatory cytokines in rat astrocytes, Neurochem. Int., 60, 276, 10.1016/j.neuint.2011.12.016 Takano, 2006, Astrocyte-mediated control of cerebral blood flow, Nat. Neurosci., 9, 260, 10.1038/nn1623 Theodoric, 2012, Role of gap junction protein connexin43 in astrogliosis induced by brain injury, PLoS ONE, 7, e47311, 10.1371/journal.pone.0047311 Tom, 2004, Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter, J. Neurosci., 24, 9282, 10.1523/JNEUROSCI.2120-04.2004 Van Wagoner, 1999, Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor, J. Neurosci., 19, 5236, 10.1523/JNEUROSCI.19-13-05236.1999 Verwer, 2007, Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin, Brain, 130, 3321, 10.1093/brain/awm264 Voutsinos-Porche, 2003, Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex, Neuron, 37, 275, 10.1016/S0896-6273(02)01170-4 Voutsinos-Porche, 2003, Glial glutamate transporters and maturation of the mouse somatosensory cortex, Cereb. Cortex, 13, 1110, 10.1093/cercor/13.10.1110 Wichterle, 2002, Directed differentiation of embryonic stem cells into motor neurons, Cell, 110, 385, 10.1016/S0092-8674(02)00835-8 Yamanaka, 2008, Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis, Nat. Neurosci., 11, 251, 10.1038/nn2047 Yang, 2011, Molecular comparison of GLT1+ and ALDH1L1+ astrocytes in vivo in astroglial reporter mice, Glia, 59, 200, 10.1002/glia.21089 Yu, 2008, BMP type I receptor inhibition reduces heterotopic [corrected] ossification, Nat. Med., 14, 1363, 10.1038/nm.1888 Zamanian, 2012, Genomic analysis of reactive astrogliosis, J. Neurosci., 32, 6391, 10.1523/JNEUROSCI.6221-11.2012 Agius, 2010, Role of BMPs in controlling the spatial and temporal origin of GFAP astrocytes in the embryonic spinal cord, Dev. Biol., 344, 611, 10.1016/j.ydbio.2010.05.017 Bar-Peled, 1997, Distribution of glutamate transporter subtypes during human brain development, J. Neurochem., 69, 2571, 10.1046/j.1471-4159.1997.69062571.x Benveniste, 1992, Inflammatory cytokines within the central nervous system: sources, function, and mechanism of action, Am. J. Physiol., 263, C1, 10.1152/ajpcell.1992.263.1.C1 Brunne, 2010, Origin, maturation, and astroglial transformation of secondary radial glial cells in the developing dentate gyrus, Glia, 58, 1553, 10.1002/glia.21029 Bushong, 2004, Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development, Int. J. Dev. Neurosci., 22, 73, 10.1016/j.ijdevneu.2003.12.008 Cahoy, 2008, A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function, J. Neurosci., 28, 264, 10.1523/JNEUROSCI.4178-07.2008 Deneen, 2006, The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord, Neuron, 52, 953, 10.1016/j.neuron.2006.11.019 Farina, 2007, Astrocytes are active players in cerebral innate immunity, Trends Immunol., 28, 138, 10.1016/j.it.2007.01.005 Foo, 2011, Development of a method for the purification and culture of rodent astrocytes, Neuron, 71, 799, 10.1016/j.neuron.2011.07.022 Freeman, 2010, Specification and morphogenesis of astrocytes, Science, 330, 774, 10.1126/science.1190928 Furuta, 1997, Glutamate transporter protein subtypes are expressed differentially during rat CNS development, J. Neurosci., 17, 8363, 10.1523/JNEUROSCI.17-21-08363.1997 Gronostajski, 2000, Roles of the NFI/CTF gene family in transcription and development, Gene, 249, 31, 10.1016/S0378-1119(00)00140-2 Hochstim, 2008, Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code, Cell, 133, 510, 10.1016/j.cell.2008.02.046 Kugler, 2004, Developmental expression of glutamate transporters and glutamate dehydrogenase in astrocytes of the postnatal rat hippocampus, Hippocampus, 14, 975, 10.1002/hipo.20015 Liu, 2002, Oligodendrocyte and astrocyte development in rodents: an in situ and immunohistological analysis during embryonic development, Glia, 40, 25, 10.1002/glia.10111 Liu, 2004, CD44 expression identifies astrocyte-restricted precursor cells, Dev. Biol., 276, 31, 10.1016/j.ydbio.2004.08.018 Lovatt, 2007, The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex, J. Neurosci., 27, 12255, 10.1523/JNEUROSCI.3404-07.2007 Mason, 2009, Nuclear factor one transcription factors in CNS development, Mol. Neurobiol., 39, 10, 10.1007/s12035-008-8048-6 Nadarajah, 1997, Differential expression of connexins during neocortical development and neuronal circuit formation, J. Neurosci., 17, 3096, 10.1523/JNEUROSCI.17-09-03096.1997 Neymeyer, 1997, Folate and 10-formyltetrahydrofolate dehydrogenase (FDH) expression in the central nervous system of the mature rat, Brain Res., 766, 195, 10.1016/S0006-8993(97)00528-3 Peljto, 2010, Functional diversity of ESC-derived motor neuron subtypes revealed through intraspinal transplantation, Cell Stem Cell, 7, 355, 10.1016/j.stem.2010.07.013 Piper, 2010, NFIA controls telencephalic progenitor cell differentiation through repression of the Notch effector Hes1, J. Neurosci., 30, 9127, 10.1523/JNEUROSCI.6167-09.2010 Regan, 2007, Variations in promoter activity reveal a differential expression and physiology of glutamate transporters by glia in the developing and mature CNS, J. Neurosci., 27, 6607, 10.1523/JNEUROSCI.0790-07.2007 Shibata, 1997, Glutamate transporter GLAST is expressed in the radial glia-astrocyte lineage of developing mouse spinal cord, J. Neurosci., 17, 9212, 10.1523/JNEUROSCI.17-23-09212.1997 Ullensvang, 1997, Differential developmental expression of the two rat brain glutamate transporter proteins GLAST and GLT, Eur. J. Neurosci., 9, 1646, 10.1111/j.1460-9568.1997.tb01522.x Walther, 1998, Genomic sequences of aldolase C (Zebrin II) direct lacZ expression exclusively in non-neuronal cells of transgenic mice, Proc. Natl. Acad. Sci. USA, 95, 2615, 10.1073/pnas.95.5.2615 Wichterle, 2008, Differentiation of mouse embryonic stem cells to spinal motor neurons, Curr. Protoc. Stem. Cell Biol., Chapter 1, 10.1002/9780470151808.sc01h01s5