Human stem cell-derived spinal cord astrocytes with defined mature or reactive phenotypes

Cell Reports

Volumn 4, Issue 5, 2013, Pages 1035-1048

  Roybon, Laurent ^a,c   Lamas, NunoJ ^a,d   Garcia Diaz, Alejandro ^a   Yang, EunJu ^b   Sattler, Rita ^b   Jackson Lewis, Vernice ^a   Kim, YoonA ^a   Kachel, C Alan ^a   Rothstein, JeffreyD ^b   Przedborski, Serge ^a   Wichterle, Hynek ^a   Henderson, ChristopherE ^a  

^a New York Presbyterian Morgan Stanley Children's Hospital   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LUND UNIVERSITY   (Sweden)

^d UNIVERSITY OF MINHO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CONNEXIN 43; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 1BETA; OCTAMER TRANSCRIPTION FACTOR 4; SMAD PROTEIN; TRANSCRIPTION FACTOR PAX6; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN FUNCTION; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; EMBRYO; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPINAL CORD; STEM CELL; SYNAPTIC TRANSMISSION; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MICE; NEURAL STEM CELLS; NEURONS; PHENOTYPE; PLURIPOTENT STEM CELLS; SPINAL CORD;

EID: 84884146442     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.06.021     Document Type: Article

References (77)

1. Abbott N.J. Developmental neurobiology. The milieu is the message. Nature 1988, 332:490-491.
2. Allaman I., Bélanger M., Magistretti P.J. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci. 2011, 34:76-87.
3. Amoroso M.W., Croft G.F., Williams D.J., O'Keeffe S., Carrasco M.A., Davis A.R., Roybon L., Oakley D.H., Maniatis T., Henderson C.E., Wichterle H. Accelerated high-yield generation of limb-innervating motor neurons from human stem cells. J.Neurosci. 2013, 33:574-586.
4. Anthony T.E., Heintz N. 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. 2007, 500:368-383.
5. Bernardinelli Y., Salmon C., Jones E.V., Farmer W.T., Stellwagen D., Murai K.K. Astrocytes display complex and localized calcium responses to single-neuron stimulation in the hippocampus. J.Neurosci. 2011, 31:8905-8919.
6. Bi F., Huang C., Tong J., Qiu G., Huang B., Wu Q., Li F., Xu Z., Bowser R., Xia X.G., Zhou H. Reactive astrocytes secrete lcn2 to promote neuron death. Proc. Natl. Acad. Sci. USA 2013, 110:4069-4074.
7. Bock C., Kiskinis E., Verstappen G., Gu H., Boulting G., Smith Z.D., Ziller M., Croft G.F., Amoroso M.W., Oakley D.H., et al. Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 2011, 144:439-452.
8. Boulting G.L., Kiskinis E., Croft G.F., Amoroso M.W., Oakley D.H., Wainger B.J., Williams D.J., Kahler D.J., Yamaki M., Davidow L., et al. A functionally characterized test set of human induced pluripotent stem cells. Nat. Biotechnol. 2011, 29:279-286.
9. Brederlau A., Correia A.S., Anisimov S.V., Elmi M., Paul G., Roybon L., Morizane A., Bergquist F., Riebe I., Nannmark U., et al. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson's disease: effect of invitro differentiation on graft survival and teratoma formation. Stem Cells 2006, 24:1433-1440.
10. Caldwell M.A., He X., Wilkie N., Pollack S., Marshall G., Wafford K.A., Svendsen C.N. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 2001, 19:475-479.
11. Cassina P., Pehar M., Vargas M.R., Castellanos R., Barbeito A.G., Estévez A.G., Thompson J.A., Beckman J.S., Barbeito L. Astrocyte activation by fibroblast growth factor-1 and motor neuron apoptosis: implications for amyotrophic lateral sclerosis. J.Neurochem. 2005, 93:38-46.
12. Chambers S.M., Fasano C.A., Papapetrou E.P., Tomishima M., Sadelain M., Studer L. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 2009, 27:275-280.
13. Chao X.D., Fei F., Fei Z. The role of excitatory amino acid transporters in cerebral ischemia. Neurochem. Res. 2010, 35:1224-1230.
14. Chen F., Hristova K. The physical basis of FGFR3 response to fgf1 and fgf2. Biochemistry 2011, 50:8576-8582.
15. Croitoru-Lamoury J., Guillemin G.J., Boussin F.D., Mognetti B., Gigout L.I., Chéret A., Vaslin B., Le Grand R., Brew B.J., Dormont D. 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 2003, 41:354-370.
16. Cui M., Huang Y., Tian C., Zhao Y., Zheng J. FOXO3a inhibits TNF-α- and IL-1β-induced astrocyte proliferation:Implication for reactive astrogliosis. Glia 2011, 59:641-654.
17. Dermietzel R., Traub O., Hwang T.K., Beyer E., Bennett M.V., Spray D.C., Willecke K. Differential expression of three gap junction proteins in developing and mature brain tissues. Proc. Natl. Acad. Sci. USA 1989, 86:10148-10152.
18. Di Giorgio F.P., Carrasco M.A., Siao M.C., Maniatis T., Eggan K. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci. 2007, 10:608-614.
19. Elde R., Cao Y.H., Cintra A., Brelje T.C., Pelto-Huikko M., Junttila T., Fuxe K., Pettersson R.F., Hökfelt T. Prominent expression of acidic fibroblast growth factor in motor and sensory neurons. Neuron 1991, 7:349-364.
20. Emdad L., D'Souza S.L., Kothari H.P., Qadeer Z.A., Germano I.M. Efficient differentiation of human embryonic and induced pluripotent stem cells into functional astrocytes. Stem Cells Dev. 2012, 21:404-410.
21. Faideau M., Kim J., Cormier K., Gilmore R., Welch M., Auregan G., Dufour N., Guillermier M., Brouillet E., Hantraye P., et al. Invivo expression of polyglutamine-expanded huntingtin by mouse striatal astrocytes impairs glutamate transport: a correlation with Huntington's disease subjects. Hum. Mol. Genet. 2010, 19:3053-3067.
22. Filous A.R., Miller J.H., Coulson-Thomas Y.M., Horn K.P., Alilain W.J., Silver J. Immature astrocytes promote CNS axonal regeneration when combined with chondroitinase ABC. Dev. Neurobiol. 2010, 70:826-841.
23. Fine S.M., Angel R.A., Perry S.W., Epstein L.G., Rothstein J.D., Dewhurst S., Gelbard H.A. Tumor necrosis factor alpha inhibits glutamate uptake by primary human astrocytes. Implications for pathogenesis of HIV-1 dementia. J.Biol. Chem. 1996, 271:15303-15306.
24. Garré J.M., Retamal M.A., Cassina P., Barbeito L., Bukauskas F.F., Sáez J.C., Bennett M.V., Abudara V. FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc. Natl. Acad. Sci. USA 2010, 107:22659-22664.
25. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
26. Goldshmit Y., Sztal T.E., Jusuf P.R., Hall T.E., Nguyen-Chi M., Currie P.D. Fgf-dependent glial cell bridges facilitate spinal cord regeneration in zebrafish. J.Neurosci. 2012, 32:7477-7492.
27. Gupta R.K., Kanungo M. Glial molecular alterations with mouse brain development and aging: up-regulation of the Kir4.1 and aquaporin-4. Age (Dordr) 2013, 35:59-67.
28. Gwak Y.S., Kang J., Unabia G.C., Hulsebosch C.E. Spatial and temporal activation of spinal glial cells: role of gliopathy in central neuropathic pain following spinal cord injury in rats. Exp. Neurol. 2012, 234:362-372.
29. Haidet-Phillips A.M., Hester M.E., Miranda C.J., Meyer K., Braun L., Frakes A., Song S., Likhite S., Murtha M.J., Foust K.D., et al. Astrocytes from familial and sporadic ALS patients are toxic to motor neurons. Nat. Biotechnol. 2011, 29:824-828.
30. Hirano M., Goldman J.E. Gliogenesis in rat spinal cord: evidence for origin of astrocytes and oligodendrocytes from radial precursors. J.Neurosci. Res. 1988, 21:155-167.
31. Hu B.Y., Weick J.P., Yu J., Ma L.X., Zhang X.Q., Thomson J.A., Zhang S.C. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. USA 2010, 107:4335-4340.
32. Huang Y.H., Bergles D.E. Glutamate transporters bring competition to the synapse. Curr. Opin. Neurobiol. 2004, 14:346-352.
33. Imura T., Nakano I., Kornblum H.I., Sofroniew M.V. Phenotypic and functional heterogeneity of GFAP-expressing cells invitro: differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 2006, 53:277-293.
34. Irmady K., Zechel S., Unsicker K. Fibroblast growth factor 2 regulates astrocyte differentiation in a region-specific manner in the hindbrain. Glia 2011, 59:708-719.
35. James D., Noggle S.A., Swigut T., Brivanlou A.H. Contribution of human embryonic stem cells to mouse blastocysts. Dev. Biol. 2006, 295:90-102.
36. Juopperi T.A., Kim W.R., Chiang C.H., Yu H., Margolis R.L., Ross C.A., Ming G.L., Song H. Astrocytes generated from patient induced pluripotent stem cells recapitulate features of Huntington's disease patient cells. Mol. Brain 2012, 5:17.
37. Kamo H., Haebara H., Akiguchi I., Kameyama M., Kimura H., McGeer P.L. A distinctive distribution of reactive astroglia in the precentral cortex in amyotrophic lateral sclerosis. Acta Neuropathol. 1987, 74:33-38.
38. Karumbayaram S., Novitch B.G., Patterson M., Umbach J.A., Richter L., Lindgren A., Conway A.E., Clark A.T., Goldman S.A., Plath K., et al. Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 2009, 27:806-811.
39. Krencik R., Zhang S.C. Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat. Protoc. 2011, 6:1710-1717.
40. Krencik R., Weick J.P., Liu Y., Zhang Z.J., Zhang S.C. Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat. Biotechnol. 2011, 29:528-534.
41. Kriks S., Shim J.W., Piao J., Ganat Y.M., Wakeman D.R., Xie Z., Carrillo-Reid L., Auyeung G., Antonacci C., Buch A., et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 2011, 480:547-551.
42. Kuegler P.B., Baumann B.A., Zimmer B., Keller S., Marx A., Kadereit S., Leist M. GFAP-independent inflammatory competence and trophic functions of astrocytes generated from murine embryonic stem cells. Glia 2012, 60:218-228.
43. Lafaille F.G., Pessach I.M., Zhang S.Y., Ciancanelli M.J., Herman M., Abhyankar A., Ying S.W., Keros S., Goldstein P.A., Mostoslavsky G., et al. Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 2012, 491:769-773.
44. Lee S.C., Liu W., Dickson D.W., Brosnan C.F., Berman J.W. Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J.Immunol. 1993, 150:2659-2667.
45. Li X.J., Du Z.W., Zarnowska E.D., Pankratz M., Hansen L.O., Pearce R.A., Zhang S.C. Specification of motoneurons from human embryonic stem cells. Nat. Biotechnol. 2005, 23:215-221.
46. Lie D.C., Colamarino S.A., Song H.J., Désiré L., Mira H., Consiglio A., Lein E.S., Jessberger S., Lansford H., Dearie A.R., Gage F.H. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005, 437:1370-1375.
47. Lin G., Goldman J.E. An FGF-responsive astrocyte precursor isolated from the neonatal forebrain. Glia 2009, 57:592-603.
48. McCarthy K.D., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J.Cell Biol. 1980, 85:890-902.
49. Meeuwsen S., Persoon-Deen C., Bsibsi M., Ravid R., van Noort J.M. Cytokine, chemokine and growth factor gene profiling of cultured human astrocytes after exposure to proinflammatory stimuli. Glia 2003, 43:243-253.
50. Mitani A., Tanaka K. Functional changes of glial glutamate transporter GLT-1 during ischemia: an invivo study in the hippocampal CA1 of normal mice and mutant mice lacking GLT-1. J.Neurosci. 2003, 23:7176-7182.
51. Morrow T., Song M.R., Ghosh A. Sequential specification of neurons and glia by developmentally regulated extracellular factors. Development 2001, 128:3585-3594.
52. Murayama S., Inoue K., Kawakami H., Bouldin T.W., Suzuki K. A unique pattern of astrocytosis in the primary motor area in amyotrophic lateral sclerosis. Acta Neuropathol. 1991, 82:456-461.
53. Nagai M., Re D.B., Nagata T., Chalazonitis A., Jessell T.M., Wichterle H., Przedborski S. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci. 2007, 10:615-622.
54. Okamoto M., Inoue K., Iwamura H., Terashima K., Soya H., Asashima M., Kuwabara T. Reduction in paracrine Wnt3 factors during aging causes impaired adult neurogenesis. FASEB J. 2011, 25:3570-3582.
55. Ornitz D.M., Xu J., Colvin J.S., McEwen D.G., MacArthur C.A., Coulier F., Gao G., Goldfarb M. Receptor specificity of the fibroblast growth factor family. J.Biol. Chem. 1996, 271:15292-15297.
56. Panatier A., Vallée J., Haber M., Murai K.K., Lacaille J.C., Robitaille R. Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 2011, 146:785-798.
57. Pringle N.P., Yu W.P., Howell M., Colvin J.S., Ornitz D.M., Richardson W.D. Fgfr3 expression by astrocytes and their precursors: evidence that astrocytes and oligodendrocytes originate in distinct neuroepithelial domains. Development 2003, 130:93-102.
58. Reilly J.F., Maher P.A., Kumari V.G. Regulation of astrocyte GFAP expression by TGF-beta1 and FGF-2. Glia 1998, 22:202-210.
59. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., Kuncl R.W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 1995, 38:73-84.
60. Rothstein J.D., Dykes-Hoberg M., Pardo C.A., Bristol L.A., Jin L., Kuncl R.W., Kanai Y., Hediger M.A., Wang Y., Schielke J.P., Welty D.F. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996, 16:675-686.
61. Schiffer D., Cordera S., Cavalla P., Migheli A. Reactive astrogliosis of the spinal cord in amyotrophic lateral sclerosis. J.Neurol. Sci. 1996, 139(Suppl):27-33.
62. Serio A., Bilican B., Barmada S.J., Ando D.M., Zhao C., Siller R., Burr K., Haghi G., Story D., Nishimura A.L., et al. 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 2013, 110:4697-4702.
63. Shaltouki A., Peng J., Liu Q., Rao M.S., Zeng X. Efficient generation of astrocytes from human pluripotent stem cells in defined conditions. Stem Cells 2013, 31:941-952.
64. Sofroniew M.V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009, 32:638-647.
65. Sokolova E., Aleshin S., Reiser G. Expression of protease-activated receptor (PAR)-2, but not other PARs, is regulated by inflammatory cytokines in rat astrocytes. Neurochem. Int. 2012, 60:276-285.
66. Takano T., Tian G.F., Peng W., Lou N., Libionka W., Han X., Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci. 2006, 9:260-267.
67. Theodoric N., Bechberger J.F., Naus C.C., Sin W.C. Role of gap junction protein connexin43 in astrogliosis induced by brain injury. PLoS ONE 2012, 7:e47311.
68. Tom V.J., Doller C.M., Malouf A.T., Silver J. Astrocyte-associated fibronectin is critical for axonal regeneration in adult white matter. J.Neurosci. 2004, 24:9282-9290.
69. Van Wagoner N.J., Oh J.W., Repovic P., Benveniste E.N. Interleukin-6 (IL-6) production by astrocytes: autocrine regulation by IL-6 and the soluble IL-6 receptor. J.Neurosci. 1999, 19:5236-5244.
70. Verwer R.W., Sluiter A.A., Balesar R.A., Baayen J.C., Noske D.P., Dirven C.M., Wouda J., van Dam A.M., Lucassen P.J., Swaab D.F. Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 2007, 130:3321-3335.
71. Voutsinos-Porche B., Bonvento G., Tanaka K., Steiner P., Welker E., Chatton J.Y., Magistretti P.J., Pellerin L. Glial glutamate transporters mediate a functional metabolic crosstalk between neurons and astrocytes in the mouse developing cortex. Neuron 2003, 37:275-286.
72. Voutsinos-Porche B., Knott G., Tanaka K., Quairiaux C., Welker E., Bonvento G. Glial glutamate transporters and maturation of the mouse somatosensory cortex. Cereb. Cortex 2003, 13:1110-1121.
73. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.
74. Yamanaka K., Chun S.J., Boillee S., Fujimori-Tonou N., Yamashita H., Gutmann D.H., Takahashi R., Misawa H., Cleveland D.W. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci. 2008, 11:251-253.
75. Yang Y., Vidensky S., Jin L., Jie C., Lorenzini I., Frankl M., Rothstein J.D. Molecular comparison of GLT1+ and ALDH1L1+ astrocytes invivo in astroglial reporter mice. Glia 2011, 59:200-207.
76. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., Hong D.W., McManus P.M., Katagiri T., Sachidanandan C., et al. BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 2008, 14:1363-1369.
77. Zamanian J.L., Xu L., Foo L.C., Nouri N., Zhou L., Giffard R.G., Barres B.A. Genomic analysis of reactive astrogliosis. J.Neurosci. 2012, 32:6391-6410.