Differentiation of Inflammation-Responsive Astrocytes from Glial Progenitors Generated from Human Induced Pluripotent Stem Cells

Stem Cell Reports

Volumn 8, Issue 6, 2017, Pages 1757-1769

  Santos, Renata ^a,b   Vadodaria, Krishna C ^a   Jaeger, Baptiste N ^a   Mei, Arianna ^a   Lefcochilos Fogelquist, Sabrina ^a   Mendes, Ana P D ^a   Erikson, Galina ^a   Shokhirev, Maxim ^a   Randolph Moore, Lynne ^a   Fredlender, Callie ^a   Dave, Sonia ^a   Oefner, Ruth ^a   Fitzpatrick, Conor ^a   Pena, Monique ^a   Barron, Jerika J ^a   Ku, Manching ^a   Denli, Ahmet M ^a   Kerman, Bilal E ^a,e   Charnay, Patrick ^b   Kelsoe, John R ^c,d   Marchetto, Maria C ^a   Gage, Fred H ^a   more..

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b PSL RESEARCH UNIVERSITY   (France)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e ISTANBUL MEDIPOL UNIVERSITY   (Turkey)

Author keywords

astrocytes; co culture; disease modeling; iPSCs; neurodegenerative disorders; neuroinflammation; neuropsychiatric disorders; stem cell

Indexed keywords

CALCIUM; GLUTAMIC ACID; INTERLEUKIN 1BETA; TRANSCRIPTOME; TUMOR NECROSIS FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; HYALURONIC ACID BINDING PROTEIN; LEUKEMIA INHIBITORY FACTOR; RNA;

ARTICLE; ASTROCYTE; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; INDUCED PLURIPOTENT STEM CELL; NERVE CELL DIFFERENTIATION; NERVE CELL STIMULATION; PRIORITY JOURNAL; RNA SEQUENCE; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; COCULTURE; CYTOLOGY; DRUG EFFECTS; EMBRYONIC STEM CELL; FLUORESCENCE MICROSCOPY; ISOLATION AND PURIFICATION; METABOLISM; NERVE CELL; PRINCIPAL COMPONENT ANALYSIS; SEQUENCE ANALYSIS; STEM CELL;

ASTROCYTES; CALCIUM; CELL DIFFERENTIATION; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; HUMANS; HYALURONAN RECEPTORS; INDUCED PLURIPOTENT STEM CELLS; INTERLEUKIN-1BETA; LEUKEMIA INHIBITORY FACTOR; MICROSCOPY, FLUORESCENCE; NEURONS; PRINCIPAL COMPONENT ANALYSIS; RNA; SEQUENCE ANALYSIS, RNA; STEM CELLS; TRANSCRIPTOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85020281023     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2017.05.011     Document Type: Article

References (57)

1. Anderson, M.A., Ao, Y., Sofroniew, M.V., Heterogeneity of reactive astrocytes. Neurosci. Lett. 565 (2014), 23–29.
2. Bazargani, N., Attwell, D., Astrocyte calcium signaling: the third wave. Nat. Neurosci. 19 (2016), 182–189.
3. 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 278 (1997), 477–483.
4. Campbell, A., Inflammation, neurodegenerative diseases, and environmental exposures. Ann. N.Y. Acad. Sci. 1035 (2004), 117–132.
5. Cavanaugh, S.E., Animal models of Alzheimer disease: historical pitfalls and a path forward. ALTEX 31 (2014), 279–302.
6. 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. 27 (2009), 275–280.
7. Chandrasekaran, A., Avci, H.X., Leist, M., Kobolák, J., Dinnyés, A., Astrocyte differentiation of human pluripotent stem cells: new tools for neurological disorder research. Front. Cell. Neurosci., 10, 2016, 215.
8. Chen, C., Jiang, P., Xue, H., Peterson, S.E., Tran, H.T., McCann, A.E., Parast, M.M., Li, S., Pleasure, D.E., Laurent, L.C., et al. Role of astroglia in Down's syndrome revealed by patient-derived human-induced pluripotent stem cells. Nat. Commun. 5 (2014), 1–18.
9. Colombo, E., Farina, C., Astrocytes: key regulators of neuroinflammation. Trends Immunol. 37 (2016), 608–620.
10. Cummings, J.L., Morstorf, T., Zhong, K., Alzheimer's disease drug-development pipeline: few candidates, frequent failures. Alzheimers Res. Ther., 6, 2014, 37.
11. Dell'Albani, P., Kahn, M.A., Cole, R., Condorelli, D.F., Giuffrida Stella, A.M., de Vellis, J., Oligodendroglial survival factors, PDGF-AA and CNTF, activate similar JAK/STAT signaling pathways. J. Neurosci. Res. 54 (1998), 191–205.
12. Deneen, B., Ho, R., Lukaszewicz, A., Hochstim, C.J., Gronostajski, R.M., Anderson, D.J., The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52 (2006), 953–968.
13. DiSabato, D.J., Quan, N., Godbout, J.P., Neuroinflammation: the devil is in the details. J. Neurochem. 139 (2016), 136–153.
14. 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. 21 (2012), 404–410.
15. Ennas, M.G., Cocchia, D., Silvetti, E., Sogos, V., Riva, A., Torelli, S., Gremo, F., Immunocompetent cell markers in human fetal astrocytes and neurons in culture. J. Neurosci. Res. 32 (1992), 424–436.
16. Fan, G., DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling. Development 132 (2005), 3345–3356.
17. Foo, L.C., Allen, N.J., Bushong, E.A., Ventura, P.B., Chung, W.S., Zhou, L., Cahoy, J.D., Daneman, R., Zong, H., Ellisman, M.H., Barres, B.A., Development of a method for the purification and culture of rodent astrocytes. Neuron 71 (2011), 799–811.
18. Han, X., Chen, M., Wang, F., Windrem, M., Wang, S., Shanz, S., Xu, Q., Oberheim, N.A., Bekar, L., Betstadt, S., et al. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Stem Cell 12 (2013), 342–353.
19. He, F., Ge, W., Martinowich, K., Becker-Catania, S., Coskun, V., Zhu, W., Wu, H., Castro, D., Guillemot, F., Fan, G., et al. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat. Neurosci. 8 (2005), 616–625.
20. Hochstim, C., Deneen, B., Lukaszewicz, A., Zhou, Q., Anderson, D.J., Identification of positionally distinct astrocyte subtypes whose identities are specified by a homeodomain code. Cell 133 (2008), 510–522.
21. Holmqvist, S., Brouwer, M., Djelloul, M., Diaz, A.G., Devine, M.J., Hammarberg, A., Fog, K., Kunath, T., Roybon, L., Generation of pluripotent stem cell reporter lines for the isolation of and reporting on astrocytes generated from ventral midbrain and ventral spinal cord neural progenitors. Stem Cell Res. 15 (2015), 203–220.
22. Jung, T., Schauer, U., Heusser, C., Neumann, C., Rieger, C., Detection of intracellular cytokines by flow cytometry. J. Immunol. Methods 159 (1993), 197–207.
23. 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. 6 (2004), 547–554.
24. Khakh, B.S., Sofroniew, M.V., Diversity of astrocyte functions and phenotypes in neural circuits. Nat. Neurosci. 18 (2015), 942–952.
25. Kim, K., Lee, S.G., Kegelman, T.P., Su, Z.Z., Das, S.K., Dash, R., Dasgupta, S., Barral, P.M., Hedvat, M., Diaz, P., et al. Role of excitatory amino acid transporter-2 (EAAT2) and glutamate in neurodegeneration: opportunities for developing novel therapeutics. J. Cell. Physiol. 226 (2011), 2484–2493.
26. Krencik, R., Zhang, S.C., Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat. Protoc. 6 (2011), 1710–1717.
27. Krencik, R., Hokanson, K.C., Narayan, A.R., Dvornik, J., Rooney, G.E., Rauen, K.A., Weiss, L.A., Rowitch, D.H., Ullian, E.M., Dysregulation of astrocyte extracellular signaling in Costello syndrome. Sci. Transl. Med., 7, 2015, 286ra66.
28. 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-1β. J. Immunol. 150 (1993), 2659–2667.
29. Marchetto, M.C.N., Carromeu, C., Acab, A., Yu, D., Yeo, G.W., Mu, Y., Chen, G., Gage, F.H., Muotri, A.R., A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143 (2010), 527–539.
30. McCarthy, K.D., de Vellis, J., Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85 (1980), 890–902.
31. Mertens, J., Wang, Q.W., Kim, Y., Yu, D.X., Pham, S., Yang, B., Zheng, Y., Diffenderfer, K.E., Zhang, J., Soltani, S., et al. Differential responses to lithium in hyperexcitable neurons from patients with bipolar disorder. Nature 527 (2015), 95–99.
32. Molofsky, A.V., Krenick, R., Ullian, E., Tsai, H.H., Deneen, B., Richardson, W.D., Barres, B.A., Rowitch, D.H., Astrocytes and disease: a neurodevelopmental perspective. Genes Dev. 26 (2012), 891–907.
33. Morrison, S.J., Perez, S.E., Qiao, Z., Verdi, J.M., Hicks, C., Weinmaster, G., Anderson, D.J., Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101 (2000), 499–510.
34. Oberheim, N.A., Wang, X., Goldman, S., Nedergaard, M., Astrocytic complexity distinguishes the human brain. Trends Neurosci. 29 (2006), 547–553.
35. Oberheim, N.A., Takano, T., Han, X., He, W., Lin, J.H.C., Wang, F., Xu, Q., Wyatt, J.D., Pilcher, W., Ojemann, J.G., et al. Uniquely hominid features of adult human astrocytes. J. Neurosci. 29 (2009), 3276–3287.
36. Pekny, M., Pekna, M., Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol. Rev. 94 (2014), 1077–1098.
37. Pekny, M., Pekna, M., Messing, A., Steinhäuser, C., Lee, J.M., Parpura, V., Hol, E.M., Sofroniew, M.V., Verkhratsky, A., Astrocytes: a central element in neurological diseases. Acta Neuropathol. 131 (2015), 323–345.
38. Picker, L.J., Singh, M.K., Zdraveski, Z., Treer, J.R., Waldrop, S.L., Bergstresser, P.R., Maino, V.C., Direct demonstration of cytokine synthesis heterogeneity among human memory/effector T cells by flow cytometry. Blood 86 (1995), 1408–1419.
39. Robinson, M.B., Jackson, J.G., Astroglial glutamate transporters coordinate excitatory signaling and brain energetics. Neurochem. Int. 98 (2016), 56–71.
40. Rothstein, J.D., Of mice and men: reconciling preclinical ALS mouse studies and human clinical trials. Ann. Neurol. 53 (2003), 423–426.
41. Roybon, L., Lamas, N.J., Garcia-Diaz, A., Yang, E.J., Sattler, R., Jackson-Lewis, V., Kim, Y.A., Kachel, C.A., Rothstein, J.D., Przedborski, S., et al. Human stem cell-derived spinal cord astrocytes with defined mature or reactive phenotypes. Cell Rep. 4 (2013), 1035–1048.
42. Rusakov, D.A., Disentangling calcium-driven astrocyte physiology. Nat. Rev. Neurosci. 16 (2015), 226–233.
43. 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 110 (2013), 4697–4702.
44. 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 31 (2013), 941–952.
45. Shigetomi, E., Patel, S., Khakh, B.S., Probing the complexities of astrocyte calcium signaling. Trends Cell Biol. 26 (2016), 300–312.
46. Sofroniew, M.V., Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32 (2009), 638–647.
47. Sofroniew, M.V., Astrocyte barriers to neurotoxic inflammation. Nat. Rev. Neurosci. 16 (2015), 249–263.
48. Sofroniew, M.V., Vinters, H.V., Astrocytes: biology and pathology. Acta Neuropathol. 119 (2010), 7–35.
49. Stout, C.E., Costantin, J.L., Naus, C.C.G., Charles, A.C., Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J. Biol. Chem. 277 (2002), 10482–10488.
50. Takizawa, T., Nakashima, K., Namihira, M., Ochiai, W., Uemura, A., Yanagisawa, M., Fujita, N., Nakao, M., Taga, T., DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell 1 (2001), 749–758.
51. Tian, E., Sun, G., Sun, G., Chao, J., Ye, P., Warden, C., Riggs, A.D., Shi, Y., Small-molecule-based lineage reprogramming creates functional astrocytes. Cell Rep. 16 (2016), 781–792.
52. Tsai, H.H., Li, H., Fuentealba, L.C., Molofsky, A.V., Taveira-Marques, R., Zhuang, H., Tenney, A., Murnen, A.T., Fancy, S.P.J., Merkle, F., et al. Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337 (2012), 358–362.
53. Tyzack, G., Lakatos, A., Patani, R., Human stem cell-derived astrocytes: specification and relevance for neurological disorders. Curr. Stem Cell Rep. 2 (2016), 236–247.
54. Waldmeier, P., Bozyczko-Coyne, D., Williams, M., Vaught, J.L., Recent clinical failures in Parkinson's disease with apoptosis inhibitors underline the need for a paradigm shift in drug discovery for neurodegenerative diseases. Biochem. Pharmacol. 72 (2006), 1197–1206.
55. Yu, D.X., Di Giorgio, F.P., Yao, J., Marchetto, M.C., Brennand, K., Wright, R., Mei, A., McHenry, L., Lisuk, D., Grasmick, J.M., et al. Modeling hippocampal neurogenesis using human pluripotent stem cells. Stem Cell Reports 2 (2014), 295–310.
56. 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. 32 (2012), 6391–6410.
57. Zhang, Y., Sloan, S.A., Clarke, L.E., Caneda, C., Plaza, C.A., Blumenthal, P.D., Vogel, H., Steinberg, G.K., Edwards, M.S.B., Li, G., et al. Purification and characterization of progenitor and mature human astrocytes reveals transcriptional and functional differences with mouse. Neuron 89 (2016), 37–53.