Small-Molecule-Based Lineage Reprogramming Creates Functional Astrocytes

Cell Reports

Volumn 16, Issue 3, 2016, Pages 781-792

  Tian, E ^a   Sun, Guoqiang ^a   Sun, Guihua ^b   Chao, Jianfei ^a   Ye, Peng ^a   Warden, Charles ^a   Riggs, Arthur D ^b   Shi, Yanhong ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b Diabetes and Metabolism Research Institute   (United States)

Author keywords

Alexander disease; chemical reprogramming; direct conversion; induced astrocytes; small molecules

Indexed keywords

6 [[2 [[4 (2,4 DICHLOROPHENYL) 5 (4 METHYL 1H IMIDAZOL 2 YL) 2 PYRIMIDINYL]AMINO]ETHYL]AMINO]NICOTINONITRILE; ENZYME INHIBITOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; OCTAMER TRANSCRIPTION FACTOR 4; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1 KINASE INHIBITOR; TRANYLCYPROMINE; UNCLASSIFIED DRUG;

ALEXANDER DISEASE; ARTICLE; ASTROCYTE; CALCIUM SIGNALING; CELL LINEAGE; CELL MATURATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DOSE RESPONSE; EPIGENETICS; FIBROBLAST; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ASSOCIATION; GFAP GENE; HUMAN; IN VIVO STUDY; MOLECULAR LIBRARY; MUTATIONAL ANALYSIS; NERVE CELL; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR REPROGRAMMING; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SMALL MOLECULE; TRANSGENE; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; COCULTURE; METABOLISM; MOUSE; MUTATION; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PHYSIOLOGY; PROCEDURES; PROTEINOSIS; STEM CELL; TRANSGENIC MOUSE;

ALEXANDER DISEASE; ANIMALS; ASTROCYTES; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELLS, CULTURED; CELLULAR REPROGRAMMING; COCULTURE TECHNIQUES; EPIGENOMICS; FIBROBLASTS; GENE EXPRESSION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; HUMANS; MICE; MICE, TRANSGENIC; MUTATION; NEUROGENESIS; NEURONS; PROTEIN AGGREGATION, PATHOLOGICAL; STEM CELLS;

EID: 84989912774     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.042     Document Type: Article

References (55)

1. Bachetti, T., Caroli, F., Bocca, P., Prigione, I., Balbi, P., Biancheri, R., Filocamo, M., Mariotti, C., Pareyson, D., Ravazzolo, R., Ceccherini, I., Mild functional effects of a novel GFAP mutant allele identified in a familial case of adult-onset Alexander disease. Eur. J. Hum. Genet. 16 (2008), 462–470.
2. Bachetti, T., Di Zanni, E., Balbi, P., Bocca, P., Prigione, I., Deiana, G.A., Rezzani, A., Ceccherini, I., Sechi, G., In vitro treatments with ceftriaxone promote elimination of mutant glial fibrillary acidic protein and transcription down-regulation. Exp. Cell Res. 316 (2010), 2152–2165.
3. Banker, G.A., Trophic interactions between astroglial cells and hippocampal neurons in culture. Science 209 (1980), 809–810.
4. Barres, B.A., The mystery and magic of glia: a perspective on their roles in health and disease. Neuron 60 (2008), 430–440.
5. Bonaguidi, M.A., McGuire, T., Hu, M., Kan, L., Samanta, J., Kessler, J.A., LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132 (2005), 5503–5514.
6. Caiazzo, M., Dell'Anno, M.T., Dvoretskova, E., Lazarevic, D., Taverna, S., Leo, D., Sotnikova, T.D., Menegon, A., Roncaglia, P., Colciago, G., et al. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476 (2011), 224–227.
7. Caiazzo, M., Giannelli, S., Valente, P., Lignani, G., Carissimo, A., Sessa, A., Colasante, G., Bartolomeo, R., Massimino, L., Ferroni, S., et al. Direct conversion of fibroblasts into functional astrocytes by defined transcription factors. Stem Cell Reports 4 (2015), 25–36.
8. Cassady, J.P., D'Alessio, A.C., Sarkar, S., Dani, V.S., Fan, Z.P., Ganz, K., Roessler, R., Sur, M., Young, R.A., Jaenisch, R., Direct lineage conversion of adult mouse liver cells and B lymphocytes to neural stem cells. Stem Cell Reports 3 (2014), 948–956.
9. Chaudhry, F.A., Lehre, K.P., van Lookeren Campagne, M., Ottersen, O.P., Danbolt, N.C., Storm-Mathisen, J., Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 15 (1995), 711–720.
10. Cheng, L., Hu, W., Qiu, B., Zhao, J., Yu, Y., Guan, W., Wang, M., Yang, W., Pei, G., Generation of neural progenitor cells by chemical cocktails and hypoxia. Cell Res. 24 (2014), 665–679.
11. Davis, R.L., Weintraub, H., Lassar, A.B., Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51 (1987), 987–1000.
12. Eroglu, C., Barres, B.A., Regulation of synaptic connectivity by glia. Nature 468 (2010), 223–231.
13. Gellibert, F., Woolven, J., Fouchet, M.H., Mathews, N., Goodland, H., Lovegrove, V., Laroze, A., Nguyen, V.L., Sautet, S., Wang, R., et al. Identification of 1,5-naphthyridine derivatives as a novel series of potent and selective TGF-beta type I receptor inhibitors. J. Med. Chem. 47 (2004), 4494–4506.
14. Gross, R.E., Mehler, M.F., Mabie, P.C., Zang, Z., Santschi, L., Kessler, J.A., Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17 (1996), 595–606.
15. Hagemann, T.L., Connor, J.X., Messing, A., Alexander disease-associated glial fibrillary acidic protein mutations in mice induce Rosenthal fiber formation and a white matter stress response. J. Neurosci. 26 (2006), 11162–11173.
16. Hama, H., Hara, C., Yamaguchi, K., Miyawaki, A., PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 41 (2004), 405–415.
17. Han, D.W., Tapia, N., Hermann, A., Hemmer, K., Höing, S., Araúzo-Bravo, M.J., Zaehres, H., Wu, G., Frank, S., Moritz, S., et al. Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 10 (2012), 465–472.
18. Hatada, I., Namihira, M., Morita, S., Kimura, M., Horii, T., Nakashima, K., Astrocyte-specific genes are generally demethylated in neural precursor cells prior to astrocytic differentiation. PLoS ONE, 3, 2008, e3189.
19. Hawley, R.G., Does retroviral insertional mutagenesis play a role in the generation of induced pluripotent stem cells?. Mol. Ther. 16 (2008), 1354–1355.
20. Hou, P., Li, Y., Zhang, X., Liu, C., Guan, J., Li, H., Zhao, T., Ye, J., Yang, W., Liu, K., et al. Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341 (2013), 651–654.
21. Hu, W., Qiu, B., Guan, W., Wang, Q., Wang, M., Li, W., Gao, L., Shen, L., Huang, Y., Xie, G., et al. Direct conversion of normal and Alzheimer's disease human fibroblasts into neuronal cells by small molecules. Cell Stem Cell 17 (2015), 204–212.
22. Ichida, J.K., Blanchard, J., Lam, K., Son, E.Y., Chung, J.E., Egli, D., Loh, K.M., Carter, A.C., Di Giorgio, F.P., Koszka, K., et al. A small-molecule inhibitor of tgf-Beta signaling replaces sox2 in reprogramming by inducing nanog. Cell Stem Cell 5 (2009), 491–503.
23. Inman, G.J., Nicolás, F.J., Callahan, J.F., Harling, J.D., Gaster, L.M., Reith, A.D., Laping, N.J., Hill, C.S., SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62 (2002), 65–74.
24. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U., Speed, T.P., Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 (2003), 249–264.
25. Kim, J., Efe, J.A., Zhu, S., Talantova, M., Yuan, X., Wang, S., Lipton, S.A., Zhang, K., Ding, S., Direct reprogramming of mouse fibroblasts to neural progenitors. Proc. Natl. Acad. Sci. USA 108 (2011), 7838–7843.
26. Kohyama, J., Sanosaka, T., Tokunaga, A., Takatsuka, E., Tsujimura, K., Okano, H., Nakashima, K., BMP-induced REST regulates the establishment and maintenance of astrocytic identity. J. Cell Biol. 189 (2010), 159–170.
27. Li, W., Tian, E., Chen, Z.X., Sun, G., Ye, P., Yang, S., Lu, D., Xie, J., Ho, T.V., Tsark, W.M., et al. Identification of Oct4-activating compounds that enhance reprogramming efficiency. Proc. Natl. Acad. Sci. USA 109 (2012), 20853–20858.
28. Li, X., Zuo, X., Jing, J., Ma, Y., Wang, J., Liu, D., Zhu, J., Du, X., Xiong, L., Du, Y., et al. Small-molecule-driven direct reprogramming of mouse fibroblasts into functional neurons. Cell Stem Cell 17 (2015), 195–203.
29. Lin, T., Ambasudhan, R., Yuan, X., Li, W., Hilcove, S., Abujarour, R., Lin, X., Hahm, H.S., Hao, E., Hayek, A., Ding, S., A chemical platform for improved induction of human iPSCs. Nat. Methods 6 (2009), 805–808.
30. Lujan, E., Chanda, S., Ahlenius, H., Südhof, T.C., Wernig, M., Direct conversion of mouse fibroblasts to self-renewing, tripotent neural precursor cells. Proc. Natl. Acad. Sci. USA 109 (2012), 2527–2532.
31. Maherali, N., Hochedlinger, K., Tgfbeta signal inhibition cooperates in the induction of iPSCs and replaces Sox2 and cMyc. Curr. Biol. 19 (2009), 1718–1723.
32. Messing, A., Brenner, M., Feany, M.B., Nedergaard, M., Goldman, J.E., Alexander disease. J. Neurosci. 32 (2012), 5017–5023.
33. Molofsky, A.V., Krencik, R., Ullian, E.M., 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.
34. Najm, F.J., Lager, A.M., Zaremba, A., Wyatt, K., Caprariello, A.V., Factor, D.C., Karl, R.T., Maeda, T., Miller, R.H., Tesar, P.J., Transcription factor-mediated reprogramming of fibroblasts to expandable, myelinogenic oligodendrocyte progenitor cells. Nat. Biotechnol. 31 (2013), 426–433.
35. Okita, K., Nakagawa, M., Hyenjong, H., Ichisaka, T., Yamanaka, S., Generation of mouse induced pluripotent stem cells without viral vectors. Science 322 (2008), 949–953.
36. Pang, Z.P., Yang, N., Vierbuchen, T., Ostermeier, A., Fuentes, D.R., Yang, T.Q., Citri, A., Sebastiano, V., Marro, S., Südhof, T.C., Wernig, M., Induction of human neuronal cells by defined transcription factors. Nature 476 (2011), 220–223.
37. Rajan, P., McKay, R.D., Multiple routes to astrocytic differentiation in the CNS. J. Neurosci. 18 (1998), 3620–3629.
38. Ring, K.L., Tong, L.M., Balestra, M.E., Javier, R., Andrews-Zwilling, Y., Li, G., Walker, D., Zhang, W.R., Kreitzer, A.C., Huang, Y., Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 11 (2012), 100–109.
39. Schildge, S., Bohrer, C., Beck, K., Schachtrup, C., Isolation and culture of mouse cortical astrocytes. J. Vis. Exp., 2013 pii: 50079.
40. Simard, M., Nedergaard, M., The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129 (2004), 877–896.
41. Smith, J.R., Vallier, L., Lupo, G., Alexander, M., Harris, W.A., Pedersen, R.A., Inhibition of Activin/Nodal signaling promotes specification of human embryonic stem cells into neuroectoderm. Dev. Biol. 313 (2008), 107–117.
42. Sofroniew, M.V., Vinters, H.V., Astrocytes: biology and pathology. Acta Neuropathol. 119 (2010), 7–35.
43. Song, H., Stevens, C.F., Gage, F.H., Astroglia induce neurogenesis from adult neural stem cells. Nature 417 (2002), 39–44.
44. Szabó, P.E., Hübner, K., Schöler, H., Mann, J.R., Allele-specific expression of imprinted genes in mouse migratory primordial germ cells. Mech. Dev. 115 (2002), 157–160.
45. Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126 (2006), 663–676.
46. Thier, M., Wörsdörfer, P., Lakes, Y.B., Gorris, R., Herms, S., Opitz, T., Seiferling, D., Quandel, T., Hoffmann, P., Nöthen, M.M., et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 10 (2012), 473–479.
47. Tojo, M., Hamashima, Y., Hanyu, A., Kajimoto, T., Saitoh, M., Miyazono, K., Node, M., Imamura, T., The ALK-5 inhibitor A-83-01 inhibits Smad signaling and epithelial-to-mesenchymal transition by transforming growth factor-beta. Cancer Sci. 96 (2005), 791–800.
48. Verkhratsky, A., Sofroniew, M.V., Messing, A., deLanerolle, N.C., Rempe, D., Rodríguez, J.J., Nedergaard, M., Neurological diseases as primary gliopathies: a reassessment of neurocentrism. ASN Neuro, 4, 2012, e00082.
49. Vierbuchen, T., Ostermeier, A., Pang, Z.P., Kokubu, Y., Südhof, T.C., Wernig, M., Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463 (2010), 1035–1041.
50. Wang, D.D., Bordey, A., The astrocyte odyssey. Prog. Neurobiol. 86 (2008), 342–367.
51. Xu, R.H., Sampsell-Barron, T.L., Gu, F., Root, S., Peck, R.M., Pan, G., Yu, J., Antosiewicz-Bourget, J., Tian, S., Stewart, R., Thomson, J.A., NANOG is a direct target of TGFbeta/activin-mediated SMAD signaling in human ESCs. Cell Stem Cell 3 (2008), 196–206.
52. Yang, N., Zuchero, J.B., Ahlenius, H., Marro, S., Ng, Y.H., Vierbuchen, T., Hawkins, J.S., Geissler, R., Barres, B.A., Wernig, M., Generation of oligodendroglial cells by direct lineage conversion. Nat. Biotechnol. 31 (2013), 434–439.
53. Yoo, A.S., Sun, A.X., Li, L., Shcheglovitov, A., Portmann, T., Li, Y., Lee-Messer, C., Dolmetsch, R.E., Tsien, R.W., Crabtree, G.R., MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476 (2011), 228–231.
54. Zhang, L., Yin, J.C., Yeh, H., Ma, N.X., Lee, G., Chen, X.A., Wang, Y., Lin, L., Chen, L., Jin, P., et al. Small molecules efficiently reprogram human astroglial cells into functional neurons. Cell Stem Cell 17 (2015), 735–747.
55. Zhuo, L., Sun, B., Zhang, C.L., Fine, A., Chiu, S.Y., Messing, A., Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev. Biol. 187 (1997), 36–42.