Global Transcriptome Profiling of Genes that Are Differentially Regulated During Differentiation of Mouse Embryonic Neural Stem Cells into Astrocytes

Journal of Molecular Neuroscience

Volumn 55, Issue 1, 2015, Pages 109-125

  Han, Dalmuri ^a   Choi, Mi Ran ^a   Jung, Kyoung Hwa ^a   Kim, Namshin ^c   Kim, Se kye ^a   Chai, Jin Choul ^a   Lee, Young Seek ^a   Chai, Young Gyu ^a,b  

^a Hanyang University   (South Korea)

^b Hanyang University   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Astrocytes; Cell differentiation; Neural stem cells; TGF beta; WNTs

Indexed keywords

TRANSCRIPTOME;

ANIMAL; ASTROCYTE; CELL CULTURE; CYTOLOGY; EMBRYONIC STEM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; METABOLISM; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; WNT SIGNALING PATHWAY;

ANIMALS; ASTROCYTES; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; NEURAL STEM CELLS; NEUROGENESIS; TRANSCRIPTOME; WNT SIGNALING PATHWAY;

EID: 84925197133     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-014-0382-8     Document Type: Article

References (59)

1. Anderson JT (2005) RNA turnover: unexpected consequences of being tailed. Curr Biol CB 15(16):R635–R638. doi:10.1016/j.cub.2005.08.002
2. Andersson ER, Salto C, Villaescusa JC, Cajanek L, Yang S, Bryjova L, Nagy II, Vainio SJ, Ramirez C, Bryja V, Arenas E (2013) Wnt5a cooperates with canonical Wnts to generate midbrain dopaminergic neurons in vivo and in stem cells. Proc Natl Acad Sci U S A 110(7):E602–E610. doi:10.1073/pnas.1208524110
3. Andres-Barquin PJ, Hernandez MC, Israel MA (1998) Injury selectively down-regulates the gene encoding for the Id4 transcription factor in primary cultures of forebrain astrocytes. Neuroreport 9(18):4075–4080
4. Angelastro JM, Mason JL, Ignatova TN, Kukekov VG, Stengren GB, Goldman JE, Greene LA (2005) Downregulation of activating transcription factor 5 is required for differentiation of neural progenitor cells into astrocytes. J Neurosci Off J Soc Neurosci 25(15):3889–3899. doi:10.1523/jneurosci.3447-04.2005
5. Beckervordersandforth R, Tripathi P, Ninkovic J, Bayam E, Lepier A, Stempfhuber B, Kirchhoff F, Hirrlinger J, Haslinger A, Lie DC, Beckers J, Yoder B, Irmler M, Gotz M (2010) In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7(6):744–758. doi:10.1016/j.stem.2010.11.017
6. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2):315–326. doi:10.1016/j.cell.2006.02.041
7. Beutner C, Linnartz-Gerlach B, Schmidt SV, Beyer M, Mallmann MR, Staratschek-Jox A, Schultze JL, Neumann H (2013) Unique transcriptome signature of mouse microglia. Glia 61(9):1429–1442. doi:10.1002/glia.22524
8. Brun M, Coles JE, Monckton EA, Glubrecht DD, Bisgrove D, Godbout R (2009) Nuclear factor I regulates brain fatty acid-binding protein and glial fibrillary acidic protein gene expression in malignant glioma cell lines. J Mol Biol 391(2):282–300. doi:10.1016/j.jmb.2009.06.041
9. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci Off J Soc Neurosci 28(1):264–278. doi:10.1523/JNEUROSCI.4178-07.2008
10. Chen H, Wang S, Chen L, Chen Y, Wu M, Zhang Y, Yu K, Huang Z, Qin L, Mo D (2013) MicroRNA-344 inhibits 3T3-L1 cell differentiation via targeting GSK3beta of Wnt/beta-catenin signaling pathway. FEBS Lett. doi:10.1016/j.febslet.2013.12.002
11. Choi MR, Jung KH, Park JH, Das ND, Chung MK, Choi IG, Lee BC, Park KS, Chai YG (2011) Ethanol-induced small heat shock protein genes in the differentiation of mouse embryonic neural stem cells. Arch Toxicol 85(4):293–304. doi:10.1007/s00204-010-0591-z
12. da Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44–57. doi:10.1038/nprot.2008.211
13. Davis AA, Temple S (1994) A self-renewing multipotential stem cell in embryonic rat cerebral cortex. Nature 372(6503):263–266. doi:10.1038/372263a0
14. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 4(5):P3
15. Foo LC, Dougherty JD (2013) Aldh1L1 is expressed by postnatal neural stem cells in vivo. Glia 61(9):1533–1541. doi:10.1002/glia.22539
16. Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway–its role in innate immunity and evolution. Immunol Rev 198:185–202
17. Gage FH (2000) Mammalian neural stem cells. Science 287(5457):1433–1438
18. Gamsiz ED, Ouyang Q, Schmidt M, Nagpal S, Morrow EM (2012) Genome-wide transcriptome analysis in murine neural retina using high-throughput RNA sequencing. Genomics 99(1):44–51. doi:10.1016/j.ygeno.2011.09.003
19. Han DM, Choi MR, Jung KH, Lee HT, Park JH, Ohn T, Chai YG (2012) Proteomic analysis of the copper ion-induced stress response in a human embryonic carcinoma cell line. Int J Toxicol 31(4):397–406. doi:10.1177/1091581812446869
20. Hirai S, Miwa A, Ohtaka-Maruyama C, Kasai M, Okabe S, Hata Y, Okado H (2012) RP58 controls neuron and astrocyte differentiation by downregulating the expression of Id1-4 genes in the developing cortex. EMBO J 31(5):1190–1202. doi:10.1038/emboj.2011.486
21. Hsieh FY, Ma TL, Shih HY, Lin SJ, Huang CW, Wang HY, Cheng YC (2013) Dner inhibits neural progenitor proliferation and induces neuronal and glial differentiation in zebrafish. Dev Biol 375(1):1–12. doi:10.1016/j.ydbio.2013.01.007
22. Jovicic A, Roshan R, Moisoi N, Pradervand S, Moser R, Pillai B, Luthi-Carter R (2013) Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J Neurosci Off J Soc Neurosci 33(12):5127–5137. doi:10.1523/jneurosci.0600-12.2013
23. Jungblut M, Tiveron MC, Barral S, Abrahamsen B, Knobel S, Pennartz S, Schmitz J, Perraut M, Pfrieger FW, Stoffel W, Cremer H, Bosio A (2012) Isolation and characterization of living primary astroglial cells using the new GLAST-specific monoclonal antibody ACSA-1. Glia 60(6):894–907. doi:10.1002/glia.22322
24. Kamel G, Hoyos T, Rochard L, Dougherty M, Kong Y, Tse W, Shubinets V, Grimaldi M, Liao EC (2013) Requirement for frzb and fzd7a in cranial neural crest convergence and extension mechanisms during zebrafish palate and jaw morphogenesis. Dev Biol. doi:10.1016/j.ydbio.2013.06.012
25. Kang P, Lee HK, Glasgow SM, Finley M, Donti T, Gaber ZB, Graham BH, Foster AE, Novitch BG, Gronostajski RM, Deneen B (2012) Sox9 and NFIA coordinate a transcriptional regulatory cascade during the initiation of gliogenesis. Neuron 74(1):79–94. doi:10.1016/j.neuron.2012.01.024
26. Katoh M (2006) Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther 5(9):1059–1064
27. Kettenmann H, Ransom BR (1988) Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia 1(1):64–73. doi:10.1002/glia.440010108
28. Krencik R, Weick JP, Liu Y, Zhang ZJ, Zhang SC (2011) Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat Biotechnol 29(6):528–534. doi:10.1038/nbt.1877
29. Laneve P, Gioia U, Andriotto A, Moretti F, Bozzoni I, Caffarelli E (2010) A minicircuitry involving REST and CREB controls miR-9-2 expression during human neuronal differentiation. Nucleic Acids Res 38(20):6895–6905. doi:10.1093/nar/gkq604
30. Lim J, Thiery JP (2012) Epithelial-mesenchymal transitions: insights from development. Development 139(19):3471–3486. doi:10.1242/dev.071209
31. Linhart C, Halperin Y, Shamir R (2008) Transcription factor and microRNA motif discovery: the Amadeus platform and a compendium of metazoan target sets. Genome Res 18(7):1180–1189. doi:10.1101/gr.076117.108
32. Liu HT, Tashmukhamedov BA, Inoue H, Okada Y, Sabirov RZ (2006) Roles of two types of anion channels in glutamate release from mouse astrocytes under ischemic or osmotic stress. Glia 54(5):343–357. doi:10.1002/glia.20400
33. Marei HE, Ahmed AE, Michetti F, Pescatori M, Pallini R, Casalbore P, Cenciarelli C, Elhadidy M (2012) Gene expression profile of adult human olfactory bulb and embryonic neural stem cell suggests distinct signaling pathways and epigenetic control. PLoS One 7(4):e33542. doi:10.1371/journal.pone.0033542
34. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, Lee W, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C, Lander ES, Bernstein BE (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448(7153):553–560. doi:10.1038/nature06008
35. Miyawaki T, Uemura A, Dezawa M, Yu RT, Ide C, Nishikawa S, Honda Y, Tanabe Y, Tanabe T (2004) Tlx, an orphan nuclear receptor, regulates cell numbers and astrocyte development in the developing retina. J Neurosci Off J Soc Neurosci 24(37):8124–8134. doi:10.1523/JNEUROSCI.2235-04.2004
36. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5(7):621–628. doi:10.1038/nmeth.1226
37. Naka H, Nakamura S, Shimazaki T, Okano H (2008) Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat Neurosci 11(9):1014–1023. doi:10.1038/nn.2168
38. Nieto-Estevez V, Pignatelli J, Arauzo-Bravo MJ, Hurtado-Chong A, Vicario-Abejon C (2013) A global transcriptome analysis reveals molecular hallmarks of neural stem cell death, survival, and differentiation in response to partial FGF-2 and EGF deprivation. PLoS One 8(1):e53594. doi:10.1371/journal.pone.0053594
39. Obayashi S, Tabunoki H, Kim SU, Satoh J (2009) Gene expression profiling of human neural progenitor cells following the serum-induced astrocyte differentiation. Cell Mol Neurobiol 29(3):423–438. doi:10.1007/s10571-008-9338-2
40. Park JH, Choi MR, Park KS, Kim SH, Jung KH, Chai YG (2012) The characterization of gene expression during mouse neural stem cell differentiation in vitro. Neurosci Lett 506(1):50–54. doi:10.1016/j.neulet.2011.10.046
41. Pekny M, Nilsson M (2005) Astrocyte activation and reactive gliosis. Glia 50(4):427–434. doi:10.1002/glia.20207
42. Pino D, Choe Y, Pleasure SJ (2011) Wnt5a controls neurite development in olfactory bulb interneurons. ASN Neurol 3(3):e00059. doi:10.1042/an20100038
43. Rowitch DH, Kriegstein AR (2010) Developmental genetics of vertebrate glial-cell specification. Nature 468(7321):214–222. doi:10.1038/nature09611
44. Samanta J, Kessler JA (2004) Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131(17):4131–4142. doi:10.1242/dev.01273
45. Sancho-Martinez I, Baek SH, Izpisua Belmonte JC (2012) Lineage conversion methodologies meet the reprogramming toolbox. Nat Cell Biol 14(9):892–899. doi:10.1038/ncb2567
46. Sanosaka T, Namihira M, Asano H, Kohyama J, Aisaki K, Igarashi K, Kanno J, Nakashima K (2008) Identification of genes that restrict astrocyte differentiation of midgestational neural precursor cells. Neuroscience 155(3):780–788. doi:10.1016/j.neuroscience.2008.06.039
47. Sanosaka T, Namihira M, Nakashima K (2009) Epigenetic mechanisms in sequential differentiation of neural stem cells. Epigenetics Off J DNA Methylation Soc 4(2):89–92
48. Singh SK, Wilczynska KM, Grzybowski A, Yester J, Osrah B, Bryan L, Wright S, Griswold-Prenner I, Kordula T (2011) The unique transcriptional activation domain of nuclear factor-I-X3 is critical to specifically induce marker gene expression in astrocytes. J Biol Chem 286(9):7315–7326. doi:10.1074/jbc.M110.152421
49. Skreka K, Schafferer S, Nat IR, Zywicki M, Salti A, Apostolova G, Griehl M, Rederstorff M, Dechant G, Huttenhofer A (2012) Identification of differentially expressed non-coding RNAs in embryonic stem cell neural differentiation. Nucleic Acids Res 40(13):6001–6015. doi:10.1093/nar/gks311
50. Swiss VA, Nguyen T, Dugas J, Ibrahim A, Barres B, Androulakis IP, Casaccia P (2011) Identification of a gene regulatory network necessary for the initiation of oligodendrocyte differentiation. PLoS One 6(4):e18088. doi:10.1371/journal.pone.0018088
51. Tan PP, French L, Pavlidis P (2013) Neuron-enriched gene expression patterns are regionally anti-correlated with oligodendrocyte-enriched patterns in the adult mouse and human brain. Front Neurosci 7:5. doi:10.3389/fnins.2013.00005
52. Tanaka S, Terada K, Nohno T (2011) Canonical Wnt signaling is involved in switching from cell proliferation to myogenic differentiation of mouse myoblast cells. J Mol Signal 6:12. doi:10.1186/1750-2187-6-12
53. Telese F, Gamliel A, Skowronska-Krawczyk D, Garcia-Bassets I, Rosenfeld MG (2013) “Seq-ing” insights into the epigenetics of neuronal gene regulation. Neuron 77(4):606–623. doi:10.1016/j.neuron.2013.01.034
54. Ueno T, Ito J, Hoshikawa S, Ohori Y, Fujiwara S, Yamamoto S, Ohtsuka T, Kageyama R, Akai M, Nakamura K, Ogata T (2012) The identification of transcriptional targets of Ascl1 in oligodendrocyte development. Glia 60(10):1495–1505. doi:10.1002/glia.22369
55. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63. doi:10.1038/nrg2484
56. Whyte WA, Orlando DA, Hnisz D, Abraham BJ, Lin CY, Kagey MH, Rahl PB, Lee TI, Young RA (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153(2):307–319. doi:10.1016/j.cell.2013.03.035
57. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, Ray P, Whitaker JW, Tian S, Hawkins RD, Leung D, Yang H, Wang T, Lee AY, Swanson SA, Zhang J, Zhu Y, Kim A, Nery JR, Urich MA, Kuan S, Yen CA, Klugman S, Yu P, Suknuntha K, Propson NE, Chen H, Edsall LE, Wagner U, Li Y, Ye Z, Kulkarni A, Xuan Z, Chung WY, Chi NC, Antosiewicz-Bourget JE, Slukvin I, Stewart R, Zhang MQ, Wang W, Thomson JA, Ecker JR, Ren B (2013) Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153(5):1134–1148. doi:10.1016/j.cell.2013.04.022
58. Yamashita R, Wakaguri H, Sugano S, Suzuki Y, Nakai K (2010) DBTSS provides a tissue specific dynamic view of transcription start sites. Nucleic Acids Res 38(Database issue):D98–D104. doi:10.1093/nar/gkp1017
59. Zhang HM, Chen H, Liu W, Liu H, Gong J, Wang H, Guo AY (2012) AnimalTFDB: a comprehensive animal transcription factor database. Nucleic Acids Res 40(Database issue):D144–D149. doi:10.1093/nar/gkr965