Zac1 regulates astroglial differentiation of neural stem cells through Socs3

Stem Cells

Volumn 31, Issue 8, 2013, Pages 1621-1632

  Schmidt Edelkraut, Udo ^a   Hoffmann, Anke ^a   Daniel, Guillaume ^a   Spengler, Dietmar ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Astrocytes; Differentiation; Imprinting; Neural stem cell; Socs3; Zac1

Indexed keywords

JANUS KINASE; PROTEIN ZAC1; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL CYCLE ARREST; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ASTROCYTES; DIFFERENTIATION; IMPRINTING; NEURAL STEM CELL; SOCS3; ZAC1;

ANIMALS; APOPTOSIS; ASTROCYTES; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; DNA METHYLATION; GENE EXPRESSION REGULATION; GENES, TUMOR SUPPRESSOR; HUMANS; JANUS KINASES; MICE; NEURAL STEM CELLS; PLASMIDS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84883376375     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1405     Document Type: Article

References (70)

1. Ming GL, Song HJ. Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron 2011;70:687-702.
2. Hirabayashi Y, Gotoh Y. Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 2010;11:377-388.
3. He F, Ge WH, Martinowich K et al. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 2005;8:616-625.
4. Lie DC, Colamarino SA, Gage FH et al. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005;437:1370-1375.
5. Ferron SR, Charalambous M, Radford E et al. Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 2011;475:381-385.
6. Wilkinson LS, Davies W, Isles AR. Genomic imprinting effects on brain development and function. Nat Rev Neurosci 2007;8:832-843.
7. Constancia M, Kelsey G, Reik W. Resourceful imprinting. Nature 2004;432:53-57.
8. Alam S, Zinyk D, Ma L et al. Members of the Plag gene family are expressed in complementary and overlapping regions in the developing murine nervous system. Dev Dyn 2005;234:772-782.
9. Chung SH, Marzban H, Aldinger K et al. Zac1 plays a key role in the development of specific neuronal subsets in the mouse cerebellum. Neural Dev 2011;6:25.
10. Valente T, Auladell C. Expression pattern of Zac1 mouse gene, a new zinc-finger protein that regulates apoptosis and cellular cycle arrest, in both adult brain and along development. Mech Dev 2001;108: 207-211.
11. Valente T, Junyent F, Auladell C. Zac1 is expressed in progenitor/stem cells of the neuroectoderm and mesoderm during embryogenesis: Differential phenotype of the Zac1-expressing cells during development. Dev Dyn 2005;233:667-679.
12. Ciani E, Frenquelli M, Contestabile A. Developmental expression of the cell cycle and apoptosis controlling gene, Lot1, in the rat cerebellum and in cultures of cerebellar granule cells. Dev Brain Res 2003; 142:193-202.
13. Ma L, Cantrup R, Varrault A et al. Zac1 functions through TGF beta II to negatively regulate cell number in the developing retina. Neural Dev 2007;2:11.
14. Ma L, Hocking JC, Hehr CL et al. Zac1 promotes a müller glial cell fate and interferes with retinal ganglion cell differentiation in Xenopus retina. Dev Dyn 2007;236:192-202.
15. Bilanges B, Varrault A, Mazumdar A et al. Alternative splicing of the imprinted candidate tumor suppressor gene ZAC regulates its antiproliferative and DNA binding activities. Oncogene 2001;20:1246-1253.
16. Hoffmann A, Ciani E, Boeckardt J et al. Transcriptional activities of the zinc finger protein Zac are differentially controlled by DNA binding. Mol Cell Biol 2003;23:988-1003.
17. Varrault A, Ciani E, Apiou F et al. hZAC encodes a zinc finger protein with antiproliferative properties and maps to a chromosomal region frequently lost in cancer. Proc Natl Acad Sci USA 1998;95: 8835-8840.
18. Barz T, Hoffmann A, Panhuysen M et al. Peroxisome proliferator-activated receptor gamma is a Zac target gene mediating Zac antiproliferation. Cancer Res 2006;66:11975-11982.
19. Ciani E, Hoffmann A, Schmidt P et al. Induction of the PAC1-R (PACAP-type I receptor) gene by p53 and Zac. Mol Brain Res 1999; 69:290-294.
20. Rodriguez-Henche N, Jamen F, Leroy C et al. Transcription of the mouse PAC1 receptor gene: Cell-specific expression and regulation by Zac1. BBA-GENE Struct Expr 2002;1576:157-162.
21. Spengler D, Villalba M, Hoffmann A et al. Regulation of apopotosis and cell cycle arrest by Zac1, a novel zinc finger protein expressed in the pituitary gland and the brain. EMBO J 1997;16:2814-2825.
22. Hoffmann A, Spengler D. Transient neonatal diabetes mellitus gene Zac1 impairs insulin secretion in mice through Rasgrf1. Mol Cell Biol 2012;32:2549-2560.
23. Liu PY, Hsieh TY, Liu ST et al. Zac1, a Sp1-like protein, regulates human p21WAF1Cip1 gene expression in HeLa cells. Exp Cell Res 2011;317:2925-2937.
24. Snyder EY, Deitcher DL, Walsh C et al. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 1992;68:33-51.
25. Conti L, Pollard SM, Gorba T et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. Plos Biol 2005;3: 1594-1606.
26. Pollard SM, Conti L, Sun Y et al. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex 2006;16:112-120.
27. Fath T, Ke YD, Gunning P et al. Primary support cultures of hippocampal and substantia nigra neurons. Nat Protoc 2008;4:78-85.
28. Hoffmann A, Barz T, Spengler D. Multitasking C2H2 zinc fingers link Zac DNA binding to coordinated regulation of p300-histone acetyltransferase activity. Mol Cell Biol 2006;26:5544-5557.
29. Auernhammer CJ, Bousquet C, Melmed S. Autoregulation of pituitary corticotroph SOCS-3 expression: Characterization of the murine SOCS-3 promoter. Proc Natl Acad Sci USA 1999;96:6964-6969.
30. Matthews J, Almlöf T, Kietz S et al. Estrogen receptor-[alpha] regulates SOCS-3 expression in human breast cancer cells. Biochem Biophys Res Commun 2005;335:168-174.
31. Murgatroyd C, Hoffmann A, Spengler D. In vivo ChIP for the analysis of microdissected tissue samples. In: Ales Vancura, ed. Transcriptional Regulation: Methods in Molecular Biology. Vol 809. Totowa: Humana Press, 2012;809:135-148.
32. Hoffmann A, Spengler D. A new coactivator function for Zac1's C2H2 zinc finger DNA-binding domain in selectively controlling PCAF activity. Mol Cell Biol 2008;28:6078-6093.
33. Hoffmann A, Villalba M, Journot L et al. A novel tetracycline-dependent expression vector with low basal expression and potent regulatory properties in various mammalian cell lines. Nucleic Acids Res 1997;25:1078-1079.
34. Pagotto U, Arzberger T, Ciani E et al. Inhibition of Zac1, a new gene differentially expressed in the anterior pituitary, increases cell proliferation. Endocrinology 1999;140:987-996.
35. He B, Hou L, Uematsu K et al. Cloning and characterization of a functional promoter of the human SOCS-3 gene. Biochem Biophys Res Com 2003;301:386-391.
36. Glaser T, Pollard SM, Smith A et al. Tripotential differentiation of adherently expandable neural stem (NS) cells. Plos One 2007;2.
37. Bonni A, Sun Y, NadalVicens M et al. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 1997;278:477-483.
38. Babon J, Kershaw N, Murphy J et al. Suppression of cytokine signaling by SOCS3: Characterization of the mode of inhibition and the basis of its specificity. Immunity 2012;36:239-250.
39. Saito M, Kitamura H, Sugiyama K. The specificity of monoclonal antibody A2B5 to c-series gangliosides. J Neurochem 2001;78:64-74.
40. Rao MS, Mayer-Proschel M. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 1997;188: 48-63.
41. Lee KH, Moon KJ, Kim HS et al. Increased cytoplasmic levels of CIS, SOCS1, SOCS2, or SOCS3 are required for nuclear translocation. FEBS Lett 2008;582:2319-2324.
42. White GE, Cotterill A, Addley MR et al. Suppressor of cytokine signalling protein SOCS3 expression is increased at sites of acute and chronic inflammation. J Mol Histol 2011;42:137-151.
43. Raff M. Intracellular developmental timers. Cold Spring Harb Symp 2007;72:431-435.
44. Li H, Grumet M. BMP and LIF signaling coordinately regulate lineage restriction of radial glia in the developing forebrain. Glia 2007;55: 24-35.
45. Lillien LE, Sendtner M, Raff MC. Extracellular-matrix associated molecules collaborate with ciliary neurotrophic factor to induce type-2 astrocyte development. J Cell Biol 1990;111:635-644.
46. Bonaguidi MA, McGuire T, Hu M et al. LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 2005;132:5503-5514.
47. Qian X, Qin S, Temple S et al. Timing of CNS cell generation: A programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 2000;28:69-80.
48. Starr R, Willson TA, Viney EM et al. A family of cytokine-inducible inhibitors of signalling. Nature 1997;387:917-921.
49. Freeman MR. Specification and Morphogenesis of astrocytes. Science 2010;330:774-778.
50. Fukuda S, Abematsu M, Mori H et al. Potentiation of astrogliogenesis by STAT3-mediated activation of bone morphogenetic protein-Smad signaling in neural stem cells. Mol Cell Biol 2007;27:4931-4937.
51. Bugga L, Gadient RA, Kwan K et al. Analysis of neuronal and glial phenotypes in brains of mice deficient in leukemia inhibitory factor. J Neurobiol 1998;36:509-524.
52. Nakashima K, Wiese S, Yanagisawa M et al. Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation. J Neurosci 1999;19:5429-5434.
53. Cao F, Hata R, Zhu P et al. Overexpression of SOCS3 inhibits astrogliogenesis and promotes maintenance of neural stem cells. J Neurochem 2006;98:459-470.
54. Roberts AW, Robb L, Alexander WS et al. Placental defects and embryonic lethality in mice lacking suppressor of cytokine signaling 3. Proc Natl Acad Sci USA 2001;98:9324-9329.
55. Emery B, Merson TD, Kilpatrick TJ et al. SOCS3 negatively regulates LIF signaling in neural precursor cells. Mol Cell Neurosci 2006;31: 739-747.
56. Miller JP, Yeh N, Vidal A et al. Interweaving the cell cycle machinery with cell differentiation. Cell Cycle 2007;6:2932-2938.
57. Li VC, Ballabeni A, Kirschner MW. Gap 1 phase length and mouse embryonic stem cell self-renewal. Proc Natl Acad Sci USA 2012;109: 12550-12555.
58. Varrault A, Gueydan C, Journot L et al. Zac1 regulates an imprinted gene network critically involved in the control of embryonic growth. Dev Cell 2006;11:711-722.
59. Yuasa S, Onizuka T, Fukuda K et al. Zac1 is an essential transcription factor for cardiac morphogenesis. Circ Res 2010;106:1083-1091.
60. Abdollahi A, Bao R, Hamilton TC. LOT1 is a growth suppressor gene down-regulated by the epidermal growth factor receptor ligands and encodes a nuclear zinc-finger protein. Oncogene 1999;18:6477-6487.
61. Ordway JM, Williams K, Curran T. Transcription repression in oncogenic transformation: Common targets of epigenetic repression in cells transformed by Fos, Ras Or Dnmt1 Oncogene 2004;23:3737-3748.
62. Gazin C, Wajapeyee N, Green MR et al. An elaborate pathway required for Ras-mediated epigenetic silencing. Nature 2007;449: 1073-1077.
63. Mattar P, Britz O, Schuurmans C et al. A screen for downstream effectors of Neurogenin2 in the embryonic neocortex. Dev Biol 2004; 273:373-389.
64. Sangster-Guity N, Yu LM, McCormick P. Molecular profiling of embryonal carcinoma cells following retinoic acid or histone deacetylase inhibitor treatment. Cancer Biol Ther 2004;3:1109-1120.
65. Eifert C, Sangster-Guity N, McCormick PJ et al. Global gene expression profiles associated with retinoic acid-induced differentiation of embryonal carcinoma cells. Mol Reprod Dev 2006;73:796-824.
66. Contestabile A, Fila T, Ciani E et al. Cyclic AMP-mediated regulation of transcription factor Lot1 expression in cerebellar granule cells. J Biol Chem 2005;280:33541-33551.
67. Fila T, Trazzi S, Ciani E et al. Lot1 is a key element of the pituitary adenylate cyclase-activating polypeptide (PACAP)/cyclic AMP pathway that negatively regulates neuronal precursor proliferation. J Biol Chem 2009;284:15325-15338.
68. Badcock C, Crespi B. Battle of the sexes may set the brain. Nature 2008;454:1054-1055.
69. Tollkuhn J, Xu X, Shah NM. A custody battle for the mind: Evidence for extensive imprinting in the brain. Neuron 2010;67:359-362.
70. Milosavljevic A. Emerging patterns of epigenomic variation. Trends Genet 2011;27:242-250.