Signal transducer and activator of transcription-3 maintains the stemness of radial glia at mid-neurogenesis

Journal of Neuroscience

Volumn 35, Issue 3, 2015, Pages 1011-1023

  Hong, Seulgi ^a   Song, Mi Ryoung ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

Neurogenesis; Radial glia; STAT3

Indexed keywords

4',6 DIAMIDINO 2 PHENYLINDOLE; ALPHA TUBULIN; COMPLEMENTARY DNA; EDOXUDINE; EOMESODERMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GREEN FLUORESCENT PROTEIN; JANUS KINASE; KI 67 ANTIGEN; LEUKEMIA INHIBITORY FACTOR; NESTIN; RETROVIRUS VECTOR; SHORT HAIRPIN RNA; STAT1 PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX2; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRDU ASSAY; CELL DIVISION; CELL POPULATION; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DOWN REGULATION; ELECTROPORATION; EMBRYO; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GLIA; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MOUSE; MUTANT MOUSE STRAIN; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; RADIAL GLIA; TIME LAPSE IMAGING; TRANSCRIPTION REGULATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CYTOLOGY; GENETICS; MACROGLIA; METABOLISM; NERVE CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; EPENDYMOGLIAL CELLS; MICE; NEURAL STEM CELLS; NEUROGENESIS; NEURONS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84921521100     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2119-14.2015     Document Type: Article

References (48)

1. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD (2005) Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45:207-221. CrossRef Medline
2. Asami M, Pilz GA, Ninkovic J, Godinho L, Schroeder T, Huttner WB, Götz M (2011) The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development 138: 5067-5078. CrossRef Medline
3. Barnabé-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD (2005) Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48:253-265. CrossRef Medline
4. Bauer S, Patterson PH (2006) Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 26:12089-12099. CrossRef Medline
5. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278: 477-483. CrossRef Medline
6. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell JE Jr (1999) Stat3 as an oncogene. Cell 98:295-303. CrossRef Medline
7. Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH (2009) Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189-202. CrossRef Medline
8. Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notchl immunoreactivity in mammalian neurogenesis. Cell 82:631-641. CrossRef Medline
9. Coqueret O, Bérubé G, Nepveu A (1998) The mammalian Cut homeodomain protein functions as a cell-cycle-dependent transcriptional repressor which downmodulates p21WAF1/CIP1/SDI1 in S phase. EMBO J 17:4680-4694. CrossRef Medline
10. Cubelos B, Sebastián-Serrano A, Kim S, Moreno-Ortiz C, Redondo JM, Walsh CA, Nieto M (2008) Cux-2 controls the proliferation of neuronal intermediate precursors of the cortical subventricular zone. Cereb Cortex 18:1758-1770. CrossRef Medline
11. Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR, Ramos C, Müller U (2012) Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337:746-749. CrossRef Medline
12. Fukada T, Ohtani T, Yoshida Y, Shirogane T, Nishida K, Nakajima K, Hibi M, Hirano T (1998) STAT3 orchestrates contradictory signals in cytokineinduced G1 to S cell-cycle transition. EMBO J 17:6670-6677. CrossRef Medline
13. Gal JS, Morozov YM, Ayoub AE, Chatterjee M, Rakic P, Haydar TF (2006) Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci 26:1045-1056. CrossRef Medline
14. Gallagher D, Norman AA, Woodard CL, Yang G, Gauthier-Fisher A, Fujitani M, Vessey JP, Cancino GI, Sachewsky N, Woltjen K, Fatt MP, Morshead CM, Kaplan DR, Miller FD (2013) Transient maternal IL-6 mediates long-lasting changes in neural stem cell pools by deregulating an endogenous self-renewal pathway. Cell Stem cell 13:564-576. CrossRef Medline
15. Götz M, Huttner WB (2005) The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788. CrossRef Medline
16. Gregg C, Weiss S (2005) CNTF/LIF/gp130 receptor complex signaling maintains a VZ precursor differentiation gradient in the developing ventral forebrain. Development 132:565-578. CrossRef Medline
17. Hatta T, Moriyama K, Nakashima K, Taga T, Otani H (2002) The Role of gp130 in cerebral cortical development: in vivo functional analysis in a mouse exo utero system. J Neurosci 22:5516-5524. Medline
18. He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G, de Vellis J, Sun YE (2005) A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 8:616-625. CrossRef Medline
19. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JL (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353-366. CrossRef Medline
20. Hong S, Song MR (2014) STAT3 but not STAT1 is required for astrocyte differentiation. PLoS One 9:e86851. CrossRef Medline
21. Imayoshi I, Isomura A, Harima Y, Kawaguchi K, Kori H, Miyachi H, Fujiwara T, Ishidate F, Kageyama R (2013) Oscillatory control of factors determining multipotency and fate in mouse neural progenitors. Science 342: 1203-1208. CrossRef Medline
22. Iulianella A, Sharma M, Durnin M, Vanden Heuvel GB, Trainor PA (2008) Cux2 (Cutl2) integrates neural progenitor development with cell-cycle progression during spinal cord neurogenesis. Development 135:729-741. CrossRef Medline
23. Kamakura S, Oishi K, Yoshimatsu T, Nakafuku M, Masuyama N, Gotoh Y (2004) Hes binding to STAT3 mediates crosstalk between Notch and JAK-STAT signalling. Nat Cell Biol 6:547-554. CrossRef Medline
24. Kang K, Song MR (2010) Diverse FGF receptor signaling controls astrocyte specification and proliferation. Biochemical and biophysical research communications 395:324-329. CrossRef Medline
25. Kang K, Lee D, Hong S, Park SG, Song MR (2013) The E3 ligase Mind bomb-1 (mib1) modulates Delta-Notch signaling to control neurogenesis and gliogenesis in the developing spinal cord. J Biol Chem 288:2580-2592. CrossRef Medline
26. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184. CrossRef Medline
27. Levy DE, Darnell JE Jr (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651-662. CrossRef Medline
28. Nieto M, Monuki ES, Tang H, Imitola J, Haubst N, Khoury SJ, Cunningham J, Gotz M, Walsh CA (2004) Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J Comp Neurol 479:168-180. CrossRef Medline
29. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714-720. CrossRef Medline
30. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136-144. CrossRef Medline
31. Ochiai W, Nakatani S, Takahara T, Kainuma M, Masaoka M, Minobe S, Namihira M, Nakashima K, Sakakibara A, Ogawa M, Miyata T (2009) Periventricular notch activation and asymmetric Ngn2 and Tbr2 expression in pair-generated neocortical daughter cells. Mol Cell Neurosci 40: 225-233. CrossRef Medline
32. Pinto L, Drechsel D, Schmid MT, Ninkovic J, Irmler M, Brill MS, Restani L, Gianfranceschi L, Cerri C, Weber SN, Tarabykin V, Baer K, Guillemot F, Beckers J, Zecevic N, Dehay C, Caleo M, Schorle H, Götz M (2009) AP2gamma regulates basal progenitor fate in a region-and layer-specific manner in the developing cortex. Nat Neurosci 12:1229-1237. CrossRef Medline
33. Pitman M, Emery B, Binder M, Wang S, Butzkueven H, Kilpatrick TJ (2004) LIF receptor signaling modulates neural stem cell renewal. Mol Cell Neurosci 27:255-266. CrossRef Medline
34. Postiglione MP, Jüschke C, Xie Y, Haas GA, Charalambous C, Knoblich JA (2011) Mouse inscuteable induces apical-basal spindle orientation to facilitate intermediate progenitor generation in the developing neocortex. Neuron 72:269-284. CrossRef Medline
35. Shimazaki T, Shingo T, Weiss S (2001) The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci 21:7642-7653. Medline
36. Shimojo H, Ohtsuka T, Kageyama R (2008) Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 58:52-64. CrossRef Medline
37. Shitamukai A, Konno D, Matsuzaki F (2011) Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 31:3683-3695. CrossRef Medline
38. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19: 10357-10371. Medline
39. Takeda K, Noguchi K, Shi W, Tanaka T, Matsumoto M, Yoshida N, Kishimoto T, Akira S (1997) Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci U S A 94:3801-3804. CrossRef Medline
40. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1:749-758. CrossRef Medline
41. Wang X, Tsai JW, LaMonica B, Kriegstein AR (2011) A new subtype of progenitor cell in the mouse embryonic neocortex. Nat Neurosci 14:555-561. CrossRef Medline
42. Xie Y, Jüschke C, Esk C, Hirotsune S, Knoblich JA (2013) The phosphatase PP4c controls spindle orientation to maintain proliferative symmetric divisions in the developing neocortex. Neuron 79:254-265. CrossRef Medline
43. Yoshimatsu T, Kawaguchi D, Oishi K, Takeda K, Akira S, Masuyama N, Gotoh Y (2006) Non-cell-autonomous action of STAT3 in maintenance of neural precursor cells in the mouse neocortex. Development 133:2553-2563. CrossRef Medline
44. Yoshiura S, Ohtsuka T, Takenaka Y, Nagahara H, Yoshikawa K, Kageyama R (2007) Ultradian oscillations of Stat, Smad, and Hes1 expression in response to serum. Proc Natl Acad Sci U S A 104:11292-11297. CrossRef Medline
45. Zhao X, Heng JI-T, Guardavaccaro D, Jiang R, Pagano M, Guillemot F, Iavarone A, Lasorella A (2008) The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat Cell Biol 10:643-653. CrossRef Medline
46. Zhong W, Chia W (2008) Neurogenesis and asymmetric cell division. Curr Opin Neurobiol 18:4-11. CrossRef Medline
47. Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN (1996) Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17:43-53. CrossRef Medline
48. Zimmer C, Tiveron MC, Bodmer R, Cremer H (2004) Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb Cortex 14:1408-1420. CrossRef Medline