Necdin controls proliferation and apoptosis of embryonic neural stem cells in an oxygen tension-dependent manner

Journal of Neuroscience

Volumn 33, Issue 25, 2013, Pages 10362-10373

  Huang, Zhenyu ^a   Fujiwara, Kazushiro ^a   Minamide, Ryohei ^a   Hasegawa, Koichi ^a   Yoshikawa, Kazuaki ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 2ALPHA; NECDIN; VASCULOTROPIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; HYPOXIA; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MOUSE; NEURAL STEM CELL; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UBIQUITINATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CELL PROLIFERATION; CELL SEPARATION; DNA FRAGMENTATION; FEMALE; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; LENTIVIRUS; MICE; NERVE TISSUE PROTEINS; NEURAL STEM CELLS; NUCLEAR PROTEINS; OXYGEN; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; UBIQUITIN;

EID: 84879165939     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5682-12.2013     Document Type: Article

References (55)

1. Aizawa T, Hasegawa K, Ohkumo T, Haga S, Ikeda K, Yoshikawa K (2011) Neural stem cell-like gene expression in a mouse ependymoma cell line transformed by human BK polyomavirus. Cancer Sci 102:122-129. CrossRef Medline
2. Barker PA, Salehi A (2002) The MAGE proteins: emerging roles in cell cycle progression, apoptosis, and neurogenetic disease. J Neurosci Res 67:705-712. CrossRef Medline
3. Bischof JM, Ekker M, Wevrick R (2003) A MAGE/NDN-like gene in zebrafish. Dev Dyn 228:475-479. CrossRef Medline
4. Brunelli S, Tagliafico E, De Angelis FG, Tonlorenzi R, Baesso S, Ferrari S, Niinobe M, Yoshikawa K, Schwartz RJ, Bozzoni I, Ferrari S, Cossu G (2004) Msx2 and necdin combined activities are required for smooth muscle differentiation in mesoangioblast stem cells. Circ Res 94:1571-1578. CrossRef Medline
5. Chen HL, Pistollato F, Hoeppner DJ, Ni HT, McKay RD, Panchision DM (2007) Oxygen tension regulates survival and fate of mouse central nervous system precursors at multiple levels. Stem Cells 25:2291-2301. CrossRef Medline
6. Chen X, Tian Y, Yao L, Zhang J, Liu Y (2010) Hypoxia stimulates proliferation of rat neural stem cells with influence on the expression of cyclin D1 and c-Jun N-terminal protein kinase signaling pathway in vitro. Neuroscience 165:705-714. CrossRef Medline
7. Clarke L, van der Kooy D (2009) Low oxygen enhances primitive and definitive neural stem cell colony formation by inhibiting distinct cell death pathways. Stem Cells 27:1879-1886. CrossRef Medline
8. Dang EV, Barbi J, Yang HY, Jinasena D, Yu H, Zheng Y, Bordman Z, Fu J, Kim Y, Yen HR, Luo W, Zeller K, Shimoda L, Topalian SL, Semenza GL, Dang CV, Pardoll DM, Pan F (2011) Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 146:772-784. CrossRef Medline
9. Deponti D, François S, Baesso S, Sciorati C, Innocenzi A, Broccoli V, Muscatelli F, Meneveri R, Clementi E, Cossu G, Brunelli S (2007) Necdin mediates skeletal muscle regeneration by promoting myoblast survival and differentiation. J Cell Biol 179:305-319. CrossRef Medline
10. Ereciska M, Silver IA (2001) Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol 128:263-276. CrossRef Medline
11. Friedman ER, Fan CM (2007) Separate necdin domains bind ARNT2 and HIF1alpha and repress transcription. Biochem Biophys Res Commun 363:113-118. CrossRef Medline
12. Fujiwara K, Hasegawa K, Ohkumo T, Miyoshi H, Tseng YH, Yoshikawa K (2012) Necdin controls proliferation of white adipocyte progenitor cells. PLoS One 7:e30948. CrossRef Medline
13. Gavrieli Y, Sherman Y, Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501. CrossRef Medline
14. Greer SN, Metcalf JL, Wang Y, Ohh M (2012) The updated biology of hypoxia-inducible factor. EMBO J 31: 2448-2460. CrossRef Medline
15. Hasegawa K, Yoshikawa K (2008) Necdin regulates p53 acetylation via Sirtuin1 to modulate DNA damage response in cortical neurons. J Neurosci 28:8772-8784. CrossRef Medline
16. Hasegawa K, Kawahara T, Fujiwara K, Shimpuku M, Sasaki T, Kitamura T, Yoshikawa K (2012) Necdin controls Foxo1 acetylation in hypothalamic arcuate neurons to modulate the thyroid axis. J Neurosci 32:5562-5572. CrossRef Medline
17. Hayashi Y, Matsuyama K, Takagi K, Sugiura H, Yoshikawa K (1995) Arrest of cell growth by necdin, a nuclear protein expressed in postmitotic neurons. Biochem Biophys Res Commun 213:317-324. CrossRef Medline
18. Ko CY, Tsai MY, Tseng WF, Cheng CH, Huang CR, Wu JS, Chung HY, Hsieh CS, Sun CK, Hwang SP, Yuh CH, Huang CJ, Pai TW, Tzou WS, Hu CH (2011) Integration of CNS survival and differentiation by HIF2alpha. Cell Death Differ 18:1757-1770. CrossRef Medline
19. Kobayashi M, Taniura H, Yoshikawa K (2002) Ectopic expression of necdin induces differentiation of mouse neuroblastoma cells. J Biol Chem 277: 42128-42135. CrossRef Medline
20. Kubota Y, Osawa M, Jakt LM, Yoshikawa K, Nishikawa S (2009) Necdin restricts proliferation of hematopoietic stem cells during hematopoietic regeneration. Blood 114:4383-4392. CrossRef Medline
21. Kurita M, Kuwajima T, Nishimura I, Yoshikawa K (2006) Necdin down regulates cdc2 expression to attenuate neuronal apoptosis. J Neurosci 26:12003-12013. CrossRef Medline
22. Kuwajima T, Taniura H, Nishimura I, Yoshikawa K (2004) Necdin interacts with the Msx2 homeodomain protein via MAGE-D1 to promote myogenic differentiation of C2C12 cells. J Biol Chem 279:40484-40493. CrossRef Medline
23. Kuwajima T, Nishimura I, Yoshikawa K (2006) Necdin promotes GABAergic neuron differentiation in cooperation with Dlx homeodomain proteins. J Neurosci 26:5383-5392. CrossRef Medline
24. Kuwajima T, Hasegawa K, Yoshikawa K (2010) Necdin promotes tangential migration of neocortical interneurons from basal forebrain. J Neurosci 30:3709-3714. CrossRef Medline
25. Kuwako K, Taniura H, Yoshikawa K (2004) Necdin-related MAGE proteins differentially interact with the E2F1 transcription factor and the p75 neurotrophin receptor. J Biol Chem 279:1703-1712. CrossRef Medline
26. Kuwako K, Hosokawa A, Nishimura I, Uetsuki T, Yamada M, Nada S, Okada M, Yoshikawa K (2005) Disruption of the paternal necdin gene diminishes TrkA signaling for sensory neuron survival. J Neurosci 25:7090-7099. CrossRef Medline
27. Lavi-Itzkovitz A, Tcherpakov M, Levy Z, Itzkovitz S, Muscatelli F, Fainzilber M (2012) Functional consequences of necdin nucleocytoplasmic localization. PLoS One 7:e33786. CrossRef Medline
28. Liu Y, Elf SE, Miyata Y, Sashida G, Liu Y, Huang G, Di Giandomenico S, Lee JM, Deblasio A, Menendez S, Antipin J, Reva B, Koff A, Nimer SD (2009) p53 Regulates hematopoietic stem cell quiescence. Cell Stem Cell 4:37-48. CrossRef Medline
29. López-Sánchez N, González-Fernández Z, Niinobe M, Yoshikawa K, Frade JM (2007) Single mage gene in the chicken genome encodes CMage, a protein with functional similarities to mammalian type II Mage proteins. Physiol Genomics 30:156-171. CrossRef Medline
30. Maruyama K, Usami M, Aizawa T, Yoshikawa K (1991) A novel brain specific mRNA encoding nuclear protein (necdin) expressed in neutrally differentiated embryonal carcinoma cells. Biochem Biophys Res Commun 178:291-296. CrossRef Medline
31. Mazumdar J, O'Brien WT, Johnson RS, LaManna JC, Chavez JC, Klein PS, Simon MC (2010) O2 regulates stem cells through Wnt/beta-catenin signalling. Nat Cell Biol 12:1007-1013. CrossRef Medline
32. Miyoshi H, Blömer U, Takahashi M, Gage FH, Verma IM (1998) Development of a self-inactivating lentivirus vector. J Virol 72:8150-8157. Medline
33. Moon HE, Ahn MY, Park JA, Min KJ, Kwon YW, Kim KW (2005) Negative regulation of hypoxia inducible factor-1alpha by necdin. FEBS Lett 579: 3797-3801. CrossRef Medline
34. Morrison SJ, Csete M, Groves AK, Melega W, Wold B, Anderson DJ (2000) Culture in reduced levels of oxygen promotes clonogenic sympathoadrenal differentiation by isolated neural crest stem cells. J Neurosci 20:7370-7376. Medline
35. Mutoh T, Sanosaka T, Ito K, Nakashima K (2012) Oxygen levels epigenetically regulate fate switching of neural precursor cells via hypoxia inducible factor 1alpha-notch signal interaction in the developing brain. Stem Cells 30:561-569. CrossRef Medline
36. Nishimura I, Shimizu S, Sakoda JY, Yoshikawa K (2007) Expression of Drosophila MAGE gene encoding a necdin homologous protein in postembryonic neurogenesis. Gene Expr Patterns 7:244-251. CrossRef Medline
37. Nishimura I, Sakoda JY, Yoshikawa K (2008) Drosophila MAGE controls neural precursor proliferation in postembryonic neurogenesis. Neuroscience 154:572-581. CrossRef Medline
38. Panchision DM (2009) The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 220:562-568. CrossRef Medline
39. Pfenninger CV, Roschupkina T, Hertwig F, Kottwitz D, Englund E, Bengzon J, Jacobsen SE, Nuber UA (2007) CD133 is not present on neurogenic astrocytes in the adult subventricular zone, but on embryonic neural stem cells, ependymal cells, and glioblastoma cells. Cancer Res 67:5727-5736. CrossRef Medline
40. Reynolds BA, Weiss S (1996) Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1-13. CrossRef Medline
41. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574. Medline
42. Rodrigues CA, Diogo MM, da Silva CL, Cabral JM (2010) Hypoxia enhances proliferation of mouse embryonic stem cell-derived neural stem cells. Biotechnol Bioeng 106:260-270. Medline
43. Studer L, Csete M, Lee SH, Kabbani N, Walikonis J, Wold B, McKay R (2000) Enhanced proliferation, survival, and dopaminergic differentiation of CNS precursors in lowered oxygen. J Neurosci 20:7377-7383.
44. Medline Taniura H, Taniguchi N, Hara M, Yoshikawa K (1998) Necdin, a postmitotic neuron-specific growth suppressor, interacts with viral transforming proteins and cellular transcription factor E2F1. J Biol Chem 273:720-728. CrossRef Medline
45. Taniura H, Matsumoto K, Yoshikawa K (1999) Physical and functional interactions of neuronal growth suppressor necdin with p53. J Biol Chem 274:16242-16248. CrossRef Medline
46. Taniura H, Kobayashi M, Yoshikawa K (2005) Functional domains of necdin for protein-protein interaction, nuclear matrix targeting, and cell growth suppression. J Cell Biochem 94:804-815. CrossRef Medline
47. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63:479-506. Medline
48. Tseng YH, Butte AJ, Kokkotou E, Yechoor VK, Taniguchi CM, Kriauciunas KM, Cypess AM, Niinobe M, Yoshikawa K, Patti ME, Kahn CR (2005) Prediction of preadipocyte differentiation by gene expression reveals role of insulin receptor substrates and necdin. Nat Cell Biol 7:601-611. CrossRef Medline
49. Uchida N, Buck DW, He D, Reitsma MJ, Masek M, Phan TV, Tsukamoto AS, Gage FH, Weissman IL (2000) Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci U S A 97:14720-14725. CrossRef Medline
50. Uetsuki T, Takagi K, Sugiura H, Yoshikawa K (1996) Structure and expression of the mouse necdin gene. Identification of a postmitotic neuronrestrictive core promoter. J Biol Chem 271:918-924. CrossRef Medline
51. Uetsuki T, Takemoto K, Nishimura I, Okamoto M, Niinobe M, Momoi T, Miura M, Yoshikawa K (1999) Activation of neuronal caspase-3 by in tracellular accumulation of wild-type Alzheimer amyloid precursor protein. J Neurosci 19:6955-6964. Medline
52. Wada T, Haigh JJ, Ema M, Hitoshi S, Chaddah R, Rossant J, Nagy A, van der Kooy D (2006) Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival. J Neurosci 26:6803-6812. CrossRef Medline
53. Wiesener MS, Jurgensen JS, Rosenberger C, Scholze CK, Hörstrup JH, Warnecke C, Mandriota S, Bechmann I, Frei UA, Pugh CW, Ratcliffe PJ, Bachmann S, Maxwell PH, Eckardt KU (2003) Widespread hypoxia inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J 17:271-273. Medline
54. Zhao T, Zhang CP, Liu ZH, Wu LY, Huang X, Wu HT, Xiong L, Wang X, Wang XM, Zhu LL, Fan M (2008) Hypoxia-driven proliferation of embryonic neural stem/progenitor cells-role of hypoxia-inducible transcription factor-1alpha. FEBS J 275:1824-1834. CrossRef Medline
55. Zimmer M, Ebert BL, Neil C, Brenner K, Papaioannou I, Melas A, Tolliday N, Lamb J, Pantopoulos K, Golub T, Iliopoulos O (2008) Small-molecule inhibitors of HIF-2a translation link its 5 UTR iron-responsive element to oxygen sensing. Mol Cell 32:838-848. CrossRef Medline