Transgenic overexpression of Sox17 promotes oligodendrocyte development and attenuates demyelination

Journal of Neuroscience

Volumn 33, Issue 30, 2013, Pages 12528-12542

  Ming, Xiaotian ^a   Chew, Li Jin ^a   Gallo, Vittorio ^a  

^a CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BCL 2; T CELL FACTOR PROTEIN; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR SOX17;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; EPIFLUORESCENCE MICROSCOPY; FEMALE; GENOTYPE; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; APOPTOSIS; CELL LINEAGE; CORPUS CALLOSUM; DEMYELINATING DISEASES; FEMALE; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; HMGB PROTEINS; IMMUNOHISTOCHEMISTRY; LYSOPHOSPHATIDYLCHOLINES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGODENDROGLIA; PROTO-ONCOGENE PROTEINS C-BCL-2; SIGNAL TRANSDUCTION; SOXF TRANSCRIPTION FACTORS;

EID: 84880587825     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0536-13.2013     Document Type: Article

References (56)

1. Aguirre A, Gallo V (2004) Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci 24:10530-10541. CrossRef Medline
2. Aguirre AA, Chittajallu R, Belachew S, Gallo V (2004) NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J Cell Biol 165:575-589. CrossRef Medline
3. Aguirre A, Dupree JL, Mangin JM, Gallo V (2007) A functional role for EGFR signalling in myelination and remyelination. Nat Neurosci 10:990-1002. CrossRef Medline
4. Alvarez-Medina R, Cayuso J, Okubo T, Takada S, Martí E (2008) Wnt canonical pathway restricts graded SHH/Gli patterning activity through the regulation of Gli3 expression. Development 135:237-247. Medline
5. Alvarez-Medina R, Le Dreau G, Ros M, Martí E (2009) Hedgehog activation is required upstream of Wnt signalling to control neural progenitor proliferation. Development 136:3301-3309. CrossRef Medline
6. Bai CB, Joyner AL (2001) Gli1 can rescue the in vivo function of Gli2. Development 128:5161-5172. Medline
7. Bai CB, Auerbach W, Lee JS, Stephen D, Joyner AL (2002) Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129:4753-4761. Medline
8. Bai CB, Stephen D, Joyner AL (2004) All mouse ventral spinal cord patterning by Hedgehog is Gli dependent and involves an activator function in Gli3. Dev Cell 6:103-115. CrossRef Medline
9. Borycki A, Brown AM, Emerson CP Jr (2000) Shh and Wnt signaling pathways converge to control Gli gene activation in avia somites. Development 127:2075-2087. Medline
10. Chen HL, Chew LJ, Packer RJ, Gallo V (2013) Modulation of the Wnt/betacatenin pathway in human oligodendroglioma cells by Sox17 regulates proliferation and differentiation. Cancer Lett 335:361-371. CrossRef Medline
11. Chew LJ, Gallo V (2009) The yin and yang of Sox proteins: activation and repression in development and disease. J Neurosci Res 87:3277-3287. CrossRef Medline
12. Chew LJ, Shen W, Ming X, Senatorov VV Jr, Chen HL, Cheng Y, Hong E, Knoblach S, Gallo V (2011) SRY-box containing gene 17 regulates the Wnt/beta-catenin signaling pathway in oligodendrocyte progenitor cells. J Neurosci 31:13921-13935. CrossRef Medline
13. Copray S, Balasubramaniyan V, Levenga J, de Bruijn J, Liem R, Boddeke E (2006) Olig2 overexpression induces the in vitro differentiation of neural stem cells into mature oligodendrocytes. Stem Cells 24:1001-1010. CrossRef Medline
14. Dierks C, Grbic J, Zirlik K, Beigi R, Englund NP, Guo GR, Veelken H, Engelhardt M, Mertelsmann R, Kelleher JF, Schultz P, Warmuth M (2007) Essential role of stromally induced hedgehog signaling in B-cell malignancies. Nat Med 13:944-951. CrossRef Medline
15. Etxeberria A, Mangin JM, Aguirre A, Gallo V (2010) Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci 13:287-289. CrossRef Medline
16. Fancy SP, Baranzini SE, Zhao C, Yuk DI, Irvine KA, Kaing S, Sanai N, Franklin RJ, Rowitch DH (2009) Dysregulation of the Wnt pathway inhibits timely myelination and remyelination in the mammalian CNS. Genes and Development 23:1571-1585. CrossRef Medline
17. Fu H, Kesari S, Cai J (2012) Tcf7L2 is tightly controlled during myelin formation. Cell Mol Neurobiol 32:345-352. CrossRef Medline
18. Gravel M, Di Polo A, Valera PB, Braun PE (1998) Four kilobase sequence of the mouse CNP gene directs spatial and temporal expression of lacZ in transgenic mice. J Neurosci Res 53:393-404. CrossRef Medline
19. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Munsterberg A, Vivian N, Goodfellow P, Lovell-Badge R (1990) A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346:245-250. CrossRef Medline
20. He J, Sheng T, Stelter AA, Li C, Zhang X, Sinha M, Luxon BA, Xie J (2006) Suppressing Wnt signaling by the hedgehog pathway through sFRP1. J Biol Chem 281:35598-35602. CrossRef Medline
21. He S, Kim I, Lim MS, Morrison SJ (2011) Sox17 expression confers selfrenewal potential and fetal stem cell characteristics upon adult hematopoietic progenitors. Genes Dev 25:1613-1627. CrossRef Medline
22. Holowacz T, Huelsken J, Dufort D, van der Kooy D (2011) Neural stem cells are increased after loss of beta-catenin, but neural progenitors undergo cell death. Eur J Neurosci 33:1366-1375. CrossRef Medline
23. Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor KA, Ming GL, Song H, Gallo V (2010) Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci 13:541-550. CrossRef Medline
24. Joshi M, Keith Pittman H, Haisch C, Verbanac K (2008) Real-time PCR to determine transgene copy number and to quantitate the biolocalization of adoptively transferred cells from EGFP-transgenic mice. Biotechniques 45:247-258. CrossRef Medline
25. Kanai Y, Kanai-Azuma M, Noce T, Saido TC, Shiroishi T, Hayashi Y, Yazaki K (1996) Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis. J Cell Biol 133:667-681. CrossRef Medline
26. Katoh Y, Katoh M (2006) WNT antagonist, SFRP1, is Hedgehog signaling target. Int J Mol Med 17:171-175. Medline
27. Kenney AM, Rowitch DH (2000) Sonic hedgehog promotes G1 cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol Cell Biol 20:9055-9067. CrossRef Medline
28. Kump E, Ji J, Wernli M, Häusermann P, Erb P (2008) Gli2 upregulates cFlip and renders basal cell carcinoma cells resistant to death ligand-mediated apoptosis. Oncogene 27:3856-3864. CrossRef Medline
29. Kuspert M, Weider M, Muller J, Hermans-Borgmeyer I, Meijer D, Wegner M (2012) Desert hedgehog links transcription factor Sox10 to perineurial development. J Neurosci 32:5472-5480. CrossRef Medline
30. Lei Q, Zelman AK, Kuang E, Li S, Matise MP (2004) Transduction of graded Hedgehog signaling by a combination of Gli2 and Gli3 activator functions in the developing spinal cord. Development 131:3593-3604. CrossRef Medline
31. Lei Q, Jeong Y, Misra K, Li S, Zelman AK, Epstein DJ, Matise MP (2006) Wnt signaling inhibitors regulate the transcriptional response to morphogenetic Shh-Gli signaling in the neural tube. Dev Cell 11:325-337. CrossRef Medline
32. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75-86. CrossRef Medline
33. Mazumdar T, DeVecchio J, Shi T, Jones J, Agyeman A, Houghton JA (2011a) Hedgehog signaling drives cellular survival in human colon carcinoma cells. Cancer Res 71:1092-1102. CrossRef Medline
34. Mazumdar T, Devecchio J, Agyeman A, Shi T, Houghton JA (2011b) Blocking Hedgehog survival signaling at the level of the GLI genes induces DNA damage and extensive cell death in human colon carcinoma cells. Cancer Res 71:5904-5914. CrossRef Medline
35. Nery S, Wichterle H, Fishell G (2001) Sonic hedgehog contributes to oligodendrocyte specification in the mammalian forebrain. Development 128: 527-540. Medline
36. Nicolay DJ, Doucette JR, Nazarali AJ (2007) Transcriptional control of oligodendrogenesis. Glia 55:1287-1299. CrossRef Medline
37. Poncet C, Soula C, Trousse F, Kan P, Hirsinger E, Pourquié O, Duprat AM, Cochard P (1996) Induction of oligodendrocyte progenitors in the trunk neural tube by ventralizing signals: effects of notochord and floor plate grafts, and of sonic hedgehog. Mech Dev 60:13-32. CrossRef Medline
38. Potzner MR, Griffel C, Lutjen-Drecoll E, Bösl MR, Wegner M, Sock E (2007) Prolonged Sox4 expression in oligodendrocytes interferes with normal myelination in the central nervous system. Mol Cell Biol 27:5316-5326. CrossRef Medline
39. Qi Y, Tan M, Hui CC, Qiu M (2003) Gli2 is required for normal Shh signaling and oligodendrocyte development in the spinal cord. Mol Cell Neurosci 23:440-450. CrossRef Medline
40. Regl G, Kasper M, Schnidar H, Eichberger T, Neill GW, Philpott MP, Esterbauer H, Hauser-Kronberger C, Frischauf AM, Aberger F (2004) Activation of the Bcl2 promoter in response to Hedgehog/GLI signal transduction is predominantly mediated by GLI2. Cancer Res 64:7724-7731. CrossRef Medline
41. Rowitch DH, S-Jacques B, Lee SM, Flax JD, Snyder EY, McMahon AP (1999) Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J Neurosci 19:8954-8965. Medline
42. Schneider FT, Schänzer A, Czupalla CJ, Thom S, Engels K, Schmidt MH, Plate KH, Liebner S (2010) Sonic hedgehog acts as a negative regulator of beta-catenin signaling in the adult tongue epithelium. Am J Pathol 177: 404-414. CrossRef Medline
43. Serrano AG, Gandillet A, Pearson S, Lacaud G, Kouskoff V (2010) Contrasting effects of Sox17-and Sox18-sustained expression at the onset of blood specification. Blood 115:3895-3898. CrossRef Medline
44. Shen S, Sandoval J, Swiss VA, Li J, Dupree J, Franklin RJ, Casaccia-Bonnefil P (2008) Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci 11:1024-1034. CrossRef Medline
45. Sinner D, Kordich JJ, Spence JR, Opoka R, Rankin S, Lin SC, Jonatan D, Zorn AM, Wells JM (2007) Sox17 and Sox4 differentially regulate betacatenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 27:7802-7815. CrossRef Medline
46. Sohn J, Natale J, Chew LJ, Belachew S, Cheng Y, Aguirre A, Lytle J, Nait-Oumesmar B, Kerninon C, Kanai-Azuma M, Kanai Y, Gallo V (2006) Identification of Sox17 as a transcription factor that regulates oligodendrocyte development. J Neurosci 26:9722-9735. CrossRef Medline
47. Stolt CC, Wegner M (2010) SoxE function in vertebrate nervous system development. Int J Biochem Cell Biol 42:437-440. CrossRef Medline
48. Stolt CC, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, Bartsch U, Wegner M (2002) Terminal differentiation of myelinforming oligodendrocytes depends on the transcription factor Sox10. Genes Dev 16:165-170. CrossRef Medline
49. Stolt CC, Lommes P, Sock E, Chaboissier MC, Schedl A, Wegner M (2003) The Sox9 transcription factor determines glial fate choice in the developing spinal cord. Genes Dev 17:1677-1689. CrossRef Medline
50. Tawk M, Makoukji J, Belle M, Fonte C, Trousson A, Hawkins T, Li H, Ghandour S, Schumacher M, Massaad C (2011) Wnt/β-catenin signaling is an essential and direct driver of myelin gene expression and myelinogenesis. J Neurosci 31:3729-3742. CrossRef Medline
51. Wu M, Hernandez M, Shen S, Sabo JK, Kelkar D, Wang J, O'Leary R, Phillips GR, Cate HS, Casaccia P (2012) Differential modulation of the oligodendrocyte transcriptome by sonic hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation. J Neurosci 32:6651-6664. CrossRef Medline
52. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12:829-838. CrossRef Medline
53. Yuan X, Chittajallu R, Belachew S, Anderson S, McBain CJ, Gallo V (2002) Expression of the green fluorescent protein in the oligodendrocyte lineage: a transgenic mouse for developmental and physiological studies. J Neurosci Res 70:529-545. CrossRef Medline
54. Yu W, McDonnell K, Taketo MM, Bai CB (2008) Wnt signaling determines ventral spinal cord cell fates in a time-dependent manner. Development 135:3687-3696. CrossRef Medline
55. Yu Y, Chen Y, Kim B, Wang H, Zhao C, He X, Liu L, Liu W, Wu LM, Mao M, Chan JR, Wu J, Lu QR (2013) Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 152:248-261. CrossRef Medline
56. Zhang J, Huang K, Shi Z, Zou J, Wang Y, Jia Z, Zhang A, Han L, Yue X, Liu N, Jiang T, You Y, Pu P, Kang C (2011) Highβ-catenin/Tcf-4 activity confers glioma progression via direct regulation of AKT2 gene expression. Neuro Oncol 13:600-609. CrossRef Medline