SWI/SNF Enzymes Promote SOX10- Mediated Activation of Myelin Gene Expression

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Marathe, Himangi G ^a   Mehta, Gaurav ^a   Zhang, Xiaolu ^a   Datar, Ila ^a   Mehrotra, Aanchal ^a   Yeung, Kam C ^a   de la Serna, Ivana L ^a  

^a MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BRG1 PROTEIN; BRM PROTEIN; MYELIN; MYELIN BASIC PROTEIN; PROTEIN KROX20; PROTEIN SWI; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNF; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL IMMORTALIZATION; CELL STRAIN 3T3; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; FIBROBLAST; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE LOCUS; GENE MUTATION; MYELIN GENE; MYELIN PROTEIN ZERO GENE; NONHUMAN; NUCLEAR REPROGRAMMING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SCHWANN CELL; TRANSCRIPTION REGULATION; TRANSIENT TRANSFECTION;

ANIMALS; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA HELICASES; EARLY GROWTH RESPONSE PROTEIN 2; FLOW CYTOMETRY; IMMUNOBLOTTING; MICE; MYELIN SHEATH; NUCLEAR PROTEINS; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; SOXE TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 84880471468     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069037     Document Type: Article

References (59)

1. Pereira JA, Lebrun-Julien F, Suter U, (2012) Molecular mechanisms regulating myelination in the peripheral nervous system. Trends Neurosci 35: 123-134. doi:10.1016/j.tins.2011.11.006. PubMed: 22192173.
2. Stys PK, Zamponi GW, van Minnen J, Geurts JJ, (2012) Will the real multiple sclerosis please stand up? Nat Rev Neurosci 13: 507-514. doi:10.1038/nrn3275. PubMed: 22714021.
3. Berger P, Niemann A, Suter U, (2006) Schwann cells and the pathogenesis of inherited motor and sensory neuropathies (Charcot-Marie-Tooth disease). Glia 54: 243-257. doi:10.1002/glia.20386. PubMed: 16856148.
4. Britsch S, Goerich DE, Riethmacher D, Peirano RI, Rossner M, et al. (2001) The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev 15: 66-78. doi:10.1101/gad.186601. PubMed: 11156606.
5. Zhang SM, Marsh R, Ratner N, Brackenbury R, (1995) Myelin glycoprotein P0 is expressed at early stages of chicken and rat embryogenesis. J Neurosci Res 40: 241-250. doi:10.1002/jnr.490400213. PubMed: 7745617.
6. Jagalur NB, Ghazvini M, Mandemakers W, Driegen S, Maas A, et al. (2011) Functional dissection of the Oct6 Schwann cell enhancer reveals an essential role for dimeric Sox10 binding. J Neurosci 31: 8585-8594. doi:10.1523/JNEUROSCI.0659-11.2011. PubMed: 21653862.
7. Ghislain J, Charnay P, (2006) Control of myelination in Schwann cells: a Krox20 cis-regulatory element integrates Oct6, Brn2 and Sox10 activities. EMBO Rep 7: 52-58. doi:10.1038/sj.embor.7400573. PubMed: 16311519.
8. LeBlanc SE, Jang SW, Ward RM, Wrabetz L, Svaren J, (2006) Direct regulation of myelin protein zero expression by the Egr2 transactivator. J Biol Chem 281: 5453-5460. PubMed: 16373334.
9. Jones EA, Jang SW, Mager GM, Chang LW, Srinivasan R, et al. (2007) Interactions of Sox10 and Egr2 in myelin gene regulation. Neuron Glia Biol 3: 377-387. PubMed: 18634568.
10. Guth SI, Wegner M, (2008) Having it both ways: Sox protein function between conservation and innovation. Cell Mol Life Sci 65: 3000-3018. doi:10.1007/s00018-008-8138-7. PubMed: 18516494.
11. Weider M, Küspert M, Bischof M, Vogl MR, Hornig J, et al. (2012) Chromatin-remodeling factor Brg1 is required for Schwann cell differentiation and myelination. Dev Cell 23: 193-201. doi:10.1016/j.devcel.2012.05.017. PubMed: 22814607.
12. Imbalzano AN, (1998) Energy-dependent chromatin remodelers: complex complexes and their components. Crit Rev Eukaryot Gene Expr 8: 225-255. doi:10.1615/CritRevEukarGeneExpr.v8.i3-4.10. PubMed: 9807695.
13. Phelan ML, Sif S, Narlikar GJ, Kingston RE, (1999) Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol Cell 3: 247-253. doi:10.1016/S1097-2765(00)80315-9. PubMed: 10078207.
14. Belandia B, Orford RL, Hurst HC, Parker MG, (2002) Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J 21: 4094-4103. doi:10.1093/emboj/cdf412. PubMed: 12145209.
15. Hsiao PW, Fryer CJ, Trotter KW, Wang W, Archer TK, (2003) BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23: 6210-6220. doi:10.1128/MCB.23.17.6210-6220.2003. PubMed: 12917342.
16. Ito T, Yamauchi M, Nishina M, Yamamichi N, Mizutani T, et al. (2001) Identification of SWI.SNF complex subunit BAF60a as a determinant of the transactivation potential of Fos/Jun dimers. J Biol Chem 276: 2852-2857. doi:10.1074/jbc.M009633200. PubMed: 11053448.
17. Link KA, Burd CJ, Williams E, Marshall T, Rosson G, et al. (2005) BAF57 governs androgen receptor action and androgen-dependent proliferation through SWI/SNF. Mol Cell Biol 25: 2200-2215. doi:10.1128/MCB.25.6.2200-2215.2005. PubMed: 15743818.
18. Park J, Wood MA, Cole MD, (2002) BAF53 forms distinct nuclear complexes and functions as a critical c-Myc-interacting nuclear cofactor for oncogenic transformation. Mol Cell Biol 22: 1307-1316. doi:10.1128/MCB.22.5.1307-1316.2002. PubMed: 11839798.
19. Forcales SV, Albini S, Giordani L, Malecova B, Cignolo L, et al. (2012) Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J 31: 301-316. PubMed: 22068056.
20. Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, et al. (2000) A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6: 1287-1295. doi:10.1016/S1097-2765(00)00127-1. PubMed: 11163203.
21. Roberts CW, Galusha SA, McMenamin ME, Fletcher CD, Orkin SH, (2000) Haploinsufficiency of Snf5 (integrase interactor 1) predisposes to malignant rhabdoid tumors in mice. Proc Natl Acad Sci U S A 97: 13796-13800. doi:10.1073/pnas.250492697. PubMed: 11095756.
22. Klochendler-Yeivin A, Fiette L, Barra J, Muchardt C, Babinet C, et al. (2000) The murine SNF5/INI1 chromatin remodeling factor is essential for embryonic development and tumor suppression. EMBO Rep 1: 500-506. PubMed: 11263494.
23. Guidi CJ, Sands AT, Zambrowicz BP, Turner TK, Demers DA, et al. (2001) Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Mol Cell Biol 21: 3598-3603. doi:10.1128/MCB.21.10.3598-3603.2001. PubMed: 11313485.
24. de la Serna IL, Ohkawa Y, Imbalzano AN, (2006) Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 7: 461-473. doi:10.1038/nrg1882. PubMed: 16708073.
25. de la Serna IL, Carlson KA, Imbalzano AN, (2001) Mammalian SWI/SNF complexes promote MyoD-mediated muscle differentiation. Nat Genet 27: 187-190. doi:10.1038/84826. PubMed: 11175787.
26. Seo S, Richardson GA, Kroll KL, (2005) The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 132: 105-115. PubMed: 15576411.
27. Pedersen TA, Kowenz-Leutz E, Leutz A, Nerlov C, (2001) Cooperation between C/EBPalpha TBP/TFIIB and SWI/SNF recruiting domains is required for adipocyte differentiation. Genes Dev 15: 3208-3216. doi:10.1101/gad.209901. PubMed: 11731483.
28. de la Serna IL, Ohkawa Y, Higashi C, Dutta C, Osias J, et al. (2006) The microphthalmia-associated transcription factor requires SWI/SNF enzymes to activate melanocyte-specific genes. J Biol Chem 281: 20233-20241. doi:10.1074/jbc.M512052200. PubMed: 16648630.
29. Kowenz-Leutz E, Leutz A, (1999) A C/EBP beta isoform recruits the SWI/SNF complex to activate myeloid genes. Mol Cell 4: 735-743. doi:10.1016/S1097-2765(00)80384-6. PubMed: 10619021.
30. Limpert AS, Bai S, Narayan M, Wu J, Yoon SO, et al. (2013) NF-κB forms a complex with the chromatin remodeler BRG1 to regulate Schwann cell differentiation. J Neurosci 33: 2388-2397. doi:10.1523/JNEUROSCI.3223-12.2013. PubMed: 23392668.
31. Yu Y, Chen Y, Kim B, Wang H, Zhao C, et al. (2013) Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 152: 248-261. doi:10.1016/j.cell.2012.12.006. PubMed: 23332759.
32. Salma N, Xiao H, Mueller E, Imbalzano AN, (2004) Temporal recruitment of transcription factors and SWI/SNF chromatin-remodeling enzymes during adipogenic induction of the peroxisome proliferator-activated receptor gamma nuclear hormone receptor. Mol Cell Biol 24: 4651-4663. doi:10.1128/MCB.24.11.4651-4663.2004. PubMed: 15143161.
33. de la Serna IL, Ohkawa Y, Berkes CA, Bergstrom DA, Dacwag CS, et al. (2005) MyoD targets chromatin remodeling complexes to the myogenin locus prior to forming a stable DNA-bound complex. Mol Cell Biol 25: 3997-4009. doi:10.1128/MCB.25.10.3997-4009.2005. PubMed: 15870273.
34. Soutoglou E, Talianidis I, (2002) Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295: 1901-1904. doi:10.1126/science.1068356. PubMed: 11884757.
35. de la Serna IL, Carlson KA, Hill DA, Guidi CJ, Stephenson RO, et al. (2000) Mammalian SWI-SNF complexes contribute to activation of the hsp70 gene. Mol Cell Biol 20: 2839-2851. doi:10.1128/MCB.20.8.2839-2851.2000. PubMed: 10733587.
36. Reyes JC, Barra J, Muchardt C, Camus A, Babinet C, et al. (1998) Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha). EMBO J 17: 6979-6991. doi:10.1093/emboj/17.23.6979. PubMed: 9843504.
37. Wei Q, Miskimins WK, Miskimins R, (2004) Sox10 acts as a tissue-specific transcription factor enhancing activation of the myelin basic protein gene promoter by p27Kip1 and Sp1. J Neurosci Res 78: 796-802. doi:10.1002/jnr.20342. PubMed: 15523643.
38. Potterf SB, Furumura M, Dunn KJ, Arnheiter H, Pavan WJ, (2000) Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet 107: 1-6. doi:10.1007/s004390050001. PubMed: 10982026.
39. Nagarajan R, Svaren J, Le N, Araki T, Watson M, et al. (2001) EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron 30: 355-368. doi:10.1016/S0896-6273(01)00282-3. PubMed: 11394999.
40. Keenen B, Qi H, Saladi SV, Yeung M, de la Serna IL, (2010) Heterogeneous SWI/SNF chromatin remodeling complexes promote expression of microphthalmia-associated transcription factor target genes in melanoma. Oncogene 29: 81-92. doi:10.1038/onc.2009.304. PubMed: 19784067.
41. Peirano RI, Goerich DE, Riethmacher D, Wegner M, (2000) Protein zero gene expression is regulated by the glial transcription factor Sox10. Mol Cell Biol 20: 3198-3209. doi:10.1128/MCB.20.9.3198-3209.2000. PubMed: 10757804.
42. Küspert M, Weider M, Müller J, Hermans-Borgmeyer I, Meijer D, et al. (2012) Desert hedgehog links transcription factor Sox10 to perineurial development. J Neurosci 32: 5472-5480. doi:10.1523/JNEUROSCI.5759-11.2012. PubMed: 22514309.
43. Jang SW, Svaren J, (2009) Induction of myelin protein zero by early growth response 2 through upstream and intragenic elements. J Biol Chem 284: 20111-20120. doi:10.1074/jbc.M109.022426. PubMed: 19487693.
44. Lee M, Brennan A, Blanchard A, Zoidl G, Dong Z, et al. (1997) P0 is constitutively expressed in the rat neural crest and embryonic nerves and is negatively and positively regulated by axons to generate non-myelin-forming and myelin-forming Schwann cells, respectively. Mol Cell Neurosci 8: 336-350. doi:10.1006/mcne.1996.0589. PubMed: 9073396.
45. Stewart HJ, Morgan L, Jessen KR, Mirsky R, (1993) Changes in DNA synthesis rate in the Schwann cell lineage in vivo are correlated with the precursor--Schwann cell transition and myelination. Eur J Neurosci 5: 1136-1144. doi:10.1111/j.1460-9568.1993.tb00968.x. PubMed: 7506619.
46. LeBlanc SE, Ward RM, Svaren J, (2007) Neuropathy-associated Egr2 mutants disrupt cooperative activation of myelin protein zero by Egr2 and Sox10. Mol Cell Biol 27: 3521-3529. doi:10.1128/MCB.01689-06. PubMed: 17325040.
47. Simone C, Forcales SV, Hill DA, Imbalzano AN, Latella L, et al. (2004) p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat Genet 36: 738-743. doi:10.1038/ng1378. PubMed: 15208625.
48. Ohkawa Y, Marfella CG, Imbalzano AN, (2006) Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1. EMBO J 25: 490-501. doi:10.1038/sj.emboj.7600943. PubMed: 16424906.
49. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, et al. (2005) Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19: 1723-1734. doi:10.1101/gad.1319105. PubMed: 16024661.
50. Eroglu B, Wang G, Tu N, Sun X, Mivechi NF, (2006) Critical role of Brg1 member of the SWI/SNF chromatin remodeling complex during neurogenesis and neural crest induction in zebrafish. Dev Dyn 235: 2722-2735. doi:10.1002/dvdy.20911. PubMed: 16894598.
51. Matsumoto S, Banine F, Struve J, Xing R, Adams C, et al. (2006) Brg1 is required for murine neural stem cell maintenance and gliogenesis. Dev Biol 289: 372-383. doi:10.1016/j.ydbio.2005.10.044. PubMed: 16330018.
52. Reinke H, Hörz W, (2003) Histones are first hyperacetylated and then lose contact with the activated PHO5 promoter. Mol Cell 11: 1599-1607. doi:10.1016/S1097-2765(03)00186-2. PubMed: 12820972.
53. Bryant GO, Prabhu V, Floer M, Wang X, Spagna D, et al. (2008) Activator control of nucleosome occupancy in activation and repression of transcription. PLOS Biol 6: 2928-2939. PubMed: 19108605.
54. Svaren J, Meijer D, (2008) The molecular machinery of myelin gene transcription in Schwann cells. Glia 56: 1541-1551. doi:10.1002/glia.20767. PubMed: 18803322.
55. Wegner M, (2005) Secrets to a healthy Sox life: lessons for melanocytes. Pigment Cell Res 18: 74-85. doi:10.1111/j.1600-0749.2005.00218.x. PubMed: 15760336.
56. Tapscott SJ, Davis RL, Thayer MJ, Cheng PF, Weintraub H, et al. (1988) MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts. Science 242: 405-411. doi:10.1126/science.3175662. PubMed: 3175662.
57. Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, et al. (1989) Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci U S A 86: 5434-5438. doi:10.1073/pnas.86.14.5434. PubMed: 2748593.
58. Weintraub H, Dwarki VJ, Verma I, Davis R, Hollenberg S, et al. (1991) Muscle-specific transcriptional activation by MyoD. Genes Dev 5: 1377-1386. doi:10.1101/gad.5.8.1377. PubMed: 1651276.
59. Penn BH, Bergstrom DA, Dilworth FJ, Bengal E, Tapscott SJ, (2004) A MyoD-generated feed-forward circuit temporally patterns gene expression during skeletal muscle differentiation. Genes Dev 18: 2348-2353. doi:10.1101/gad.1234304. PubMed: 15466486.