The nucleosome remodeling and deacetylase chromatin remodeling (NuRD) complex is required for peripheral nerve myelination

Journal of Neuroscience

Volumn 32, Issue 5, 2012, Pages 1517-1527

  Hung, Holly ^a,c   Kohnken, Rebecca ^c   Svaren, John ^b,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 32; DNA BINDING PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; EARLY GROWTH RESPONSE FACTOR 2; HELICASE; HISTONE DEACETYLASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; INHIBITOR OF DIFFERENTIATION 2; MEMBRANE PROTEIN; MTA2 PROTEIN; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN PROTEIN ZERO; NAB2 PROTEIN; NERVE CELL ADHESION MOLECULE L1; NOTCH1 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 6; PERIPHERAL MYELIN PROTEIN 22; PROTEIN P75; SQUALENE MONOOXYGENASE; TRANSCRIPTION FACTOR SOX10; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MICROARRAY; ELECTRON MICROSCOPY; GENE EXPRESSION; GENOTYPE; HINDLIMB; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LATENT PERIOD; MOTOR COORDINATION; MOUSE; MYELINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE C JUN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROTAROD TEST; SCHWANN CELL; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NUCLEOSOMES; PERIPHERAL NERVES; SCHWANN CELLS;

EID: 84856668802     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2895-11.2012     Document Type: Article

References (61)

1. Ayers MM, Anderson R (1975) Development of onion bulb neuropathy in the Trembler mouse. Comparison with normal nerve maturation. Acta Neuropathol 32:43-59.
2. Baloh RH, Strickland A, Ryu E, Le N, Fahrner T, Yang M, Nagarajan R, Milbrandt J (2009) Congenital hypomyelinating neuropathy with lethal conduction failure in mice carrying the Egr2 I268N mutation. J Neurosci 29:2312-2321.
3. Bermingham JR Jr, Scherer SS, O'Connell S, Arroyo E, Kalla KA, Powell FL, Rosenfeld MG (1996) Tst-1/Oct-6/SCIP regulates a unique step in peripheral myelination and is required for normal respiration. Genes Dev 10:1751-1762.
4. Blanchard AD, Sinanan A, Parmantier E, Zwart R, Broos L, Meijer D, Meier C, Jessen KR, Mirsky R (1996) Oct-6 (SCIP/Tst-1) is expressed in Schwann cell precursors, embryonic Schwann cells, and postnatal myelinating Schwann cells: comparison with Oct-1, Krox-20, and Pax-3. J Neurosci Res 46:630-640.
5. Bondurand N, Girard M, Pingault V, Lemort N, Dubourg O, Goossens M (2001) Human Connexin 32, a gap junction protein altered in the X-linked form of Charcot-Marie-Tooth disease, is directly regulated by the transcription factor SOX10. Hum Mol Genet 10:2783-2795.
6. Bremer J, O'Connor T, Tiberi C, Rehrauer H, Weis J, Aguzzi A (2010) Ablation of Dicer from murine Schwann cells increases their proliferation while blocking myelination. PLoS One 5:e12450.
7. Chen Y, Wang H, Yoon SO, Xu X, Hottiger MO, Svaren J, Nave KA, Kim HA, Olson EN, Lu QR (2011) HDAC-mediated deacetylation of NF-KB is critical for Schwann cell myelination. Nat Neurosci 14:437-441.
8. Decker L, Desmarquet-Trin-Dinh C, Taillebourg E, Ghislain J, Vallat JM, Charnay P (2006) Peripheral myelin maintenance is a dynamic process requiring constant Krox20 expression. J Neurosci 26:9771-9779.
9. Denslow SA, Wade PA (2007) The human Mi-2/NuRD complex and gene regulation. Oncogene 26:5433-5438.
10. Desmazières A, Decker L, Vallat JM, Charnay P, Gilardi-Hebenstreit P (2008) Disruption of Krox20-Nab interaction in the mouse leads to peripheral neuropathy with biphasic evolution. J Neurosci 28:5891-5900.
11. Feltri ML, D'Antonio M, Previtali S, Fasolini M, Messing A, Wrabetz L (1999) P0-Cre transgenic mice for inactivation of adhesion molecules in Schwann cells. Ann N Y Acad Sci 883:116-123.
12. Feltri ML, Graus Porta D, Previtali SC, Nodari A, Migliavacca B, Cassetti A, Littlewood-Evans A, Reichardt LF, Messing A, Quattrini A, Mueller U, Wrabetz L (2002) Conditional disruption of beta 1 integrin in Schwann cells impedes interactions with axons. J Cell Biol 156:199-209.
13. Finzsch M, Schreiner S, Kichko T, Reeh P, Tamm ER, Bösl MR, Meijer D, Wegner M (2010) Sox10 is required for Schwann cell identity and progression beyond the immature Schwann cell stage. J Cell Biol 189:701-712.
14. Friede RL, Samorajski T (1968) Myelin formation in the sciatic nerve of the rat. A quantitative electron microscopic, histochemical and radioautographic study. J Neuropathol Exp Neurol 27:546-570.
15. Garbay B, Heape AM, Sargueil F, Cassagne C (2000) Myelin synthesis in the peripheral nervous system. Prog Neurobiol 61:267-304.
16. Giese KP, Martini R, Lemke G, Soriano P, Schachner M (1992) Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell 71:565-576.
17. Gillespie CS, Sherman DL, Fleetwood-Walker SM, Cottrell DF, Tait S, Garry EM, Wallace VC, Ure J, Griffiths IR, Smith A, Brophy PJ (2000) Peripheral demyelination and neuropathic pain behavior in periaxin-deficient mice. Neuron 26:523-531.
18. He Y, Kim JY, Dupree J, Tewari A, Melendez-Vasquez C, Svaren J, Casaccia P (2010) Yy1 as a molecular link between neuregulin and transcriptional modulation of peripheral myelination. Nat Neurosci 13:1472-1480.
19. Jacob C, Christen CN, Pereira JA, Somandin C, Baggiolini A, Lötscher P, Ozçelik M, Tricaud N, Meijer D, Yamaguchi T, Matthias P, Suter U (2011) HDAC1 and HDAC2 control the transcriptional program of myelination and the survival of Schwann cells. Nat Neurosci 14:429-436.
20. Jaegle M, Mandemakers W, Broos L, Zwart R, Karis A, Visser P, Grosveld F, Meijer D (1996) The POU factor Oct-6 and Schwann cell differentiation. Science 273:507-510.
21. 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.
22. Jang SW, LeBlanc SE, Roopra A, Wrabetz L, Svaren J (2006) In vivo detection of Egr2 binding to target genes during peripheral nerve myelination. J Neurochem 98:1678-1687.
23. Jang SW, Srinivasan R, Jones EA, Sun G, Keles S, Krueger C, Chang LW, Nagarajan R, Svaren J (2010) Locus-wide identification of Egr2/Krox20 regulatory targets in myelin genes. J Neurochem 115:1409-1420.
24. Jessen KR, Mirsky R (2008) Negative regulation of myelination: relevance for development, injury, and demyelinating disease. Glia 56:1552-1565.
25. Jones EA, Lopez-Anido C, Srinivasan R, Krueger C, Chang LW, Nagarajan R, Svaren J (2011) Regulation of the PMP22 gene through an intronic enhancer. J Neurosci 31:4242-4250.
26. Kao SC, Wu H, Xie J, Chang CP, Ranish JA, Graef IA, Crabtree GR (2009) Calcineurin/NFAT signaling is required for neuregulin-regulated Schwann cell differentiation. Science 323:651-654.
27. Le N, Nagarajan R, Wang JY, Araki T, Schmidt RE, Milbrandt J (2005a) Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of Schwann cell differentiation and myelination. Proc Natl Acad Sci U S A 102:2596-2601.
28. Le N, Nagarajan R, Wang JY, Svaren J, LaPash C, Araki T, Schmidt RE, Milbrandt J (2005b) Nab proteins are essential for peripheral nervous system myelination. Nat Neurosci 8:932-940.
29. 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.
30. Lee SL, Wang Y, Milbrandt J (1996) Unimpaired macrophage differentiation and activation in mice lacking the zinc finger transplantation factor NGFI-A (EGR1). Mol Cell Biol 16:4566-4572.
31. Liu J, Casaccia P (2010) Epigenetic regulation of oligodendrocyte identity. Trends Neurosci 33:193-201.
32. -Δ ΔC(T) method. Methods 25:402-408.
33. Mager GM, Ward RM, Srinivasan R, Jang SW, Wrabetz L, Svaren J (2008) Active gene repression by the EGR2/NAB complex during peripheral nerve myelination. J Biol Chem 283:18187-18197.
34. Marfella CG, Imbalzano AN (2007) The Chd family of chromatin remodelers. Mutat Res 618:30-40.
35. Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P (2002) Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 22:10333-10345.
36. Miccio A, Blobel GA (2010) Role of the GATA-1/FOG-1/NuRD pathway in the expression of human beta-like globin genes. Mol Cell Biol 30:3460-3470.
37. Miccio A, Wang Y, Hong W, Gregory GD, Wang H, Yu X, Choi JK, Shelat S, Tong W, Poncz M, Blobel GA (2010) NuRD mediates activating and repressive functions of GATA-1 and FOG-1 during blood development. EMBO J 29:442-456.
38. Nagarajan R, Svaren J, Le N, Araki T, Watson M, Milbrandt J (2001) EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron 30:355-368.
39. Nave KA, Trapp BD (2008) Axon-glial signaling and the glial support of axon function. Annu Rev Neurosci 31:535-561.
40. Nishioka K, Chuikov S, Sarma K, Erdjument-Bromage H, Allis CD, Tempst P, Reinberg D (2002) Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev 16:479-489.
41. Parkinson DB, Bhaskaran A, Droggiti A, Dickinson S, D'Antonio M, Mirsky R, Jessen KR (2004) Krox-20 inhibits Jun-NH2-terminal kinase/c-Jun to control Schwann cell proliferation and death. J Cell Biol 164:385-394.
42. Parkinson DB, Bhaskaran A, Arthur-Farraj P, Noon LA, Woodhoo A, Lloyd AC, Feltri ML, Wrabetz L, Behrens A, Mirsky R, Jessen KR (2008) c-Jun is a negative regulator of myelination. J Cell Biol 181:625-637.
43. Pegoraro G, Misteli T (2009) The central role of chromatin maintenance in aging. Aging (Albany NY) 1:1017-1022.
44. Pereira JA, Baumann R, Norrmèn C, Somandin C, Miehe M, Jacob C, Lühmann T, Hall-Bozic H, Mantei N, Meijer D, Suter U (2010) Dicer in Schwann cells is required for myelination and axonal integrity. J Neurosci 30:6763-6775.
45. Ramírez J, Hagman J (2009) The Mi-2/NuRD complex: a critical epigenetic regulator of hematopoietic development, differentiation and cancer. Epigenetics 4:532-536.
46. Russo MW, Sevetson BR, Milbrandt J (1995) Identification of NAB1, a repressor of NGFI-A and Krox20 mediated transcription. Proc Natl Acad Sci U S A 92:6873-6877.
47. Scherer SS, Wrabetz L (2008) Molecular mechanisms of inherited demyelinating neuropathies. Glia 56:1578-1589.
48. Scherer SS, Wang DY, Kuhn R, Lemke G, Wrabetz L, Kamholz J (1994) Axons regulate Schwann cell expression of the POU transcription factor SCIP. J Neurosci 14:1930-1942.
49. Srinivasan R, Mager GM, Ward RM, Mayer J, Svaren J (2006) NAB2 represses transcription by interacting with the CHD4 subunit of the NuRD complex. J Biol Chem 281:15129-15137.
50. Svaren J, Sevetson BR, Apel ED, Zimonjic DB, Popescu NC, Milbrandt J (1996) NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol Cell Biol 16:3545-3553.
51. Topilko P, Schneider-Maunoury S, Levi G, Baron-Van Evercooren A, Chennoufi AB, Seitanidou T, Babinet C, Charnay P (1994) Krox-20 controls myelination in the peripheral nervous system. Nature 371:796-799.
52. Topilko P, Levi G, Merlo G, Mantero S, Desmarquet C, Mancardi G, Charnay P (1997) Differential regulation of the zinc finger genes Krox-20 and Krox-24 (Egr-1) suggests antagonistic roles in Schwann cells. J Neurosci Res 50:702-712.
53. Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W, Liang J, Sun L, Yang X, Shi L, Li R, Li Y, Zhang Y, Li Q, Yi X, Shang Y (2009) LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138:660-672.
54. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138:1019-1031.
55. Williams CJ, Naito T, Arco PG, Seavitt JR, Cashman SM, De Souza B, Qi X, Keables P, Von Andrian UH, Georgopoulos K (2004) The chromatin remodeler Mi-2beta is required for CD4 expression and T cell development. Immunity 20:719-733.
56. Woodhoo A, Alonso MB, Droggiti A, Turmaine M, D'Antonio M, Parkinson DB, Wilton DK, Al-Shawi R, Simons P, Shen J, Guillemot F, Radtke F, Meijer D, Feltri ML, Wrabetz L, Mirsky R, Jessen KR (2009) Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 12:839-847.
57. 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) HDAC1andHDAC2regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12:829-838.
58. Yoshida T, Hazan I, Zhang J, Ng SY, Naito T, Snippert HJ, Heller EJ, Qi X, Lawton LN, Williams CJ, Georgopoulos K (2008) The role of the chromatin remodeler Mi-2beta in hematopoietic stem cell self-renewal and multilineage differentiation. Genes Dev 22:1174-1189.
59. Yun B, Anderegg A, Menichella D, Wrabetz L, Feltri ML, Awatramani R (2010) MicroRNA-deficient Schwann cells display congenital hypomyelination. J Neurosci 30:7722-7728.
60. Zegerman P, Canas B, Pappin D, Kouzarides T (2002) Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J Biol Chem 277:11621-11624.
61. Zorick TS, Syroid DE, Brown A, Gridley T, Lemke G (1999) Krox-20 controls SCIP expression, cell cycle exit and susceptibility to apoptosis in developing myelinating Schwann cells. Development 126:1397-1406.