Emerin and histone deacetylase 3 (HDAC3) cooperatively regulate expression and nuclear positions of MyoD, Myf5, and Pax7 genes during myogenesis

Chromosome Research

Volumn 21, Issue 8, 2013, Pages 765-779

  Demmerle, Justin ^a,b   Koch, Adam J ^a   Holaska, James M ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Chromatin remodeling; Emerin; HDAC3; Lamina; Myogenesis; Nuclear organization nuclear; Nucleoskeleton

Indexed keywords

EMERIN; HISTONE DEACETYLASE 3; MYOD PROTEIN; MYOGENIC FACTOR 5; TRANSCRIPTION FACTOR PAX7;

ANIMAL CELL; ARTICLE; BIOCATALYSIS; CELL DIFFERENTIATION; CELL NUCLEUS MEMBRANE; CHROMATIN; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE LOCUS; GENE REPRESSION; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; MYOD GENE; MYOGENIC FACTOR 5 GENE; NONHUMAN; NUCLEAR LAMINA; PRIORITY JOURNAL; SPATIOTEMPORAL ANALYSIS; STEM CELL CULTURE; TRANSCRIPTION FACTOR PAX7 GENE; TRANSCRIPTION INITIATION; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL NUCLEUS; CELL PROLIFERATION; CHROMATIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; HISTONE DEACETYLASES; MEMBRANE PROTEINS; MICE; MUSCLE DEVELOPMENT; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; NUCLEAR PROTEINS; PAX7 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 84891808429     PISSN: 09673849     EISSN: 15736849     Source Type: Journal    
DOI: 10.1007/s10577-013-9381-9     Document Type: Article

References (47)

1. Bakay M, Wang Z, Melcon G et al (2006) Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 129:996-1013. doi: 10.1093/brain/awl023
2. Barnes PJ (2003) Theophylline: new perspectives for an old drug. Am J Respir Crit Care Med 167:813-818. doi: 10.1164/rccm.200210-1142PP
3. Berk JM, Tifft KE, Wilson KL (2013) The nuclear envelope LEM-domain protein emerin. Nucleus 4(4):298-314. doi: 10.4161/nucl.25751
4. Cao Y, Yao Z, Sarkar D et al (2010) Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 18:662-674. doi: 10.1016/j.devcel.2010.02.014
5. Demmerle J, Koch AJ, Holaska JM (2012) The Nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J Biol Chem 287:22080-22088. doi: 10.1074/jbc.M111.325308
6. Finlan LE, Sproul D, Thomson I et al (2008) Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4(3):e1000039. doi: 10.1371/journal.pgen.1000039
7. Frock RL, Kudlow BA, Evans AM et al (2006) Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev 20:486-500. doi: 10.1101/gad.1364906
8. Guelen L, Pagie L, Brasset E et al (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948-951
9. Holaska JM (2008) Emerin and the nuclear lamina in muscle and cardiac disease. Circ Res 103:16-23. doi: 10.1161/CIRCRESAHA.108.172197
10. Holaska JM, Wilson KL (2007) An emerin "proteome": purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture. Biochemistry 46:8897-8908. doi: 10.1021/bi602636m
11. Holaska JM, Lee KK, Kowalski AK, Wilson KL (2003) Transcriptional repressor germ cell-less (GCL) and barrier to autointegration factor (BAF) compete for binding to emerin in vitro. J Biol Chem 278:6969-6975. doi: 10.1074/jbc.M208811200
12. Holaska JM, Kowalski AK, Wilson KL (2004) Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLoS Biol 2:E231. doi: 10.1371/journal.pbio.0020231
13. Holaska JM, Rais-Bahrami S, Wilson KL (2006) Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum Mol Genet 15:3459-3472. doi: 10.1093/hmg/ddl423
14. Huber MD, Guan T, Gerace L (2009) Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation. Mol Cell Biol 29:5718-5728. doi: 10.1128/MCB.00270-09
15. Ikegami K, Egelhofer TA, Strome S, Lieb JD (2010) Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2. Genome Biol 11:R120. doi: 10.1186/gb-2010-11-12-r120
16. Ito K, Lim S, Caramori G et al (2002) A molecular mechanism of action of theophylline: Induction of histone deacetylase activity to decrease inflammatory gene expression. Proc Natl Acad Sci U S A 99:8921-8926. doi: 10.1073/pnas.132556899
17. Karalaki M, Fili S, Philippou A, Koutsilieris M (2009) Muscle regeneration: cellular and molecular events. In Vivo 23:779-796
18. Kind J, Pagie L, Ortabozkoyun H et al (2013) Single-cell dynamics of genome-nuclear lamina interactions. Cell 153:178-192. doi: 10.1016/j.cell.2013. 02.028
19. Koch AJ, Holaska JM (2012) Loss of emerin alters myogenic signaling and miRNA Expression in mouse myogenic progenitors. PLoS ONE 7:e37262. doi: 10.1371/journal.pone.0037262.t002
20. Kuang S, Gillespie MA, Rudnicki MA (2008) Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2:22-31. doi: 10.1016/j.stem.2007.12.012
21. Lagha M, Sato T, Bajard L et al (2008) Regulation of skeletal muscle stem cell behavior by Pax3 and Pax7. Cold Spring Harb Symp Quant Biol 73:307-315. doi: 10.1101/sqb.2008.73.006
22. Lee KK, Haraguchi T, Lee RS et al (2001) Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci 114:4567-4573
23. Lee H, Quinn JC, Prasanth KV et al (2006) PIAS1 confers DNA-binding specificity on the Msx1 homeoprotein. Genes Dev 20:784-794. doi: 10.1101/gad.1392006
24. Meaburn KJ, Cabuy E, Bonne G et al (2007) Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 6:139-153. doi: 10.1111/j.1474-9726.2007.00270.x
25. Mehta IS, Amira M, Harvey AJ, Bridger JM (2010) Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol 11:R5. doi: 10.1186/gb-2010-11-1-r5
26. Melcon G, Kozlov S, Cutler DA et al (2006) Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum Mol Genet 15:637-651. doi: 10.1093/hmg/ddi479
27. Mewborn SK, Puckelwartz MJ, Abuisneineh F et al (2010) Altered chromosomal positioning, compaction, and gene expression with a Lamin A/C gene mutation. PLoS ONE 5:e14342. doi: 10.1371/journal.pone.0014342.t002
28. Misteli T (2010) Higher-order genome organization in human disease. Cold Spring Harb Perspect Biol 2:a000794. doi: 10.1101/cshperspect.a000794
29. Muchir A, Worman HJ (2007) Emery-Dreifuss muscular dystrophy. Curr Neurol Neurosci Rep 7:78-83. doi: 10.1007/s11910-007-0025-3
30. Ognibene A, Sabatelli P, Petrini S et al (1999) Nuclear changes in a case of X-linked Emery-Dreifuss muscular dystrophy. Muscle Nerve 22:864-869
31. Peric-Hupkes D, van Steensel B (2011) Role of the nuclear lamina in genome organization and gene expression. Cold Spring Harb Symp Quant Biol 75:517-524. doi: 10.1101/sqb.2010.75.014
32. Peric-Hupkes D, Meuleman W, Pagie L et al (2010) Molecular maps of the reorganization of genome-Nuclear lamina interactions during differentiation. Mol Cell 38:603-613. doi: 10.1016/j.molcel.2010.03.016
33. Pickersgill H, Kalverda B, de Wit E et al (2006) Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet 38:1005-1014. doi: 10.1038/ng1852
34. Reddy KL, Zullo JM, Bertolino E, Singh H (2008) Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 452:243-247. doi: 10.1038/nature06727
35. Rudnicki MA, Le Grand F, McKinnell I, Kuang S (2008) The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 73:323-331. doi: 10.1101/sqb.2008.73.064
36. Salpingidou G, Smertenko A, Hausmanowa-Petrucewicz I et al (2007) A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. J Cell Biol 178:897-904. doi: 10.1083/jcb.200702026
37. Simon DN, Wilson KL (2013) Partners and post-translational modifications of nuclear lamins. Chromosoma 122:13-31. doi: 10.1007/s00412-013-0399-8
38. Solovei I, Cavallo A, Schermelleh L et al (2002) Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 276:10-23. doi: 10.1006/excr.2002.5513
39. Somech R, Shaklai S, Geller O et al (2005) The nuclear-envelope protein and transcriptional repressor LAP2beta interacts with HDAC3 at the nuclear periphery, and induces histone H4 deacetylation. J Cell Sci 118:4017-4025. doi: 10.1242/jcs.02521
40. Tang J, Yan H, Zhuang S (2013) Histone deacetylases as targets for treatment of multiple diseases. Clin Sci 124:651-662. doi: 10.1042/CS20120504
41. Van De Vosse DW, Wan Y, Wozniak RW, Aitchison JD (2010) Role of the nuclear envelope in genome organization and gene expression. WIREs Syst Biol Med 3:147-166. doi: 10.1002/wsbm.101
42. Wang YX, Rudnicki MA (2011) Satellite cells, the engines of muscle repair. Nat Rev Mol Cell Biol 13:127-133. doi: 10.1038/nrm3265
43. Wilson KL, Berk JM (2010) The nuclear envelope at a glance. J Cell Sci 123:1973-1978. doi: 10.1242/jcs.019042
44. Yao J, Fetter RD, Hu P et al (2011) Subnuclear segregation of genes and core promoter factors in myogenesis. Genes Dev 25:569-580. doi: 10.1101/gad.2021411
45. Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006a) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54:1177-1191. doi: 10.1369/jhc.6R6995.2006
46. Zammit PS, Relaix F, Nagata Y et al (2006b) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824-1832. doi: 10.1242/jcs.02908
47. Zullo JM, Demarco IA, Pique-Regi R et al (2012) DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149:1474-1487. doi: 10.1016/j.cell.2012.04.035