title: Nuclear myosin 1c facilitates the chromatin modifications required to activate rRNA gene transcription and cell cycle progression.
abstract: Actin and nuclear myosin 1c (NM1) cooperate in RNA polymerase I (pol I) transcription. NM1 is also part of a multiprotein assembly, B-WICH, which is involved in transcription. This assembly contains the chromatin remodeling complex WICH with its subunits WSTF and SNF2h. We report here that NM1 binds SNF2h with enhanced affinity upon impairment of the actin-binding function. ChIP analysis revealed that NM1, SNF2h, and actin gene occupancies are cell cycle-dependent and require intact motor function. At the onset of cell division, when transcription is temporarily blocked, B-WICH is disassembled due to WSTF phosphorylation, to be reassembled on the active gene at exit from mitosis. NM1 gene knockdown and motor function inhibition, or stable expression of NM1 mutants that do not interact with actin or chromatin, overall repressed rRNA synthesis by stalling pol I at the gene promoter, led to chromatin alterations by changing the state of H3K9 acetylation at gene promoter, and delayed cell cycle progression. These results suggest a unique structural role for NM1 in which the interaction with SNF2h stabilizes B-WICH at the gene promoter and facilitates recruitment of the HAT PCAF. This leads to a permissive chromatin structure required for transcription activation.
authors.affiliation: Department of Cell and Molecular Biology, Karolinska Institute, Stockholm, Sweden.
authors.forename: Aishe
authors.initials: A
authors.lastname: Sarshad
authors.forename: Fatemeh
authors.initials: F
authors.lastname: Sadeghifar
authors.forename: Emilie
authors.initials: E
authors.lastname: Louvet
authors.forename: Raffaele
authors.initials: R
authors.lastname: Mori
authors.forename: Stefanie
authors.initials: S
authors.lastname: Böhm
authors.forename: Bader
authors.initials: B
authors.lastname: Al-Muzzaini
authors.forename: Anna
authors.initials: A
authors.lastname: Vintermist
authors.forename: Nathalie
authors.initials: N
authors.lastname: Fomproix
authors.forename: Ann-Kristin
authors.initials: AK
authors.lastname: Östlund
authors.forename: Piergiorgio
authors.initials: P
authors.lastname: Percipalle
mesh_terms: D000107:Acetylation; D000199:Actins / Q000235:genetics / Q000378:metabolism; D000251:Adenosine Triphosphatases / Q000235:genetics / Q000378:metabolism; D059447:Cell Cycle Checkpoints; D002467:Cell Nucleus / Q000378:metabolism; D042002:Chromatin Assembly and Disassembly / Q000235:genetics*; D002868:Chromosomal Proteins, Non-Histone / Q000235:genetics / Q000378:metabolism; D057809:HEK293 Cells; D006367:HeLa Cells; D011495:Histone-Lysine N-Methyltransferase / Q000378:metabolism; D006801:Humans; D024461:Myosin Type I / Q000235:genetics / Q000378:metabolism; D011401:Promoter Regions, Genetic; D011485:Protein Binding; D012318:RNA Polymerase I / Q000378:metabolism; D012335:RNA, Ribosomal / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism; D014158:Transcription, Genetic; D000092468:Bromodomain Containing Proteins
chemical_list: D000199:Actins; D000251:Adenosine Triphosphatases; D002868:Chromosomal Proteins, Non-Histone; D011495:Histone-Lysine N-Methyltransferase; D024461:Myosin Type I; D012318:RNA Polymerase I; D012335:RNA, Ribosomal; D014157:Transcription Factors; C116750:BAZ1B protein, human; D000092468:Bromodomain Containing Proteins; C409462:SMARCA5 protein, human; C460367:MYO1C protein, human
references.citation: J Cell Biol. 1996 Apr;133(2):235-46
references.pmid: 8609158
references.citation: Biochem Cell Biol. 2006 Aug;84(4):418-26
references.pmid: 16936815
references.citation: Proc Natl Acad Sci U S A. 2010 Apr 13;107(15):6799-804
references.pmid: 20351242
references.citation: Cell. 2008 Jul 11;134(1):74-84
references.pmid: 18614012
references.citation: Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9357-9
references.pmid: 10944206
references.citation: PLoS One. 2011 Apr 29;6(4):e19184
references.pmid: 21559432
references.citation: EMBO Rep. 2006 May;7(5):525-30
references.pmid: 16514417
references.citation: Biochem Cell Biol. 2009 Feb;87(1):283-306
references.pmid: 19234542
references.citation: J Biol Chem. 1999 Jul 30;274(31):21575-80
references.pmid: 10419463
references.citation: Curr Opin Cell Biol. 2006 Jun;18(3):267-74
references.pmid: 16574391
references.citation: Mol Biol Cell. 2005 Jun;16(6):2862-71
references.pmid: 15814843
references.citation: Annu Rev Cell Dev Biol. 2008;24:131-57
references.pmid: 18616426
references.citation: J Biol Chem. 2002 Jun 14;277(24):21514-21
references.pmid: 11940582
references.citation: Nature. 2007 Jun 7;447(7145):730-4
references.pmid: 17554310
references.citation: Curr Opin Cell Biol. 2004 Feb;16(1):61-7
references.pmid: 15037306
references.citation: Nat Struct Mol Biol. 2005 Sep;12(9):742-6
references.pmid: 16142228
references.citation: Cold Spring Harb Perspect Biol. 2010 Apr;2(4):a000620
references.pmid: 20452941
references.citation: Nat Cell Biol. 2011 Nov 02;13(11):1282-8
references.pmid: 22048410
references.citation: J Cell Biol. 1996 Apr;133(2):225-34
references.pmid: 8609157
references.citation: J Cell Biol. 2008 Dec 29;183(7):1259-74
references.pmid: 19103806
references.citation: J Biol Chem. 2006 Jun 16;281(24):16264-71
references.pmid: 16603771
references.citation: J Biol Chem. 2009 Nov 20;284(47):32472-82
references.pmid: 19776015
references.citation: J Cell Biol. 1996 Mar;132(6):1053-60
references.pmid: 8601584
references.citation: Mol Biol Cell. 2002 Jan;13(1):25-39
references.pmid: 11809820
references.citation: Mol Cell Biol. 2008 Oct;28(20):6342-57
references.pmid: 18710935
references.citation: Nat Cell Biol. 2004 Dec;6(12):1165-72
references.pmid: 15558034
references.citation: Exp Cell Res. 2004 Mar 10;294(1):140-8
references.pmid: 14980509
references.citation: Curr Opin Genet Dev. 2006 Apr;16(2):191-6
references.pmid: 16495046
references.citation: Methods Mol Biol. 2012;809:519-33
references.pmid: 22113298
references.citation: Nucleus. 2011 Jan-Feb;2(1):72-9
references.pmid: 21647301
references.citation: Mol Biol Cell. 2006 Jun;17(6):2537-46
references.pmid: 16540521
references.citation: Biochem Soc Trans. 2005 Dec;33(Pt 6):1441-3
references.pmid: 16246141
references.citation: BMC Cell Biol. 2003 Jun 03;4:5
references.pmid: 12783627
references.citation: Proteomics. 2009 Aug;9(16):4098-101
references.pmid: 19658103
references.citation: Histochem Cell Biol. 2008 Jan;129(1):13-31
references.pmid: 18046571
references.citation: J Cell Biol. 2001 May 28;153(5):1097-110
references.pmid: 11381093
references.citation: Genes Dev. 2008 Feb 1;22(3):322-30
references.pmid: 18230700