Nuclear myosin 1c facilitates the chromatin modifications required to activate rRNA gene transcription and cell cycle progression

• Published in: PLoS genetics 2013-03, Vol.9 (3), p.e1003397-e1003397
• Main Authors: Sarshad, Aishe, Sadeghifar, Fatemeh, Louvet, Emilie, Mori, Raffaele, Böhm, Stefanie, Al-Muzzaini, Bader, Vintermist, Anna, Fomproix, Nathalie, Östlund, Ann-Kristin, Percipalle, Piergiorgio
• Format: Article
• Language: English
• Subjects: Acetylation; Actins; Actins - genetics; Actins - metabolism; Adenosine Triphosphatases; Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - metabolism; Basic Medicine; Biology; Biosynthesis; Cell Biology; Cell cycle; Cell Cycle Checkpoints; Cell Nucleus; Cell Nucleus - metabolism; Cell- och molekylärbiologi; cellbiologi; Chromatin; Chromatin Assembly and Disassembly; Chromatin Assembly and Disassembly - genetics; Chromosomal Proteins; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - metabolism; Experiments; Genes; Genetic; Genetic aspects; Genetic transcription; Genetics; Health aspects; HEK293 Cells; HeLa Cells; Histone-Lysine N-Methyltransferase; Histone-Lysine N-Methyltransferase - metabolism; Humans; Medicin och hälsovetenskap; Medicinska grundvetenskaper; Medicinska och farmaceutiska grundvetenskaper; metabolism; Myosin; Myosin Type I; Myosin Type I - genetics; Myosin Type I - metabolism; Non-Histone; Physiological aspects; Promoter Regions; Promoter Regions, Genetic; Protein Binding; Proteins; Ribosomal; RNA; RNA Polymerase I; RNA Polymerase I - metabolism; RNA, Ribosomal - genetics; RNA, Ribosomal - metabolism; Standard deviation; Transcription; Transcription Factors; Transcription Factors - genetics; Transcription Factors - metabolism; Transcription, Genetic
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1003397

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.