scholarly journals Deacetylation enhances ParB–DNA interactions affecting chromosome segregation in Streptomyces coelicolor

2020 ◽  
Vol 48 (9) ◽  
pp. 4902-4914
Author(s):  
Peng Li ◽  
Hong Zhang ◽  
Guo-Ping Zhao ◽  
Wei Zhao
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Direct Evidence ◽  
Streptomyces Coelicolor ◽  
Cell Metabolism ◽  
Lysine Acetylation ◽  
Biological Processes ◽  
Dna Interactions ◽  
Dna Binding Affinity ◽  
Metabolism Gene

Abstract Reversible lysine acetylation plays regulatory roles in diverse biological processes, including cell metabolism, gene transcription, cell apoptosis and ageing. Here, we show that lysine acetylation is involved in the regulation of chromosome segregation, a pivotal step during cell division in Streptomyces coelicolor. Specifically, deacetylation increases the DNA-binding affinity of the chromosome segregation protein ParB to the centromere-like sequence parS. Both biochemical and genetic experiments suggest that the deacetylation process is mainly modulated by a sirtuin-like deacetylase ScCobB1. The Lys-183 residue in the helix-turn-helix region of ParB is the major deacetylation site responsible for the regulation of ParB-parS binding. In-frame deletion of SccobB1 represses formation of ParB segregation complexes and leads to generation of abnormal spores. Taken together, these observations provide direct evidence that deacetylation participates in the regulation of chromosome segregation by targeting ParB in S. coelicolor.

scholarly journals Genes Required for Aerial Growth, Cell Division, and Chromosome Segregation Are Targets of WhiA before Sporulation in Streptomyces venezuelae

mBio ◽  
2013 ◽  
Vol 4 (5) ◽  
Author(s):  
Matthew J. Bush ◽  
Maureen J. Bibb ◽  
Govind Chandra ◽  
Kim C. Findlay ◽  
Mark J. Buttner
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Regulatory Networks ◽  
Liquid Culture ◽  
Biological Processes ◽  
Streptomyces Venezuelae ◽  
Content Type ◽  
Master Regulators ◽  
Aerial Growth ◽  
Genes Encoding

ABSTRACTWhiA is a highly unusual transcriptional regulator related to a family of eukaryotic homing endonucleases. WhiA is required for sporulation in the filamentous bacteriumStreptomyces, but WhiA homologues of unknown function are also found throughout the Gram-positive bacteria. To better understand the role of WhiA inStreptomycesdevelopment and its function as a transcription factor, we identified the WhiA regulon through a combination of chromatin immunoprecipitation-sequencing (ChIP-seq) and microarray transcriptional profiling, exploiting a new model organism for the genus,Streptomyces venezuelae, which sporulates in liquid culture. The regulon encompasses ~240 transcription units, and WhiA appears to function almost equally as an activator and as a repressor. Bioinformatic analysis of the upstream regions of the complete regulon, combined with DNase I footprinting, identified a short but highly conserved asymmetric sequence, GACAC, associated with the majority of WhiA targets. Construction of a null mutant showed thatwhiAis required for the initiation of sporulation septation and chromosome segregation inS. venezuelae, and several genes encoding key proteins of theStreptomycescell division machinery, such asftsZ,ftsW, andftsK, were found to be directly activated by WhiA during development. Several other genes encoding proteins with important roles in development were also identified as WhiA targets, including the sporulation-specific sigma factor σWhiGand the diguanylate cyclase CdgB. Cell division is tightly coordinated with the orderly arrest of apical growth in the sporogenic cell, andfilP, encoding a key component of the polarisome that directs apical growth, is a direct target for WhiA-mediated repression during sporulation.IMPORTANCESince the initial identification of the genetic loci required forStreptomycesdevelopment, all of thebldandwhidevelopmental master regulators have been cloned and characterized, and significant progress has been made toward understanding the cell biological processes that drive morphogenesis. A major challenge now is to connect the cell biological processes and the developmental master regulators by dissecting the regulatory networks that link the two. Studies of these regulatory networks have been greatly facilitated by the recent introduction ofStreptomyces venezuelaeas a new model system for the genus, a species that sporulates in liquid culture. Taking advantage ofS. venezuelae, we have characterized the regulon of genes directly under the control of one of these master regulators, WhiA. Our results implicate WhiA in the direct regulation of key steps in sporulation, including the cessation of aerial growth, the initiation of cell division, and chromosome segregation.

scholarly journals Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor

Open Biology ◽  
2013 ◽  
Vol 3 (3) ◽  
pp. 130006 ◽  
Author(s):  
Bartosz Ditkowski ◽  
Neil Holmes ◽  
Joanna Rydzak ◽  
Magdalena Donczew ◽  
Martyna Bezulska ◽  
...  
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Tip Growth ◽  
Streptomyces Coelicolor ◽  
Proximal Region ◽  
Cytoskeletal Protein ◽  
Mutant Form ◽  
Bacterial Cell Division ◽  
Aerial Hyphae ◽  
Dynamic Interplay

Prior to bacterial cell division, the ATP-dependent polymerization of the cytoskeletal protein, ParA, positions the newly replicated origin-proximal region of the chromosome by interacting with ParB complexes assembled on parS sites located close to the origin. During the formation of unigenomic spores from multi-genomic aerial hyphae compartments of Streptomyces coelicolor , ParA is developmentally triggered to form filaments along the hyphae; this promotes the accurate and synchronized segregation of tens of chromosomes into prespore compartments. Here, we show that in addition to being a segregation protein, ParA also interacts with the polarity protein, Scy, which is a component of the tip-organizing centre that controls tip growth. Scy recruits ParA to the hyphal tips and regulates ParA polymerization. These results are supported by the phenotype of a strain with a mutant form of ParA that uncouples ParA polymerization from Scy. We suggest that the ParA–Scy interaction coordinates the transition from hyphal elongation to sporulation.

scholarly journals Differential Requirements for the CENP-O Complex Reveal Parallel PLK1 Kinetochore Recruitment Pathways

2021 ◽  
pp. mbc.E20-11-0751
Author(s):  
Alexandra L. Nguyen ◽  
Marie Diane Fadel ◽  
Iain M. Cheeseman
Keyword(s):  
Cell Division ◽  
Cell Lines ◽  
Chromosome Segregation ◽  
Human Cell ◽  
Threshold Level ◽  
The Other ◽  
Biological Processes ◽  
Human Cell Lines ◽  
State Dependent ◽  
Genome Wide

Similar to other core biological processes, the vast majority of cell division components are essential for viability across human cell lines. However, recent genome‐wide screens have identified a number of proteins that exhibit cell line‐specific essentiality. Defining the behaviors of these proteins is critical to our understanding of complex biological processes. Here, we harness differential essentiality to reveal the contributions of the 4‐subunit centromere‐localized CENP‐O complex, whose precise function has been difficult to define. Our results support a model in which the CENP‐O complex and BUB1 act in parallel pathways to recruit a threshold level of PLK1 to mitotic kinetochores, ensuring accurate chromosome segregation. We demonstrate that targeted changes to either pathway sensitizes cells to the loss of the other component, resulting in cell‐state dependent requirements. This approach also highlights the advantage of comparing phenotypes across diverse cell lines to define critical functional contributions and behaviors that could be exploited for the targeted treatment of disease.

scholarly journals Role of an FtsK-Like Protein in Genetic Stability in Streptomyces coelicolor A3(2)

2007 ◽  
Vol 189 (6) ◽  
pp. 2310-2318 ◽  
Author(s):  
Lei Wang ◽  
Yanfei Yu ◽  
Xinyi He ◽  
Xiufen Zhou ◽  
Zixin Deng ◽  
...  
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Fluorescent Protein ◽  
Streptomyces Coelicolor ◽  
Complex Life Cycle ◽  
Specific Gene ◽  
Chromosomal Dna ◽  
Protein Fusion ◽  
Fluorescent Reporter ◽  
Green Fluorescent

ABSTRACT Streptomyces coelicolor A3(2) does not have a canonical cell division cycle during most of its complex life cycle, yet it contains a gene (ftsKSC ) encoding a protein similar to FtsK, which couples the completion of cell division and chromosome segregation in unicellular bacteria such as Escherichia coli. Here, we show that various constructed ftsKSC mutants all grew apparently normally and sporulated but upon restreaking gave rise to many aberrant colonies and to high frequencies of chloramphenicol-sensitive mutants, a phenotype previously associated with large terminal deletions from the linear chromosome. Indeed, most of the aberrant colonies had lost large fragments near one or both chromosomal termini, as if chromosome ends had failed to reach their prespore destination before the closure of sporulation septa. A constructed FtsKSC-enhanced green fluorescent protein fusion protein was particularly abundant in aerial hyphae, forming distinctive complexes before localizing to each sporulation septum, suggesting a role for FtsKSC in chromosome segregation during sporulation. Use of a fluorescent reporter showed that when ftsKSC was deleted, several spore compartments in most spore chains failed to express the late-sporulation-specific sigma factor gene sigF, even though they contained chromosomal DNA. This suggested that sigF expression is autonomously activated in each spore compartment in response to completion of chromosome transfer, which would be a previously unknown checkpoint for late-sporulation-specific gene expression. These results provide new insight into the genetic instability prevalent among streptomycetes, including those used in the industrial production of antibiotics.

scholarly journals Differential Requirements for the CENP-O Complex Reveal Parallel PLK1 Kinetochore Recruitment Pathways

2020 ◽  
Author(s):  
Alexandra L. Nguyen ◽  
Marie Diane Fadel ◽  
Iain M. Cheeseman
Keyword(s):  
Cell Division ◽  
Cell Lines ◽  
Chromosome Segregation ◽  
Human Cell ◽  
Threshold Level ◽  
The Other ◽  
Biological Processes ◽  
Human Cell Lines ◽  
State Dependent ◽  
Genome Wide

AbstractSimilar to other core biological processes, the vast majority of cell division components are essential for viability across human cell lines. However, genome-wide screens have identified a number of proteins that exhibit cell line-specific essentiality. Defining the behaviors of these proteins is critical to our understanding of complex biological processes. Here, we harness differential essentiality to reveal the contributions of the 4-subunit centromere-localized CENP-O complex, whose precise function has been difficult to define. Our results support a model in which the CENP-O complex and BUB1 act in parallel pathways to recruit a threshold level of PLK1 to mitotic kinetochores, ensuring accurate chromosome segregation. We demonstrate that targeted changes to either pathway sensitizes cells to the loss of the other component, resulting in cell-state dependent requirements. This approach also highlights the advantage of comparing phenotypes across diverse cell lines to define critical functional contributions and behaviors that could be exploited for the targeted treatment of disease.

scholarly journals Pulling in new directions: Myosin 2, Piezo, and metabolism

F1000Research ◽  
2019 ◽  
Vol 8 ◽  
pp. 1486 ◽  
Author(s):  
Melissa A. Quintanilla ◽  
John A. Hammer III ◽  
Jordan R. Beach
Keyword(s):  
Cell Migration ◽  
Cell Division ◽  
Ion Channels ◽  
Cell Metabolism ◽  
Biological Processes ◽  
New Directions ◽  
Impact Tension

Myosin 2 plays a central role in numerous, fundamental, actin-based biological processes, including cell migration, cell division, and the adhesion of cells to substrates and other cells. Here, we highlight recent studies in which the forces created by actomyosin 2 have been shown to also impact tension-sensitive ion channels and cell metabolism.

scholarly journals The SUMO-Specific Protease SENP5 Is Required for Cell Division

2006 ◽  
Vol 26 (12) ◽  
pp. 4489-4498 ◽  
Author(s):  
Alessandra Di Bacco ◽  
Jian Ouyang ◽  
Hsiang-Ying Lee ◽  
Andre Catic ◽  
Hidde Ploegh ◽  
...  
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Posttranslational Modification ◽  
Catalytic Domain ◽  
Biological Processes ◽  
Nucleocytoplasmic Trafficking ◽  
Binucleate Cells ◽  
Specific Protease

ABSTRACT Posttranslational modification of substrates by the small ubiquitin-like modifier, SUMO, regulates diverse biological processes, including transcription, DNA repair, nucleocytoplasmic trafficking, and chromosome segregation. SUMOylation is reversible, and several mammalian homologs of the yeast SUMO-specific protease Ulp1, termed SENPs, have been identified. We demonstrate here that SENP5, a previously uncharacterized Ulp1 homolog, has SUMO C-terminal hydrolase and SUMO isopeptidase activities. In contrast to other SENPs, the C-terminal catalytic domain of SENP5 preferentially processed SUMO-3 compared to SUMO-1 precursors and preferentially removed SUMO-2 and SUMO-3 from SUMO-modified RanGAP1 in vitro. In cotransfection assays, SENP5 preferentially reduced high-molecular-weight conjugates of SUMO-2 compared to SUMO-1 in vivo. Full-length SENP5 localized to the nucleolus. Deletion of the noncatalytic N-terminal domain led to loss of nucleolar localization and increased de-SUMOylation activity in vivo. Knockdown of SENP5 by RNA interference resulted in increased levels of SUMO-1 and SUMO-2/3 conjugates, inhibition of cell proliferation, defects in nuclear morphology, and appearance of binucleate cells, revealing an essential role for SENP5 in mitosis and/or cytokinesis. These findings establish SENP5 as a SUMO-specific protease required for cell division and suggest that mechanisms involving both the catalytic and noncatalytic domains determine the distinct substrate specificities of the mammalian SUMO-specific proteases.

scholarly journals Cell division protein DivIB influences the Spo0J/Soj system of chromosome segregation in Bacillus subtilis

2004 ◽  
Vol 55 (2) ◽  
pp. 349-367 ◽  
Author(s):  
Gonçalo Real ◽  
Sabine Autret ◽  
Elizabeth J. Harry ◽  
Jeffery Errington ◽  
Adriano O. Henriques
Keyword(s):  
Bacillus Subtilis ◽  
Cell Division ◽  
Chromosome Segregation ◽  
Cell Division Protein

fumble Encodes a Pantothenate Kinase Homolog Required for Proper Mitosis and Meiosis in Drosophila melanogaster

Genetics ◽  
2001 ◽  
Vol 157 (3) ◽  
pp. 1267-1276
Author(s):  
Katayoun Afshar ◽  
Pierre Gönczy ◽  
Stephen DiNardo ◽  
Steven A Wasserman
Keyword(s):  
Cell Division ◽  
Chromosome Segregation ◽  
Cell Division Cycle ◽  
Protein Isoforms ◽  
Pantothenate Kinase ◽  
Male Germline ◽  
Dividing Cells ◽  
Mutant Cells ◽  
Mitosis And Meiosis

Abstract A number of fundamental processes comprise the cell division cycle, including spindle formation, chromosome segregation, and cytokinesis. Our current understanding of these processes has benefited from the isolation and analysis of mutants, with the meiotic divisions in the male germline of Drosophila being particularly well suited to the identification of the required genes. We show here that the fumble (fbl) gene is required for cell division in Drosophila. We find that dividing cells in fbl-deficient testes exhibit abnormalities in bipolar spindle organization, chromosome segregation, and contractile ring formation. Cytological analysis of larval neuroblasts from null mutants reveals a reduced mitotic index and the presence of polyploid cells. Molecular analysis demonstrates that fbl encodes three protein isoforms, all of which contain a domain with high similarity to the pantothenate kinases of A. nidulans and mouse. The largest Fumble isoform is dispersed in the cytoplasm during interphase, concentrates around the spindle at metaphase, and localizes to the spindle midbody at telophase. During early embryonic development, the protein localizes to areas of membrane deposition and/or rearrangement, such as the metaphase and cellularization furrows. Given the role of pantothenate kinase in production of Coenzyme A and in phospholipid biosynthesis, this pattern of localization is suggestive of a role for fbl in membrane synthesis. We propose that abnormalities in synthesis and redistribution of membranous structures during the cell division cycle underlie the cell division defects in fbl mutant cells.

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