A novel chromatin‐forming histone H1 homologue is encoded by a dispensable and growth‐regulated gene in <i>Bordetella pertussis</i>

Scarlato, Vincenzo; Aricò, Beatrice; Goyard, Sophie; Ricci, Stefano; Manetti, Riccardo; Prugnola, Anna; Manetti, Roberto; Polverino-De-Laureto, Patrizia; Ullmann, Agnès; Rappuoli, Rino

doi:10.1111/j.1365-2958.1995.tb02357.x

Cited by 20 publications

(23 citation statements)

References 42 publications

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“…Furthermore, this type of regulation is not typical of genes in GAS strain JRS4 either, since we found that the expression of two housekeeping genes, recA and rpsL, remained constant from mid-exponential phase until at least 2 h into stationary phase. The few examples of genes in other bacteria that are expressed only in exponential phase include those encoding small DNA-binding proteins, such as the nucleoid-associated proteins Fis in E. coli and the histone H1 homolog BPH1 in B. pertussis (51,67), genes encoding cell-surface virulence factors in S. aureus (6,29,63), and the regulator abrB in Bacillus subtilis (39,61). The mechanism involved in stationary-phase shutoff has not been completely elucidated in any case, although in S. aureus it involves the complex control network including the regulatory factors Sar, Agr, and Xpr (13,27,55).…”

Section: Discussionmentioning

confidence: 99%

Role of mga in growth phase regulation of virulence genes of the group A streptococcus

1997

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To determine whether growth phase affects the expression of mga and other virulence-associated genes in the group A streptococcus (GAS), total RNA was isolated from the serotype M6 GAS strain JRS4 at different phases of growth and transcript levels were quantitated by hybridization with radiolabeled DNA probes. Expression of mga (which encodes a multiple gene regulator) and the Mga-regulated genes emm (which encodes M protein) and scpA (which encodes a complement C5a peptidase) was found to be maximal in exponential phase and shut off as the bacteria entered stationary phase, while the housekeeping genes recA and rpsL showed constant transcript levels over the same period of growth. Expression of mga from a foreign phage promoter in a mga-deleted GAS strain (JRS519) altered the wild-type growth phase-dependent transcription profile seen for emm and scpA, as well as for mga. Therefore, the temporal control of mga expression requires its upstream promoter region, and the subsequent growth phase regulation of emm and scpA is Mga dependent. A number of putative virulence genes in JRS4 were shown not to require Mga for their expression, although several exhibited growth phase-dependent regulation that was similar to mga, i.e., slo (which encodes streptolysin O) and plr (encoding the plasmin receptor/glyceraldehyde-3-phosphate dehydrogenase). Still others showed a markedly different pattern of expression (the genes for the superantigen toxins MF and SpeC). These results suggest the existence of complex levels of global regulation sensitive to growth phase that directly control the expression of virulence genes and mga in GAS.

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Section: Discussionmentioning

confidence: 99%

Role of mga in growth phase regulation of virulence genes of the group A streptococcus

1997

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“…As shown in Fig. 1, several proteins were identified: the BpH1 protein (which migrates with an apparent molecular mass of 30 kDa) described recently by Scarlato et al (29) was eluted at 600 mM NaCl; in addition, two proteins (of approximately 16 and 9 kDa) were eluted at 800 mM NaCl and an 18-kDa protein eluted at 1 M NaCl.…”

Section: Resultsmentioning

confidence: 99%

“…Scarlato et al (29) have described the isolation of BpH1, a histone H1 homolog in B. pertussis, by Southwestern blot techniques; they also detected additional protein bands of lower molecular weights that can also bind to DNA. In order to identify these DNA-binding proteins, crude extracts of B. pertussis 18323 were subjected to affinity chromatography on a heparin-Sepharose column as described in Materials and Methods.…”

Section: Resultsmentioning

confidence: 99%

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Identification and characterization of BpH2, a novel histone H1 homolog in Bordetella pertussis

Goyard

1996

J Bacteriol

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A basic protein, BpH2, with an apparent molecular mass of 18 kDa was purified from Bordetella pertussis, and the corresponding gene, bph2, was cloned. Sequence analysis revealed some homology to the H1 class of eukaryotic histones and to AlgP protein of Pseudomonas aeruginosa. BpH2 binds both single-and double-stranded DNA in a nonspecific manner. Deletion of the corresponding gene in B. pertussis generated a BpH2 null mutant with an altered growth rate in which the expression of two virulence factors, adenylate cyclase-hemolysin (CyaA) and filamentous hemagglutinin (FhaB), was reduced. It is suggested that BpH2 may exhibit specific regulatory functions through its interaction with chromosomal DNA.Eubacteria maintain their DNA in a negatively supercoiled form, achieved by DNA topoisomerase and by architectural elements called histone-like proteins. Among these, the best characterized are HU, HNS, and IHF (10,20,24). These chromatin-associated proteins organize the bacterial chromosome and also exert regulatory influence on transcription, recombination, and DNA replication (11,20,30,35). For many pathogenic bacteria, it has been suggested that the expression of certain virulence genes, which are regulated by a specific regulatory element, can also be affected by DNA topology (9). In line with this hypothesis, a new class of chromatin-associated proteins which present homology with the eukaryotic histone H1 protein have been found in some pathogenic bacteria. These proteins include the Hc1 and Hc2 proteins of Chlamydia species (15,16,23) and the AlgP protein of Pseudomonas aeruginosa (8). It has been established that AlgP is involved in the regulation of the algD gene, which plays a key role in mucoidy, necessary for virulence of this bacterium (7,8,17). Recently, Scarlato et al. (29) have identified and characterized BpH1, a new member of the family with homology to histone H1 which is involved in chromatin formation in Bordetella pertussis (29). B. pertussis, the etiological agent of whooping cough, encodes a large number of virulence factors, including pertussis toxin (Ptx), filamentous hemagglutinin (FhaB), and adenylate cyclase-hemolysin (CyaA) (6, 36). The expression of virulence factors in Bordetella species is coordinately regulated by the bvg locus, which encodes two proteins, BvgA and BvgS, members of the histidine-kinase response regulator family of signal transduction systems (2,26,33). Mutations in the bvg locus abolish the expression of virulence factors and result in avirulent-phase bacteria.In the present paper, I report the identification of a second protein of B. pertussis, with homology to eukaryotic histone H1 protein, named BpH2. The bph2 gene has been sequenced, and the deduced amino acid sequence showed homology with eukaryotic histone H1 proteins and AlgP of P. aeruginosa. The BpH2 protein was purified, and its interaction with DNA in vitro was analyzed. A B. pertussis strain lacking the bph2 gene was constructed, and the effects of the deletion on growth rate and on the expression of two v...

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“…In animal cells, the chromatin found in interphase nuclei contains DNA molecules and nuclear proteins, including histones (4,5,25,(32)(33)(34). The nuclei of interphase cells contain chromatin located within a specific territory or ''domain'' (5,29,31).…”

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Differences in spatial localization and chromatin pattern during different phases of cell cycle between normal and cancer cells

et al. 1997

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We studied differences in chromatin patterns and the spatial localization of centromeres of chromosome 11 during the cell cycle between normal peripheral blood lymphocytes (PBL) and human promyclocytic leukemia cells (HL‐60) using fluorescence in situ hybridization. The pericentromeres in both cells were located at the periphery during Gq (quiescent) phase, but moved towards the nuclear center in G1 and mid‐S phase. During G2, the pericentromeres of PBL continued to move towards the nuclear center whereas those of HL‐60 returned to the periphery. The angle defining the spatial location of two pericentromeres, in reference to the center of the nucleus, increased in PBL cells from a mean of 67° during Gq phase to 106° during G1 phase (P < 0.01), and the two pericentromeres remained wide apart throughout the entire cell cycle. In HL‐60, the angle also increased during G1, but then decreased during mid‐S and G2 phases. Both cells exhibited pericentromeric signals during Gq that were round and compact, and the entire chromatin was loosely condensed. The signal became more loose and dispersed during the G1 and mid‐S phases. The pericentromere signal varied during G2 and was generally rod‐like or bipartite with condensation of the entire chromatin or chromosome‐like. Our results suggest that subtle but important differences in spatial localization of pericentromeres are present during the interphase between normal PBL and HL‐60 cells. Cytometry 27:327–335, 1997. © 1997 Wiley‐Liss, Inc.

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A novel chromatin‐forming histone H1 homologue is encoded by a dispensable and growth‐regulated gene in Bordetella pertussis

Cited by 20 publications

References 42 publications

Role of mga in growth phase regulation of virulence genes of the group A streptococcus

Role of mga in growth phase regulation of virulence genes of the group A streptococcus

Identification and characterization of BpH2, a novel histone H1 homolog in Bordetella pertussis

Differences in spatial localization and chromatin pattern during different phases of cell cycle between normal and cancer cells

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