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Article ; Online: Strict Conservation yet Non-Essential Nature of Plasmid Gene

Kasumba, Irene N / Tilly, Kit / Lin, Tao / Norris, Steven J / Rosa, Patricia A

2023 Volume 11, Issue 3, Page(s) e0047723

Abstract: The highly segmented genome of Borrelia burgdorferi, the tick-borne bacterium that causes Lyme disease, is composed of a linear chromosome and more than 20 co-existing endogenous plasmids. Many plasmid-borne genes are unique to B. burgdorferi and some ... ...

Abstract	The highly segmented genome of Borrelia burgdorferi, the tick-borne bacterium that causes Lyme disease, is composed of a linear chromosome and more than 20 co-existing endogenous plasmids. Many plasmid-borne genes are unique to B. burgdorferi and some have been shown to provide essential functions at discrete points of the infectious cycle between a tick vector and rodent host. In this study, we investigated the role of
MeSH term(s)	Mice ; Animals ; Borrelia burgdorferi/genetics ; Lyme Disease ; Plasmids/genetics ; Ixodes/genetics ; Ixodes/microbiology
Language	English
Publishing date	2023-04-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2807133-5
ISSN	2165-0497 ; 2165-0497
ISSN (online)	2165-0497
ISSN	2165-0497
DOI	10.1128/spectrum.00477-23
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Article ; Online: Functional Equivalence of OspA and OspB, but Not OspC, in Tick Colonization by Borrelia burgdorferi.

Tilly, Kit / Bestor, Aaron / Rosa, Patricia A

Infection and immunity

2016 Volume 84, Issue 5, Page(s) 1565–1573

Abstract: Borrelia burgdorferi, a Lyme disease agent, makes different major outer surface lipoproteins at different stages of its mouse-tick infectious cycle. Outer surface protein A (OspA) coats the spirochetes from the time they enter ticks until they are ... ...

Abstract	Borrelia burgdorferi, a Lyme disease agent, makes different major outer surface lipoproteins at different stages of its mouse-tick infectious cycle. Outer surface protein A (OspA) coats the spirochetes from the time they enter ticks until they are transmitted to a mammal. OspA is required for normal tick colonization and has been shown to bind a tick midgut protein, indicating that OspA may serve as a tick midgut adhesin. Tick colonization by spirochetes lacking OspA is increased when the infecting blood meal is derived from mice that do not produce antibody, indicating that OspA may protect the spirochetes from host antibody, which will not recognize tick-specific proteins such as OspA. To further study the importance of OspA during tick colonization, we constructed a form of B. burgdorferi in which the ospA open reading frame, on lp54, was replaced with the ospC gene or the ospB gene, encoding a mammal-specific or tick-specific lipoprotein, respectively. These fusions yielded a strain that produces OspC within a tick (from the fusion gene) and during early mammalian infection (from the normal ospC locus) and a strain that produces OspB in place of OspA within ticks. Here we show that the related, tick-specific protein OspB can fully substitute for OspA, whereas the unrelated, mammal-specific protein OspC cannot. These data were derived from three different methods of infecting ticks, and they confirm and extend previous studies indicating that OspA both protects spirochetes within ticks from mammalian antibody and serves an additional role during tick colonization.
MeSH term(s)	Animals ; Antibodies, Bacterial/immunology ; Antigens, Bacterial/genetics ; Antigens, Bacterial/metabolism ; Antigens, Surface/genetics ; Antigens, Surface/metabolism ; Bacterial Outer Membrane Proteins/genetics ; Bacterial Outer Membrane Proteins/metabolism ; Bacterial Vaccines/genetics ; Bacterial Vaccines/metabolism ; Borrelia burgdorferi/growth & development ; Borrelia burgdorferi/immunology ; Gene Deletion ; Gene Expression ; Lipoproteins/genetics ; Lipoproteins/metabolism ; Mice ; Mice, SCID ; Recombination, Genetic ; Ticks/microbiology
Chemical Substances	Antibodies, Bacterial ; Antigens, Bacterial ; Antigens, Surface ; Bacterial Outer Membrane Proteins ; Bacterial Vaccines ; Lipoproteins ; OspA protein ; OspC protein ; OspB protein, Borrelia burgdorferi (149719-59-5)
Language	English
Publishing date	2016-04-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	218698-6
ISSN	1098-5522 ; 0019-9567
ISSN (online)	1098-5522
ISSN	0019-9567
DOI	10.1128/IAI.00063-16
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Article ; Online: Infection history of the blood-meal host dictates pathogenic potential of the Lyme disease spirochete within the feeding tick vector.

Bhatia, Bharti / Hillman, Chad / Carracoi, Valentina / Cheff, Britney N / Tilly, Kit / Rosa, Patricia A

PLoS pathogens

2018 Volume 14, Issue 4, Page(s) e1006959

Abstract: Lyme disease in humans is caused by several genospecies of the Borrelia burgdorferi sensu lato (s.l.) complex of spirochetal bacteria, including B. burgdorferi, B. afzelii and B. garinii. These bacteria exist in nature as obligate parasites in an ... ...

Abstract	Lyme disease in humans is caused by several genospecies of the Borrelia burgdorferi sensu lato (s.l.) complex of spirochetal bacteria, including B. burgdorferi, B. afzelii and B. garinii. These bacteria exist in nature as obligate parasites in an enzootic cycle between small vertebrate hosts and Ixodid tick vectors, with humans representing incidental hosts. During the natural enzootic cycle, infected ticks in endemic areas feed not only upon naïve hosts, but also upon seropositive infected hosts. In the current study, we considered this environmental parameter and assessed the impact of the immune status of the blood-meal host on the phenotype of the Lyme disease spirochete within the tick vector. We found that blood from a seropositive host profoundly attenuates the infectivity (>104 fold) of homologous spirochetes within the tick vector without killing them. This dramatic neutralization of vector-borne spirochetes was not observed, however, when ticks and blood-meal hosts carried heterologous B. burgdorferi s.l. strains, or when mice lacking humoral immunity replaced wild-type mice as blood-meal hosts in similar experiments. Mechanistically, serum-mediated neutralization does not block induction of host-adapted OspC+ spirochetes during tick feeding, nor require tick midgut components. Significantly, this study demonstrates that strain-specific antibodies elicited by B. burgdorferi s.l. infection neutralize homologous bacteria within feeding ticks, before the Lyme disease spirochetes enter a host. The blood meal ingested from an infected host thereby prevents super-infection by homologous spirochetes, while facilitating transmission of heterologous B. burgdorferi s.l. strains. This finding suggests that Lyme disease spirochete diversity is stably maintained within endemic populations in local geographic regions through frequency-dependent selection of rare alleles of dominant polymorphic surface antigens.
MeSH term(s)	Animals ; Borrelia burgdorferi/isolation & purification ; Borrelia burgdorferi/pathogenicity ; Disease Vectors ; Host-Pathogen Interactions ; Humans ; Ixodes/growth & development ; Ixodes/microbiology ; Lyme Disease/blood ; Lyme Disease/immunology ; Lyme Disease/microbiology ; Lyme Disease/transmission ; Mice ; Mice, Inbred C57BL ; Nymph/growth & development ; Nymph/microbiology
Language	English
Publishing date	2018
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1006959
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Article ; Online: Virulence of the Lyme disease spirochete before and after the tick bloodmeal: a quantitative assessment.

Kasumba, Irene N / Bestor, Aaron / Tilly, Kit / Rosa, Patricia A

Parasites & vectors

2016 Volume 9, Page(s) 129

Abstract: Background: Borrelia burgdorferi, the tick-transmitted agent of Lyme disease, adapts to different environments as it cycles between an arthropod vector and vertebrate host. Signals encountered during nymphal tick feeding prior to transmission activate a ...

Abstract	Background: Borrelia burgdorferi, the tick-transmitted agent of Lyme disease, adapts to different environments as it cycles between an arthropod vector and vertebrate host. Signals encountered during nymphal tick feeding prior to transmission activate a regulon that is controlled by the alternative sigma factors RpoN and RpoS, which are required for mammalian infection. The ingested bloodmeal also provides nutrients that stimulate spirochete replication. Although the influence of tick feeding on spirochete growth and gene expression is well documented, a quantitative assessment of spirochete virulence before and after tick feeding has not been made. Methods: Homogenates were prepared from unfed and fed infected Ixodes scapularis nymphs that had acquired B. burgdorferi as larvae. Serially diluted tick homogenates were needle-inoculated into mice to determine the infectious dose of tick-derived spirochetes before and after the bloodmeal. Mouse infection was assessed by sero-reactivity with B. burgdorferi whole cell lysates on immunoblots and attempted isolation of spirochetes from mouse tissues. Viable spirochetes in tick-derived inocula were quantified by colony formation in solid media. Results: We found that an inoculum containing as many as 10(4) B. burgdorferi from unfed ticks is largely non-infectious, while the calculated ID50 for spirochetes from fed ticks is ~30 organisms. Engineered constitutive production of the essential virulence factor OspC by spirochetes within unfed ticks did not confer an infectious phenotype. Conclusion: Conditional priming of B. burgdorferi during tick feeding induces changes in addition to OspC that are required for infection of the mammalian host.
MeSH term(s)	Animals ; Bacterial Load ; Blood ; Borrelia burgdorferi/drug effects ; Borrelia burgdorferi/pathogenicity ; Disease Models, Animal ; Ixodes/microbiology ; Lyme Disease/microbiology ; Lyme Disease/pathology ; Mice ; Virulence
Language	English
Publishing date	2016-03-07
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	2409480-8
ISSN	1756-3305 ; 1756-3305
ISSN (online)	1756-3305
ISSN	1756-3305
DOI	10.1186/s13071-016-1380-1
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Article ; Online: Infection history of the blood-meal host dictates pathogenic potential of the Lyme disease spirochete within the feeding tick vector.

Bharti Bhatia / Chad Hillman / Valentina Carracoi / Britney N Cheff / Kit Tilly / Patricia A Rosa

PLoS Pathogens, Vol 14, Iss 4, p e

2018 Volume 1006959

Abstract	Lyme disease in humans is caused by several genospecies of the Borrelia burgdorferi sensu lato (s.l.) complex of spirochetal bacteria, including B. burgdorferi, B. afzelii and B. garinii. These bacteria exist in nature as obligate parasites in an enzootic cycle between small vertebrate hosts and Ixodid tick vectors, with humans representing incidental hosts. During the natural enzootic cycle, infected ticks in endemic areas feed not only upon naïve hosts, but also upon seropositive infected hosts. In the current study, we considered this environmental parameter and assessed the impact of the immune status of the blood-meal host on the phenotype of the Lyme disease spirochete within the tick vector. We found that blood from a seropositive host profoundly attenuates the infectivity (>104 fold) of homologous spirochetes within the tick vector without killing them. This dramatic neutralization of vector-borne spirochetes was not observed, however, when ticks and blood-meal hosts carried heterologous B. burgdorferi s.l. strains, or when mice lacking humoral immunity replaced wild-type mice as blood-meal hosts in similar experiments. Mechanistically, serum-mediated neutralization does not block induction of host-adapted OspC+ spirochetes during tick feeding, nor require tick midgut components. Significantly, this study demonstrates that strain-specific antibodies elicited by B. burgdorferi s.l. infection neutralize homologous bacteria within feeding ticks, before the Lyme disease spirochetes enter a host. The blood meal ingested from an infected host thereby prevents super-infection by homologous spirochetes, while facilitating transmission of heterologous B. burgdorferi s.l. strains. This finding suggests that Lyme disease spirochete diversity is stably maintained within endemic populations in local geographic regions through frequency-dependent selection of rare alleles of dominant polymorphic surface antigens.
Keywords	Immunologic diseases. Allergy ; RC581-607 ; Biology (General) ; QH301-705.5
Subject code	630
Language	English
Publishing date	2018-04-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
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Article ; Online: Use of an endogenous plasmid locus for stable in trans complementation in Borrelia burgdorferi.

Kasumba, Irene N / Bestor, Aaron / Tilly, Kit / Rosa, Patricia A

Applied and environmental microbiology

2015 Volume 81, Issue 3, Page(s) 1038–1046

Abstract: Targeted mutagenesis and complementation are important tools for studying genes of unknown function in the Lyme disease spirochete Borrelia burgdorferi. A standard method of complementation is reintroduction of a wild-type copy of the targeted gene on a ... ...

Abstract	Targeted mutagenesis and complementation are important tools for studying genes of unknown function in the Lyme disease spirochete Borrelia burgdorferi. A standard method of complementation is reintroduction of a wild-type copy of the targeted gene on a shuttle vector. However, shuttle vectors are present at higher copy numbers than B. burgdorferi plasmids and are potentially unstable in the absence of selection, thereby complicating analyses in the mouse-tick infectious cycle. B. burgdorferi has over 20 plasmids, with some, such as linear plasmid 25 (lp25), carrying genes required by the spirochete in vivo but relatively unstable during in vitro cultivation. We propose that complementation on an endogenous plasmid such as lp25 would overcome the copy number and in vivo stability issues of shuttle vectors. In addition, insertion of a selectable marker on lp25 could ensure its stable maintenance by spirochetes in culture. Here, we describe the construction of a multipurpose allelic-exchange vector containing a multiple-cloning site and either of two selectable markers. This suicide vector directs insertion of the complementing gene into the bbe02 locus, a site on lp25 that was previously shown to be nonessential during both in vitro and in vivo growth. We demonstrate the functional utility of this strategy by restoring infectivity to an ospC mutant through complementation at this site on lp25 and stable maintenance of the ospC gene throughout mouse infection. We conclude that this represents a convenient and widely applicable method for stable gene complementation in B. burgdorferi.
MeSH term(s)	Animals ; Borrelia burgdorferi/genetics ; Borrelia burgdorferi/growth & development ; Disease Models, Animal ; Genetic Complementation Test ; Genetic Vectors ; Genetics, Microbial/methods ; Genomic Instability ; Lyme Disease/microbiology ; Mice ; Molecular Biology/methods ; Plasmids
Language	English
Publishing date	2015-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	223011-2
ISSN	1098-5336 ; 0099-2240
ISSN (online)	1098-5336
ISSN	0099-2240
DOI	10.1128/AEM.03657-14
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Article ; Online: Long-term survival of Borrelia burgdorferi lacking the hibernation promotion factor homolog in the unfed tick vector.

Fazzino, Lisa / Tilly, Kit / Dulebohn, Daniel P / Rosa, Patricia A

Infection and immunity

2015 Volume 83, Issue 12, Page(s) 4800–4810

Abstract: Borrelia burgdorferi, a causative agent of Lyme borreliosis, is a zoonotic pathogen that survives in nutrient-limited environments within a tick, prior to transmission to its mammalian host. Survival under these prolonged nutrient-limited conditions is ... ...

Abstract	Borrelia burgdorferi, a causative agent of Lyme borreliosis, is a zoonotic pathogen that survives in nutrient-limited environments within a tick, prior to transmission to its mammalian host. Survival under these prolonged nutrient-limited conditions is thought to be similar to survival during stationary phase, which is characterized by growth cessation and decreased protein production. Multiple ribosome-associated proteins are implicated in stationary-phase survival of Escherichia coli. These proteins include hibernation-promoting factor (HPF), which dimerizes ribosomes and prevents translation of mRNA. Bioinformatic analyses indicate that B. burgdorferi harbors an hpf homolog, the bb0449 gene. BB0449 protein secondary structure modeling also predicted HPF-like structure and function. However, BB0449 protein was not localized in the ribosome-associated protein fraction of in vitro-grown B. burgdorferi. In wild-type B. burgdorferi, bb0449 transcript and BB0449 protein levels are low during various growth phases. These results are inconsistent with patterns of synthesis of HPF-like proteins in other bacterial species. In addition, two independently derived bb0449 mutants successfully completed the mouse-tick infectious cycle, indicating that bb0449 is not required for prolonged survival in the nutrient-limited environment in the unfed tick or any other stage of infection by B. burgdorferi. We suggest either that BB0449 is associated with ribosomes under specific conditions not yet identified or that BB0449 of B. burgdorferi has a function other than ribosome conformation modulation.
MeSH term(s)	Amino Acid Sequence ; Animals ; Arachnid Vectors/microbiology ; Bacterial Proteins/genetics ; Bacterial Proteins/immunology ; Base Sequence ; Borrelia burgdorferi/genetics ; Borrelia burgdorferi/pathogenicity ; Conserved Sequence ; Escherichia coli/genetics ; Escherichia coli/metabolism ; Female ; Gene Expression Regulation, Bacterial ; Hibernation/genetics ; Ixodes/growth & development ; Ixodes/microbiology ; Larva/growth & development ; Larva/microbiology ; Lyme Disease/immunology ; Lyme Disease/microbiology ; Lyme Disease/pathology ; Lyme Disease/transmission ; Mice ; Microbial Viability ; Molecular Sequence Data ; Protein Structure, Secondary ; Recombinant Proteins/genetics ; Recombinant Proteins/immunology ; Ribosomal Proteins/genetics ; Ribosomal Proteins/immunology ; Ribosomes/genetics ; Ribosomes/metabolism ; Sequence Alignment ; Transcription, Genetic
Chemical Substances	Bacterial Proteins ; Recombinant Proteins ; Ribosomal Proteins
Language	English
Publishing date	2015-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	218698-6
ISSN	1098-5522 ; 0019-9567
ISSN (online)	1098-5522
ISSN	0019-9567
DOI	10.1128/IAI.00925-15
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Article ; Online: Lipoprotein succession in Borrelia burgdorferi: similar but distinct roles for OspC and VlsE at different stages of mammalian infection.

Tilly, Kit / Bestor, Aaron / Rosa, Patricia A

Molecular microbiology

2013 Volume 89, Issue 2, Page(s) 216–227

Abstract: Borrelia burgdorferi alternates between ticks and mammals, requiring variable gene expression and protein production to adapt to these diverse niches. These adaptations include shifting among the major outer surface lipoproteins OspA, OspC, and VlsE at ... ...

Abstract	Borrelia burgdorferi alternates between ticks and mammals, requiring variable gene expression and protein production to adapt to these diverse niches. These adaptations include shifting among the major outer surface lipoproteins OspA, OspC, and VlsE at different stages of the infectious cycle. We hypothesize that these proteins carry out a basic but essential function, and that OspC and VlsE fulfil this requirement during early and persistent stages of mammalian infection respectively. Previous work by other investigators suggested that several B. burgdorferi lipoproteins, including OspA and VlsE, could substitute for OspC at the initial stage of mouse infection, when OspC is transiently but absolutely required. In this study, we assessed whether vlsE and ospA could restore infectivity to an ospC mutant, and found that neither gene product effectively compensated for the absence of OspC during early infection. In contrast, we determined that OspC production was required by B. burgdorferi throughout SCID mouse infection if the vlsE gene were absent. Together, these results indicate that OspC can substitute for VlsE when antigenic variation is unnecessary, but that these two abundant lipoproteins are optimized for their related but specific roles during early and persistent mammalian infection by B. burgdorferi.
MeSH term(s)	Animals ; Antigenic Variation ; Antigens, Bacterial/genetics ; Antigens, Bacterial/metabolism ; Antigens, Surface/genetics ; Antigens, Surface/metabolism ; Bacterial Outer Membrane Proteins/genetics ; Bacterial Outer Membrane Proteins/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Bacterial Vaccines/genetics ; Bacterial Vaccines/metabolism ; Borrelia burgdorferi/pathogenicity ; Lipoproteins/genetics ; Lipoproteins/metabolism ; Lyme Disease/microbiology ; Mice ; Mice, Inbred C3H ; Mice, SCID ; Mutation
Chemical Substances	Antigens, Bacterial ; Antigens, Surface ; Bacterial Outer Membrane Proteins ; Bacterial Proteins ; Bacterial Vaccines ; Lipoproteins ; OspA protein ; OspC protein ; VlsE protein, Borrelia burgdorferi
Language	English
Publishing date	2013-06-07
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/mmi.12271
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Article ; Online: Requirements for Borrelia burgdorferi plasmid maintenance.

Tilly, Kit / Checroun, Claire / Rosa, Patricia A

Plasmid

2012 Volume 68, Issue 1, Page(s) 1–12

Abstract: Borrelia burgdorferi has multiple linear and circular plasmids that are faithfully replicated and partitioned as the bacterium grows and divides. The low copy number of these replicons implies that active partitioning contributes to plasmid stability. ... ...

Abstract	Borrelia burgdorferi has multiple linear and circular plasmids that are faithfully replicated and partitioned as the bacterium grows and divides. The low copy number of these replicons implies that active partitioning contributes to plasmid stability. Analyzing the requirements for plasmid replication and partition in B. burgdorferi is complicated by the complexity of the genome and the possibility that products may act in trans. Consequently, we have studied the replication-partition region (bbb10-13) of the B. burgdorferi 26kb circular plasmid (cp26) in Escherichia coli, by fusion with a partition-defective miniF plasmid. Our analysis demonstrated that bbb10, bbb11, and bbb13 are required for stable miniF maintenance, whereas bbb12 is dispensable. To validate these results, we attempted to inactivate two of these genes in B. burgdorferi. bbb12 mutants were obtained at a typical frequency, suggesting that the bbb12 product is dispensable for cp26 maintenance as well. We could not directly measure cp26 stability in the bbb12 mutant, because cp26 carries essential genes, and bacteria that have lost cp26 are inviable. Conversely, we were unable to inactivate bbb10 on cp26 of B. burgdorferi. Our results suggest that bbb12 is dispensable for cp26 maintenance, whereas bbb10, bbb11, and bbb13 play crucial roles in that process.
MeSH term(s)	Base Sequence ; Borrelia burgdorferi/genetics ; Cloning, Molecular ; DNA Replication ; Escherichia coli/genetics ; Gene Dosage ; Genes, Essential ; Genetic Complementation Test ; Molecular Sequence Data ; Mutation ; Plasmids
Language	English
Publishing date	2012-01-24
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Intramural
ZDB-ID	282384-6
ISSN	1095-9890 ; 0147-619X
ISSN (online)	1095-9890
ISSN	0147-619X
DOI	10.1016/j.plasmid.2012.01.009
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Article: Requirements for Borrelia burgdorferi plasmid maintenance

Tilly, Kit / Checroun, Claire / Rosa, Patricia A

Plasmid. 2012 July, v. 68, no. 1

2012

Abstract	Borrelia burgdorferi has multiple linear and circular plasmids that are faithfully replicated and partitioned as the bacterium grows and divides. The low copy number of these replicons implies that active partitioning contributes to plasmid stability. Analyzing the requirements for plasmid replication and partition in B. burgdorferi is complicated by the complexity of the genome and the possibility that products may act in trans. Consequently, we have studied the replication–partition region (bbb10–13) of the B. burgdorferi 26kb circular plasmid (cp26) in Escherichia coli, by fusion with a partition-defective miniF plasmid. Our analysis demonstrated that bbb10, bbb11, and bbb13 are required for stable miniF maintenance, whereas bbb12 is dispensable. To validate these results, we attempted to inactivate two of these genes in B. burgdorferi. bbb12 mutants were obtained at a typical frequency, suggesting that the bbb12 product is dispensable for cp26 maintenance as well. We could not directly measure cp26 stability in the bbb12 mutant, because cp26 carries essential genes, and bacteria that have lost cp26 are inviable. Conversely, we were unable to inactivate bbb10 on cp26 of B. burgdorferi. Our results suggest that bbb12 is dispensable for cp26 maintenance, whereas bbb10, bbb11, and bbb13 play crucial roles in that process.
Keywords	Borrelia burgdorferi ; Escherichia coli ; bacteria ; essential genes ; mutants ; plasmids
Language	English
Dates of publication	2012-07
Size	p. 1-12.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	282384-6
ISSN	1095-9890 ; 0147-619X
ISSN (online)	1095-9890
ISSN	0147-619X
DOI	10.1016/j.plasmid.2012.01.009
Database	NAL-Catalogue (AGRICOLA)

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