Real-Time High Resolution 3D Imaging of the Lyme Disease Spirochete Adhering to and Escaping from the Vasculature of a Living Host
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{"title"=>"Real-time high resolution 3D imaging of the lyme disease spirochete adhering to and escaping from the vasculature of a living host", "type"=>"journal", "authors"=>[{"first_name"=>"Tara J.", "last_name"=>"Moriarty", "scopus_author_id"=>"55202362800"}, {"first_name"=>"M. Ursula", "last_name"=>"Norman", "scopus_author_id"=>"9632587400"}, {"first_name"=>"Pina", "last_name"=>"Colarusso", "scopus_author_id"=>"57191056246"}, {"first_name"=>"Troy", "last_name"=>"Bankhead", "scopus_author_id"=>"7801647471"}, {"first_name"=>"Paul", "last_name"=>"Kubes", "scopus_author_id"=>"7103272204"}, {"first_name"=>"George", "last_name"=>"Chaconas", "scopus_author_id"=>"7003818877"}], "year"=>2008, "source"=>"PLoS Pathogens", "identifiers"=>{"isbn"=>"1553-7374 (Electronic)", "scopus"=>"2-s2.0-46449086457", "pui"=>"351930623", "doi"=>"10.1371/journal.ppat.1000090", "sgr"=>"46449086457", "pmid"=>"18566656", "issn"=>"15537366"}, "id"=>"f1970a95-eeb6-3e31-bd84-fc668eb56a7a", "abstract"=>"Pathogenic spirochetes are bacteria that cause a number of emerging and re-emerging diseases worldwide, including syphilis, leptospirosis, relapsing fever, and Lyme borreliosis. They navigate efficiently through dense extracellular matrix and cross the blood-brain barrier by unknown mechanisms. Due to their slender morphology, spirochetes are difficult to visualize by standard light microscopy, impeding studies of their behavior in situ. We engineered a fluorescent infectious strain of Borrelia burgdorferi, the Lyme disease pathogen, which expressed green fluorescent protein (GFP). Real-time 3D and 4D quantitative analysis of fluorescent spirochete dissemination from the microvasculature of living mice at high resolution revealed that dissemination was a multi-stage process that included transient tethering-type associations, short-term dragging interactions, and stationary adhesion. Stationary adhesions and extravasating spirochetes were most commonly observed at endothelial junctions, and translational motility of spirochetes appeared to play an integral role in transendothelial migration. To our knowledge, this is the first report of high resolution 3D and 4D visualization of dissemination of a bacterial pathogen in a living mammalian host, and provides the first direct insight into spirochete dissemination in vivo.", "link"=>"http://www.mendeley.com/research/realtime-high-resolution-3d-imaging-lyme-disease-spirochete-adhering-escaping-vasculature-living-hos", "reader_count"=>78, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Librarian"=>1, "Researcher"=>21, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>2, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Librarian"=>1, "Researcher"=>21, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>8, "Lecturer"=>2, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Engineering"=>3, "Biochemistry, Genetics and Molecular Biology"=>6, "Materials Science"=>1, "Medicine and Dentistry"=>12, "Agricultural and Biological Sciences"=>39, "Design"=>1, "Philosophy"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Physics and Astronomy"=>4, "Chemistry"=>2, "Immunology and Microbiology"=>4, "Business, Management and Accounting"=>1}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>12}, "Physics and Astronomy"=>{"Physics and Astronomy"=>4}, "Unspecified"=>{"Unspecified"=>3}, "Design"=>{"Design"=>1}, "Engineering"=>{"Engineering"=>3}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>39}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Philosophy"=>{"Philosophy"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>1, "Sweden"=>1, "Hungary"=>2, "United States"=>3, "Brazil"=>1, "Uzbekistan"=>1, "United Kingdom"=>2}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/928586"], "description"=>"<p>The PECAM-1-expressing surface of the endothelium is shown in red, and the position of the lumen is indicated. Initially, spirochetes transiently tether, then drag over the endothelial surface along their entire length. “Stationary” adhesions align lengthwise in the same direction as blood flow, and are at least partially “embedded” in the PECAM-1 region of vessels, with one end being more stably and deeply embedded than the other. Transmigrating <i>B. burgdorferi</i> escape the vessel end-first, a process which may be driven by translational motility. It is unknown if stationary adhesions represent an obligate step in the progression toward escape, or if they fulfill other biological functions.</p>", "links"=>[], "tags"=>["stages", "vascular", "disseminating"], "article_id"=>599031, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000090.g006", "stats"=>{"downloads"=>6, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_of_the_stages_of_vascular_escape_by_disseminating_B_burgdorferi_/599031", "title"=>"Model of the stages of vascular escape by disseminating <i>B. burgdorferi</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-20 02:30:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/927971"], "description"=>"<p>A) Schematic of plasmid pTM61, which was used to constitutively express green fluorescent protein (GFP) under the control of the <i>B. burgdorferi flaB</i> promoter (P<i><sub>flaB</sub></i>). The construct also carries determinants for replication in both <i>E. coli</i> and <i>B. burgdorferi</i>, as well as a gentamycin resistance (<i>aacC1)</i> cassette. B) Phase contrast and epifluorescent visualization of spirochetes cultured from mouse ears. Ear punches obtained from infected C3H/HeN mice 13 days after inoculation were cultured in BSK-II medium in the absence of gentamycin selection before visualization. C) Visualization of live fluorescent <i>B. burgdorferi</i> in a living mouse ear by spinning disk confocal IVM. The spirochetes, indicated by yellow arrows, were observed four weeks after intraperitoneal inoculation of a C57 BL/6 mouse. Blood vessels were visualized by jugular vein injection of FITC-labeled albumin. Video footage of fluorescent <i>B. burgdorferi</i> moving in the ear of a living C57 mouse is presented in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s002\" target=\"_blank\">Video S1</a>.</p>", "links"=>[], "tags"=>["visualization", "infectious", "fluorescent"], "article_id"=>598420, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000090.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Engineering_and_in_situ_visualization_of_infectious_fluorescent_B_burgdorferi_/598420", "title"=>"Engineering and <i>in situ</i> visualization of infectious fluorescent <i>B. burgdorferi</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-20 02:20:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/928209"], "description"=>"<p>A) Graphical summary of the distribution of different types of <i>B. burgdorferi</i> interactions in postcapillary venules of the skin microvasculature. The percentage of interacting spirochetes escaping from blood vessels is indicated in the last column. Interactions were scored from video footage of conventional epifluorescence IVM. A total of 10,920 spirochete interactions in 174 venules from 30 mice were analyzed. Standard error values are indicated above each column in the graph. Sample footage of the videos used to measure spirochete interactions is presented in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s005\" target=\"_blank\">Video S4</a>. B) 3D spinning disk confocal IVM analysis of two green fluorescent spirochetes within a single venule: the upper spirochete is a short-term interaction and the lower one is a stationary adhesion. Endothelial cells were labeled with Alexa Fluor 555-conjugated antibody to PECAM-1 as noted in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat-1000090-g002\" target=\"_blank\">Fig. 2</a>. Blood flow direction is upward. The top left micrograph is a view of spirochetes in the xy plane. Micrographs below the xy view show the bacteria and blood vessel in the xz plane, reconstructed from a series of z slices. Each micrograph in the xz series indicates the xz view of a single position along the length of each spirochete (positions labeled 1–4). To the right of the xy panel are lumenal and exterior views of a 3D reconstruction of the z-series. A rotating view.of this vessel reconstructed in 3D is shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s006\" target=\"_blank\">Video S5</a>. C) Graphical summary of the average percentages of short-term interactions versus stationary adhesions that are partially or fully embedded in the anti-PECAM-1-stained vascular region. One hundred seventy-nine stable adhesions and 896 short-term interactions from z-series obtained from 29 vessels in 10 mice were analyzed. Standard error values are represented as bars above each column. Sample footage of short-term interactions and stationary adhesions visualized by spinning disk confocal IVM is shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s004\" target=\"_blank\">Video S3</a>.</p>", "links"=>[], "tags"=>["interactions", "stationary", "adhesions", "postcapillary"], "article_id"=>598653, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000090.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Visualization_of_B_burgdorferi_short_term_interactions_and_stationary_adhesions_in_postcapillary_venules_/598653", "title"=>"Visualization of <i>B. burgdorferi</i> short term interactions and stationary adhesions in postcapillary venules.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-20 02:24:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/458026", "https://ndownloader.figshare.com/files/458079", "https://ndownloader.figshare.com/files/458093", "https://ndownloader.figshare.com/files/458110", "https://ndownloader.figshare.com/files/458131", "https://ndownloader.figshare.com/files/458146", "https://ndownloader.figshare.com/files/458175", "https://ndownloader.figshare.com/files/458190"], "description"=>"<div><p>Pathogenic spirochetes are bacteria that cause a number of emerging and re-emerging diseases worldwide, including syphilis, leptospirosis, relapsing fever, and Lyme borreliosis. They navigate efficiently through dense extracellular matrix and cross the blood–brain barrier by unknown mechanisms. Due to their slender morphology, spirochetes are difficult to visualize by standard light microscopy, impeding studies of their behavior <em>in situ</em>. We engineered a fluorescent infectious strain of <em>Borrelia burgdorferi</em>, the Lyme disease pathogen, which expressed green fluorescent protein (GFP). Real-time 3D and 4D quantitative analysis of fluorescent spirochete dissemination from the microvasculature of living mice at high resolution revealed that dissemination was a multi-stage process that included transient tethering-type associations, short-term dragging interactions, and stationary adhesion. Stationary adhesions and extravasating spirochetes were most commonly observed at endothelial junctions, and translational motility of spirochetes appeared to play an integral role in transendothelial migration. To our knowledge, this is the first report of high resolution 3D and 4D visualization of dissemination of a bacterial pathogen in a living mammalian host, and provides the first direct insight into spirochete dissemination <em>in vivo</em>.</p></div>", "links"=>[], "tags"=>["Real-time", "3d", "imaging", "lyme", "spirochete", "adhering", "escaping", "vasculature"], "article_id"=>150222, "categories"=>["Cancer", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000090.s001", "https://dx.doi.org/10.1371/journal.ppat.1000090.s002", "https://dx.doi.org/10.1371/journal.ppat.1000090.s003", "https://dx.doi.org/10.1371/journal.ppat.1000090.s004", "https://dx.doi.org/10.1371/journal.ppat.1000090.s005", "https://dx.doi.org/10.1371/journal.ppat.1000090.s006", "https://dx.doi.org/10.1371/journal.ppat.1000090.s007", "https://dx.doi.org/10.1371/journal.ppat.1000090.s008"], "stats"=>{"downloads"=>7, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Real_Time_High_Resolution_3D_Imaging_of_the_Lyme_Disease_Spirochete_Adhering_to_and_Escaping_from_the_Vasculature_of_a_Living_Host/150222", "title"=>"Real-Time High Resolution 3D Imaging of the Lyme Disease Spirochete Adhering to and Escaping from the Vasculature of a Living Host", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-06-20 00:03:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/928322"], "description"=>"<p>A) 3D micrographs of a fluorescent spirochete adhered to an endothelial cell. Each micrograph in the yz and xz series indicates the yz or xz view of a single position along the length of the spirochete (positions labeled 1–3). Blood flow direction is down and to the left. A junction trace diagram in which junctions are indicated by yellow lines is provided in the bottom right panel to facilitate interpretation of the unmarked xy panel. B) Graphical summary of the average percentage of stationary adhesions or short-term interactions that are adhered at junctions, or adhered to cells. Eighty-two stable adhesions and 392 short-term interactions from z-series obtained from 20 vessels in 10 mice were analyzed. Standard error values are represented as bars above each column.</p>", "links"=>[], "tags"=>["sites", "postcapillary"], "article_id"=>598775, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000090.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_B_burgdorferi_interaction_sites_in_postcapillary_venules_/598775", "title"=>"Characterization of <i>B. burgdorferi</i> interaction sites in postcapillary venules.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-20 02:26:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/928446"], "description"=>"<p>A) Time lapse series of a spirochete escaping end-first from a postcapillary venule. Blood flow direction is up and to the left. Micrographs are projection views of z-series captured at the indicated time points. Exterior and lumenal 3D reconstruction views of the escaping spirochete (indicated by yellow arrows) at 1.8 minutes after the start of the time course are shown in B). C) Tabular summary of time span and velocity of escape for spirochetes visualized emigrating from postcapillary venules. Data were derived from analysis of 3D time lapse series obtained for a total of 30 emigrating spirochetes in 8 venules from 5 mice (emigration was determined by analyzing the direction of net spirochete displacement over time). Twenty-two of 30 spirochetes analyzed eventually fully escaped the PECAM-1-stained region, confirming that this outward movement constituted extravasation. Time span and velocity of escape were calculated for 11 spirochetes for which the start and endpoints of escape could be determined. The time span and velocity of escape for the remaining 19 spirochetes could not be calculated because either the start or end point of emigration was unknown. D) Graphical representation of reciprocal translational movement in a spirochete escaping from a postcapillary venule. The trajectories of each end of the spirochete (indicated by labels 1 and 2) are plotted. The total displacement and displacement velocities of this spirochete in the indicated time period were 19.7 µm and 6.6 µm/min, respectively, but the spirochete traveled a total of 610 µm as a result of reciprocal translation. The video footage from which this trajectory mapping was obtained is presented in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s008\" target=\"_blank\">Video S7</a>.</p>", "links"=>[], "tags"=>["escaping", "postcapillary"], "article_id"=>598899, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000090.g005", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Visualization_of_B_burgdorferi_escaping_from_postcapillary_venules_/598899", "title"=>"Visualization of <i>B. burgdorferi</i> escaping from postcapillary venules.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-20 02:28:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/928087"], "description"=>"<p>A time-lapse microscopy series of two GFP-expressing <i>B. burgdorferi</i> in the capillary of the skin of a living C57 mouse is shown. The top spirochete is motile while the bottom spirochete is stationary. Time (t) in seconds (s) is shown above or below each micrograph in the series. Images were obtained by spinning disk confocal IVM after jugular vein injection of fluorescent <i>B. burgdorferi.</i> Endothelial cells were labeled with Alexa Fluor 555-conjugated antibody to PECAM-1, which is expressed on endothelial cells and concentrates at intercellular junctions <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090-Albelda1\" target=\"_blank\">[38]</a>. Direction of blood flow in this vessel is unknown. The video from which these micrographs were extracted is presented as <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s003\" target=\"_blank\">Video S2</a>. <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000090#ppat.1000090.s004\" target=\"_blank\">Video S3</a> is a representative video of spirochete interactions in a postcapillary venule.</p>", "links"=>[], "tags"=>["visualization", "microvasculature", "murine"], "article_id"=>598532, "categories"=>["Infectious Diseases", "Microbiology"], "users"=>["Tara J. Moriarty", "M. Ursula Norman", "Pina Colarusso", "Troy Bankhead", "Paul Kubes", "George Chaconas"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000090.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Real_time_visualization_of_B_burgdorferi_in_the_microvasculature_of_a_living_murine_host_/598532", "title"=>"Real-time visualization of <i>B. burgdorferi</i> in the microvasculature of a living murine host.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-20 02:22:12"}

PMC Usage Stats | Further Information

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Relative Metric

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