HIV-1 Buds Predominantly at the Plasma Membrane of Primary Human Macrophages
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{"title"=>"HIV-1 buds predominantly at the plasma membrane of primary human macrophages", "type"=>"journal", "authors"=>[{"first_name"=>"Sonja", "last_name"=>"Welsch", "scopus_author_id"=>"26638582400"}, {"first_name"=>"Oliver T.", "last_name"=>"Keppler", "scopus_author_id"=>"6602696738"}, {"first_name"=>"Anja", "last_name"=>"Habermann", "scopus_author_id"=>"7004898723"}, {"first_name"=>"Ina", "last_name"=>"Allespach", "scopus_author_id"=>"8371032500"}, {"first_name"=>"Jacomine", "last_name"=>"Krijnse-Locker", "scopus_author_id"=>"6602308258"}, {"first_name"=>"Hans Georg", "last_name"=>"Kräusslich", "scopus_author_id"=>"7006112877"}], "year"=>2007, "source"=>"PLoS Pathogens", "identifiers"=>{"doi"=>"10.1371/journal.ppat.0030036", "scopus"=>"2-s2.0-34047225272", "pui"=>"46535810", "isbn"=>"1553-7374 (Electronic)\\r1553-7366 (Linking)", "pmid"=>"17381240", "issn"=>"15537366", "sgr"=>"34047225272"}, "id"=>"722519e9-4c28-31d4-b732-791b3b71ba2c", "abstract"=>"HIV-1 assembly and release are believed to occur at the plasma membrane in most host cells with the exception of primary macrophages, for which exclusive budding at late endosomes has been reported. Here, we applied a novel ultrastructural approach to assess HIV-1 budding in primary macrophages in an immunomarker-independent manner. Infected macrophages were fed with BSA-gold and stained with the membrane-impermeant dye ruthenium red to identify endosomes and the plasma membrane, respectively. Virus-filled vacuolar structures with a seemingly intracellular localization displayed intense staining with ruthenium red, but lacked endocytosed BSA-gold, defining them as plasma membrane. Moreover, HIV budding profiles were virtually excluded from gold-filled endosomes while frequently being detected on ruthenium red-positive membranes. The composition of cellular marker proteins incorporated into HIV-1 supported a plasma membrane-derived origin of the viral envelope. Thus, contrary to current opinion, the plasma membrane is the primary site of HIV-1 budding also in infected macrophages.", "link"=>"http://www.mendeley.com/research/hiv1-buds-predominantly-plasma-membrane-primary-human-macrophages", "reader_count"=>79, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>5, "Researcher"=>24, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>3, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>1, "Unspecified"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>5, "Researcher"=>24, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>3, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>1, "Unspecified"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>13, "Agricultural and Biological Sciences"=>48, "Medicine and Dentistry"=>7, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1, "Chemistry"=>3, "Immunology and Microbiology"=>2, "Materials Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>3}, "Materials Science"=>{"Materials Science"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>48}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>13}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>2, "United Kingdom"=>2, "France"=>1}, "group_count"=>2}

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  • {"files"=>["https://ndownloader.figshare.com/files/469337", "https://ndownloader.figshare.com/files/469408"], "description"=>"<div><p>HIV-1 assembly and release are believed to occur at the plasma membrane in most host cells with the exception of primary macrophages, for which exclusive budding at late endosomes has been reported. Here, we applied a novel ultrastructural approach to assess HIV-1 budding in primary macrophages in an immunomarker-independent manner. Infected macrophages were fed with BSA-gold and stained with the membrane-impermeant dye ruthenium red to identify endosomes and the plasma membrane, respectively. Virus-filled vacuolar structures with a seemingly intracellular localization displayed intense staining with ruthenium red, but lacked endocytosed BSA-gold, defining them as plasma membrane. Moreover, HIV budding profiles were virtually excluded from gold-filled endosomes while frequently being detected on ruthenium red–positive membranes. The composition of cellular marker proteins incorporated into HIV-1 supported a plasma membrane–derived origin of the viral envelope. Thus, contrary to current opinion, the plasma membrane is the primary site of HIV-1 budding also in infected macrophages.</p></div>", "links"=>[], "tags"=>["hiv-1", "buds", "predominantly", "plasma", "membrane", "macrophages"], "article_id"=>152538, "categories"=>["Cancer", "Cell Biology", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.0030036.sg001", "https://dx.doi.org/10.1371/journal.ppat.0030036.sg002"], "stats"=>{"downloads"=>0, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/HIV_1_Buds_Predominantly_at_the_Plasma_Membrane_of_Primary_Human_Macrophages/152538", "title"=>"HIV-1 Buds Predominantly at the Plasma Membrane of Primary Human Macrophages", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2007-03-23 00:42:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/952443"], "description"=>"<div><p>(A) Flow diagram of macrophage differentiation, infection, and processing for EM. CA, capsid protein.</p><p>(B) Low magnification profile of an infected MDM displaying RR stain on the cell surface and on seemingly intracellular plasma membrane invaginations (arrows). Note that the bottom surface (indicated as “bottom”) that was previously attached to the substrate is not RR-stained, whereas the top surface is. The inset shows a mature virus particle on the tip of a finger-like plasma membrane protrusion.</p><p>(C) Collection of RR-stained protrusions with RR-stained mature virus particles.</p><p>(D) Large cell-surface invagination that is directly connected to the RR-stained cell surface and contains numerous RR-stained virions. The inset shows a multivesicular BSA-gold-filled endosome inside the same cell.</p><p>(E and F) RR-stained vacuole-like structures harboring virus particles and displaying structures resembling clathrin-coated pits (small arrows). Arrowheads in (E) indicate gold-filled endosomes that are not RR-stained and significantly smaller than the virus-filled structures.</p><p>(G) RR-stained virus particles accumulating between the RR-stained plasma membranes of two neighboring cells; arrowheads, BSA-gold-filled endosomes. The inset in (G) shows an enlargement of a BSA-gold-filled endosome in the boxed area.</p><p>(H–K) Virus-budding profiles (open arrows) (H) on the RR-stained cell surface and (I) on a RR-stained cell surface invagination.</p><p>(J) Early virus bud on the tip of a finger-like protrusion in a vacuolar structure devoid of RR and BSA-gold.</p><p>(K) Late virus buds on RR-negative membranes next to BSA-gold-filled endosomes (arrowheads). Nu, nucleus; PM, plasma membrane. Bars, 2 μm (B–D) and 500 nm (E–K).</p></div>", "links"=>[], "tags"=>["buds", "accumulates", "rr-stained"], "article_id"=>622746, "categories"=>["Virology", "Cell Biology", "Infectious Diseases", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0030036.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIV_1_Buds_and_Accumulates_in_RR_Stained_Domains_/622746", "title"=>"HIV-1 Buds and Accumulates in RR-Stained Domains", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:45:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/952978"], "description"=>"<div><p>(A and B) Labeling densities for CD63 and CD44 were quantified on late endosomes (identified by the presence of internalized gold and by their morphology) and the cell surface (only clearly identifiable plasma membrane was considered) of uninfected or infected MDM. In infected cells, the labeling densities on viral particles (“virus”) and on the limiting membrane of virus-containing vacuolar structures (“vacuolar membrane”) was also included. Values represent the average from two independent labeling experiments and two different grids per experiment. The quantification was performed for MDM from the same donor 1 as in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.0030036#ppat-0030036-g004\" target=\"_blank\">Figure 4</a>; the results for the two other donors are shown in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.0030036#ppat-0030036-sg002\" target=\"_blank\">Figure S2</a>. Error bars denote standard error.</p><p>(C) Remaining infectivity in supernatants of HIV-infected MDM after virus immunoprecipitation with anti-CD63 or anti-CD44, analyzed by infection of a HIV-1-permissive reporter cell line. Values obtained after precipitation with isotype control antibodies were set at 100%. Virus was obtained from MDM culture supernatant of the same donor as in (A and B). Error bars denote standard deviation.</p></div>", "links"=>[], "tags"=>["labeling", "precipitation", "antibodies", "cellular", "membrane"], "article_id"=>623284, "categories"=>["Virology", "Cell Biology", "Infectious Diseases", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0030036.g006", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantification_of_Labeling_Density_and_Virus_Precipitation_by_Antibodies_to_Cellular_Membrane_Proteins_/623284", "title"=>"Quantification of Labeling Density and Virus Precipitation by Antibodies to Cellular Membrane Proteins", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:49:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/952601"], "description"=>"<div><p>Three types of cellular membranes, either surrounding free virus or displaying budding sites, were considered: (i) RR-positive without internalized BSA-gold (RR<sup>+</sup>, BSA-gold<sup>−</sup>), (ii) RR-negative without BSA-gold (RR<sup>−</sup>, BSA-gold<sup>−</sup>), and (iii) RR-negative with BSA-gold (RR<sup>−</sup>, BSA-gold<sup>+</sup>). No RR-positive, BSA-gold-positive structures were observed.</p><p>(A) Numbers of viral structures (sum of free virus particles and budding profiles) seen on the three types of membrane structures in infected MDM prepared from three blood donors (designated 1–3). Free virus included mature virions with a typical conical core and immature particles displaying an electron dense Gag shell. Budding sites include “late buds” consisting of spherical profiles that are connected to a membrane via a stalk (see, for instance, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.0030036#ppat-0030036-g003\" target=\"_blank\">Figure 3</a>K and “early buds”) and half-moon-shaped membrane profiles with an electron-dense Gag shell on their concave side (see, for instance, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.0030036#ppat-0030036-g003\" target=\"_blank\">Figure 3</a>H).</p><p>(B) Distribution of budding profiles over the same three membrane structures and of the same three donors as in (A).</p></div>", "links"=>[], "tags"=>["membrane", "structures", "hiv-1", "accumulates"], "article_id"=>622906, "categories"=>["Virology", "Cell Biology", "Infectious Diseases", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0030036.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantification_of_Membrane_Structures_Where_HIV_1_Accumulates_and_Buds_/622906", "title"=>"Quantification of Membrane Structures Where HIV-1 Accumulates and Buds", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:46:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/952189"], "description"=>"<div><p>MDM were fed with BSA-gold and fixed in the presence of RR.</p><p>(A) A cell profile at low magnification contacting a neighboring cell. The smooth left side was previously attached to the substrate (indicated as “bottom”); the right side displaying many RR-positive protrusions is the side facing the extracellular medium (“top”). Seemingly intracellular structures also appear RR-positive. At the tight-fitting contact zones between two cells (arrows) the stain appears more electron-dense than on single lipid bilayers.</p><p>(B) Higher magnification of the boxed area in (A) showing the collection of vacuolar-like invaginations stained with RR.</p><p>(C) Higher magnification of the boxed area in (B) showing a RR-positive structure next to a BSA-gold-filled endosome (arrowhead).</p><p>(D) Comparison of RR-positive cell surface protrusions and similar RR-positive protrusions, which appeared intracellular in this section. Arrowheads indicate gold-filled endosomes. The inset in (D) shows an enlargement of a BSA-gold-filled endosome in the boxed area.</p><p>(E) Two identical looking structures with stacked protrusions; in the upper one the membranes are not RR-stained, indicating that not all vacuolar structures are accessible to the stain.</p><p>(F) A collection of BSA-gold-filled endosomes (arrowheads) next to RR-stained vacuolar structures to emphasize the differences in size and morphology. The inset in (F) shows an enlargement of a BSA-gold-filled endosome in the boxed area. Nu, nucleus. Bars, 2 μm (A and B) and 500 nm (C–F).</p></div>", "links"=>[], "tags"=>["staining", "uninfected", "mdm", "reveals", "plasma", "membrane"], "article_id"=>622460, "categories"=>["Virology", "Cell Biology", "Infectious Diseases", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0030036.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RR_Staining_of_Uninfected_MDM_Reveals_a_Complex_Plasma_Membrane_Organization_/622460", "title"=>"RR Staining of Uninfected MDM Reveals a Complex Plasma Membrane Organization", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-03-23 00:41:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/951969"], "description"=>"<div><p>Cells were infected with HIV-1 strain Ba-L (A–C, E, F, and H–J) or YU-2 (D, G, and K).</p><p>(A–C) Shows plastic-embedded sections displaying extra- and seemingly intracellular virions and budding profiles (open arrows).</p><p>(D–K) Thawed cryo-sections were labeled with anti-capsid followed by 10 nm (D–G, J, and K) or 5 nm (H and I) protein A gold.</p><p>(D and E) Labeled virions accumulated inside vacuolar structures.</p><p>(F) Labeled virions in a plasma membrane invagination that is directly connected to the extracellular space.</p><p>(G) A virus-budding profile (open arrow) and several virus particles on the plasma membrane.</p><p>(H) A virus-budding profile (open arrow) next to a structure resembling a clathrin-coated pit (arrow) inside a vacuolar structure.</p><p>(I) A virus-containing vacuole with a structure resembling a clathrin-coated pit (arrow).</p><p>(J and K) Virus-budding profiles (open arrows) next to structures resembling clathrin-coated pits (arrows) on the cell surface. PM, plasma membrane. Bar, 200 nm.</p></div>", "links"=>[], "tags"=>["mdm", "infected", "hiv-1", "strains", "yu-2"], "article_id"=>622277, "categories"=>["Virology", "Cell Biology", "Infectious Diseases", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0030036.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_Gallery_of_Primary_Human_MDM_Infected_with_HIV_1_Strains_YU_2_and_Ba_L_/622277", "title"=>"A Gallery of Primary Human MDM Infected with HIV-1 Strains YU-2 and Ba-L", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2007-03-23 00:37:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/952831"], "description"=>"<div><p>HIV-1 strain Ba-L-infected MDM were fed with 10 nm BSA-gold (except in G) for 2 h before fixing. Thawed cryo-sections were single-labeled with anti-CD63 (A and B, 15 nm gold) or anti-CD44 (F, 15 nm gold); or double-labeled with anti-capsid (C–E, G, and H, 5 nm gold) and anti-CD63 (C–E, 15 nm gold); or anti-CD44 (G, 10 nm gold and H, 15 nm gold).</p><p>(A) CD63 (arrows) on endosomes efficiently filled with BSA-gold and on tubular vesicular membranes nearby.</p><p>(B) CD63 (arrows) on plasma membrane protrusions of two adjacent cells.</p><p>(C) A virus-budding profile labeled for anti-capsid (5 nm gold, open arrows) and anti-CD63 (15 nm gold) at the plasma membrane.</p><p>(D and E) Virions inside vacuolar structures, labeled with anti-capsid (5 nm), are significantly labeled with anti-CD63. The inset in (D) shows the enlargement of double-labeled virions in the boxed area of (D). CD63 also localizes to BSA-gold-filled endosomes (arrowheads in E). Note that the virus-filled structure in (E) is devoid of 10 nm BSA-gold and displays a structure that resembles a clathrin-coated pit (small arrow).</p><p>(F) CD44 at the plasma membrane.</p><p>(G and H) CD44 on virions and on a budding profile (open arrow in G). The inset in (H) is an enlargement of the boxed area in (H) and shows several double-labeled virions inside a vacuolar structure.</p><p>Note that CD44 is excluded from BSA-gold-filled endosomes (arrowheads in F and H). PM, plasma membrane. Bars, 200 nm.</p></div>", "links"=>[], "tags"=>["cd63", "cd44", "hiv-1-infected"], "article_id"=>623141, "categories"=>["Virology", "Cell Biology", "Infectious Diseases", "Immunology"], "users"=>["Sonja Welsch", "Oliver T Keppler", "Anja Habermann", "Ina Allespach", "Jacomine Krijnse-Locker", "Hans-Georg Kräusslich"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0030036.g005", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_CD63_and_CD44_in_HIV_1_Infected_MDM_/623141", "title"=>"Localization of CD63 and CD44 in HIV-1-Infected MDM", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 12:48:10"}

PMC Usage Stats | Further Information

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Relative Metric

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