Early Dengue Virus Protein Synthesis Induces Extensive Rearrangement of the Endoplasmic Reticulum Independent of the UPR and SREBP-2 Pathway
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{"title"=>"Early dengue virus protein synthesis induces extensive rearrangement of the endoplasmic reticulum independent of the UPR and SREBP-2 pathway", "type"=>"journal", "authors"=>[{"first_name"=>"José", "last_name"=>"Peña", "scopus_author_id"=>"57189525425"}, {"first_name"=>"Eva", "last_name"=>"Harris", "scopus_author_id"=>"7403257174"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"22675522", "sgr"=>"84872749486", "scopus"=>"2-s2.0-84872749486", "isbn"=>"1932-6203 (Electronic)\\n1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0038202", "pui"=>"364955425", "issn"=>"19326203"}, "id"=>"6b828e5b-109e-322a-b9ad-165b9cbb0ff6", "abstract"=>"The rearrangement of intracellular membranes has been long reported to be a common feature in diseased cells. In this study, we used dengue virus (DENV) to study the role of the unfolded protein response (UPR) and sterol-regulatory-element-binding-protein-2 (SREBP-2) pathway in the rearrangement and expansion of the endoplasmic reticulum (ER) early after infection. Using laser scanning confocal and differential interference contrast microscopy, we demonstrate that rearrangement and expansion of the ER occurs early after DENV-2 infection. Through the use of mouse embryonic fibroblast cells deficient in XBP1 and ATF6, we show that ER rearrangement early after DENV infection is independent of the UPR. We then demonstrate that enlargement of the ER is independent of the SREBP-2 activation and upregulation of 3-hydroxy-3-methylglutaryl-Coenzyme-A reductase, the rate-limiting enzyme in the cholesterol biosynthesis pathway. We further show that this ER rearrangement is not inhibited by the treatment of DENV-infected cells with the cholesterol-inhibiting drug lovastatin. Using the transcription inhibitor actinomycin D and the translation elongation inhibitor cycloheximide, we show that de novo viral protein synthesis but not host transcription is necessary for expansion and rearrangement of the ER. Lastly, we demonstrate that viral infection induces the reabsorption of lipid droplets into the ER. Together, these results demonstrate that modulation of intracellular membrane architecture of the cell early after DENV-2 infection is driven by viral protein expression and does not require the induction of the UPR and SREBP-2 pathways. This work paves the way for further study of virally-induced membrane rearrangements and formation of cubic membranes.", "link"=>"http://www.mendeley.com/research/early-dengue-virus-protein-synthesis-induces-extensive-rearrangement-endoplasmic-reticulum-independe", "reader_count"=>70, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>16, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>9, "Other"=>2, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>2, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>16, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>21, "Student > Postgraduate"=>3, "Student > Master"=>9, "Other"=>2, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>2, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>45, "Medicine and Dentistry"=>7, "Chemistry"=>4, "Social Sciences"=>1, "Immunology and Microbiology"=>5}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>4}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>45}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"United States"=>3, "French Polynesia"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/628586"], "description"=>"<p>XBP1<sup>+/+</sup> (A–D) and XBP1<sup>−/−</sup> (E–H) MEF cells were infected with DENV-2 for 12 h and stained intracellularly for cellular proteins using antibodies against (A and E) GRP78, (B and F) GRP94, (C) XBP1, and (G) ATF6 (magenta), followed by secondary antibodies conjugated to Alexa Fluor® 647. DENV proteins were detected with mouse MAbs against DENV E (green) and NS3 (red) directly conjugated to Alexa Fluor® 488 and Alexa Fluor® 594, respectively. Nuclear staining (blue) was performed using DAPI stain. Images were acquired and processed as described in Fig. 1. Total magnification 630×.</p>", "links"=>[], "tags"=>["er", "rearrangement", "xbp-1"], "article_id"=>299084, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_induced_ER_rearrangement_and_expansion_is_independent_of_the_XBP_1_pathway_/299084", "title"=>"DENV-induced ER rearrangement and expansion is independent of the XBP-1 pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:31:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/628428"], "description"=>"<p>2fTGH cells were (A) mock-infected or (B–E) infected with DENV-2 for 12 h and stained intracellularly for UPR markers and viral proteins E and NS3. (A) Mock-infected 2fTGH cells were stained with mouse MAbs against DENV E (4G2; green) and NS3 (E1D8; red) directly conjugated to Alexa Fluor® 488 and Alexa Fluor® 594, respectively. Nuclear staining (blue) was performed using DAPI stain. Intracellular staining of DENV-infected cells was carried out as in (A); in addition primary antibodies specific for cellular proteins (B) GRP78, (C) GRP94, (D) XBP1 and (E) ATF6 (magenta) were used, followed by secondary antibodies conjugated to Alexa Fluor® 647. The multiple-exposure images were captured using 63X/1.25 Plan-Neofluar DIC oil objective on Zeiss 510 LSM using bandpass filter sets appropriate for DAPI, Alexa Fluor® 488, Alexa Fluor® 594 and Alexa Fluor® 647. For individual images, the additional channels were turned OFF post-acquisition using the Zeiss operating software. Co-localization is observed in the “Merged” image as a yellow hue. Merged and DIC images represent a single image with all detector channels ON. Total magnification 630×. (F) Western blot analysis of GRP78 over a 12-h course of DENV infection. Actin was used as a loading control, and expression of DENV NS1 was used to confirm viral infection.</p>", "links"=>[], "tags"=>["induces", "rearrangement", "er"], "article_id"=>298926, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_induces_rearrangement_of_the_ER_early_after_infection_/298926", "title"=>"DENV induces rearrangement of the ER early after infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:28:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/325829", "https://ndownloader.figshare.com/files/325902", "https://ndownloader.figshare.com/files/325925"], "description"=>"<div><p>The rearrangement of intracellular membranes has been long reported to be a common feature in diseased cells. In this study, we used dengue virus (DENV) to study the role of the unfolded protein response (UPR) and sterol-regulatory-element-binding-protein-2 (SREBP-2) pathway in the rearrangement and expansion of the endoplasmic reticulum (ER) early after infection. Using laser scanning confocal and differential interference contrast microscopy, we demonstrate that rearrangement and expansion of the ER occurs early after DENV-2 infection. Through the use of mouse embryonic fibroblast cells deficient in XBP1 and ATF6, we show that ER rearrangement early after DENV infection is independent of the UPR. We then demonstrate that enlargement of the ER is independent of the SREBP-2 activation and upregulation of 3-hydroxy-3-methylglutaryl-Coenzyme-A reductase, the rate-limiting enzyme in the cholesterol biosynthesis pathway. We further show that this ER rearrangement is not inhibited by the treatment of DENV-infected cells with the cholesterol-inhibiting drug lovastatin. Using the transcription inhibitor actinomycin D and the translation elongation inhibitor cycloheximide, we show that <em>de novo</em> viral protein synthesis but not host transcription is necessary for expansion and rearrangement of the ER. Lastly, we demonstrate that viral infection induces the reabsorption of lipid droplets into the ER. Together, these results demonstrate that modulation of intracellular membrane architecture of the cell early after DENV-2 infection is driven by viral protein expression and does not require the induction of the UPR and SREBP-2 pathways. This work paves the way for further study of virally-induced membrane rearrangements and formation of cubic membranes.</p> </div>", "links"=>[], "tags"=>["dengue", "synthesis", "induces", "rearrangement", "endoplasmic", "reticulum", "upr", "srebp-2", "pathway"], "article_id"=>124311, "categories"=>["Cancer", "Microbiology", "Biochemistry", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0038202.s001", "https://dx.doi.org/10.1371/journal.pone.0038202.s002", "https://dx.doi.org/10.1371/journal.pone.0038202.s003"], "stats"=>{"downloads"=>5, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Early_Dengue_Virus_Protein_Synthesis_Induces_Extensive_Rearrangement_of_the_Endoplasmic_Reticulum_Independent_of_the_UPR_and_SREBP_2_Pathway/124311", "title"=>"Early Dengue Virus Protein Synthesis Induces Extensive Rearrangement of the Endoplasmic Reticulum Independent of the UPR and SREBP-2 Pathway", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-06-04 01:11:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/628894"], "description"=>"<p>2fTGH cells were mock-treated (A) or treated with DTT (B) for 6 h. Cells were then fixed and stained intracellularly for cellular proteins using antibodies against SREBP-2 (green) and HMGCR (red) followed by secondary antibodies conjugated to Alexa Fluor® 488 and Alexa Fluor® 546, respectively. 2fTGH cells were infected with DENV-2 for 12 h and stained intracellularly for (C) SREBP-2 (magenta) and (D) HMGCR (magenta) followed by secondary antibodies conjugated to Alexa Fluor® 647; mouse MAbs against DENV E (green) and NS3 (red) directly conjugated to Alexa Fluor® 488 and Alexa Fluor® 594, respectively, were used to detect DENV proteins. Nuclear staining (blue) was performed using DAPI stain. The multiple-exposure images were captured using a 40×/1.4 Plan-Apochromat DIC oil objective on a Zeiss 710 LSM using bandpass filter sets appropriate for DAPI, Alexa Fluor® 488, Alexa Fluor® 594 and Alexa Fluor® 647 and were processed as previously described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038202#pone-0038202-g001\" target=\"_blank\">Figure 1</a>. (E) SREBP-2 proteolyic processing by immunoblot analysis. Actin was used as a loading control. In (F), 2fTGH cells were infected with DENV-2 over a 3–12 h time-course. Lysates were collected and analyzed for SREBP-2 and HMGCR expression by immunoblot analysis. Actin was used as a loading control, and expression of DENV NS1 was used to confirm viral infection. A time-matched mock-infected control was included at each time-point. Total magnification 600×.</p>", "links"=>[], "tags"=>["induce", "srebp-2", "pathway", "upreglation", "hmgcr"], "article_id"=>299384, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g004", "stats"=>{"downloads"=>1, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_does_not_induce_the_SREBP_2_pathway_or_upreglation_of_HMGCR_early_after_infection_/299384", "title"=>"DENV does not induce the SREBP-2 pathway or upreglation of HMGCR early after infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:36:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/628729"], "description"=>"<p>ATF6<sup>+/+</sup> (A–C) and ATF6<sup>−/−</sup> (D–F) MEF cells were infected with DENV-2 for 12 h and intracellularly stained for cellular proteins (A and D) GRP78, (B and E) GRP94, and (C and F) XBP1 (magenta), followed by secondary antibodies conjugated to Alexa Fluor® 647. DENV proteins were detected with mouse MAbs against DENV E (green) and NS3 (red) directly conjugated to Alexa Fluor® 488 and Alexa Fluor® 594, respectively. Nuclear staining (blue) was performed using DAPI stain. Images were acquired and processed as described in Fig. 1. Total Magnification 630×.</p>", "links"=>[], "tags"=>["er", "rearrangement", "atf6"], "article_id"=>299222, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_induced_ER_rearrangement_and_expansion_is_independent_of_the_ATF6_pathway_/299222", "title"=>"DENV-induced ER rearrangement and expansion is independent of the ATF6 pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:33:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/629367"], "description"=>"<p>DENV-2-infected 2fTGH cells were fixed and stained with mouse MAbs against DENV-2 E-protein (4G2; pseudo-colored green) and NS3 (red). Lipid droplets (LD; pseudo-colored magenta) were stained using Bodipy 493/503 dye. (B) Three-dimensional reconstruction of the rearranged and expanded ER early after DENV-2 infection. The deconvolved image was rotated 180° on the X-axis relative to Fig. 7A. Images were obtained using a Zeiss 710 LSM as previously described. Z-stack series (61 panels) were deconvolved using Huygens software (Scientific Volume Imaging), and an iso-surface model was generated using Imaris 7.2 software (Bitplane Scientific Software). LD (pseudo-color magenta), E (pseudo-color green) and NS3 (red). Total magnification 600×.</p>", "links"=>[], "tags"=>["er", "induces", "lipid", "droplet"], "article_id"=>299862, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g007", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_induced_ER_expansion_induces_lipid_droplet_reabsorption_/299862", "title"=>"DENV-induced ER expansion induces lipid droplet reabsorption.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:44:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/629235"], "description"=>"<p>Mock-infected 2fTGH cells were (A) treated with 10 µg/mL actinomycin D (Act D) or (B) treated with 50 µg/mL cycloheximide (CHX), fixed and stained intracellularly for viral proteins E (green) and NS3 (red); nuclear staining (blue) was performed with DAPI. DENV-infected 2fTGH cells were (C) mock-treated or treated with (D) Act D or (E) CHX at the time of infection. Cells were fixed and stained as in A and B. Figures (F) and (G) are increased magnification of figures C and D, respectively. Black arrows point to lamellar stack-like structures and white arrows point to vesicle-like pore openings on the enlarged ER. Scale bar  = 2 µm. Total magnification 600×.</p>", "links"=>[], "tags"=>["er", "rearrangement", "requires", "viral"], "article_id"=>299730, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g006", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DENV_induced_ER_rearrangement_requires_viral_protein_synthesis_/299730", "title"=>"DENV-induced ER rearrangement requires viral protein synthesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:42:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/629059"], "description"=>"<p>Mock-infected 2fTGH cells were treated with 10 µM lovastatin for 12 h and were stained intracellularly for (A) SREBP-2 (green) and HMGCR (red). (B) Cells were also stained for DENV proteins E (green) and NS3 (red). 2fTGH cells were infected with DENV-2 and mock-treated for 12 h. Cells were fixed and stained intracellularly for (C) SREBP-2 (magenta) and (D) HMGCR (magenta), followed by DENV E (green) and NS3 (red) staining. Nuclear staining (blue) was performed using DAPI. DENV-infected 2fTGH cells were treated with 10 µM lovastatin at the time of infection and incubated for 12 h. Cells were fixed and stained as described above for (E) SREBP2 (magenta) and (F) HMGCR (magenta) and DENV E (green) and NS3 (red). Nuclear staining (blue) was performed using DAPI, and images were acquired as previously described. Total magnification 630×.</p>", "links"=>[], "tags"=>["denv-infected", "cells", "inhibit", "er"], "article_id"=>299551, "categories"=>["Microbiology", "Virology", "Biochemistry", "Infectious Diseases", "Molecular Biology", "Genetics"], "users"=>["José Peña", "Eva Harris"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038202.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lovastatin_treatment_of_DENV_infected_cells_does_not_inhibit_ER_rearrangement_/299551", "title"=>"Lovastatin treatment of DENV-infected cells does not inhibit ER rearrangement.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-06-04 02:39:11"}

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Relative Metric

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