Immunological Tolerance to Muscle Autoantigens Involves Peripheral Deletion of Autoreactive CD8+ T Cells
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{"title"=>"Immunological tolerance to muscle autoantigens involves peripheral deletion of autoreactive CD8+ T cells", "type"=>"journal", "authors"=>[{"first_name"=>"Emilie", "last_name"=>"Franck", "scopus_author_id"=>"55204954300"}, {"first_name"=>"Carole", "last_name"=>"Bonneau", "scopus_author_id"=>"55205028600"}, {"first_name"=>"Laetitia", "last_name"=>"Jean", "scopus_author_id"=>"16740247300"}, {"first_name"=>"Jean Paul", "last_name"=>"Henry", "scopus_author_id"=>"7403671873"}, {"first_name"=>"Yann", "last_name"=>"Lacoume", "scopus_author_id"=>"12770377900"}, {"first_name"=>"Anna", "last_name"=>"Salvetti", "scopus_author_id"=>"7102817409"}, {"first_name"=>"Olivier", "last_name"=>"Boyer", "scopus_author_id"=>"6701730415"}, {"first_name"=>"Sahil", "last_name"=>"Adriouch", "scopus_author_id"=>"6506385250"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"364730466", "sgr"=>"84860525286", "doi"=>"10.1371/journal.pone.0036444", "scopus"=>"2-s2.0-84860525286", "pmid"=>"22570714"}, "id"=>"d2a55d8a-bf4a-3295-b4dc-a16ea77b3e5d", "abstract"=>"Muscle potentially represents the most abundant source of autoantigens of the body and can be targeted by a variety of severe autoimmune diseases. Yet, the mechanisms of immunological tolerance toward muscle autoantigens remain mostly unknown. We investigated this issue in transgenic SM-Ova mice that express an ovalbumin (Ova) neo-autoantigen specifically in skeletal muscle. We previously reported that antigen specific CD4(+) T cell are immunologically ignorant to endogenous Ova in this model but can be stimulated upon immunization. In contrast, Ova-specific CD8(+) T cells were suspected to be either unresponsive to Ova challenge or functionally defective. We now extend our investigations on the mechanisms governing CD8(+) tolerance in SM-Ova mice. We show herein that Ova-specific CD8(+) T cells are not detected upon challenge with strongly immunogenic Ova vaccines even after depletion of regulatory T cells. Ova-specific CD8(+) T cells from OT-I mice adoptively transferred to SM-Ova mice started to proliferate in vivo, acquired CD69 and PD-1 but subsequently down-regulated Bcl-2 and disappeared from the periphery, suggesting a mechanism of peripheral deletion. Peripheral deletion of endogenous Ova-specific cells was formally demonstrated in chimeric SM-Ova mice engrafted with bone marrow cells containing T cell precursors from OT-I TCR-transgenic mice. Thus, the present findings demonstrate that immunological tolerance to muscle autoantigens involves peripheral deletion of autoreactive CD8(+) T cells.", "link"=>"http://www.mendeley.com/research/immunological-tolerance-muscle-autoantigens-involves-peripheral-deletion-autoreactive-cd8-t-cells", "reader_count"=>12, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>2, "Researcher"=>1, "Student > Ph. D. Student"=>3, "Student > Master"=>1, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>2, "Researcher"=>1, "Student > Ph. D. Student"=>3, "Student > Master"=>1, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>5, "Medicine and Dentistry"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/643873"], "description"=>"<p>(<b>A</b>) Double Tg [SM-Ova×OT-I]F1 mice (n = 3) and control OT-I mice (n = 3) were either left unmanipulated or immunized i.v. with an Ova-encoding lentiviral vector as described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036444#pone.0036444-Rowe1\" target=\"_blank\">[37]</a>. Representative flow cytometry overlay profiles illustrate the level of CD44 or Ki-67 in the gated CD8<sup>+</sup>Vα2<sup>+</sup> T cells population collected from the spleens of OT-I (blue histograms) or [SM-Ova×OT-I]F1 (red dashed histograms) mice 7 days later. (<b>B</b>) Naive double transgenic [SM-Ova×OT-I]F1 (n = 8), OT-I mice (n = 8) and naive control B6 mice (n = 2) were injected i.v with a 1∶1 mixture of CFSE<sup>high</sup> unpulsed cells and CFSE<sup>low</sup> SIINFEKL pulsed cells as described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036444#pone.0036444-Calbo1\" target=\"_blank\">[15]</a>. Spleens were harvested 5 hours later and analyzed for detection of CFSE-labeled cells. <i>In vivo</i> specific cytotoxic activities were determined by calculating the percentage of specific lysis, as described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036444#pone.0036444-Calbo1\" target=\"_blank\">[15]</a>. (<b>C</b>) Naive [SM-Ova×OT-I]F1 (n = 5), control OT-I mice (n = 5) mice and naive B6 mice (n = 6) were inoculated with 3×10<sup>6</sup> Ova-bearing EG-7 tumor cells and monitored during 30–40 days for tumor development, as described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0036444#pone.0036444-Hubert1\" target=\"_blank\">[19]</a>.</p>", "links"=>[], "tags"=>["cells", "tg", "mice", "functionally"], "article_id"=>314356, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g006", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CD8_cells_from_SM_Ova_215_OT_I_F1_double_Tg_mice_are_not_functionally_defective_/314356", "title"=>"CD8<sup>+</sup> cells from [SM-Ova×OT-I]F1 double Tg mice are not functionally defective.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:39:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/643522"], "description"=>"<p>Indicated numbers of purified CD8<sup>+</sup> T cells from CD45.1<sup>+</sup> OT-I mice were adoptively transferred into B6 or SM-Ova mice. Recipients were immunized one day later (<b>A</b>) or 3 weeks later (<b>B</b>) with Lm-Ova and splenocytes were collected, enumerated and analyzed 7 days after immunization by flow cytometry. Bar graphs show the total numbers of CD8<sup>+</sup>CD45.1<sup>+</sup> cells per spleen and the mean percentage of cells expressing PD-1 in the CD8<sup>+</sup>CD45.1<sup>+</sup> gated population. Representative flow cytometry overlay profiles are shown in (<b>B</b>), illustrating the intensity of PD-1 staining in the CD8<sup>+</sup>CD45.1<sup>+</sup> gated cells recovered from B6 (black histograms) or SM-Ova mice (open histograms) when 10<sup>5</sup> or 10<sup>4</sup> OT-I cells were adoptively transferred. Negative staining controls obtained with an isotype-matched irrelevant antibody are also shown (dashed grey lines). Data are representative of 2 independent experiments each one performed with 5–8 mice per group.</p>", "links"=>[], "tags"=>["transferred", "ot-i", "cells", "tolerized", "sm-ova"], "article_id"=>314007, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Adoptively_transferred_OT_I_CD8_T_cells_are_tolerized_in_SM_Ova_recipient_mice_/314007", "title"=>"Adoptively transferred OT-I CD8<sup>+</sup> T cells are tolerized in SM-Ova recipient mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:37:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/643978"], "description"=>"<p>B6 (n = 8) and SM-Ova (n = 13) recipient mice were lethally irradiated and reconstituted one day after with bone marrow cells collected from B6 donor mice mixed with 10% bone marrow cells collected from CD45.1<sup>+</sup> OT-I donor mice. (<b>A</b>) Left bar graph illustrates the percentages of cells in the CD4<sup>+</sup>, CD19<sup>+</sup> or CD8<sup>+</sup> gated populations expressing the CD45.1 marker in blood samples from B6 (black bars) or SM-Ova (open bars) recipient mice 6 weeks after bone marrow transplantation. Right bar graph illustrates the percentage of CD8<sup>+</sup> PBL expressing the CD45.1 marker 6, 8 or 10 weeks after bone marrow transplantation. (<b>B</b>) Absolute numbers of CD8<sup>+</sup> CD45.1<sup>+</sup> OT-I T cells found in LN, spleen, blood and thymus of chimeric mice were enumerated and analyzed by flow cytometry 10 weeks after bone marrow engraftment. (<b>C, D</b>) Bar graphs show the percentages of cells expressing CD69, PD-1, CD44 or Ki-67 marker in the gated CD8<sup>+</sup>CD45.1<sup>+</sup> population. (<b>E</b>) Representative flow cytometry overlay profiles illustrate the level of Bcl-2 expression in the gated CD8<sup>+</sup>CD45.1<sup>+</sup> T cells population collected from the LN and spleen of B6 (dark histograms) or SM-Ova (open histograms) recipient mice 10 weeks after bone marrow transplantation. Isotype-matched negative staining controls are also shown (dashed grey lines). The corresponding bar graph illustrating the mean fluorescence intensities (MFI) of Bcl-2 expression is shown in the right panel.</p>", "links"=>[], "tags"=>["deletion", "endogenously", "produced", "ova-specific", "cells", "chimeric", "sm-ova"], "article_id"=>314458, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g007", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peripheral_deletion_of_endogenously_produced_Ova_specific_CD8_T_cells_in_chimeric_SM_Ova_mice_/314458", "title"=>"Peripheral deletion of endogenously produced Ova-specific CD8<sup>+</sup> T cells in chimeric SM-Ova mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:40:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/643357"], "description"=>"<p>(<b>A</b>) B6 (n = 3) and SM-Ova (n = 3) mice were injected i.p. at day −4 and day −1 with 250 µg of anti-CD25 (PC-61) antibody to inactivate endogenous Treg, or with PBS, followed by the injection of rAAV-Ova at day 0. Splenocytes from treated mice were collected 14 days after immunization and analyzed as before by flow cytometry for the presence of Ova-specific CD8<sup>+</sup> cells using H-2K<sup>b</sup>/Ova<sub>257–264</sub> pentamer staining. Representative FACS profiles and bar graphs are shown and numbers correspond to percentages of cells positively stained with the H-2K<sup>b</sup>/Ova<sub>257–264</sub> pentamer in the gated CD8<sup>+</sup> population. (<b>B</b>) 2×10<sup>7</sup> purified CD8<sup>+</sup> T cells originating from B6 or SM-Ova donor mice were adoptively transferred into syngenic CD3<sup>−/−</sup> recipient mice (n = 6) together with 3×10<sup>7</sup> purified CD4<sup>+</sup> T cells originating exclusively from B6 donors. Recipient CD3<sup>−/−</sup> mice were immunized with rAAV-Ova one day later and splenocytes were collected, enumerated and analyzed 14 days after by flow cytometry to evaluate the percentages and absolute numbers of Ova-specific CD8<sup>+</sup> cells. Representative profiles gated on the CD8<sup>+</sup> population are shown in the left panel and the total numbers of Ova-specific CD8<sup>+</sup> per spleen are shown in the right bar graph.</p>", "links"=>[], "tags"=>["depletion", "adoptive", "mice", "ova-specific"], "article_id"=>313839, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Treg_depletion_or_adoptive_cell_transfer_to_CD3_8722_8722_mice_is_not_sufficient_to_restore_an_Ova_specific_CD8_T_cell_response_/313839", "title"=>"Treg depletion or adoptive cell transfer to CD3<sup>−/−</sup> mice is not sufficient to restore an Ova-specific CD8<sup>+</sup> T cell response.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:36:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/643771"], "description"=>"<p>(<b>A</b>) Double transgenic [OT-I×SM-Ova]F1 and control OT-I mice were thymectomized at day 0. The total numbers of Vα2<sup>+</sup>Vβ5<sup>+</sup>CD8<sup>+</sup> cells were determined from blood samples one day before thymectomy and 60 or 90 days after thymectomy. (<b>B</b>) Representative flow cytometry overlay profile illustrating the level of CD44 expression in peripheral blood cells from unmanipulated [OT-I×SM-Ova]F1 or OT-I control mice in the gated Vα2<sup>+</sup>Vβ5<sup>+</sup>CD8<sup>+</sup> population. (<b>C</b>) Representative flow cytometry profiles and a scatter plot graph illustrating the percentage of CD44<sup>high</sup>CD62L<sup>high</sup> cells found in blood samples from unmanipulated [OT-I×SM-Ova]F1 or OT-I control mice in the gated Vα2<sup>+</sup>Vβ5<sup>+</sup>CD8<sup>+</sup> population. Data are representative of 2 independent experiments with 8–9 mice per group.</p>", "links"=>[], "tags"=>["deletion", "ova-specific", "evidenced", "transgenic", "mice"], "article_id"=>314253, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Peripheral_deletion_of_Ova_specific_CD8_can_be_evidenced_in_double_transgenic_OT_I_215_SM_Ova_F1_mice_after_thymectomy_/314253", "title"=>"Peripheral deletion of Ova-specific CD8<sup>+</sup> can be evidenced in double transgenic [OT-I×SM-Ova]F1 mice after thymectomy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:39:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/643239"], "description"=>"<p>(<b>A</b>) B6 or SM-Ova mice were immunized with rAAV-Ova, replicative VSV-Ova or live Lm-Ova. Seven days after infection with VSV-Ova or Lm-Ova, or 14 days after injection of rAAV-Ova, mice were inoculated with 1×10<sup>6</sup> Ova-bearing EG-7 tumor cells and monitored during 30–40 days for tumor development. (<b>B</b>) In other groups of mice, animals were immunized with the same vaccines and splenocytes were analyzed 7 or 14 days after by flow cytometry to evaluate the percentage of CD8<sup>+</sup> T cell recognizing the immunodominant peptides of Ova or VSV-associated nucleoprotein using H-2K<sup>b</sup>/Ova<sub>257–264</sub> or H-2K<sup>b</sup>/VSV pentamers staining, respectively. Representative flow cytometry profiles are shown and numbers indicate percentage of pentamer-positive cells in the CD8<sup>+</sup>-gated population. Background staining using H-2K<sup>b</sup>/VSV pentamers were always below 0.3% of CD8<sup>+</sup> cells as also shown for the staining using H-2K<sup>b</sup>/Ova<sub>257–264</sub> pentamers (<b>C</b>) Bar graphs represent mean percentages of CD8<sup>+</sup> T cells positively stained with the indicated H-2K<sup>b</sup>/Ova<sub>257–264</sub> or H-2K<sup>b</sup>/VSV pentamers in B6 (black bars) or SM-Ova (open bars). Data are representative of 3 independent experiments, each one performed with 5–7 mice per group.</p>", "links"=>[], "tags"=>["detectable", "ova-specific", "responses", "immunized", "sm-ova"], "article_id"=>313710, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g001", "stats"=>{"downloads"=>1, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lack_of_detectable_Ova_specific_CD8_T_cell_responses_in_immunized_SM_Ova_mice_/313710", "title"=>"Lack of detectable Ova-specific CD8<sup>+</sup> T cell responses in immunized SM-Ova mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:36:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/643681"], "description"=>"<p>(<b>A</b>) 5×10<sup>6</sup> purified CD8<sup>+</sup>CD45.1<sup>+</sup> OT-I cells were adoptively transferred into SM-Ova or control B6 mice. Recipients were euthanized 2 days or 11 weeks after to determine the percentages (indicated in the representative flow cytometry panels on top) and total numbers (represented below in the bar graphs) of CD8<sup>+</sup>CD45.1<sup>+</sup> OT-I cells recovered from the LNs and spleen of recipient mice. (<b>B</b>) 5×10<sup>6</sup> CFSE-labeled CD8<sup>+</sup>CD45.1<sup>+</sup> OT-I cells were injected i.v. into SM-Ova or B6 control mice. Proliferation of gated CD8<sup>+</sup>CD45.1<sup>+</sup> cells was evaluated in the LN and spleen of recipient mice by flow cytometry 7 or 15 days after their adoptive transfer. Representative profiles are shown and the indicated numbers correspond to the percentage of gated cells that have diluted CFSE upon cell division. Data are representative of 2 independent experiments performed with 10 mice per group.</p>", "links"=>[], "tags"=>["transferred", "ot-i", "cells", "deleted", "sm-ova"], "article_id"=>314159, "categories"=>["Physiology", "Immunology"], "users"=>["Emilie Franck", "Carole Bonneau", "Laetitia Jean", "Jean-Paul Henry", "Yann Lacoume", "Anna Salvetti", "Olivier Boyer", "Sahil Adriouch"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036444.g004", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Adoptively_transferred_OT_I_CD8_T_cells_are_deleted_in_SM_Ova_mice_/314159", "title"=>"Adoptively transferred OT-I CD8<sup>+</sup> T cells are deleted in SM-Ova mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 05:38:33"}

PMC Usage Stats | Further Information

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Relative Metric

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