MHC-Matched Induced Pluripotent Stem Cells Can Attenuate Cellular and Humoral Immune Responses but Are Still Susceptible to Innate Immunity in Pigs
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{"title"=>"MHC-matched induced pluripotent stem cells can attenuate cellular and humoral immune responses but are still susceptible to innate immunity in pigs", "type"=>"journal", "authors"=>[{"first_name"=>"Yoshihisa", "last_name"=>"Mizukami", "scopus_author_id"=>"55566630500"}, {"first_name"=>"Tomoyuki", "last_name"=>"Abe", "scopus_author_id"=>"36514231000"}, {"first_name"=>"Hiroaki", "last_name"=>"Shibata", "scopus_author_id"=>"35273672000"}, {"first_name"=>"Yukitoshi", "last_name"=>"Makimura", "scopus_author_id"=>"56412717700"}, {"first_name"=>"Shuh Hei", "last_name"=>"Fujishiro", "scopus_author_id"=>"55966779000"}, {"first_name"=>"Kimihide", "last_name"=>"Yanase", "scopus_author_id"=>"56226708100"}, {"first_name"=>"Shuji", "last_name"=>"Hishikawa", "scopus_author_id"=>"6701496908"}, {"first_name"=>"Eiji", "last_name"=>"Kobayashi", "scopus_author_id"=>"55676636900"}, {"first_name"=>"Yutaka", "last_name"=>"Hanazono", "scopus_author_id"=>"7003524172"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84903136134", "sgr"=>"84903136134", "pui"=>"373380234", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"24927426", "doi"=>"10.1371/journal.pone.0098319"}, "id"=>"8dcaf60d-4c43-3ab0-b94e-bcebdfa73fb9", "abstract"=>"Recent studies have revealed negligible immunogenicity of induced pluripotent stem (iPS) cells in syngeneic mice and in autologous monkeys. Therefore, human iPS cells would not elicit immune responses in the autologous setting. However, given that human leukocyte antigen (HLA)-matched allogeneic iPS cells would likely be used for medical applications, a more faithful model system is needed to reflect HLA-matched allogeneic settings. Here we examined whether iPS cells induce immune responses in the swine leukocyte antigen (SLA)-matched setting. iPS cells were generated from the SLA-defined C1 strain of Clawn miniature swine, which were confirmed to develop teratomas in mice, and transplanted into the testes (n = 4) and ovary (n = 1) of C1 pigs. No teratomas were found in pigs on 47 to 125 days after transplantation. A Mixed lymphocyte reaction revealed that T-cell responses to the transplanted MHC-matched (C1) iPS cells were significantly lower compared to allogeneic cells. The humoral immune responses were also attenuated in the C1-to-C1 setting. More importantly, even MHC-matched iPS cells were susceptible to innate immunity, NK cells and serum complement. iPS cells lacked the expression of SLA class I and sialic acids. The in vitro cytotoxic assay showed that C1 iPS cells were targeted by NK cells and serum complement of C1. In vivo, the C1 iPS cells developed larger teratomas in NK-deficient NOG (T-B-NK-) mice (n = 10) than in NK-competent NOD/SCID (T-B-NK+) mice (n = 8) (p<0.01). In addition, C1 iPS cell failed to form teratomas after incubation with the porcine complement-active serum. Taken together, MHC-matched iPS cells can attenuate cellular and humoral immune responses, but still susceptible to innate immunity in pigs.", "link"=>"http://www.mendeley.com/research/mhcmatched-induced-pluripotent-stem-cells-attenuate-cellular-humoral-immune-responses-still-suscepti", "reader_count"=>33, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>8, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>3, "Student > Master"=>1, "Lecturer"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>8, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>3, "Student > Master"=>1, "Lecturer"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Medicine and Dentistry"=>13, "Agricultural and Biological Sciences"=>11, "Neuroscience"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemical Engineering"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>13}, "Neuroscience"=>{"Neuroscience"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1534912"], "description"=>"<p>(A) Immunocytochemical staining with an anti-porcine SLA class I antibody. Porcine PEFs showed positive staining for SLA class I, but C1 iPS cells were negative. (B) Reverse-transcription polymerase chain reaction (RT-PCR) analysis of the expression of <i>SLA class I</i> and ligands for NK cells. Lane 1, PEF; 2, C1 iPS cells; 3, STO feeder cells; 4, no reverse transcriptase; and 5, RT-PCR buffer alone. <i>MICA</i> and <i>ULBP1</i>, ligands for NK cells, were expressed on C1 iPS cells. <i>GAPDH</i> was used as a loading control. (C) Cell injury by NK cells was assessed by measuring LDH released in the supernatants as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098319#s2\" target=\"_blank\">Materials and Methods</a>. Triton-X (2%) was used as a positive control. The percent cytotoxicity was quantified and shown as mean of triplicate. Two independent experiments were performed and similar results were obtained. (D) Estimated volumes of the teratomas in immunodeficient mice and SLA-matched pigs. C1 iPS cells were transplanted into NK-competent NOD/SCID (<i>n</i> = 14) and NK-deficient NOG (<i>n</i> = 14) mice, and C1 pigs (<i>n</i> = 5). After transplantation of C1 iPS cells (1×10<sup>6</sup> cells/site) into immunodeficient mice, the teratomas were dissected and their size (diameter) was measured (<sup>*</sup><i>p</i><0.01). After transplantation of C1 iPS cells (3×10<sup>7</sup> cells/site) into C1 pigs, no teratomas were observed.</p>", "links"=>[], "tags"=>["cell biology", "Cellular types", "Animal cells", "stem cells", "Induced pluripotent stem cells", "Molecular cell biology", "developmental biology", "immunology", "Clinical immunology", "Major histocompatibility complex", "Immune response", "Model organisms", "Animal models", "Mouse models", "research design", "Clinical research design", "Preclinical models", "c1", "ips", "cells", "nk"], "article_id"=>1057325, "categories"=>["Biological Sciences"], "users"=>["Yoshihisa Mizukami", "Tomoyuki Abe", "Hiroaki Shibata", "Yukitoshi Makimura", "Shuh-hei Fujishiro", "Kimihide Yanase", "Shuji Hishikawa", "Eiji Kobayashi", "Yutaka Hanazono"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098319.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Susceptibility_of_C1_iPS_cells_to_NK_cells_/1057325", "title"=>"Susceptibility of C1 iPS cells to NK cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-13 04:14:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1534911"], "description"=>"<p>(A) Mixed lymphocyte reactions (MLRs) against allogeneic (C2) porcine embryonic fibroblasts (PEFs), C1 iPS cells and STO feeder cells. Peripheral blood mononuclear cells (PBMCs) supplemented with concanavalin A (Con A) and C2 PEFs were used as positive controls, and autologous PBMCs (C1) were used as a negative control. The stimulation index of C1 iPS cells was significantly lower than that of allogeneic cells (<sup>*</sup><i>p</i><0.01), but significantly higher than that of autologous cells (<sup>*</sup><i>p</i><0.01). MLR was performed in triplicate and repeated three times and a typical result was shown. (B) Immunohistochemical staining with anti-CD3 and anti-CD79 antibodies. Pig spleen was stained with the anti-CD3 antibody as a positive control. Slight infiltration of CD3+ T-cells and CD79+ B cells was detected at the transplantation site in the SLA-matched pig CT19. (C) Porcine IgG antibodies against C1 iPS cells were determined by flow cytometry. As SLA-mismatched recipients, miniature pigs that were not C1 or C2 were used. The porcine IgG against C1 iPS cells was detected at much lower levels in the SLA-matched C1 pigs (CT19 and CU65) than in the SLA-mismatched allogeneic pigs. Cells labeled with secondary antibody without porcine serum as a negative control.</p>", "links"=>[], "tags"=>["cell biology", "Cellular types", "Animal cells", "stem cells", "Induced pluripotent stem cells", "Molecular cell biology", "developmental biology", "immunology", "Clinical immunology", "Major histocompatibility complex", "Immune response", "Model organisms", "Animal models", "Mouse models", "research design", "Clinical research design", "Preclinical models", "humoral", "responses", "sla-matched"], "article_id"=>1057324, "categories"=>["Biological Sciences"], "users"=>["Yoshihisa Mizukami", "Tomoyuki Abe", "Hiroaki Shibata", "Yukitoshi Makimura", "Shuh-hei Fujishiro", "Kimihide Yanase", "Shuji Hishikawa", "Eiji Kobayashi", "Yutaka Hanazono"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098319.g001", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cellular_and_humoral_immune_responses_in_an_SLA_matched_setting_/1057324", "title"=>"Cellular and humoral immune responses in an SLA-matched setting.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-13 04:14:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1534916"], "description"=>"<div><p>Recent studies have revealed negligible immunogenicity of induced pluripotent stem (iPS) cells in syngeneic mice and in autologous monkeys. Therefore, human iPS cells would not elicit immune responses in the autologous setting. However, given that human leukocyte antigen (HLA)-matched allogeneic iPS cells would likely be used for medical applications, a more faithful model system is needed to reflect HLA-matched allogeneic settings. Here we examined whether iPS cells induce immune responses in the swine leukocyte antigen (SLA)-matched setting. iPS cells were generated from the SLA-defined C1 strain of Clawn miniature swine, which were confirmed to develop teratomas in mice, and transplanted into the testes (<i>n</i> = 4) and ovary (<i>n</i> = 1) of C1 pigs. No teratomas were found in pigs on 47 to 125 days after transplantation. A Mixed lymphocyte reaction revealed that T-cell responses to the transplanted MHC-matched (C1) iPS cells were significantly lower compared to allogeneic cells. The humoral immune responses were also attenuated in the C1-to-C1 setting. More importantly, even MHC-matched iPS cells were susceptible to innate immunity, NK cells and serum complement. iPS cells lacked the expression of SLA class I and sialic acids. The in vitro cytotoxic assay showed that C1 iPS cells were targeted by NK cells and serum complement of C1. In vivo, the C1 iPS cells developed larger teratomas in NK-deficient NOG (T-B-NK-) mice (<i>n</i> = 10) than in NK-competent NOD/SCID (T-B-NK+) mice (<i>n</i> = 8) (<i>p</i><0.01). In addition, C1 iPS cell failed to form teratomas after incubation with the porcine complement-active serum. Taken together, MHC-matched iPS cells can attenuate cellular and humoral immune responses, but still susceptible to innate immunity in pigs.</p></div>", "links"=>[], "tags"=>["cell biology", "Cellular types", "Animal cells", "stem cells", "Induced pluripotent stem cells", "Molecular cell biology", "developmental biology", "immunology", "Clinical immunology", "Major histocompatibility complex", "Immune response", "Model organisms", "Animal models", "Mouse models", "research design", "Clinical research design", "Preclinical models", "induced", "pluripotent", "cells", "attenuate", "cellular", "humoral", "responses", "susceptible", "innate", "immunity"], "article_id"=>1057329, "categories"=>["Biological Sciences"], "users"=>["Yoshihisa Mizukami", "Tomoyuki Abe", "Hiroaki Shibata", "Yukitoshi Makimura", "Shuh-hei Fujishiro", "Kimihide Yanase", "Shuji Hishikawa", "Eiji Kobayashi", "Yutaka Hanazono"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098319", "stats"=>{"downloads"=>2, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MHC_Matched_Induced_Pluripotent_Stem_Cells_Can_Attenuate_Cellular_and_Humoral_Immune_Responses_but_Are_Still_Susceptible_to_Innate_Immunity_in_Pigs_/1057329", "title"=>"MHC-Matched Induced Pluripotent Stem Cells Can Attenuate Cellular and Humoral Immune Responses but Are Still Susceptible to Innate Immunity in Pigs", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-13 04:14:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1534914"], "description"=>"<p>(A) Expression of CD47 was evaluated by immunocytochemistry and semi-quantitative PCR (<i>n</i> = 3). C1 iPS cells expressed CD47 to the same extent as fibroblasts. (B) Phagocytosis index (PI) was the number of iPS cells phagocytosed per 100 iPS cells, and it was 33.7±1.5%. The anti-CD47 antibody was then used to block the binding of CD47 to SIRPα. The PI value increased to 63.4±2.8%, showing that CD47 is responsible for the escape of iPS cells from phagocytosis by macrophages (<sup>*</sup><i>p</i><0.01).</p>", "links"=>[], "tags"=>["cell biology", "Cellular types", "Animal cells", "stem cells", "Induced pluripotent stem cells", "Molecular cell biology", "developmental biology", "immunology", "Clinical immunology", "Major histocompatibility complex", "Immune response", "Model organisms", "Animal models", "Mouse models", "research design", "Clinical research design", "Preclinical models", "ips", "cells", "evade", "phagocytosis", "macrophages", "cd47"], "article_id"=>1057327, "categories"=>["Biological Sciences"], "users"=>["Yoshihisa Mizukami", "Tomoyuki Abe", "Hiroaki Shibata", "Yukitoshi Makimura", "Shuh-hei Fujishiro", "Kimihide Yanase", "Shuji Hishikawa", "Eiji Kobayashi", "Yutaka Hanazono"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098319.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_C1_iPS_cells_evade_phagocytosis_by_macrophages_through_CD47_ligand_/1057327", "title"=>"C1 iPS cells evade phagocytosis by macrophages through CD47 ligand.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-13 04:14:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1534915"], "description"=>"<p>The teratoma formation in SLA-matched pigs and immunodeficient mice following injection of C1 iPS cells.</p>", "links"=>[], "tags"=>["cell biology", "Cellular types", "Animal cells", "stem cells", "Induced pluripotent stem cells", "Molecular cell biology", "developmental biology", "immunology", "Clinical immunology", "Major histocompatibility complex", "Immune response", "Model organisms", "Animal models", "Mouse models", "research design", "Clinical research design", "Preclinical models", "teratoma", "sla-matched", "pigs", "immunodeficient", "mice", "injection", "c1", "ips"], "article_id"=>1057328, "categories"=>["Biological Sciences"], "users"=>["Yoshihisa Mizukami", "Tomoyuki Abe", "Hiroaki Shibata", "Yukitoshi Makimura", "Shuh-hei Fujishiro", "Kimihide Yanase", "Shuji Hishikawa", "Eiji Kobayashi", "Yutaka Hanazono"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098319.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_teratoma_formation_in_SLA_matched_pigs_and_immunodeficient_mice_following_injection_of_C1_iPS_cells_/1057328", "title"=>"The teratoma formation in SLA-matched pigs and immunodeficient mice following injection of C1 iPS cells.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-13 04:14:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1534913"], "description"=>"<p>(A) Cytochemical assay for sialic acids using lectins. The expression of sialic acids was examined with SNA lectin and MAL lectin, both of which specifically bind to sialic acids. C1 iPS cells exhibited very low levels of sialic acids compared to fibroblasts. C1 iPS cells, but not PEFs, expressed Oct3/4. (B) Cell injury by complement was assessed by measuring LDH released in the supernatants described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0098319#s2\" target=\"_blank\">Materials and Methods</a>. Triton-X (2%) was used as a positive control, and 30% of heat-inactivated (complement-inactivated) serum was used as a negative control. The percent cytotoxicity was indicated as average values of triplicate (<sup>*</sup><i>p</i><0.01, <sup>**</sup><i>p</i><0.05). Three independent experiments were conducted and similar results were obtained.</p>", "links"=>[], "tags"=>["cell biology", "Cellular types", "Animal cells", "stem cells", "Induced pluripotent stem cells", "Molecular cell biology", "developmental biology", "immunology", "Clinical immunology", "Major histocompatibility complex", "Immune response", "Model organisms", "Animal models", "Mouse models", "research design", "Clinical research design", "Preclinical models", "cytotoxicity", "c1", "ips"], "article_id"=>1057326, "categories"=>["Biological Sciences"], "users"=>["Yoshihisa Mizukami", "Tomoyuki Abe", "Hiroaki Shibata", "Yukitoshi Makimura", "Shuh-hei Fujishiro", "Kimihide Yanase", "Shuji Hishikawa", "Eiji Kobayashi", "Yutaka Hanazono"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0098319.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Complement_mediated_cytotoxicity_to_C1_iPS_cells_/1057326", "title"=>"Complement-mediated cytotoxicity to C1 iPS cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-13 04:14:43"}

PMC Usage Stats | Further Information

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