Contribution of Bone Marrow-Derived Hematopoietic Stem/Progenitor Cells to the Generation of Donor-Marker+ Cardiomyocytes In Vivo
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{"title"=>"Contribution of Bone Marrow-Derived Hematopoietic Stem/Progenitor Cells to the Generation of Donor-Marker+ Cardiomyocytes In Vivo", "type"=>"journal", "authors"=>[{"first_name"=>"Mitsuhiro", "last_name"=>"Fukata", "scopus_author_id"=>"7003379816"}, {"first_name"=>"Fumihiko", "last_name"=>"Ishikawa", "scopus_author_id"=>"7102679543"}, {"first_name"=>"Yuho", "last_name"=>"Najima", "scopus_author_id"=>"7801689775"}, {"first_name"=>"Takuji", "last_name"=>"Yamauchi", "scopus_author_id"=>"25640415200"}, {"first_name"=>"Yoriko", "last_name"=>"Saito", "scopus_author_id"=>"7406268880"}, {"first_name"=>"Katsuto", "last_name"=>"Takenaka", "scopus_author_id"=>"55520882700"}, {"first_name"=>"Kohta", "last_name"=>"Miyawaki", "scopus_author_id"=>"56524183900"}, {"first_name"=>"Hideki", "last_name"=>"Shimazu", "scopus_author_id"=>"55916177700"}, {"first_name"=>"Kazuya", "last_name"=>"Shimoda", "scopus_author_id"=>"55236799200"}, {"first_name"=>"Takaaki", "last_name"=>"Kanemaru", "scopus_author_id"=>"6701473302"}, {"first_name"=>"Kei ichiro", "last_name"=>"Nakamura", "scopus_author_id"=>"8726194800"}, {"first_name"=>"Keita", "last_name"=>"Odashiro", "scopus_author_id"=>"6602944330"}, {"first_name"=>"Koji", "last_name"=>"Nagafuji", "scopus_author_id"=>"7003431203"}, {"first_name"=>"Mine", "last_name"=>"Harada", "scopus_author_id"=>"56642270900"}, {"first_name"=>"Koichi", "last_name"=>"Akashi", "scopus_author_id"=>"35298525700"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"368859891", "sgr"=>"84877105755", "doi"=>"10.1371/journal.pone.0062506", "scopus"=>"2-s2.0-84877105755", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"23667482"}, "id"=>"bcac2403-6449-36d7-8b2a-1aeb205520f2", "abstract"=>"BACKGROUND: Definite identification of the cell types and the mechanism relevant to cardiomyogenesis is essential for effective cardiac regenerative medicine. We aimed to identify the cell populations that can generate cardiomyocytes and to clarify whether generation of donor-marker(+) cardiomyocytes requires cell fusion between BM-derived cells and recipient cardiomyocytes.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Purified BM stem/progenitor cells from green fluorescence protein (GFP) mice were transplanted into C57BL/6 mice or cyan fluorescence protein (CFP)-transgenic mice. Purified human hematopoietic stem cells (HSCs) from cord blood were transplanted into immune-compromised NOD/SCID/IL2rγ(null) mice. GFP(+) cells in the cardiac tissue were analyzed for the antigenecity of a cardiomyocyte by confocal microscopy following immunofluorescence staining. GFP(+) donor-derived cells, GFP(+)CFP(+) fused cells, and CFP(+) recipient-derived cells were distinguished by linear unmixing analysis. Hearts of xenogeneic recipients were evaluated for the expression of human cardiomyocyte genes by real-time quantitative polymerase chain reaction. In C57BL/6 recipients, Lin(-/low)CD45(+) hematopoietic cells generated greater number of GFP(+) cardiomyocytes than Lin(-/low)CD45(-) mesenchymal cells (37.0+/-23.9 vs 0.00+/-0.00 GFP(+) cardiomyocytes per a recipient, P = 0.0095). The number of transplanted purified HSCs (Lin(-/low)Sca-1(+) or Lin(-)Sca-1(+)c-Kit(+) or CD34(-)Lin(-)Sca-1(+)c-Kit(+)) showed correlation to the number of GFP(+) cardiomyocytes (P<0.05 in each cell fraction), and the incidence of GFP(+) cardiomyocytes per injected cell dose was greatest in CD34(-)Lin(-)Sca-1(+)c-Kit(+) recipients. Of the hematopoietic progenitors, total myeloid progenitors generated greater number of GFP(+) cardiomyocytes than common lymphoid progenitors (12.8+/-10.7 vs 0.67+/-1.00 GFP(+) cardiomyocytes per a recipient, P = 0.0021). In CFP recipients, all GFP(+) cardiomyocytes examined coexpressed CFP. Human troponin C and myosin heavy chain 6 transcripts were detected in the cardiac tissue of some of the xenogeneic recipients.\\n\\nCONCLUSIONS/SIGNIFICANCE: Our results indicate that HSCs resulted in the generation of cardiomyocytes via myeloid intermediates by fusion-dependent mechanism. The use of myeloid derivatives as donor cells could potentially allow more effective cell-based therapy for cardiac repair.", "link"=>"http://www.mendeley.com/research/contribution-bone-marrowderived-hematopoietic-stemprogenitor-cells-generation-donormarker-cardiomyoc", "reader_count"=>24, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>5, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>5, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Unspecified"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Medicine and Dentistry"=>9, "Agricultural and Biological Sciences"=>5, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>9}, "Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Japan"=>1, "United Kingdom"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1055258"], "description"=>"<p>(A) LSKs or CD34<sup>−</sup>LSKs were purified by FACS from Lin<sup>−/low</sup>c-Kit<sup>+</sup> BM fraction of GFP mice. GFP and Lineage+propidium iodide (PI) expression of unfractionated BM cells is shown as a control. (B) Total myeloid progenitors (My-P) and CLPs were purified by FACS from Lin<sup>−/low</sup>Thy1.2<sup>−/low</sup>MNCs of GFP mice. (C-E) Correlational analyses between injected cell numbers and the numbers of GFP<sup>+</sup> cardiomyocytes per a recipient mouse in recipients transplanted with Lin<sup>−/low</sup>Sca-1<sup>+</sup> cells (C), LSKs (D), and CD34<sup>−</sup>LSKs (E). (F) Comparison of the number of GFP<sup>+</sup> cardiomyocytes at the same injected cell dose in Lin<sup>−/low</sup>Sca-1<sup>+</sup> cells, LSKs, and CD34<sup>−</sup>LSKs recipients. The means of the number of GFP<sup>+</sup> cardiomyocytes in recipients transplanted with each injected cell number are plotted. In the transplantation of LSKs, injected cell number of 1–1.8×10<sup>5</sup> cells is plotted at 10<sup>5</sup>, that of 1–4×10<sup>4</sup> cells is plotted at 10<sup>4</sup>, and that of 1–2×10<sup>3</sup> cells is plotted at 10<sup>3</sup>. The greater cardiomyogenic ability existed in CD34<sup>−</sup>LSKs than LSKs, and in LSKs than Lin<sup>−/low</sup>Sca-1<sup>+</sup> cells.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Heart development", "regeneration", "stem cells", "Hematopoietic stem cells", "hematology", "Bone marrow and stem cell transplantation", "hscs", "hematopoietic"], "article_id"=>699069, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Mitsuhiro Fukata", "Fumihiko Ishikawa", "Yuho Najima", "Takuji Yamauchi", "Yoriko Saito", "Katsuto Takenaka", "Kohta Miyawaki", "Hideki Shimazu", "Kazuya Shimoda", "Takaaki Kanemaru", "Kei-ichiro Nakamura", "Keita Odashiro", "Koji Nagafuji", "Mine Harada", "Koichi Akashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062506.g002", "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transplantation_of_HSCs_and_hematopoietic_progenitors_/699069", "title"=>"Transplantation of HSCs and hematopoietic progenitors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-07 02:31:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1055269", "https://ndownloader.figshare.com/files/1055271", "https://ndownloader.figshare.com/files/1055272", "https://ndownloader.figshare.com/files/1055274", "https://ndownloader.figshare.com/files/1055275", "https://ndownloader.figshare.com/files/1055276", "https://ndownloader.figshare.com/files/1055277", "https://ndownloader.figshare.com/files/1055278"], "description"=>"<div><p>Background</p><p>Definite identification of the cell types and the mechanism relevant to cardiomyogenesis is essential for effective cardiac regenerative medicine. We aimed to identify the cell populations that can generate cardiomyocytes and to clarify whether generation of donor-marker<sup>+</sup> cardiomyocytes requires cell fusion between BM-derived cells and recipient cardiomyocytes.</p><p>Methodology/Principal Findings</p><p>Purified BM stem/progenitor cells from green fluorescence protein (GFP) mice were transplanted into C57BL/6 mice or cyan fluorescence protein (CFP)-transgenic mice. Purified human hematopoietic stem cells (HSCs) from cord blood were transplanted into immune-compromised NOD/SCID/IL2rγ<sup>null</sup> mice. GFP<sup>+</sup> cells in the cardiac tissue were analyzed for the antigenecity of a cardiomyocyte by confocal microscopy following immunofluorescence staining. GFP<sup>+</sup> donor-derived cells, GFP<sup>+</sup>CFP<sup>+</sup> fused cells, and CFP<sup>+</sup> recipient-derived cells were distinguished by linear unmixing analysis. Hearts of xenogeneic recipients were evaluated for the expression of human cardiomyocyte genes by real-time quantitative polymerase chain reaction. In C57BL/6 recipients, Lin<sup>−/low</sup>CD45<sup>+</sup> hematopoietic cells generated greater number of GFP<sup>+</sup> cardiomyocytes than Lin<sup>−/low</sup>CD45<sup>−</sup> mesenchymal cells (37.0+/−23.9 vs 0.00+/−0.00 GFP<sup>+</sup> cardiomyocytes per a recipient, P = 0.0095). The number of transplanted purified HSCs (Lin<sup>−/low</sup>Sca-1<sup>+</sup> or Lin<sup>−</sup>Sca-1<sup>+</sup>c-Kit<sup>+</sup> or CD34<sup>−</sup>Lin<sup>−</sup>Sca-1<sup>+</sup>c-Kit<sup>+</sup>) showed correlation to the number of GFP<sup>+</sup> cardiomyocytes (P<0.05 in each cell fraction), and the incidence of GFP<sup>+</sup> cardiomyocytes per injected cell dose was greatest in CD34<sup>−</sup>Lin<sup>−</sup>Sca-1<sup>+</sup>c-Kit<sup>+</sup> recipients. Of the hematopoietic progenitors, total myeloid progenitors generated greater number of GFP<sup>+</sup> cardiomyocytes than common lymphoid progenitors (12.8+/−10.7 vs 0.67+/−1.00 GFP<sup>+</sup> cardiomyocytes per a recipient, P = 0.0021). In CFP recipients, all GFP<sup>+</sup> cardiomyocytes examined coexpressed CFP. Human troponin C and myosin heavy chain 6 transcripts were detected in the cardiac tissue of some of the xenogeneic recipients.</p><p>Conclusions/Significance</p><p>Our results indicate that HSCs resulted in the generation of cardiomyocytes via myeloid intermediates by fusion-dependent mechanism. The use of myeloid derivatives as donor cells could potentially allow more effective cell-based therapy for cardiac repair.</p></div>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Heart development", "regeneration", "stem cells", "Hematopoietic stem cells", "hematology", "Bone marrow and stem cell transplantation", "marrow-derived", "hematopoietic", "cells", "cardiomyocytes"], "article_id"=>699078, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Mitsuhiro Fukata", "Fumihiko Ishikawa", "Yuho Najima", "Takuji Yamauchi", "Yoriko Saito", "Katsuto Takenaka", "Kohta Miyawaki", "Hideki Shimazu", "Kazuya Shimoda", "Takaaki Kanemaru", "Kei-ichiro Nakamura", "Keita Odashiro", "Koji Nagafuji", "Mine Harada", "Koichi Akashi"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0062506.s001", "https://dx.doi.org/10.1371/journal.pone.0062506.s002", "https://dx.doi.org/10.1371/journal.pone.0062506.s003", "https://dx.doi.org/10.1371/journal.pone.0062506.s004", "https://dx.doi.org/10.1371/journal.pone.0062506.s005", "https://dx.doi.org/10.1371/journal.pone.0062506.s006", "https://dx.doi.org/10.1371/journal.pone.0062506.s007", "https://dx.doi.org/10.1371/journal.pone.0062506.s008"], "stats"=>{"downloads"=>10, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Contribution_of_Bone_Marrow_Derived_Hematopoietic_Stem_Progenitor_Cells_to_the_Generation_of_Donor_Marker_Cardiomyocytes_In_Vivo_/699078", "title"=>"Contribution of Bone Marrow-Derived Hematopoietic Stem/Progenitor Cells to the Generation of Donor-Marker<sup>+</sup> Cardiomyocytes <i>In Vivo</i>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-05-07 02:31:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1055267"], "description"=>"a<p>P = 0.0095 by Mann-Whitney U test, Lin<sup>−/low</sup>CD45<sup>+</sup> versus Lin<sup>−/low</sup>CD45<sup>−.</sup></p>b<p>P = 0.0021 by Mann-Whitney U test, Myeloid progenitor versus CLP.</p>c<p>P = 0.0004 by Mann-Whitney U test, CMP versus CLP.</p>d<p>P = 0.1142 by Mann-Whitney U test, Myeloid progenitor versus CLP.</p>*<p>GFP<sup>+</sup> cardiomyocytes were counted in 40 contiguous sections from apex of the heart per a mouse. Detailed information of histological analysis is described in Materials and Methods, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0062506#pone.0062506.s008\" target=\"_blank\">Materials and Methods S1</a>.</p><p>Abbreviations. BM: bone marrow, PB: peripheral blood, HSC: hematopoietic stem cell, LSK: Lin<sup>−</sup>Sca-1<sup>+</sup>c-Kit<sup>+</sup>, CMP: common myeloid progenitor, GMP: granulocyte/monocyte progenitor, CLP: common lymphoid progenitor.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Heart development", "regeneration", "stem cells", "Hematopoietic stem cells", "hematology", "Bone marrow and stem cell transplantation", "donor-derived", "cardiomyocytes", "transplantation", "purified", "bm"], "article_id"=>699076, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Mitsuhiro Fukata", "Fumihiko Ishikawa", "Yuho Najima", "Takuji Yamauchi", "Yoriko Saito", "Katsuto Takenaka", "Kohta Miyawaki", "Hideki Shimazu", "Kazuya Shimoda", "Takaaki Kanemaru", "Kei-ichiro Nakamura", "Keita Odashiro", "Koji Nagafuji", "Mine Harada", "Koichi Akashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062506.t001", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_number_of_donor_derived_cardiomyocytes_after_transplantation_of_purified_BM_cells_/699076", "title"=>"The number of donor-derived cardiomyocytes after transplantation of purified BM cells.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-07 02:31:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/1055264"], "description"=>"<p>(A) Representative image of fluorescence detection from cardiac tissue of the CFP-transgenic recipient transplanted with GFP<sup>+</sup> BM cells. Detected fluorescence images between 417 and 706 nm wavelength at 10–11 nm interval from a cardiac section stained with anti-TnI (Cy3), anti-Cx43 (Cy5), and DAPI are shown sequentially. (B) The expressions of DAPI, CFP, GFP, Cy3, and Cy5 in the cardiomyocyte shown in (A). Composition of GFP and CFP was examined simultaneously from each detected image between 449 and 663 nm wavelength (linear unmixing analysis). Detection wavebands used to visualize each fluorescence are described in each fluorescence image. The cardiomyocyte shown in (A) expressed donor-derived GFP, recipient-derived CFP, cardiac TnI, and Cx43. (C) Three dimensional analysis of the cardiomyocyte shown in (A) and (B) at the position of each nucleus. In every cross-section of three planes including nuclei, this cardiomyocyte expressed both GFP and CFP. Merged images (B and C) were obtained from the same confocal plane. Scale bars = 20 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Heart development", "regeneration", "stem cells", "Hematopoietic stem cells", "hematology", "Bone marrow and stem cell transplantation", "bm-derived", "cardiomyocyte", "cfp-transgenic"], "article_id"=>699073, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Mitsuhiro Fukata", "Fumihiko Ishikawa", "Yuho Najima", "Takuji Yamauchi", "Yoriko Saito", "Katsuto Takenaka", "Kohta Miyawaki", "Hideki Shimazu", "Kazuya Shimoda", "Takaaki Kanemaru", "Kei-ichiro Nakamura", "Keita Odashiro", "Koji Nagafuji", "Mine Harada", "Koichi Akashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062506.g003", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CFP_expression_in_the_GFP_BM_derived_cardiomyocyte_of_a_CFP_transgenic_recipient_mouse_/699073", "title"=>"CFP expression in the GFP<sup>+</sup> BM-derived cardiomyocyte of a CFP-transgenic recipient mouse.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-07 02:31:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/1055255"], "description"=>"<p>(A) Representative image of CD11b-expressing GFP<sup>+</sup> myeloid cells. GFP<sup>+</sup> hematopoietic cells in recipient cardiac tissue appeared in small and round shape. Cardiac section was stained with anti-CD11b (red, Cy3) and DAPI (blue). Inset: high magnification of GFP<sup>+</sup>CD11b<sup>+</sup> cells. (B) Representative image of a vimentin-expressing GFP<sup>+</sup> fibroblast. Cardiac section was stained with anti-vimentin (red, Cy3). The fibroblast was present adjacent to striated cardiomyocytes in differential interference contrast (DIC) image. (C and D) Representative images of a TnI- (C) or Cx43- (D) expressing GFP<sup>+</sup> striated cardiomyocyte. Cardiac sections were stained with anti-TnI (C; red, Cy3), anti-Cx43 (D; yellow, Cy5), and DAPI (blue). Cardiac sections are from recipients transplanted with unfractionated BM cells. All merged images were obtained from the same confocal plane. Scale bars = 50 µm, (A)-inset 10 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Heart development", "regeneration", "stem cells", "Hematopoietic stem cells", "hematology", "Bone marrow and stem cell transplantation", "bm-derived", "cells", "injured"], "article_id"=>699066, "categories"=>["Medicine", "Biological Sciences"], "users"=>["Mitsuhiro Fukata", "Fumihiko Ishikawa", "Yuho Najima", "Takuji Yamauchi", "Yoriko Saito", "Katsuto Takenaka", "Kohta Miyawaki", "Hideki Shimazu", "Kazuya Shimoda", "Takaaki Kanemaru", "Kei-ichiro Nakamura", "Keita Odashiro", "Koji Nagafuji", "Mine Harada", "Koichi Akashi"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0062506.g001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_donor_BM_derived_GFP_cells_in_injured_heart_/699066", "title"=>"Characterization of donor BM-derived GFP<sup>+</sup> cells in injured heart.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-07 02:31:06"}

PMC Usage Stats | Further Information

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Relative Metric

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