Fibrinogen-like protein 2/fibroleukin induces long-term allograft survival in a rat model through regulatory B cells

We previously described that in a rat model of heart transplantation tolerance was dependent on CD8+CD45RClow Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms...

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Published inPloS one Vol. 10; no. 3; p. e0119686
Main Authors Bézie, Séverine, Picarda, Elodie, Tesson, Laurent, Renaudin, Karine, Durand, Justine, Ménoret, Séverine, Mérieau, Emmanuel, Chiffoleau, Elise, Guillonneau, Carole, Caron, Lise, Anegon, Ignacio
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 12.03.2015
Public Library of Science (PLoS)
Subjects
Adenoviruses
Adoptive transfer
Allografts
Allografts - transplantation
Animals
B cells
B-Lymphocytes, Regulatory - metabolism
CD4 antigen
CD8 antigen
Cell proliferation
Cell survival
Dendritic cells
Fgl2 protein
Fibrin
Fibrinogen
Fibrinogen - administration & dosage
Fibrinogen - genetics
Gene expression
Gene transfer
Gene Transfer Techniques
Genomes
Graft rejection
Graft Rejection - genetics
Graft Rejection - metabolism
Graft Rejection - prevention & control
Graft Rejection - therapy
Graft Survival
Haplotypes
Heart
Heart diseases
Heart transplantation
Human health and pathology
Immunological tolerance
Immunoregulation
Iterative methods
Life Sciences
Lymphocytes
Lymphocytes B
Lymphocytes T
Male
Overexpression
Plasmids
Proteins
Rats
Rejection
Rodents
Splenocytes
Studies
Survival
T cells
Transplantation
Transplants & implants
Viruses
France
Norway
Online AccessGet full text

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Abstract We previously described that in a rat model of heart transplantation tolerance was dependent on CD8+CD45RClow Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4+ T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.
AbstractList We previously described that in a rat model of heart transplantation tolerance was dependent on CD8 + CD45RC low Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibro-leukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus-mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4 + T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transfer-able and B cells were the main cells responsible for this effect.
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8 + CD45RC low Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4 + T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8 + CD45RC low Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4 + T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8+CD45RClow Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4+ T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8.sup.+ CD45RC.sup.low Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4.sup.+ T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8+CD45RClow Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4+ T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.We previously described that in a rat model of heart transplantation tolerance was dependent on CD8+CD45RClow Tregs that over-expressed fibrinogen-like protein 2 (FGL2)/fibroleukin. Little is known on the immunoregulatory properties of FGL2. Here we analyzed the transplantation tolerance mechanisms that are present in Lewis 1A rats treated with FGL2. Over-expression of FGL2 in vivo through adenovirus associated virus -mediated gene transfer without any further treatment resulted in inhibition of cardiac allograft rejection. Adoptive cell transfer of splenocytes from FGL2-treated rats with long-term graft survival (> 80 days) in animals that were transplanted with cardiac allografts inhibited acute and chronic organ rejection in a donor-specific and transferable tolerance manner, since iterative adoptive transfer up to a sixth consecutive recipient resulted in transplantation tolerance. Adoptive cell transfer also efficiently inhibited anti-donor antibody production. Analysis of all possible cell populations among splenocytes revealed that B lymphocytes were sufficient for this adoptive cell tolerance. These B cells were also capable of inhibiting the proliferation of CD4+ T cells in response to allogeneic stimuli. Moreover, gene transfer of FGL2 in B cell deficient rats did not prolong graft survival. Thus, this is the first description of FGL2 resulting in long-term allograft survival. Furthermore, allograft tolerance was transferable and B cells were the main cells responsible for this effect.
Audience Academic
Author Durand, Justine
Chiffoleau, Elise
Caron, Lise
Anegon, Ignacio
Ménoret, Séverine
Bézie, Séverine
Tesson, Laurent
Mérieau, Emmanuel
Guillonneau, Carole
Picarda, Elodie
Renaudin, Karine
AuthorAffiliation Université Paris Descartes, FRANCE
1 INSERM UMR 1064-ITUN, Centre Hospitalier Universitaire de Nantes, Faculté de Médecine, Nantes, France
2 Centre Hospitalier Universitaire de Nantes, Faculté de Médecine. Nantes, France
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ContentType Journal Article
Copyright COPYRIGHT 2015 Public Library of Science
2015 Bézie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Distributed under a Creative Commons Attribution 4.0 International License
2015 Bézie et al 2015 Bézie et al
Copyright_xml – notice: COPYRIGHT 2015 Public Library of Science
– notice: 2015 Bézie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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– notice: 2015 Bézie et al 2015 Bézie et al
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PMCID: PMC4357433
Conceived and designed the experiments: IA LC EC. Performed the experiments: SB EP LT JD SM EM. Analyzed the data: SB KR. Wrote the paper: IA LC CG SB EP.
Competing Interests: The authors have declared that no competing interests exist.
These authors are joint senior authors on this work.
ORCID 0000-0002-7195-0631
0000-0001-6167-682X
0000-0001-8700-5645
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4357433/
PMID 25763980
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SSID ssj0053866
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Snippet We previously described that in a rat model of heart transplantation tolerance was dependent on CD8+CD45RClow Tregs that over-expressed fibrinogen-like protein...
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8.sup.+ CD45RC.sup.low Tregs that over-expressed...
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8 + CD45RC low Tregs that over-expressed fibrinogen-like...
We previously described that in a rat model of heart transplantation tolerance was dependent on CD8 + CD45RC low Tregs that over-expressed fibrinogen-like...
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StartPage e0119686
SubjectTerms Adenoviruses
Adoptive transfer
Allografts
Allografts - transplantation
Animals
B cells
B-Lymphocytes, Regulatory - metabolism
CD4 antigen
CD8 antigen
Cell proliferation
Cell survival
Dendritic cells
Fgl2 protein
Fibrin
Fibrinogen
Fibrinogen - administration & dosage
Fibrinogen - genetics
Gene expression
Gene transfer
Gene Transfer Techniques
Genomes
Graft rejection
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Title Fibrinogen-like protein 2/fibroleukin induces long-term allograft survival in a rat model through regulatory B cells
URI https://www.ncbi.nlm.nih.gov/pubmed/25763980
https://www.proquest.com/docview/1662632270
https://www.proquest.com/docview/1664212690
https://inserm.hal.science/inserm-02149009
https://pubmed.ncbi.nlm.nih.gov/PMC4357433
https://doaj.org/article/814fd1891ff148c6b1f3b293c75a3246
http://dx.doi.org/10.1371/journal.pone.0119686
Volume 10
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