The IMMENSE Study: The Interplay Between iMMune and ENdothelial Cells in Mediating Cardiovascular Risk in Systemic Lupus Erythematosus
Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3 CD31 CXCR4 T cells (T ), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the co...
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Published in | Frontiers in immunology Vol. 11; p. 572876 |
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Main Authors | , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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29.10.2020
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Abstract | Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3
CD31
CXCR4
T cells (T
), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the concomitant expansion of a T
subset with immunosenescent features, such as the loss of CD28. Therefore, the aim of this study was to elucidate the interplay between T
subpopulations and endothelial cells in a group of young SLE patients without previous cardiovascular events. Twenty SLE female patients and 10 healthy controls (HCs) were recruited. Flow cytometric analysis of endothelial progenitor cells (EPCs) and T
subsets were performed and serum levels of interleukin (IL)-6, -8, matrix metalloproteinase (MMP)-9 and interferon (IFN)-
were measured. Human umbilical vein endothelial cells (HUVECs) proliferation and pro-inflammatory phenotype in response to subjects' serum stimulation were also evaluated. Results showed that the percentage of T
and EPC subsets was reduced in SLE patients compared with HCs, with a marked increase of senescent CD28
cells among T
subset. SLE disease activity index-2000 (SLEDAI-2K) was inversed related to T
cells percentage. Furthermore, IL-8 serum levels were directly correlated with the percentage of T
and inversely related to the CD28
T
subsets. We indirectly evaluated the role of the T
subset on the endothelium upon stimulation with serum from subjects with a low percentage of T
CD3
cells in HUVECs. HUVECs displayed pro-inflammatory phenotype with up-regulation of mRNA for IL-6, intercellular adhesion molecule (ICAM)-1 and endothelial leukocyte adhesion molecule (ELAM)-1. Cell proliferation rate was directly related to IL-8 serum levels and EPC percentage. In highly selected young SLE patients without previous CV events, we found that the deterioration of T
compartment is an early event in disease course, preceding the development of an overt cardiovascular disease and potentially mediated by SLE-specific mechanisms. The overcome of the CD28
subset exerts detrimental role over the T
phenotype, where T
could exert an anti-inflammatory effect on endothelial cells and might orchestrate
IL-8 the function of EPCs, ultimately modulating endothelial proliferation rate. |
---|---|
AbstractList | Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3+CD31+CXCR4+ T cells (Tang), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the concomitant expansion of a Tang subset with immunosenescent features, such as the loss of CD28. Therefore, the aim of this study was to elucidate the interplay between Tang subpopulations and endothelial cells in a group of young SLE patients without previous cardiovascular events. Twenty SLE female patients and 10 healthy controls (HCs) were recruited. Flow cytometric analysis of endothelial progenitor cells (EPCs) and Tang subsets were performed and serum levels of interleukin (IL)-6, -8, matrix metalloproteinase (MMP)-9 and interferon (IFN)-γ were measured. Human umbilical vein endothelial cells (HUVECs) proliferation and pro-inflammatory phenotype in response to subjects' serum stimulation were also evaluated. Results showed that the percentage of Tang and EPC subsets was reduced in SLE patients compared with HCs, with a marked increase of senescent CD28null cells among Tang subset. SLE disease activity index-2000 (SLEDAI-2K) was inversed related to Tang cells percentage. Furthermore, IL-8 serum levels were directly correlated with the percentage of Tang and inversely related to the CD28null Tang subsets. We indirectly evaluated the role of the Tang subset on the endothelium upon stimulation with serum from subjects with a low percentage of Tang CD3+ cells in HUVECs. HUVECs displayed pro-inflammatory phenotype with up-regulation of mRNA for IL-6, intercellular adhesion molecule (ICAM)-1 and endothelial leukocyte adhesion molecule (ELAM)-1. Cell proliferation rate was directly related to IL-8 serum levels and EPC percentage. In highly selected young SLE patients without previous CV events, we found that the deterioration of Tang compartment is an early event in disease course, preceding the development of an overt cardiovascular disease and potentially mediated by SLE-specific mechanisms. The overcome of the CD28null subset exerts detrimental role over the Tang phenotype, where Tang could exert an anti-inflammatory effect on endothelial cells and might orchestrate via IL-8 the function of EPCs, ultimately modulating endothelial proliferation rate.Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3+CD31+CXCR4+ T cells (Tang), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the concomitant expansion of a Tang subset with immunosenescent features, such as the loss of CD28. Therefore, the aim of this study was to elucidate the interplay between Tang subpopulations and endothelial cells in a group of young SLE patients without previous cardiovascular events. Twenty SLE female patients and 10 healthy controls (HCs) were recruited. Flow cytometric analysis of endothelial progenitor cells (EPCs) and Tang subsets were performed and serum levels of interleukin (IL)-6, -8, matrix metalloproteinase (MMP)-9 and interferon (IFN)-γ were measured. Human umbilical vein endothelial cells (HUVECs) proliferation and pro-inflammatory phenotype in response to subjects' serum stimulation were also evaluated. Results showed that the percentage of Tang and EPC subsets was reduced in SLE patients compared with HCs, with a marked increase of senescent CD28null cells among Tang subset. SLE disease activity index-2000 (SLEDAI-2K) was inversed related to Tang cells percentage. Furthermore, IL-8 serum levels were directly correlated with the percentage of Tang and inversely related to the CD28null Tang subsets. We indirectly evaluated the role of the Tang subset on the endothelium upon stimulation with serum from subjects with a low percentage of Tang CD3+ cells in HUVECs. HUVECs displayed pro-inflammatory phenotype with up-regulation of mRNA for IL-6, intercellular adhesion molecule (ICAM)-1 and endothelial leukocyte adhesion molecule (ELAM)-1. Cell proliferation rate was directly related to IL-8 serum levels and EPC percentage. In highly selected young SLE patients without previous CV events, we found that the deterioration of Tang compartment is an early event in disease course, preceding the development of an overt cardiovascular disease and potentially mediated by SLE-specific mechanisms. The overcome of the CD28null subset exerts detrimental role over the Tang phenotype, where Tang could exert an anti-inflammatory effect on endothelial cells and might orchestrate via IL-8 the function of EPCs, ultimately modulating endothelial proliferation rate. Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3 + CD31 + CXCR4 + T cells (T ang ), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the concomitant expansion of a T ang subset with immunosenescent features, such as the loss of CD28. Therefore, the aim of this study was to elucidate the interplay between T ang subpopulations and endothelial cells in a group of young SLE patients without previous cardiovascular events. Twenty SLE female patients and 10 healthy controls (HCs) were recruited. Flow cytometric analysis of endothelial progenitor cells (EPCs) and T ang subsets were performed and serum levels of interleukin (IL)-6, -8, matrix metalloproteinase (MMP)-9 and interferon (IFN)- γ were measured. Human umbilical vein endothelial cells (HUVECs) proliferation and pro-inflammatory phenotype in response to subjects’ serum stimulation were also evaluated. Results showed that the percentage of T ang and EPC subsets was reduced in SLE patients compared with HCs, with a marked increase of senescent CD28 null cells among T ang subset. SLE disease activity index-2000 (SLEDAI-2K) was inversed related to T ang cells percentage. Furthermore, IL-8 serum levels were directly correlated with the percentage of T ang and inversely related to the CD28 null T ang subsets. We indirectly evaluated the role of the T ang subset on the endothelium upon stimulation with serum from subjects with a low percentage of T ang CD3 + cells in HUVECs. HUVECs displayed pro-inflammatory phenotype with up-regulation of mRNA for IL-6, intercellular adhesion molecule (ICAM)-1 and endothelial leukocyte adhesion molecule (ELAM)-1. Cell proliferation rate was directly related to IL-8 serum levels and EPC percentage. In highly selected young SLE patients without previous CV events, we found that the deterioration of T ang compartment is an early event in disease course, preceding the development of an overt cardiovascular disease and potentially mediated by SLE-specific mechanisms. The overcome of the CD28 null subset exerts detrimental role over the T ang phenotype, where T ang could exert an anti-inflammatory effect on endothelial cells and might orchestrate via IL-8 the function of EPCs, ultimately modulating endothelial proliferation rate. Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3 CD31 CXCR4 T cells (T ), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the concomitant expansion of a T subset with immunosenescent features, such as the loss of CD28. Therefore, the aim of this study was to elucidate the interplay between T subpopulations and endothelial cells in a group of young SLE patients without previous cardiovascular events. Twenty SLE female patients and 10 healthy controls (HCs) were recruited. Flow cytometric analysis of endothelial progenitor cells (EPCs) and T subsets were performed and serum levels of interleukin (IL)-6, -8, matrix metalloproteinase (MMP)-9 and interferon (IFN)- were measured. Human umbilical vein endothelial cells (HUVECs) proliferation and pro-inflammatory phenotype in response to subjects' serum stimulation were also evaluated. Results showed that the percentage of T and EPC subsets was reduced in SLE patients compared with HCs, with a marked increase of senescent CD28 cells among T subset. SLE disease activity index-2000 (SLEDAI-2K) was inversed related to T cells percentage. Furthermore, IL-8 serum levels were directly correlated with the percentage of T and inversely related to the CD28 T subsets. We indirectly evaluated the role of the T subset on the endothelium upon stimulation with serum from subjects with a low percentage of T CD3 cells in HUVECs. HUVECs displayed pro-inflammatory phenotype with up-regulation of mRNA for IL-6, intercellular adhesion molecule (ICAM)-1 and endothelial leukocyte adhesion molecule (ELAM)-1. Cell proliferation rate was directly related to IL-8 serum levels and EPC percentage. In highly selected young SLE patients without previous CV events, we found that the deterioration of T compartment is an early event in disease course, preceding the development of an overt cardiovascular disease and potentially mediated by SLE-specific mechanisms. The overcome of the CD28 subset exerts detrimental role over the T phenotype, where T could exert an anti-inflammatory effect on endothelial cells and might orchestrate IL-8 the function of EPCs, ultimately modulating endothelial proliferation rate. Patients with systemic lupus erythematosus (SLE) have a significant increase in cardiovascular (CV) risk although they display a preserved number of circulating angiogenic CD3+CD31+CXCR4+ T cells (Tang), a subpopulation of T cells which promotes repair of damaged endothelium. This happens due to the concomitant expansion of a Tang subset with immunosenescent features, such as the loss of CD28. Therefore, the aim of this study was to elucidate the interplay between Tang subpopulations and endothelial cells in a group of young SLE patients without previous cardiovascular events. Twenty SLE female patients and 10 healthy controls (HCs) were recruited. Flow cytometric analysis of endothelial progenitor cells (EPCs) and Tang subsets were performed and serum levels of interleukin (IL)-6, -8, matrix metalloproteinase (MMP)-9 and interferon (IFN)-γ were measured. Human umbilical vein endothelial cells (HUVECs) proliferation and pro-inflammatory phenotype in response to subjects’ serum stimulation were also evaluated. Results showed that the percentage of Tang and EPC subsets was reduced in SLE patients compared with HCs, with a marked increase of senescent CD28null cells among Tang subset. SLE disease activity index-2000 (SLEDAI-2K) was inversed related to Tang cells percentage. Furthermore, IL-8 serum levels were directly correlated with the percentage of Tang and inversely related to the CD28null Tang subsets. We indirectly evaluated the role of the Tang subset on the endothelium upon stimulation with serum from subjects with a low percentage of Tang CD3+ cells in HUVECs. HUVECs displayed pro-inflammatory phenotype with up-regulation of mRNA for IL-6, intercellular adhesion molecule (ICAM)-1 and endothelial leukocyte adhesion molecule (ELAM)-1. Cell proliferation rate was directly related to IL-8 serum levels and EPC percentage. In highly selected young SLE patients without previous CV events, we found that the deterioration of Tang compartment is an early event in disease course, preceding the development of an overt cardiovascular disease and potentially mediated by SLE-specific mechanisms. The overcome of the CD28null subset exerts detrimental role over the Tang phenotype, where Tang could exert an anti-inflammatory effect on endothelial cells and might orchestrate via IL-8 the function of EPCs, ultimately modulating endothelial proliferation rate. |
Author | Raschi, Elena Piantoni, Silvia Tincani, Angela Meroni, Pier Luigi Franceschini, Franco Gonelli, Arianna Bodio, Caterina Govoni, Marcello Airò, Paolo Fredi, Micaela Privitera, Daniela Bortoluzzi, Alessandra Chighizola, Cecilia Beatrice Silvagni, Ettore Casciano, Fabio Cavazzana, Ilaria |
AuthorAffiliation | 3 Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia , Brescia , Italy 2 Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS , Milan , Italy 4 Department of Morphology, Surgery and Experimental Medicine and LTTA Centre, University of Ferrara , Ferrara , Italy 1 Rheumatology Unit, Department of Medical Sciences, University of Ferrara and Azienda Ospedaliero-Universitaria Sant’Anna , Cona , Italy |
AuthorAffiliation_xml | – name: 4 Department of Morphology, Surgery and Experimental Medicine and LTTA Centre, University of Ferrara , Ferrara , Italy – name: 1 Rheumatology Unit, Department of Medical Sciences, University of Ferrara and Azienda Ospedaliero-Universitaria Sant’Anna , Cona , Italy – name: 2 Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS , Milan , Italy – name: 3 Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia , Brescia , Italy |
Author_xml | – sequence: 1 givenname: Alessandra surname: Bortoluzzi fullname: Bortoluzzi, Alessandra organization: Rheumatology Unit, Department of Medical Sciences, University of Ferrara and Azienda Ospedaliero-Universitaria Sant'Anna, Cona, Italy – sequence: 2 givenname: Cecilia Beatrice surname: Chighizola fullname: Chighizola, Cecilia Beatrice organization: Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS, Milan, Italy – sequence: 3 givenname: Micaela surname: Fredi fullname: Fredi, Micaela organization: Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia, Brescia, Italy – sequence: 4 givenname: Elena surname: Raschi fullname: Raschi, Elena organization: Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS, Milan, Italy – sequence: 5 givenname: Caterina surname: Bodio fullname: Bodio, Caterina organization: Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS, Milan, Italy – sequence: 6 givenname: Daniela surname: Privitera fullname: Privitera, Daniela organization: Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS, Milan, Italy – sequence: 7 givenname: Arianna surname: Gonelli fullname: Gonelli, Arianna organization: Department of Morphology, Surgery and Experimental Medicine and LTTA Centre, University of Ferrara, Ferrara, Italy – sequence: 8 givenname: Ettore surname: Silvagni fullname: Silvagni, Ettore organization: Rheumatology Unit, Department of Medical Sciences, University of Ferrara and Azienda Ospedaliero-Universitaria Sant'Anna, Cona, Italy – sequence: 9 givenname: Marcello surname: Govoni fullname: Govoni, Marcello organization: Rheumatology Unit, Department of Medical Sciences, University of Ferrara and Azienda Ospedaliero-Universitaria Sant'Anna, Cona, Italy – sequence: 10 givenname: Ilaria surname: Cavazzana fullname: Cavazzana, Ilaria organization: Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia, Brescia, Italy – sequence: 11 givenname: Paolo surname: Airò fullname: Airò, Paolo organization: Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia, Brescia, Italy – sequence: 12 givenname: Pier Luigi surname: Meroni fullname: Meroni, Pier Luigi organization: Experimental Laboratory of Immunological and Rheumatologic Researches, Istituto Auxologico Italiano, IRCCS, Milan, Italy – sequence: 13 givenname: Angela surname: Tincani fullname: Tincani, Angela organization: Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia, Brescia, Italy – sequence: 14 givenname: Franco surname: Franceschini fullname: Franceschini, Franco organization: Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia, Brescia, Italy – sequence: 15 givenname: Silvia surname: Piantoni fullname: Piantoni, Silvia organization: Rheumatology and Clinical Immunology Unit, Department of Clinical and Experimental Sciences, ASST Spedali Civili and University of Brescia, Brescia, Italy – sequence: 16 givenname: Fabio surname: Casciano fullname: Casciano, Fabio organization: Department of Morphology, Surgery and Experimental Medicine and LTTA Centre, University of Ferrara, Ferrara, Italy |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33193356$$D View this record in MEDLINE/PubMed |
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Copyright | Copyright © 2020 Bortoluzzi, Chighizola, Fredi, Raschi, Bodio, Privitera, Gonelli, Silvagni, Govoni, Cavazzana, Airò, Meroni, Tincani, Franceschini, Piantoni and Casciano. Copyright © 2020 Bortoluzzi, Chighizola, Fredi, Raschi, Bodio, Privitera, Gonelli, Silvagni, Govoni, Cavazzana, Airò, Meroni, Tincani, Franceschini, Piantoni and Casciano 2020 Bortoluzzi, Chighizola, Fredi, Raschi, Bodio, Privitera, Gonelli, Silvagni, Govoni, Cavazzana, Airò, Meroni, Tincani, Franceschini, Piantoni and Casciano |
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Keywords | immunosenescence systemic lupus erythematosus angiogenic T cells cardiovascular risk endothelial progenitor cells |
Language | English |
License | Copyright © 2020 Bortoluzzi, Chighizola, Fredi, Raschi, Bodio, Privitera, Gonelli, Silvagni, Govoni, Cavazzana, Airò, Meroni, Tincani, Franceschini, Piantoni and Casciano. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 These authors share senior authorship Reviewed by: Fabio Malavasi, University of Turin, Italy; Artur Augusto Paiva, Coimbra Hospital and University Center, Portugal These authors have contributed equally to this work Edited by: Marta Catalfamo, Georgetown University Medical Center, United States This article was submitted to T Cell Biology, a section of the journal Frontiers in Immunology |
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SubjectTerms | Adult angiogenic T cells Animals Cardiovascular Diseases - immunology cardiovascular risk Endothelial Cells - physiology endothelial progenitor cells Female Human Umbilical Vein Endothelial Cells Humans Immunology Immunophenotyping Immunosenescence Interleukin-8 - metabolism Lupus Erythematosus, Systemic - immunology Male Risk systemic lupus erythematosus T-Lymphocyte Subsets - immunology T-Lymphocytes - immunology |
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Title | The IMMENSE Study: The Interplay Between iMMune and ENdothelial Cells in Mediating Cardiovascular Risk in Systemic Lupus Erythematosus |
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