Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate

Pietro B. Carrieri, Fortunata Carbone, Francesco Perna, Dario Bruzzese, Claudia La Rocca, Mario Galgani, Silvana Montella, Maria Petracca, Ciro Florio, Giorgia T. Maniscalco, Daniele L A Spitaleri, Gerardo Iuliano, Gioacchino Tedeschi, Marida Della Corte, Simona Bonavita, Giuseppe Matarese

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Objective We investigated the effect of glatiramer acetate (GA) on the modulation of immune cell subpopulations and serum levels of multiple immune/metabolic markers in patients with relapsing-remitting multiple sclerosis (RRMS) to understand whether the treatment with GA could induce a specific change in the immunometabolic asset of patients with RRMS. Material and methods We performed an extensive peripheral blood immunophenotyping and measured serum levels of several parameters involved in the pathogenesis of RRMS and also relevant in the pathogenesis of metabolic syndrome and obesity such as leptin, soluble leptin-receptor (sLep-R), myeloperoxidase (MPO), soluble CD40 ligand (sCD40-L), soluble tumor necrosis factor-receptor (sTNF-R), monocyte chemoattractant protein 1 (MCP-1), soluble Inter-Cellular Adhesion Molecule-1 (sICAM-1) and osteoprotegerin (OPG), in 20 naïve-to-treatment RRMS patients and 20 healthy controls. We repeated these analyses over time at 6 and 12 months after starting GA treatment. Results Our analysis showed that naïve-to-treatment RRMS patients had a lower number of CD16+CD56+ NK cells, CD19+ B cells, CD4+ T cells co-expressing the MHC class II activation marker HLA-DR (CD4+DR+) and naïve CD4+CD45RA+ T cells in basal conditions. GA treatment induced a specific and significant decrease of circulating CD19+ B cells. Naïve-to-treatment RRMS patients also showed a significantly higher number of CD4+ T cells with a memory phenotype (CD4+CD45RO+) whose peripheral frequency was not affected by GA treatment. These changes over time associated with a higher serum concentration of leptin and lower levels of MPO. GA treatment also reduced significantly the circulating levels of sCD40-L and sTNF-R overtime. Conclusions Our data suggest that the clinical outcome of GA treatment is associated with changes in immune cell subpopulations and modulation of specific immunometabolic markers. These data add substantial evidence of the immune modulating effect of GA during RRMS and could be of relevance in understanding the pathogenesis of disease and its follow-up.

Original languageEnglish
Pages (from-to)1112-1121
Number of pages10
JournalMetabolism
Volume64
Issue number9
DOIs
Publication statusPublished - Sep 1 2015

Fingerprint

Relapsing-Remitting Multiple Sclerosis
Multiple Sclerosis
CD40 Ligand
Therapeutics
Tumor Necrosis Factor Receptors
Leptin
T-Lymphocytes
Peroxidase
B-Lymphocytes
Serum
Glatiramer Acetate
Osteoprotegerin
Leptin Receptors
Immunophenotyping
Chemokine CCL2
HLA-DR Antigens
Natural Killer Cells
Obesity
Biomarkers
Phenotype

Keywords

  • Glatiramer acetate
  • Metabolism
  • Multiple sclerosis

ASJC Scopus subject areas

  • Endocrinology
  • Endocrinology, Diabetes and Metabolism
  • Medicine(all)

Cite this

Carrieri, P. B., Carbone, F., Perna, F., Bruzzese, D., La Rocca, C., Galgani, M., ... Matarese, G. (2015). Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate. Metabolism, 64(9), 1112-1121. https://doi.org/10.1016/j.metabol.2015.05.001

Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate. / Carrieri, Pietro B.; Carbone, Fortunata; Perna, Francesco; Bruzzese, Dario; La Rocca, Claudia; Galgani, Mario; Montella, Silvana; Petracca, Maria; Florio, Ciro; Maniscalco, Giorgia T.; Spitaleri, Daniele L A; Iuliano, Gerardo; Tedeschi, Gioacchino; Corte, Marida Della; Bonavita, Simona; Matarese, Giuseppe.

In: Metabolism, Vol. 64, No. 9, 01.09.2015, p. 1112-1121.

Research output: Contribution to journalArticle

Carrieri, PB, Carbone, F, Perna, F, Bruzzese, D, La Rocca, C, Galgani, M, Montella, S, Petracca, M, Florio, C, Maniscalco, GT, Spitaleri, DLA, Iuliano, G, Tedeschi, G, Corte, MD, Bonavita, S & Matarese, G 2015, 'Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate', Metabolism, vol. 64, no. 9, pp. 1112-1121. https://doi.org/10.1016/j.metabol.2015.05.001
Carrieri, Pietro B. ; Carbone, Fortunata ; Perna, Francesco ; Bruzzese, Dario ; La Rocca, Claudia ; Galgani, Mario ; Montella, Silvana ; Petracca, Maria ; Florio, Ciro ; Maniscalco, Giorgia T. ; Spitaleri, Daniele L A ; Iuliano, Gerardo ; Tedeschi, Gioacchino ; Corte, Marida Della ; Bonavita, Simona ; Matarese, Giuseppe. / Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate. In: Metabolism. 2015 ; Vol. 64, No. 9. pp. 1112-1121.
@article{eae58d69d62c48169ab9b341a577cfc5,
title = "Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate",
abstract = "Objective We investigated the effect of glatiramer acetate (GA) on the modulation of immune cell subpopulations and serum levels of multiple immune/metabolic markers in patients with relapsing-remitting multiple sclerosis (RRMS) to understand whether the treatment with GA could induce a specific change in the immunometabolic asset of patients with RRMS. Material and methods We performed an extensive peripheral blood immunophenotyping and measured serum levels of several parameters involved in the pathogenesis of RRMS and also relevant in the pathogenesis of metabolic syndrome and obesity such as leptin, soluble leptin-receptor (sLep-R), myeloperoxidase (MPO), soluble CD40 ligand (sCD40-L), soluble tumor necrosis factor-receptor (sTNF-R), monocyte chemoattractant protein 1 (MCP-1), soluble Inter-Cellular Adhesion Molecule-1 (sICAM-1) and osteoprotegerin (OPG), in 20 na{\"i}ve-to-treatment RRMS patients and 20 healthy controls. We repeated these analyses over time at 6 and 12 months after starting GA treatment. Results Our analysis showed that na{\"i}ve-to-treatment RRMS patients had a lower number of CD16+CD56+ NK cells, CD19+ B cells, CD4+ T cells co-expressing the MHC class II activation marker HLA-DR (CD4+DR+) and na{\"i}ve CD4+CD45RA+ T cells in basal conditions. GA treatment induced a specific and significant decrease of circulating CD19+ B cells. Na{\"i}ve-to-treatment RRMS patients also showed a significantly higher number of CD4+ T cells with a memory phenotype (CD4+CD45RO+) whose peripheral frequency was not affected by GA treatment. These changes over time associated with a higher serum concentration of leptin and lower levels of MPO. GA treatment also reduced significantly the circulating levels of sCD40-L and sTNF-R overtime. Conclusions Our data suggest that the clinical outcome of GA treatment is associated with changes in immune cell subpopulations and modulation of specific immunometabolic markers. These data add substantial evidence of the immune modulating effect of GA during RRMS and could be of relevance in understanding the pathogenesis of disease and its follow-up.",
keywords = "Glatiramer acetate, Metabolism, Multiple sclerosis",
author = "Carrieri, {Pietro B.} and Fortunata Carbone and Francesco Perna and Dario Bruzzese and {La Rocca}, Claudia and Mario Galgani and Silvana Montella and Maria Petracca and Ciro Florio and Maniscalco, {Giorgia T.} and Spitaleri, {Daniele L A} and Gerardo Iuliano and Gioacchino Tedeschi and Corte, {Marida Della} and Simona Bonavita and Giuseppe Matarese",
year = "2015",
month = "9",
day = "1",
doi = "10.1016/j.metabol.2015.05.001",
language = "English",
volume = "64",
pages = "1112--1121",
journal = "Metabolism: Clinical and Experimental",
issn = "0026-0495",
publisher = "W.B. Saunders Ltd",
number = "9",

}

TY - JOUR

T1 - Longitudinal assessment of immuno-metabolic parameters in multiple sclerosis patients during treatment with glatiramer acetate

AU - Carrieri, Pietro B.

AU - Carbone, Fortunata

AU - Perna, Francesco

AU - Bruzzese, Dario

AU - La Rocca, Claudia

AU - Galgani, Mario

AU - Montella, Silvana

AU - Petracca, Maria

AU - Florio, Ciro

AU - Maniscalco, Giorgia T.

AU - Spitaleri, Daniele L A

AU - Iuliano, Gerardo

AU - Tedeschi, Gioacchino

AU - Corte, Marida Della

AU - Bonavita, Simona

AU - Matarese, Giuseppe

PY - 2015/9/1

Y1 - 2015/9/1

N2 - Objective We investigated the effect of glatiramer acetate (GA) on the modulation of immune cell subpopulations and serum levels of multiple immune/metabolic markers in patients with relapsing-remitting multiple sclerosis (RRMS) to understand whether the treatment with GA could induce a specific change in the immunometabolic asset of patients with RRMS. Material and methods We performed an extensive peripheral blood immunophenotyping and measured serum levels of several parameters involved in the pathogenesis of RRMS and also relevant in the pathogenesis of metabolic syndrome and obesity such as leptin, soluble leptin-receptor (sLep-R), myeloperoxidase (MPO), soluble CD40 ligand (sCD40-L), soluble tumor necrosis factor-receptor (sTNF-R), monocyte chemoattractant protein 1 (MCP-1), soluble Inter-Cellular Adhesion Molecule-1 (sICAM-1) and osteoprotegerin (OPG), in 20 naïve-to-treatment RRMS patients and 20 healthy controls. We repeated these analyses over time at 6 and 12 months after starting GA treatment. Results Our analysis showed that naïve-to-treatment RRMS patients had a lower number of CD16+CD56+ NK cells, CD19+ B cells, CD4+ T cells co-expressing the MHC class II activation marker HLA-DR (CD4+DR+) and naïve CD4+CD45RA+ T cells in basal conditions. GA treatment induced a specific and significant decrease of circulating CD19+ B cells. Naïve-to-treatment RRMS patients also showed a significantly higher number of CD4+ T cells with a memory phenotype (CD4+CD45RO+) whose peripheral frequency was not affected by GA treatment. These changes over time associated with a higher serum concentration of leptin and lower levels of MPO. GA treatment also reduced significantly the circulating levels of sCD40-L and sTNF-R overtime. Conclusions Our data suggest that the clinical outcome of GA treatment is associated with changes in immune cell subpopulations and modulation of specific immunometabolic markers. These data add substantial evidence of the immune modulating effect of GA during RRMS and could be of relevance in understanding the pathogenesis of disease and its follow-up.

AB - Objective We investigated the effect of glatiramer acetate (GA) on the modulation of immune cell subpopulations and serum levels of multiple immune/metabolic markers in patients with relapsing-remitting multiple sclerosis (RRMS) to understand whether the treatment with GA could induce a specific change in the immunometabolic asset of patients with RRMS. Material and methods We performed an extensive peripheral blood immunophenotyping and measured serum levels of several parameters involved in the pathogenesis of RRMS and also relevant in the pathogenesis of metabolic syndrome and obesity such as leptin, soluble leptin-receptor (sLep-R), myeloperoxidase (MPO), soluble CD40 ligand (sCD40-L), soluble tumor necrosis factor-receptor (sTNF-R), monocyte chemoattractant protein 1 (MCP-1), soluble Inter-Cellular Adhesion Molecule-1 (sICAM-1) and osteoprotegerin (OPG), in 20 naïve-to-treatment RRMS patients and 20 healthy controls. We repeated these analyses over time at 6 and 12 months after starting GA treatment. Results Our analysis showed that naïve-to-treatment RRMS patients had a lower number of CD16+CD56+ NK cells, CD19+ B cells, CD4+ T cells co-expressing the MHC class II activation marker HLA-DR (CD4+DR+) and naïve CD4+CD45RA+ T cells in basal conditions. GA treatment induced a specific and significant decrease of circulating CD19+ B cells. Naïve-to-treatment RRMS patients also showed a significantly higher number of CD4+ T cells with a memory phenotype (CD4+CD45RO+) whose peripheral frequency was not affected by GA treatment. These changes over time associated with a higher serum concentration of leptin and lower levels of MPO. GA treatment also reduced significantly the circulating levels of sCD40-L and sTNF-R overtime. Conclusions Our data suggest that the clinical outcome of GA treatment is associated with changes in immune cell subpopulations and modulation of specific immunometabolic markers. These data add substantial evidence of the immune modulating effect of GA during RRMS and could be of relevance in understanding the pathogenesis of disease and its follow-up.

KW - Glatiramer acetate

KW - Metabolism

KW - Multiple sclerosis

UR - http://www.scopus.com/inward/record.url?scp=84939568140&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84939568140&partnerID=8YFLogxK

U2 - 10.1016/j.metabol.2015.05.001

DO - 10.1016/j.metabol.2015.05.001

M3 - Article

C2 - 25986733

AN - SCOPUS:84939568140

VL - 64

SP - 1112

EP - 1121

JO - Metabolism: Clinical and Experimental

JF - Metabolism: Clinical and Experimental

SN - 0026-0495

IS - 9

ER -