Suppressive regulatory T cells and latent transforming growth factor-β-expressing macrophages are altered in the peritoneal fluid of patients with endometriosis

BackgroundEndometriosis is a known cause of infertility. Differences in immune tolerance caused by regulatory T cells (Tregs) and transforming growth factor-β (TGF-β) are thought to be involved in the pathology of endometriosis. Evidence has indicated that Tregs can be separated into three functionally and phenotypically distinct subpopulations and that activated TGF-β is released from latency-associated peptide (LAP) on the surfaces of specific cells. The aim of this study was to examine differences in Treg subpopulations and LAP in the peripheral blood (PB) and peritoneal fluid (PF) of patients with and without endometriosis.MethodsPB and PF were collected from 28 women with laparoscopically and histopathologically diagnosed endometriosis and 20 disease-free women who were subjected to laparoscopic surgery. Three subpopulations of CD4+ T lymphocytes (CD45RA+FoxP3low resting Tregs, CD45RA−FoxP3high effector Tregs, and CD45RA−FoxP3low non-Tregs) and CD11b+ mononuclear cells expressing LAP were analyzed by flow cytometry using specific monoclonal antibodies.ResultsProportions of suppressive Tregs (resting and effector Tregs) were significantly higher in the PF samples of patients with endometriosis than in those of control women (P = 0.02 and P < 0.01, respectively) but did not differ between the PB samples of patients and controls. The percentage of CD11b+LAP+ macrophages was significantly lower in PF samples of patients with endometriosis than in those of controls (P < 0.01) but was not altered in the PB samples.ConclusionProportions of suppressive Tregs and LAP+ macrophages are altered locally in the PF of endometriosis patients.

• Publication year

  2018

• Venue

  Reproductive Biology and Endocrinology

• Publication date

  2018-02-01

• Fields of study

  Medicine

• Identifiers
  DOI 10.1186/s12958-018-0325-2PMID 29391020PMCID 5796574
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Stress During Development of Experimental Endometriosis Influences Nerve Growth and Disease Progression

  2018cited by this paper
• Exacerbation of Endometriosis Due To Regulatory T‐Cell Dysfunction

  2017cited by this paper
• Fresolimumab treatment decreases biomarkers and improves clinical symptoms in systemic sclerosis patients.

  2015cited by this paper
• Nickel Allergy Is a Risk Factor for Endometriosis: An 11-Year Population-Based Nested Case-Control Study

  2015cited by this paper
• Simultaneous Detection and Evaluation of Four Subsets of CD4+ T Lymphocyte in Lesions and Peripheral Blood in Endometriosis

  2015cited by this paper
• Freeze and Thaw of CD4+CD25+Foxp3+ Regulatory T Cells Results in Loss of CD62L Expression and a Reduced Capacity to Protect against Graft-versus-Host Disease

  2015cited by this paper
• Restimulation After Cryopreservation and Thawing Preserves the Phenotype and Function of Expanded Baboon Regulatory T Cells

  2015cited by this paper
• The Peritoneum Is Both a Source and Target of TGF-β in Women with Endometriosis

  2014cited by this paper
• T regulatory lymphocytes in patients with endometriosis.

  2014cited by this paper
• Vitamin D in endometriosis: a causative or confounding factor?

  2014cited by this paper
• CD4⁺ CD25⁺ FOXP3⁺ regulatory T cells in peripheral blood and peritoneal fluid of patients with endometriosis.

  2013cited by this paper
• Induction of endometriosis alters the peripheral and endometrial regulatory T cell population in the non-human primate.

  2012cited by this paper
• Human FoxP3+CD4+ regulatory T cells: their knowns and unknowns

  2011cited by this paper
• [Pathogenesis of endometriosis].

  2011cited by this paper
• Cellular and molecular basis for the regulation of inflammation by TGF-beta.

  2010cited by this paper
• Two Distinct Regions of Latency-associated Peptide Coordinate Stability of the Latent Transforming Growth Factor-β1 Complex*

  2010cited by this paper
• The role of Foxp3+ regulatory T-cells in endometriosis: a potential controlling mechanism for a complex, chronic immunological condition.

  2010cited by this paper
• Clinical practice. Endometriosis.

  2010cited by this paper
• Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor.

  2009cited by this paper
• A conditional mouse model for human MUC1-positive endometriosis shows the presence of anti-MUC1 antibodies and Foxp3+ regulatory T cells

  2009cited by this paper
• Regulatory T cells and immune tolerance.

  2008cited by this paper
• TGF-β and Regulatory T Cell in Immunity and Autoimmunity

  2008cited by this paper
• Latent TGF-β binding proteins

  2005cited by this paper
• Latent TGF-beta binding proteins.

  2005cited by this paper
• Global Natural Regulatory T Cell Depletion in Active Systemic Lupus Erythematosus1

  2005cited by this paper
• Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival

  2004cited by this paper
• Compromised Function of Regulatory T Cells in Rheumatoid Arthritis and Reversal by Anti-TNFα Therapy

  2004cited by this paper
• Compromised function of regulatory T cells in rheumatoid arthritis: Reversal by anti-TNF alpha therapy

  2004cited by this paper
• Making sense of latent TGFbeta activation.

  2003cited by this paper
• Making sense of latent TGFβ activation

  2003cited by this paper
• The Role of Cytokines in Endometriosis *

  2003cited by this paper
• Behaviour of Cytokine Levels in Serum and Peritoneal Fluid of Women with Endometriosis

  2003cited by this paper
• Latency-associated peptide prevents skin fibrosis in murine sclerodermatous graft-versus-host disease, a model for human scleroderma.

  2003cited by this paper
• Real-time Monitoring of the Interactions of Transforming Growth Factor-β (TGF-β) Isoforms with Latency-associated Protein and the Ectodomains of the TGF-β Type II and III Receptors Reveals Different Kinetic Models and Stoichiometries of Binding*

  2001cited by this paper
• Role of cytokines in endometriosis.

  2001cited by this paper
• The latent transforming growth factor binding protein (LTBP) family

  2000cited by this paper
• Modulation of transforming growth factor β response and signaling during transdifferentiation of rat hepatic stellate cells to myofibroblasts

  2000cited by this paper
• The latent transforming growth factor beta binding protein (LTBP) family.

  2000cited by this paper
• Pathogenesis of endometriosis.

  1997cited by this paper
• Latent transforming growth factor-beta: structural features and mechanisms of activation.

  1997cited by this paper
• Revised American Society for Reproductive Medicine classification of endometriosis: 1996.

  1997cited by this paper
• Peritoneal Cellular Immunity and Endometriosis

  1997cited by this paper
• Transforming growth factor-beta: a general review.

  1996cited by this paper
• Immunological aspects of endometriosis

  1995cited by this paper
• Transforming Growth Factor-β Activity is Increased in Peritoneal Fluid From Women With Endometriosis

  1994cited by this paper
• Transforming Growth Factor β in Tissue Fibrosis

  1994cited by this paper
• Transforming growth factor beta in tissue fibrosis.

  1994cited by this paper
• Epidemiology of endometriosis.

  1993cited by this paper
• Epidemiology of endometriosis.

  1993cited by this paper
• [Immunological aspects of endometriosis].

  1990cited by this paper
• Deficient cellular immunity in endometriosis.

  1981cited by this paper

• Endometriosis as a Systemic and Complex Disease: Toward Phenotype-Based Classification and Personalized Therapy

  2026cites this paper
• Endometriosis as an immune-mediated disease: pathogenetic mechanisms and therapeutic strategies

  2025cites this paper
• Experimental modeling and treatment of endometriosis using bovhyaluronidase azoximer in an animal model

  2025cites this paper
• Precision Therapeutic and Preventive Molecular Strategies for Endometriosis-Associated Infertility

  2025cites this paper
• The role of TGF-β superfamily in endometriosis: a systematic review

  2025cites this paper
• Immunopathological insights into endometriosis: from research advances to future treatments

  2025cites this paper
• IL-24 producing regulatory T and B lymphocytes in endometriosis

  2025cites this paper
• Association between the level of TGF- β expression and endometriosis: A systematic review and meta-analysis

  2025cites this paper
• Adoptive transfer of regulatory T cells inhibits the progression of endometriosis-like lesions in regulatory T-cell-depleted mice.

  2025cites this paper
• The role of regulatory T-cells in the development of endometriosis.

  2024cites this paper
• The role of systemic and local immunity in the pathogenesis of endometriosis of varying degrees of prevalence of the process: a modern view

  2024cites this paper
• Adenomyosis-associated infertility: an update of the immunological perspective.

  2024cites this paper
• The over-activated peritoneal immune environment in endometriosis is characterised by a lack of PD-1 inhibition

  2024cites this paper
• Foxp3+CD39+CD73+ regulatory T-cells are decreased in the peripheral blood of women with deep infiltrating endometriosis

  2024cites this paper
• The role of innate and adaptive immunity in endometriosis.

  2024cites this paper
• The Expression of TGF-β1, SMAD3, ILK and miRNA-21 in the Ectopic and Eutopic Endometrium of Women with Endometriosis

  2023cites this paper
• Diagnostic significance of neutrophil to lymphocyte ratio in endometriosis: a systematic review and meta-analysis

  2023cites this paper
• ATG8 inhibited endometriosis formation by regulating Treg cells differentiation via integrin α4β1 and Talin-1 interaction.

  2023cites this paper
• Immune and Endocrine Regulation in Endometriosis: What We Know

  2023cites this paper
• Impact of administering umbilical cord‐derived mesenchymal stem cells to cynomolgus monkeys with endometriosis

  2023cites this paper
• The Role of Peritoneal Immunity in Peritoneal Endometriosis and Related Infertility.

  2023cites this paper
• Understanding endometriosis from an immunomicroenvironmental perspective

  2023cites this paper
• Assessment of risk factors for progression and recurrence of ovarian endometriosis

  2023cites this paper
• The enrichment of Arg1+ILC2s and ILCregs facilitates the progression of endometriosis: A preliminary study.

  2023cites this paper
• Features of the relationship between the subpopulation composition and the content of cytokines in the peripheral blood and peritoneal fluid of women with endometriosis

  2023cites this paper
• The prospects of cell therapy for endometriosis

  2023cites this paper
• Decrease in activated regulatory T cell populations in the endometrium during ovulation in endometriosis.

  2023cites this paper
• The Sphingosine 1-Phosphate Axis: an Emerging Therapeutic Opportunity for Endometriosis

  2023cites this paper
• The Role of the Immune System in the Development of Endometriosis

  2022cites this paper
• Role of Th1, Th2, Th17, and regulatory T cells in endometriosis

  2022cites this paper
• SCM-198 Alleviates Endometriosis by Suppressing Estrogen-ERα mediated Differentiation and Function of CD4+CD25+ Regulatory T Cells

  2022cites this paper
• Immunopathogenesis of endometriosis: An overview of the role of innate and adaptive immune cells and their mediators

  2022cites this paper
• Malignant transformation of endometriosis in a laparoscopic trocar site a case report

  2022cites this paper
• Potential impact of COVID-19 pandemic on endometriosis

  2022cites this paper
• Peculiarities of changes in transforming growth factor beta-1, tumour necrosis factor alpha and glycodelin A in newly detected and recurrent external genital endometriosis

  2022cites this paper
• Decreased Fertility in Women with Cesarean Scar Syndrome Is Associated with Chronic Inflammation in the Uterine Cavity.

  2022cites this paper
• The activation of TGF-β signaling promotes cell migration and invasion of ectopic endometrium by targeting NRP2.

  2022cites this paper
• Interleukin-33 Derived from Endometriotic Lesions Promotes Fibrogenesis through Inducing the Production of Profibrotic Cytokines by Regulatory T Cells

  2022cites this paper
• Endometriosis and autoimmunity: Can autoantibodies be used as a non-invasive early diagnostic tool?

  2021cites this paper
• Peritoneal Modulators of Endometriosis-Associated Ovarian Cancer

  2021cites this paper
• 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin potential impacts on peripheral blood mononuclear cells of endometriosis women.

  2021cites this paper
• Myeloid cell subsets that express latency-associated peptide promote cancer growth by modulating T cells

  2021cites this paper
• PCOS, Hashimoto's disease, celiac disease, endometriosis - genetically conditioned autoimmune disorder causing infertility?

  2021cites this paper
• The role of the immune system in the pathogenesis of endometriosis

  2021cites this paper
• Endometriosis-associated Ovarian Clear Cell Carcinoma: A Special Entity?

  2021cites this paper
• A History of Endometriosis Is Associated With Decreased Peripheral NK Cytotoxicity and Increased Infiltration of Uterine CD68+ Macrophages

  2021cites this paper
• Effect of combined contraceptive pill on immune cell of ovarian endometriotic tissue

  2021cites this paper
• Male Sexual and Reproductive Health

  2021cites this paper
• Higher frequency of circulating, but not tissue regulatory T cells in patients with endometriosis.

  2020cites this paper
• Brassica Bioactives Could Ameliorate the Chronic Inflammatory Condition of Endometriosis

  2020cites this paper
• Alteration of systemic and uterine endometrial immune populations in patients with endometriosis

  2020cites this paper
• Effect of nervous stimulation on ovarian steroid secretion in amphibians.

  2020cites this paper
• Ascorbic Acid and Alpha-Tocopherol Contribute to the Therapy of Polycystic Ovarian Syndrome in Mouse Models

  2020cites this paper
• The Natural History of Spontaneously Occurred Endometriosis in Cynomolgus Monkeys by Monthly Follow-Up Laparoscopy for Two Years.

  2020cites this paper
• Role of Regulatory T Cells in Regulating Fetal-Maternal Immune Tolerance in Healthy Pregnancies and Reproductive Diseases

  2020cites this paper
• Fertility Treatment Resulting in Live Births in Women with Asthma – Associated with Perennial Allergy?

  2020cites this paper
• Hypothetical roadmap towards endometriosis: prenatal endocrine-disrupting chemical pollutant exposure, anogenital distance, gut-genital microbiota and subclinical infections.

  2020cites this paper
• The endometrial immune environment of women with endometriosis.

  2019cites this paper
• Anti-inflammatory cytokines in endometriosis

  2019cites this paper
• IL-2 and IL-27 synergistically promote growth and invasion of endometriotic stromal cells by maintaining the balance of IFN-γ and IL-10 in endometriosis.

  2019cites this paper
• Ovulation induction in infertile women with endometriotic ovarian cysts: current evidence and potential pitfalls.

  2019cites this paper
• Endometriosis and risk of ovarian cancer: what do we know?

  2019cites this paper
• CD4+/CD8+ mucosa-associated invariant T cells foster the development of endometriosis: a pilot study

  2019cites this paper
• Roles of regulatory T Cells in pathogenesis of endometriosis

  2019cites this paper
• The involvement of multifunctional TGF-β and related cytokines in pathogenesis of endometriosis.

  2018cites this paper
• The Immunopathophysiology of Endometriosis.

  2018cites this paper
• The link between immunity, autoimmunity and endometriosis: a literature update.

  2018cites this paper