Sex-specific regulation of IL-10 production in human adipose tissue in obesity
BackgroundObesity-associated metabolic complications display sexual dimorphism and can be impacted by cytokines. We previously showed that interleukin-10 (IL-10) was upregulated in white adipose tissue (WAT) of obese women with type 2 diabetes (T2D). Whether this pertains to men is unknown. The aim...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-10-01
|
| Series: | Frontiers in Endocrinology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fendo.2022.996954/full |
| _version_ | 1797995944349794304 |
|---|---|
| author | Narmadha Subramanian Beatriz Tavira Kaisa Hofwimmer Beate Gutsmann Lucas Massier Lucas Massier Julie Abildgaard Julie Abildgaard Anders Juul Anders Juul Mikael Rydén Peter Arner Jurga Laurencikiene |
| author_facet | Narmadha Subramanian Beatriz Tavira Kaisa Hofwimmer Beate Gutsmann Lucas Massier Lucas Massier Julie Abildgaard Julie Abildgaard Anders Juul Anders Juul Mikael Rydén Peter Arner Jurga Laurencikiene |
| author_sort | Narmadha Subramanian |
| collection | DOAJ |
| description | BackgroundObesity-associated metabolic complications display sexual dimorphism and can be impacted by cytokines. We previously showed that interleukin-10 (IL-10) was upregulated in white adipose tissue (WAT) of obese women with type 2 diabetes (T2D). Whether this pertains to men is unknown. The aim of this study was to compare the impact of obesity and T2D on WAT IL-10 levels in men versus women.MethodsPlasma and subcutaneous WAT biopsies were obtained from 108 metabolically well-characterized individuals. WAT IL10 expression/secretion and WAT-resident IL-10-secreting macrophage number were measured. Circulating sex hormone levels were correlated to WAT IL10 expression in 22 individuals and sex hormone effects on macrophage IL10 expression were investigated in vitro.ResultsObese women with T2D showed increased IL10 expression/secretion and IL-10-secreting WAT macrophage number compared to other female groups. This difference was absent in men. Non-obese women and men with T2D showed similar IL-10 levels compared to healthy controls, indicating that T2D alone does not regulate IL-10. Although WAT IL10 expression correlated with serum estrone (E1) concentrations, recombinant E1 did not affect macrophage IL10 expression in vitro.ConclusionWAT IL-10 levels are higher in women with obesity and T2D, but not in men and this effect is primarily attributed to obesity per se. This is less likely to be driven by circulating sex hormones. We propose that the WAT IL-10 might exert protective effects in obesity-associated chronic inflammation in women which could be one of the contributing factors for the decreased morbidity observed in women during obesity than men. |
| first_indexed | 2024-04-11T10:09:42Z |
| format | Article |
| id | doaj.art-981085db62a14ba8a673bc2208419650 |
| institution | Directory Open Access Journal |
| issn | 1664-2392 |
| language | English |
| last_indexed | 2024-04-11T10:09:42Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Endocrinology |
| spelling | doaj.art-981085db62a14ba8a673bc22084196502022-12-22T04:30:09ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922022-10-011310.3389/fendo.2022.996954996954Sex-specific regulation of IL-10 production in human adipose tissue in obesityNarmadha Subramanian0Beatriz Tavira1Kaisa Hofwimmer2Beate Gutsmann3Lucas Massier4Lucas Massier5Julie Abildgaard6Julie Abildgaard7Anders Juul8Anders Juul9Mikael Rydén10Peter Arner11Jurga Laurencikiene12Lipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenLipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenLipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenMedical Department III – Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center, Leipzig, GermanyLipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenMedical Department III – Endocrinology, Nephrology, Rheumatology, University of Leipzig Medical Center, Leipzig, GermanyCentre for Physical Activity Research, Rigshospitalet, University of Copenhagen, Copenhagen, DenmarkDanish Diabetes Academy, Odense University Hospital, Odense, DenmarkDepartment of Growth and Reproduction, Copenhagen University Hospital-Rigshospitalet, Copenhagen, DenmarkDepartment of Clinical Medicine, University of Copenhagen, Copenhagen, DenmarkLipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenLipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenLipid laboratory, Unit of Endocrinology, Department of Medicine Huddinge, Karolinska Institutet, Stockholm, SwedenBackgroundObesity-associated metabolic complications display sexual dimorphism and can be impacted by cytokines. We previously showed that interleukin-10 (IL-10) was upregulated in white adipose tissue (WAT) of obese women with type 2 diabetes (T2D). Whether this pertains to men is unknown. The aim of this study was to compare the impact of obesity and T2D on WAT IL-10 levels in men versus women.MethodsPlasma and subcutaneous WAT biopsies were obtained from 108 metabolically well-characterized individuals. WAT IL10 expression/secretion and WAT-resident IL-10-secreting macrophage number were measured. Circulating sex hormone levels were correlated to WAT IL10 expression in 22 individuals and sex hormone effects on macrophage IL10 expression were investigated in vitro.ResultsObese women with T2D showed increased IL10 expression/secretion and IL-10-secreting WAT macrophage number compared to other female groups. This difference was absent in men. Non-obese women and men with T2D showed similar IL-10 levels compared to healthy controls, indicating that T2D alone does not regulate IL-10. Although WAT IL10 expression correlated with serum estrone (E1) concentrations, recombinant E1 did not affect macrophage IL10 expression in vitro.ConclusionWAT IL-10 levels are higher in women with obesity and T2D, but not in men and this effect is primarily attributed to obesity per se. This is less likely to be driven by circulating sex hormones. We propose that the WAT IL-10 might exert protective effects in obesity-associated chronic inflammation in women which could be one of the contributing factors for the decreased morbidity observed in women during obesity than men.https://www.frontiersin.org/articles/10.3389/fendo.2022.996954/fullIL-10sex-specificadiposemacrophagesobesitywomen |
| spellingShingle | Narmadha Subramanian Beatriz Tavira Kaisa Hofwimmer Beate Gutsmann Lucas Massier Lucas Massier Julie Abildgaard Julie Abildgaard Anders Juul Anders Juul Mikael Rydén Peter Arner Jurga Laurencikiene Sex-specific regulation of IL-10 production in human adipose tissue in obesity Frontiers in Endocrinology IL-10 sex-specific adipose macrophages obesity women |
| title | Sex-specific regulation of IL-10 production in human adipose tissue in obesity |
| title_full | Sex-specific regulation of IL-10 production in human adipose tissue in obesity |
| title_fullStr | Sex-specific regulation of IL-10 production in human adipose tissue in obesity |
| title_full_unstemmed | Sex-specific regulation of IL-10 production in human adipose tissue in obesity |
| title_short | Sex-specific regulation of IL-10 production in human adipose tissue in obesity |
| title_sort | sex specific regulation of il 10 production in human adipose tissue in obesity |
| topic | IL-10 sex-specific adipose macrophages obesity women |
| url | https://www.frontiersin.org/articles/10.3389/fendo.2022.996954/full |
| work_keys_str_mv | AT narmadhasubramanian sexspecificregulationofil10productioninhumanadiposetissueinobesity AT beatriztavira sexspecificregulationofil10productioninhumanadiposetissueinobesity AT kaisahofwimmer sexspecificregulationofil10productioninhumanadiposetissueinobesity AT beategutsmann sexspecificregulationofil10productioninhumanadiposetissueinobesity AT lucasmassier sexspecificregulationofil10productioninhumanadiposetissueinobesity AT lucasmassier sexspecificregulationofil10productioninhumanadiposetissueinobesity AT julieabildgaard sexspecificregulationofil10productioninhumanadiposetissueinobesity AT julieabildgaard sexspecificregulationofil10productioninhumanadiposetissueinobesity AT andersjuul sexspecificregulationofil10productioninhumanadiposetissueinobesity AT andersjuul sexspecificregulationofil10productioninhumanadiposetissueinobesity AT mikaelryden sexspecificregulationofil10productioninhumanadiposetissueinobesity AT peterarner sexspecificregulationofil10productioninhumanadiposetissueinobesity AT jurgalaurencikiene sexspecificregulationofil10productioninhumanadiposetissueinobesity |