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2. Sex-specific adipose tissue imprinting of regulatory T cells

Author

Vasanthakumar, A, Chisanga, D, Blume, J, Gloury, R, Britt, K, Henstridge, DC, Zhan, Y, Torres, SV, Liene, S, Collins, N, Cao, E, Sidwell, T, Li, C, Spallanzani, RG, Liao, Y, Beavis, PA, Gebhardt, T, Trevaskis, N, Nutt, SL, Zajac, JD, Davey, RA, Febbraio, MA, Mathis, D, Shi, W, Kallies, A, Vasanthakumar, A, Chisanga, D, Blume, J, Gloury, R, Britt, K, Henstridge, DC, Zhan, Y, Torres, SV, Liene, S, Collins, N, Cao, E, Sidwell, T, Li, C, Spallanzani, RG, Liao, Y, Beavis, PA, Gebhardt, T, Trevaskis, N, Nutt, SL, Zajac, JD, Davey, RA, Febbraio, MA, Mathis, D, Shi, W, and Kallies, A

Abstract

Adipose tissue is an energy store and a dynamic endocrine organ1,2. In particular, visceral adipose tissue (VAT) is critical for the regulation of systemic metabolism3,4. Impaired VAT function-for example, in obesity-is associated with insulin resistance and type 2 diabetes5,6. Regulatory T (Treg) cells that express the transcription factor FOXP3 are critical for limiting immune responses and suppressing tissue inflammation, including in the VAT7-9. Here we uncover pronounced sexual dimorphism in Treg cells in the VAT. Male VAT was enriched for Treg cells compared with female VAT, and Treg cells from male VAT were markedly different from their female counterparts in phenotype, transcriptional landscape and chromatin accessibility. Heightened inflammation in the male VAT facilitated the recruitment of Treg cells via the CCL2-CCR2 axis. Androgen regulated the differentiation of a unique IL-33-producing stromal cell population specific to the male VAT, which paralleled the local expansion of Treg cells. Sex hormones also regulated VAT inflammation, which shaped the transcriptional landscape of VAT-resident Treg cells in a BLIMP1 transcription factor-dependent manner. Overall, we find that sex-specific differences in Treg cells from VAT are determined by the tissue niche in a sex-hormone-dependent manner to limit adipose tissue inflammation.

Published
2020

4. Sex-specific adipose tissue imprinting of regulatory T cells.

Author

Vasanthakumar A, Chisanga D, Blume J, Gloury R, Britt K, Henstridge DC, Zhan Y, Torres SV, Liene S, Collins N, Cao E, Sidwell T, Li C, Spallanzani RG, Liao Y, Beavis PA, Gebhardt T, Trevaskis N, Nutt SL, Zajac JD, Davey RA, Febbraio MA, Mathis D, Shi W, and Kallies A

Subjects
Androgens metabolism, Animals, Chemokine CCL2 immunology, Chromatin genetics, Female, Gene Expression Regulation, Inflammation immunology, Inflammation metabolism, Interleukin-33 immunology, Intra-Abdominal Fat metabolism, Male, Mice, Positive Regulatory Domain I-Binding Factor 1 metabolism, RNA-Seq, Receptors, CCR2 metabolism, Stromal Cells cytology, Stromal Cells immunology, Stromal Cells metabolism, T-Lymphocytes, Regulatory metabolism, Transcription, Genetic, Gonadal Steroid Hormones metabolism, Intra-Abdominal Fat immunology, Sex Characteristics, T-Lymphocytes, Regulatory immunology
Abstract

Adipose tissue is an energy store and a dynamic endocrine organ 1,2 . In particular, visceral adipose tissue (VAT) is critical for the regulation of systemic metabolism 3,4 . Impaired VAT function-for example, in obesity-is associated with insulin resistance and type 2 diabetes 5,6 . Regulatory T (T reg ) cells that express the transcription factor FOXP3 are critical for limiting immune responses and suppressing tissue inflammation, including in the VAT 7-9 . Here we uncover pronounced sexual dimorphism in T reg cells in the VAT. Male VAT was enriched for T reg cells compared with female VAT, and T reg cells from male VAT were markedly different from their female counterparts in phenotype, transcriptional landscape and chromatin accessibility. Heightened inflammation in the male VAT facilitated the recruitment of T reg cells via the CCL2-CCR2 axis. Androgen regulated the differentiation of a unique IL-33-producing stromal cell population specific to the male VAT, which paralleled the local expansion of T reg cells. Sex hormones also regulated VAT inflammation, which shaped the transcriptional landscape of VAT-resident T reg cells in a BLIMP1 transcription factor-dependent manner. Overall, we find that sex-specific differences in T reg cells from VAT are determined by the tissue niche in a sex-hormone-dependent manner to limit adipose tissue inflammation.

Published
2020
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