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Interleukin-10 deficiency induces thoracic perivascular adipose tissue whitening and vascular remodeling

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Highlights

Absence of endogenous IL-10 reduces total thoracic PVAT.

Brown adipose PVAT whitening is observed in thoracic aortas from IL-10-/- mice.

Thoracic PVAT adipocyte size is augmented and UCP1 expression is reduced in IL-10-/- mice.

Thoracic aortas from IL-10-/- mice display augmented thickness and vascular remodeling.

Remodeling is characterized by augmented collagen-III and reduced elastic fibers.

Abstract

Perivascular adipose tissue (PVAT) is an adipose layer, surrounding blood vessels, with a local modulatory role. Interleukin-10 (IL-10) has been shown to modulate vascular tissue. This study aimed to characterize the endogenous role of IL-10 in vascular remodeling, and PVAT phenoty**. Thoracic aortic segments from control (C57BL/6J) and IL-10 knockout (IL-10−/−) male mice were used. Analyzes of aorta/PVAT morphometry, and elastin, collagen and reticulin deposition were performed. Tissue uncoupling protein 1 (UCP1) was accessed by Western blotting. Endogenous absence of IL-10 reduced total PVAT area (p = 0.0310), and wall/lumen ratio (p = 0.0024), whereas increased vascular area and thickness (p < 0.0001). Total collagen deposition was augmented in IL-10−/−, but under polarized light, the reduction of collagen-I (p = 0.0075) and the increase of collagen-III (p = 0.0055) was found, simultaneously with reduced elastic fibers deposition (p = 0.0282) and increased deposition of reticular fibers (p < 0.0001). Adipocyte area was augmented in the IL-10 absence (p = 0.0225), and UCP1 expression was reduced (p = 0.0420). Moreover, relative frequency of white adipose cells and connective tissue was augmented in IL-10−/− (p < 0.0001), added to a reduction in brown adipose cells (p < 0.0001). Altogether, these data characterize aorta PVAT from IL-10−/− as a white-like adipocyte phenotype. Endogenous IL-10 prevents vascular remodeling and favors a brown-like adipocyte phenotype, suggesting a modulatory role for IL-10 in PVAT plasticity.

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Funding

This work was supported by grants from Fundação de Amparo à Pesquisa do Estado de Mato Grosso [(FAPEMAT), grant number 0212033/2021 (to VVL)], Conselho Nacional do Desenvolvimento Científico e Técnológico [(CNPq), grant number 306166/2019-4 (to FRG)], Federal University of Mato Grosso − 2021 Researcher Fellowship (FRG and VVL), Fundação de Amparo à Pesquisa do Estado de São Paulo [(FAPESP), grant number 2019/19749-8 (to FSC)], and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil [(CAPES), Finance Code 001 (Scholarship to RAF)], in Brazil.

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R.A.F.: Writing - Original Draft, Investigation, Formal analysis; R.R.P.J.: Investigation and methodology; F.C.A.S.: Formal analysis, Resource and Conceptualization; A.F.B.: Investigation and Methodology; F.S.C.: Resource and Methodology; V.V.L.: Project administration and Conceptualization; F.R.G.: Conceptualization, Writing - Review & Editing, Formal analysis.

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Correspondence to Fernanda R. C. Giachini.

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de Freitas, R.A., dos Passos Jr, R.R., dos Santos, F.C.A. et al. Interleukin-10 deficiency induces thoracic perivascular adipose tissue whitening and vascular remodeling. J Mol Histol (2024). https://doi.org/10.1007/s10735-024-10202-8

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  • DOI: https://doi.org/10.1007/s10735-024-10202-8

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