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

• Published in: Journal of molecular histology Vol. 55; no. 4; pp. 527 - 537
• Main Authors: de Freitas, Raiany A., dos Passos Jr, Rinaldo R., dos Santos, Fernanda C. A., Bressan, Alecsander F. M., Carneiro, Fernando S., Lima, Victor V., Giachini, Fernanda R. C.
• Format: Journal Article
• Language: English
• Published: Dordrecht Springer Netherlands 01.08.2024; Springer Nature B.V
• Subjects: Adipocytes; Adipose tissue; Aorta; Biomedical and Life Sciences; Biomedicine; Blood vessels; Body fat; Cell Biology; Collagen; Connective tissues; Coronary vessels; Cytokines; Developmental Biology; Elastin; Fibers; Interleukin 10; Life Sciences; Morphometry; Original Paper; Phenotypes; Phenotypic plasticity; Phenotyping; Polarized light; Thorax; Uncoupling protein 1; Western blotting; Extracellular matrix; PVAT; Anti-inflammatory; Morphology; Cytokine
• DOI: 10.1007/s10735-024-10202-8
• ISSN: 1567-2379; 1567-2387

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. 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 phenotyping. 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.