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Eun-Hui Lee, Michal Itan, Jinsun Jang, Hyeon-Jung Gu, Perri Rozenberg, Melissa K. Mingler, Ting Wen, Jiyoung Yoon, Shi-Young Park, Joo Young Roh, Cheol Soo Choi, Woo-Jae Park, Ariel Munitz, YunJae Jung
Abstract:

Accumulating data have indicated a fundamental role of eosinophils in regulating adipose tissue homeostasis. Here, we performed whole-genome RNA sequencing of the small intestinal tract, which suggested the presence of impaired lipid metabolism in eosinophil-deficient ΔdblGATA mice. ΔdblGATA mice fed a high-fat diet (HFD) showed reduced body fat mass, impaired enlargement of adipocytes, decreased expression of adipogenic genes, and developed glucose intolerance. HFD induced accumulation of eosinophils in the perigonadal white adipose tissue. Concordantly, adipocyte-differentiated 3T3-L1 cells promoted the migration of eosinophils through the expression of CCL11 (eotaxin-1) and likely promoted their survival through the expression of interleukin (IL)-3, IL-5, and granulocyte-macrophage colony-stimulating factor. HFD-fed ΔdblGATA mice showed increased infiltration of macrophages, CD4+ T-cells, and B-cells, increased expression of interferon-γ, and decreased expression of IL-4 and IL-13 in white adipose tissue. Interferon-γ treatment significantly decreased lipid deposition in adipocyte-differentiated 3T3-L1 cells, while IL-4 treatment promoted lipid accumulation. Notably, HFD-fed ΔdblGATA mice showed increased lipid storage in the liver as compared with wild-type mice. We propose that obesity promotes the infiltration of eosinophils into adipose tissue that subsequently contribute to the metabolic homeostasis by promoting adipocyte maturation.

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53 Citation statements (41 references)
1.
“…Excess calorie intake results in chronic inflammation in adipose tissue involving an infiltration of various immune cells [22][23][24][25][26] . In obesity, the infiltrated immune cells promote the production of pro-inflammatory cytokines that inhibit adipogenesis and insulin signalling 27,28 . The total numbers of cells isolated from the perigonadal WAT of HFD-fed ΔdblGATA and WT mice were not significantly different (p = 0.1263, data not shown).…”
2.
“…We suggest that an altered immune environment in the perigonadal fat of HFD-fed ΔdblGATA accounts for the decreased expression of adipogenic genes. The exposure of preadipocytes to pro-inflammatory cytokines inhibits adipogenesis by reducing the expression of Pparg and inhibiting the adipogenic action of insulin 28 . Th1 cytokines, including IFN-γ, can inhibit insulin signalling and lipid droplet formation 27,42 , while Th2 cytokines, including IL-4 and IL-13, can suppress inflammatory responses in adipose tissue 43 .…”
3.
“…Adipose tissue regulates energy homeostasis through the storage of excess calories and the secretion of adipocyte-derived secretory proteins such as leptin, adiponectin, and resistin 10,11 . However, excessive caloric Published: xx xx xxxx OPEN www.nature.com/scientificreports/ 2 SCIentIfIC REPORTS | (2018) 8:9894 | intake induces the overexpansion of adipocytes, which results in inflammatory responses within adipose tissue 12 .Obesity-related metabolic dysfunctions are associated with an excessive infiltration of immune cells and chronic inflammation in adipose tissue 13,14 .Here, we used eosinophil-deficient ∆dblGATA and wild-type (WT) mice to investigate the roles of eosinophils in obesity, adipose tissue maturation, and associated metabolic responses. We performed whole-genome RNA sequencing of the small intestinal tract, which suggested the presence of a defective lipid metabolism in the absence of eosinophils.…”
4.
“…Adipose tissue regulates energy homeostasis through the storage of excess calories and the secretion of adipocyte-derived secretory proteins such as leptin, adiponectin, and resistin 10,11 . However, excessive caloric Published: xx xx xxxx OPEN www.nature.com/scientificreports/ 2 SCIentIfIC REPORTS | (2018) 8:9894 | intake induces the overexpansion of adipocytes, which results in inflammatory responses within adipose tissue 12 .Obesity-related metabolic dysfunctions are associated with an excessive infiltration of immune cells and chronic inflammation in adipose tissue 13,14 .Here, we used eosinophil-deficient ∆dblGATA and wild-type (WT) mice to investigate the roles of eosinophils in obesity, adipose tissue maturation, and associated metabolic responses. We performed whole-genome RNA sequencing of the small intestinal tract, which suggested the presence of a defective lipid metabolism in the absence of eosinophils.…”
5.
“…Obesity-related metabolic dysfunctions are associated with an excessive infiltration of immune cells and chronic inflammation in adipose tissue 13,14 .…”
6.
“…Obesity-related metabolic dysfunctions are associated with an excessive infiltration of immune cells and chronic inflammation in adipose tissue 13,14 .…”
7.
“…S1). Of note, genes associated with lipid metabolism, such as Retnlg, Alox15, and Drd2 [15][16][17] were included in the top 10 downregulated genes (Table S1). Additionally, a GO analysis of the downregulated genes and visualization of a functionally grouped network using the ClueGO plugin 18 suggested a defect in lipase activity (Table S3 and Fig.…”
8.
“…S1). Of note, genes associated with lipid metabolism, such as Retnlg, Alox15, and Drd2 [15][16][17] were included in the top 10 downregulated genes (Table S1). Additionally, a GO analysis of the downregulated genes and visualization of a functionally grouped network using the ClueGO plugin 18 suggested a defect in lipase activity (Table S3 and Fig.…”
9.
“…S1). Of note, genes associated with lipid metabolism, such as Retnlg, Alox15, and Drd2 [15][16][17] were included in the top 10 downregulated genes (Table S1). Additionally, a GO analysis of the downregulated genes and visualization of a functionally grouped network using the ClueGO plugin 18 suggested a defect in lipase activity (Table S3 and Fig.…”
10.
“…Of note, genes associated with lipid metabolism, such as Retnlg, Alox15, and Drd2 [15][16][17] were included in the top 10 downregulated genes (Table S1). Additionally, a GO analysis of the downregulated genes and visualization of a functionally grouped network using the ClueGO plugin 18 suggested a defect in lipase activity (Table S3 and Fig. S2) and a significant decrease in the expression of Lpl was observed ( Fig.…”
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