Dietary fucoxanthin increases metabolic rate and upregulated mRNA expressions of the PGC-1alpha network, mitochondrial biogenesis and fusion genes in white adipose tissues of mice

Abstract

The mechanism for how fucoxanthin (FX) suppressed adipose accumulation is unclear. We aim to investigate the effects of FX on metabolic rate and expressions of genes related to thermogenesis, mitochondria biogenesis and homeostasis. Using a 2 × 2 factorial design, four groups of mice were respectively fed a high sucrose (50% sucrose) or a high-fat diet (23% butter + 7% soybean oil) supplemented with or without 0.2% FX. FX significantly increased oxygen consumption and carbon dioxide production and reduced white adipose tissue (WAT) mass. The mRNA expressions of peroxisome proliferator-activated receptor (PPAR) γ coactivator-1α (PGC-1α), cell death-inducing DFFA-like effecter a (CIDEA), PPARα, PPARγ, estrogen-related receptor α (ERRα), β3-adrenergic receptor (β3-AR) and deiodinase 2 (Dio2) were significantly upregulated in inguinal WAT (iWAT) and epididymal WAT (eWAT) by FX. Mitochondrial biogenic genes, nuclear respiratory factor 1 (NRF1) and NRF2, were increased in eWAT by FX. Noticeably, FX upregulated genes of mitochondrial fusion, mitofusin 1 (Mfn1), Mfn2 and optic atrophy 1 (OPA1), but not mitochondrial fission, Fission 1, in both iWAT and eWAT. In conclusion, dietary FX enhanced the metabolic rate and lowered adipose mass irrespective of the diet. These were associated with upregulated genes of the PGC-1α network and mitochondrial fusion in eWAT and iWAT.

Figure 1

O₂ consumption (A), CO ₂ production (B), respiratory quotient (C) and their area under the curve (AUC) of test mice at week 3. Mice were individually placed in metabolic chambers with free access to water and their respective diet and monitored for six days. Values are means and error bars are SD (n = 4). * denotes significant difference between groups HS and HS + F, p < 0.05; # denotes significant difference between groups HF and HF + F, p < 0.05, analyzed by the Student’s t-test. AUCs of O₂ consumption (VO₂), CO₂ production (VCO₂) were analyzed by two-way ANOVA. The AUC of RQ was analyzed by the Wilcoxon rank-sum test.

Figure 2

Thermogenic (A) and mitochondrial homeostasis-related (B) mRNA levels in brown adipose tissue of mice fed test diets for five weeks. Values are means, and error bars are SEM (n = 4). * denotes significant effect by either dietary factor at p < 0.05 analyzed by two-way ANOVA. When an interaction (p < 0.05) between diet and FX existed, the significance of differences among the HS, HS + F, HF and HF + F groups was further analyzed by Duncan’s multiple range test. HS, HS + F, HF and HF + F: As indicated in Figure 1. Relative mRNA expression was measured by real-time qRT-PCR using β-actin as the internal control and normalized to group HS.

Figure 3

Thermogenic gene expressions in epididymal (A) and inguinal (B) white adipose tissue. Values are means, and error bars are SEM (n = 4). * denotes significant effect by either dietary factor at p < 0.05 analyzed by two-way ANOVA. HS, HS + F, HF and HF + F: as indicated in Figure 1. The measurement of relative mRNA expression is as indicated in Figure 2.

Figure 4

Mitochondrial biogenic gene expressions in epididymal (A) and inguinal (B) white adipose tissue. Values are means, and error bars are SEM (n = 4). * denotes significant effect by either dietary factor at p < 0.05 analyzed by two-way ANOVA. HS, HS + F, HF and HF + F: As indicated in Figure 1. The measurement of relative mRNA expression is as indicated in Figure 2.

Figure 5

Mitochondrial homeostatic gene expressions in epididymal (A) and inguinal (B) white adipose tissue. Values are means, and error bars are SEM (n = 4). * denotes significant effect by either dietary factor at p < 0.05 analyzed by two-way ANOVA. HS, HS + F, HF and HF + F: As indicated in Figure 1. The measurement of relative mRNA expression is as indicated in Figure 2.