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Cited by 267Adipose Tissue and MetabolismLipid metabolism and biosynthesisPeroxisome Proliferator-Activated Receptors

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Up-Regulation of Mitochondrial Activity and Acquirement of Brown Adipose Tissue-Like Property in the White Adipose Tissue of Fsp27 Deficient Mice

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Toh, Shen Yon, Gong, Jingyi, Du, Guoli, Li, John Zhong, Yang, Shuqun, Ye, Jing, Yao, Huilan, Zhang, Yinxin, Xue, Bofu, Li, Qing, Yang, Hongyuan, Wen, Zilong, Li, Peng·2008·PLoS ONE
DOI 10.1371/journal.pone.0002890PMC PMC2483355
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Abstract

Fsp27, a member of the Cide family proteins, was shown to localize to lipid droplet and promote lipid storage in adipocytes. We aimed to understand the biological role of Fsp27 in regulating adipose tissue differentiation, insulin sensitivity and energy balance. Fsp27(-/-) mice and Fsp27/lep double deficient mice were generated and we examined the adiposity, whole body metabolism, BAT and WAT morphology, insulin sensitivity, mitochondrial activity, and gene expression changes in these mouse strains. Furthermore, we isolated mouse embryonic fibroblasts (MEFs) from wildtype and Fsp27(-/-) mice, followed by their differentiation into adipocytes in vitro. We found that Fsp27 is expressed in both brown adipose tissue (BAT) and white adipose tissue (WAT) and its levels were significantly elevated in the WAT and liver of leptin-deficient ob/ob mice. Fsp27(-/-) mice had increased energy expenditure, lower levels of plasma triglycerides and free fatty acids. Furthermore, Fsp27(-/-)and Fsp27/lep double-deficient mice are resistant to diet-induced obesity and display increased insulin sensitivity. Moreover, white adipocytes in Fsp27(-/-) mice have reduced triglycerides accumulation and smaller lipid droplets, while levels of mitochondrial proteins, mitochondrial size and activity are dramatically increased. We further demonstrated that BAT-specific genes and key metabolic controlling factors such as FoxC2, PPAR and PGC1alpha were all markedly upregulated. In contrast, factors inhibiting BAT differentiation such as Rb, p107 and RIP140 were down-regulated in the WAT of Fsp27(-/-) mice. Remarkably, Fsp27(-/-) MEFs differentiated in vitro show many brown adipocyte characteristics in the presence of the thyroid hormone triiodothyronine (T3). Our data thus suggest that Fsp27 acts as a novel regulator in vivo to control WAT identity, mitochondrial activity and insulin sensitivity.

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Figure 1 Fsp27 expression in mice tissue and the morphology of WAT and BAT in Fsp27 −/− mice. A. Tissue distributions of Fsp27 protein by western blot analysis. SI, small intestine; BAT, brown adipose tissue; GWAT, gonadal white adipose tissue; SM, skeletal muscle. β-tubulin was used as a loading control. B. Fsp27 is expressed in differentiated 3T3-L1 adipocytes. FABP (fatty acid binding protein) is used as an adipocyte differentiation marker. Day 0 represents undifferentiated 3T3-L1 fibroblasts. . C. Elevated Fsp27 protein levels in the WAT and liver of leptin deficient (ob/ob) mice. WT, wild type. D. Indirect immunofluorescence showing co-localization of Fsp27 with perilipin (Plin) on lipid droplet surface in Day 8 post differentiated 3T3-L1 cells. E & F. Genotype analyses by PCR (E) and western blot (F) assays using tail genomic DNA and gonadal white adipose tissue (GWAT) lysate, respectively. +/+, +/−, −/− represent wild-type, Fsp27 heterozygous and homozygous mice, respectively. G & H. Morphology of WAT and BAT of wild type and Fsp27 −/− mice. HE, hemotoxylin and eosin staining. EM, electron microscope image. 3 months old mice were used for the experiments. LD, lipid droplets; N, nuclei. Scale bar = 25 µm and 1 µm for HE and EM, respectively. .
Figure 1 Fsp27 expression in mice tissue and the morphology of WAT and BAT in Fsp27 −/− mice. A. Tissue distributions of Fsp27 protein by western blot analysis. SI, small intestine; BAT, brown adipose tissue; GWAT, gonadal white adipose tissue; SM, skeletal muscle. β-tubulin was used as a loading control. B. Fsp27 is expressed in differentiated 3T3-L1 adipocytes. FABP (fatty acid binding protein) is used as an adipocyte differentiation marker. Day 0 represents undifferentiated 3T3-L1 fibroblasts. . C. Elevated Fsp27 protein levels in the WAT and liver of leptin deficient (ob/ob) mice. WT, wild type. D. Indirect immunofluorescence showing co-localization of Fsp27 with perilipin (Plin) on lipid droplet surface in Day 8 post differentiated 3T3-L1 cells. E & F. Genotype analyses by PCR (E) and western blot (F) assays using tail genomic DNA and gonadal white adipose tissue (GWAT) lysate, respectively. +/+, +/−, −/− represent wild-type, Fsp27 heterozygous and homozygous mice, respectively. G & H. Morphology of WAT and BAT of wild type and Fsp27 −/− mice. HE, hemotoxylin and eosin staining. EM, electron microscope image. 3 months old mice were used for the experiments. LD, lipid droplets; N, nuclei. Scale bar = 25 µm and 1 µm for HE and EM, respectively. .CC BY · PubMed Central
Figure 2 Lean phenotype of Fsp27 deficient and leptin/Fsp27 double deficient mice. A. Total lipid content of gonadal white fat pad from 3-month old wild-type (+/+) and Fsp27 mutant (−/−) mice, showing a decrease in lipid content in the WAT of Fsp27 −/− mice. 5 pairs of mice were used for analysis. ***p<0.001. B. Body weight of wild type (WT), Fsp27 deficient (Fsp27 −/−), leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27 −/− ) mice. (wildtype: n = 12; Fsp −/−: n = 12, ob/ob, n = 10; ob/ob/ Fsp27−/−, n = 11, P<0.001)C. Adiposity index of 10 months old wild-type (+/+) and Fsp27 mutant mice (−/−) fed with a normal diet (ND) or high fat diet (HFD). Fsp27 mutant mice have significantly less adipose tissue. (ND: +/+ n = 13, −/− n = 14 , HFD: +/+ n = 12, −/− n = 15) (***p<0.001). D. Adiposity index of 3 months old ob/ob and ob/ob/Fsp27−/− mice. ob/ob: n = 8, ob/ob/ Fsp27−/−: n = 8) (***p<0.001). E. TAG content in gonadal white fat (GWAT) of wild type (WT), Fsp27 mutant (Fsp27 −/−), ob/ob, and ob/ob/ Fsp27−/− mice fed with normal diet. 3 mice were used for each genotype. **p<0.01. F. Fasting serum leptin level in mice under normal diet (ND) or high-fat diet (HFD) feeding conditions. ND: +/+ n = 11, −/− n = 8; HFD: +/+ n = 14, −/− n = 11. *p<0.05, ***p<0.001. G. Increased food intake in Fsp27 mutant and ob/ob/Fsp27 −/− mice. Wild type: n = 15, Fsp27 −/−: n = 17; ob/ob: n = 6, ob/ob/Fsp27 −/−: n = 6. **p<0.01. H. Whole body O2 consumption rate of wild-type or Fsp27 mutant mice fed with a ND or HFD. ND: +/+ n = 14, −/− n = 13, HFD: +/+ n = 16, −/− n = 18. **p<0.01, ***p<0.001. I. Lipolysis rate in GWAT of 3 months old wild type (+/+) and Fsp27 mutant (−/−) mice. Basal refers to no isoproterenol (Iso,1 µM) treatment.. N = 4 for each genotype. *p<0.05. J. Core Body temperature of wild-type (+/+) or Fsp27 mutant (−/−) mice after animals were exposed to cold ( 4°C). −1 refers to core body temperature 1 hr before transfer of mice to 4°C. Fsp27 mutant mice had lower core body temperature when exposed to cold. (+/+ n = 25, −/− n = 20, *p<0.05, **p<0.01, ***p<0.001).
Figure 2 Lean phenotype of Fsp27 deficient and leptin/Fsp27 double deficient mice. A. Total lipid content of gonadal white fat pad from 3-month old wild-type (+/+) and Fsp27 mutant (−/−) mice, showing a decrease in lipid content in the WAT of Fsp27 −/− mice. 5 pairs of mice were used for analysis. ***p<0.001. B. Body weight of wild type (WT), Fsp27 deficient (Fsp27 −/−), leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27 −/− ) mice. (wildtype: n = 12; Fsp −/−: n = 12, ob/ob, n = 10; ob/ob/ Fsp27−/−, n = 11, P<0.001)C. Adiposity index of 10 months old wild-type (+/+) and Fsp27 mutant mice (−/−) fed with a normal diet (ND) or high fat diet (HFD). Fsp27 mutant mice have significantly less adipose tissue. (ND: +/+ n = 13, −/− n = 14 , HFD: +/+ n = 12, −/− n = 15) (***p<0.001). D. Adiposity index of 3 months old ob/ob and ob/ob/Fsp27−/− mice. ob/ob: n = 8, ob/ob/ Fsp27−/−: n = 8) (***p<0.001). E. TAG content in gonadal white fat (GWAT) of wild type (WT), Fsp27 mutant (Fsp27 −/−), ob/ob, and ob/ob/ Fsp27−/− mice fed with normal diet. 3 mice were used for each genotype. **p<0.01. F. Fasting serum leptin level in mice under normal diet (ND) or high-fat diet (HFD) feeding conditions. ND: +/+ n = 11, −/− n = 8; HFD: +/+ n = 14, −/− n = 11. *p<0.05, ***p<0.001. G. Increased food intake in Fsp27 mutant and ob/ob/Fsp27 −/− mice. Wild type: n = 15, Fsp27 −/−: n = 17; ob/ob: n = 6, ob/ob/Fsp27 −/−: n = 6. **p<0.01. H. Whole body O2 consumption rate of wild-type or Fsp27 mutant mice fed with a ND or HFD. ND: +/+ n = 14, −/− n = 13, HFD: +/+ n = 16, −/− n = 18. **p<0.01, ***p<0.001. I. Lipolysis rate in GWAT of 3 months old wild type (+/+) and Fsp27 mutant (−/−) mice. Basal refers to no isoproterenol (Iso,1 µM) treatment.. N = 4 for each genotype. *p<0.05. J. Core Body temperature of wild-type (+/+) or Fsp27 mutant (−/−) mice after animals were exposed to cold ( 4°C). −1 refers to core body temperature 1 hr before transfer of mice to 4°C. Fsp27 mutant mice had lower core body temperature when exposed to cold. (+/+ n = 25, −/− n = 20, *p<0.05, **p<0.01, ***p<0.001).CC BY · PubMed Central
Figure 3 Increased insulin sensitivity in Fsp27 −/ and ob/ob/Fsp27 −/− mice. GTT (A) and ITT (B) experiments using 10-week-old wild type (WT), Fsp27 mutant (Fsp27 −/−), leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27−/−) mice. 6 mice from each group were used for the experiment. *p<0.05; **p<0.01; ***p<0.001. Western blot analysis for levels of IRS-1 and insulin stimulated IRS-1 tyrosine phosphorylation (p-IRS) in the WAT of wild type (WT) and Fsp27 mutant (Fsp27−/−) mice (C) and in the WAT of leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27−/−) mice (D). . E & F. Western blot analysis of total AKT2, phosphor-AKT2 (pAKT2) and GLUT4 protein levels in WAT of wild type (WT), Fsp27 mutant (Fsp27−/−), leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27−/−) mice. β-actin was used as loading control.
Figure 3 Increased insulin sensitivity in Fsp27 −/ and ob/ob/Fsp27 −/− mice. GTT (A) and ITT (B) experiments using 10-week-old wild type (WT), Fsp27 mutant (Fsp27 −/−), leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27−/−) mice. 6 mice from each group were used for the experiment. *p<0.05; **p<0.01; ***p<0.001. Western blot analysis for levels of IRS-1 and insulin stimulated IRS-1 tyrosine phosphorylation (p-IRS) in the WAT of wild type (WT) and Fsp27 mutant (Fsp27−/−) mice (C) and in the WAT of leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27−/−) mice (D). . E & F. Western blot analysis of total AKT2, phosphor-AKT2 (pAKT2) and GLUT4 protein levels in WAT of wild type (WT), Fsp27 mutant (Fsp27−/−), leptin deficient (ob/ob) and leptin/Fsp27 double deficient (ob/ob/Fsp27−/−) mice. β-actin was used as loading control.CC BY · PubMed Central
Figure 4 Increased mitochondria activity in the WAT of Fsp27 mutant mice. A. Electron microscope image of mitochondria in gonadal WAT (GWAT) (Scale Bar = 0.2 µm) and BAT (Scale Bar = 0.5 um) of wild-type and Fsp27−/− mice showing enlarged mitochondria in Fsp27 −/− mice. N: nucleus, L: lipid droplet, M: mitochondria. B. Cytochrome oxidase IV (Cox) activity in GWAT, BAT, muscle and liver (n = 4). COXIV activity in Fsp27 −/− mice is higher in GWAT (*p<0.05), but lower in BAT (**p<0.01) as compared with that of wild type mice. No difference in COX activity is detected in muscle or liver. C. Mitochondrial oxygen consumption rate is higher in WAT of Fsp27 −/− mice. (*p<0.05) (n = 3). D. Western blot analysis of various mitochondrial proteins in the WAT of wild-type and Fsp27 mutant mice, showing higher level in Fsp27 mutant WAT. (n = 4), CytoC, cytochrome C. β-tubulin was used as loading control. D. Relative mRNA levels of COXIV, CPT1 and CPT2 in the WAT of wild type (+/+) and Fsp27 mutant mice (−/−).
Figure 4 Increased mitochondria activity in the WAT of Fsp27 mutant mice. A. Electron microscope image of mitochondria in gonadal WAT (GWAT) (Scale Bar = 0.2 µm) and BAT (Scale Bar = 0.5 um) of wild-type and Fsp27−/− mice showing enlarged mitochondria in Fsp27 −/− mice. N: nucleus, L: lipid droplet, M: mitochondria. B. Cytochrome oxidase IV (Cox) activity in GWAT, BAT, muscle and liver (n = 4). COXIV activity in Fsp27 −/− mice is higher in GWAT (*p<0.05), but lower in BAT (**p<0.01) as compared with that of wild type mice. No difference in COX activity is detected in muscle or liver. C. Mitochondrial oxygen consumption rate is higher in WAT of Fsp27 −/− mice. (*p<0.05) (n = 3). D. Western blot analysis of various mitochondrial proteins in the WAT of wild-type and Fsp27 mutant mice, showing higher level in Fsp27 mutant WAT. (n = 4), CytoC, cytochrome C. β-tubulin was used as loading control. D. Relative mRNA levels of COXIV, CPT1 and CPT2 in the WAT of wild type (+/+) and Fsp27 mutant mice (−/−).CC BY · PubMed Central
Figure 5 Altered expression levels of crucial metabolic regulators and BAT-specific factors in Fsp27 mutant mice. A. Real-time PCR analysis of regulatory factors and BAT specific gene expression in the WAT of wild type (+/+) and Fsp27−/− mice (−/−). Significantly higher levels of BAT markers expression in Fsp27 mutant mice WAT were detected (*p<0.05; **p<0.01). B. Western blot analysis showing increased protein levels of Cidea, PGC1α, Ucp1 and FABP in the WAT of wildtype, ob/ob, Fsp27− /− and ob/ob/Fsp27− /−of Fsp27 mutant mice. β-tubulin was used as loading control. C. Densitometric reading of relative levels of the indicated proteins in western blot analysis (as in B) were quantitated in these mouse strains. Similar experiments were done five times and the intensity of individual band in each western blot was quantified by TOTAL-LAB software (Nonlinear Dynamics, UK) and used for statistical analysis. The relative protein level in wildtype and ob/ob mice was designated as 1.0. **p<0.01.
Figure 5 Altered expression levels of crucial metabolic regulators and BAT-specific factors in Fsp27 mutant mice. A. Real-time PCR analysis of regulatory factors and BAT specific gene expression in the WAT of wild type (+/+) and Fsp27−/− mice (−/−). Significantly higher levels of BAT markers expression in Fsp27 mutant mice WAT were detected (*p<0.05; **p<0.01). B. Western blot analysis showing increased protein levels of Cidea, PGC1α, Ucp1 and FABP in the WAT of wildtype, ob/ob, Fsp27− /− and ob/ob/Fsp27− /−of Fsp27 mutant mice. β-tubulin was used as loading control. C. Densitometric reading of relative levels of the indicated proteins in western blot analysis (as in B) were quantitated in these mouse strains. Similar experiments were done five times and the intensity of individual band in each western blot was quantified by TOTAL-LAB software (Nonlinear Dynamics, UK) and used for statistical analysis. The relative protein level in wildtype and ob/ob mice was designated as 1.0. **p<0.01.CC BY · PubMed Central
Figure 6 Differentiated Fsp27−/− MEFs display many brown adipocyte characteristics. A. Smaller lipid droplets in differentiated Fsp27 mutant mouse embryonic fibroblasts (MEFs). Lipid droplets were stained with BODIPY493/503, and nuclei were stained with Hochest 366243. Fields shown were visualized under fluorescence microscope at appropriate wavelengths for GFP (green) and Hoechst (blue). B. Lower TAG accumulation in differentiated Fsp27−/− MEFs (−/−) than in wildtype (+/+) cells. (n = 4) (**p<0.01; ***p<0.001). C. Increased basal lipolysis rate in differentiated Fsp27−/− MEFs in the absence or presence of T3 (10 nM) in the differentiation medium. (n = 3) (*p<0.05; **p<0.01). D. Western blot analysis showing levels of various proteins in differentiated MEF cells in the absence or presence of T3 (10 nM). β-tubulin was used as a loading control. E. Relative mRNA levels of various genes in differentiated wildtype (+/+) and Fsp27−/−(−/−)MEFs. mRNA levels for Rb were measured using MEFs that were differentiated for 3 days. (n = 4) (*p<0.05). F. Higher levels of fatty acid β-oxidation rate in differentiated Fsp27−/− (−/−) MEFs as compared to wildtype (+/+) MEFs in the presence of T3 (10nM). (n = 4) (**p<0.01). Results of relative amount of 3H2O released into the medium after four (4h) or six (6h) hours chase of pre-labelled MEFs with cold palmitate. Wildtype oxidation rate at 4h is set to 100. G. Regulatory and metabolic pathways that are altered in the WAT of Fsp27−/− mutant mice, leading to anti-obesity and insulin sensitive phenotype.
Figure 6 Differentiated Fsp27−/− MEFs display many brown adipocyte characteristics. A. Smaller lipid droplets in differentiated Fsp27 mutant mouse embryonic fibroblasts (MEFs). Lipid droplets were stained with BODIPY493/503, and nuclei were stained with Hochest 366243. Fields shown were visualized under fluorescence microscope at appropriate wavelengths for GFP (green) and Hoechst (blue). B. Lower TAG accumulation in differentiated Fsp27−/− MEFs (−/−) than in wildtype (+/+) cells. (n = 4) (**p<0.01; ***p<0.001). C. Increased basal lipolysis rate in differentiated Fsp27−/− MEFs in the absence or presence of T3 (10 nM) in the differentiation medium. (n = 3) (*p<0.05; **p<0.01). D. Western blot analysis showing levels of various proteins in differentiated MEF cells in the absence or presence of T3 (10 nM). β-tubulin was used as a loading control. E. Relative mRNA levels of various genes in differentiated wildtype (+/+) and Fsp27−/−(−/−)MEFs. mRNA levels for Rb were measured using MEFs that were differentiated for 3 days. (n = 4) (*p<0.05). F. Higher levels of fatty acid β-oxidation rate in differentiated Fsp27−/− (−/−) MEFs as compared to wildtype (+/+) MEFs in the presence of T3 (10nM). (n = 4) (**p<0.01). Results of relative amount of 3H2O released into the medium after four (4h) or six (6h) hours chase of pre-labelled MEFs with cold palmitate. Wildtype oxidation rate at 4h is set to 100. G. Regulatory and metabolic pathways that are altered in the WAT of Fsp27−/− mutant mice, leading to anti-obesity and insulin sensitive phenotype.CC BY · PubMed Central

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Authors
Toh, S. Y., Gong, J., Du, G., Li, J. Z., Yang, S., Ye, J., Yao, H., Zhang, Y., Xue, B., Li, Q., Yang, H., Wen, Z., & Li, P.
Affiliations
  • Hong Kong University of Science and Technology (HK)
  • Tsinghua University (CN)
  • Air Force Medical University (CN)
  • UNSW Sydney (AU)
Corresponding author
Li, Peng
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2008-08-06
Volume
3
Issue
8
Pages
e2890
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0002890
PMC
PMC2483355
OpenAlex
W1998949529
Cited by
267
References
47
Citations by year
2026: 7 · 2025: 9 · 2024: 10 · 2023: 7 · 2022: 10 · 2021: 7 · 2020: 8 · 2019: 11 · 2018: 11 · 2017: 17 · 2016: 11 · 2015: 21 · 2014: 24 · 2013: 28 · 2012: 25
FWCI
13.81
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • National University of Singapore
  • National Natural Science Foundation of China (30530350)
  • Ministry of Education of the People's Republic of China (704002)
  • Tsinghua University
  • Xiamen University
  • Changjiang Scholar Program of Chinese Ministry of Education
  • National Key Research and Development Program of China (2007CB914404, 2006CB503900)
  • Program for Changjiang Scholars and Innovative Research Team in University
Topics
  • Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
Keywords
FSP27, white adipose tissue, brown adipose tissue, mitochondrial activity, insulin sensitivity, energy balance, diet-induced obesity, leptin, lipid droplets, adipogenesis, FOXC2, PGC-1α, peroxisome proliferator-activated receptors, RIP140, triiodothyronine, ob/ob mice
MeSH terms
Adipose Tissue, Animals, Adipose Tissue, Brown, Gene Expression Regulation, Insulin, Mice, Obese, Mitochondria, Phenotype, Proteins, Thinness, Mice, Knockout, Leptin, Gene Expression Profiling, Mice

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