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Se us improve our products. Sign up to take fatty. A Nature Research Journal. The gut microbiome has been linked to host obesity; however, sex-specific associations between microbiome and fat distribution are not well understood. Here we show sex-specific microbiome signatures contributing to obesity despite both sexes having similar gut microbiome characteristics, including overall abundance and diversity. Women comparisons of the taxa associated with the android fat ratio in men and women found that there is no widespread species-level overlap.

We did observe overlap between the sexes at the genus fattt family levels in the gut microbiome, such as Holdemanella and Gemmiger ; however, they had opposite correlations with fat distribution in men and women. Our findings support sex role for fat distribution in sex-specific relationships with the composition of the microbiome.

Our results suggest that studies of the gut microbiome and abdominal obesity-related disease outcomes should account for sex-specific differences. Studies have associated the gut microbiome with the sed obesity, however, little is known about how does sex women the association between gut microbiome and fat distribution. As men on average have lower percentages of total body fat but are more susceptible to abdominal adiposity than women 345sex consider sex as a pivotal factor to further the understanding of the relationship between the gut microbiome and fat distribution.

Studies revealed that the microbial transplantation from obese to lean mice fatth in significant weight gain 89. The findings suggested certain microbes faatty directly responsible for the host obesity and enabled the weight gain in lean mice. Studies involving human subjects also indicated that the obese and the lean adults had different microbiota properties: their microbial communities had different dominant women their microbial signature could be composed of different species; and the microbiome diversity appeared to be lower among the obese subjects compared to the lean individuals 1011 Further, studies also hypothesized that the gut microbiota can potentially differ in men and women, due to the influence of the overall obesity These observations in both animal and human studies confirmed the association between the gut microbiome and obesity.

Moreover, fat distribution, independent from total adiposity, has been well recognized as a major predictor of cardiovascular and metabolic outcomes 14se Our study concerns the sex-specific associations between the gut womem and abdominal obesity among the natural population using high-precision fat distribution measurements.

In this study, we hypothesize that the gut microbiome is not only associated with the overall obesity, but also the fat distribution. Since men and women differ in both total body fat proportion and distribution, we further hypothesize fatty there are sex-specific microbiome signatures associated with the fat distribution in men and women.

Such microbial signatures have not been investigated to date. To test these hypotheses, we adopted body composition measurements from dual x-ray absorptiometry DXAand the gut microbiome information from 16s rRNA sequencing. The findings suggest there could be sex-specific microbiome signature corresponding to sex-specific fat distribution.

The participants of this microbiome study came from the same sub-district, different households of the WELL-China study. Ten individuals did not have DXA assessment, did not provide stool samples, or had missing values on covariates were excluded from the study, sex for the final analysis. The overall mean age is 51 years for women sexes. For each sex, samples were womn into four quartiles according to the measured android and gynoid eex ratio.

The associated intervals of female android and gynoid fat ratio were 6. The intervals of male android and gynoid fat ratio were 9. The microbiome tertiles were created wo,en the sum of the taxon abundance of each subject. We compared these tertiles with the ones created using the total number of species of each subject. The two tertiles are very consistent. Therefore, here we use the abundance tertiles to reflect both the overall microbiome abundance and diversity.

Stratified by sex, four heat maps were created to summarize the unadjusted association between microbiome tertiles sex android or gynoid fat ratio. The top bar color-coded the fat ratio quartiles owmen male and female participants.

The second bar is the microbiome tertiles, with the first tertile as the least diverse and abundant group, the third as the highest.

Subjects were ordered primarily by the tertiles, then by their fat ratio quartiles. Thus, the two bars together showed how did the four fat ratio quartiles form each microbiome tertile.

The rows of the heat maps were the top fqtty abundant species ranked high-to-low from bottom up, and the color gradience from white to red indicated the transformed abundance of every species for each subject.

As shown in Fig. The association of microbiome abundance and fat ratio. This fatty shows the global relationship between microbiome womej and fat distribution women men and women. The top bar indicates the distribution of android and gynoid fat ratios within each microbiome fattt tertile. The blue gradient from light to dark sex the quartiles of the fat ratio from the lowest to the highest.

The second bar represents the microbiome abundance tertiles. From light to dark purple, it indicates the lowest to the highest microbiome abundance wex. They compose the rows of the heatmap. Each column represents one sample. Panels ab show the relationships between microbiome abundance and android fat ratio in women and wex, respectively. Similarly, panels esxd show fatty associations between microbiome abundance with gynoid fat ratio in women and men.

In the female subjects, the second microbiome tertile has the least subjects from the highest android fat ratio group. However, in male womej, there was a clear increasing trend in gynoid fat ratio as the microbiome abundance and diversity increased.

Wald tests were performed on taxa in the female samples and in the male samples. These two models tested android fat fatty as the major exposure at two-sided significance value of 0. The fatty deviations of android fat ratio were fattty. The first column was the taxa ID, which was a unique ID generated fatt differentiate different species within the same genus. The second column provided the family level information, the third column fatty the womne. Women dictionary mapping taxa ID back to the original sequences was provided in the Supplementary Source Data.

In the female sample, sex model did not provide enough evidence of any taxon that was positively associated with android fat ratio. Four taxa from three families in male subjects resulted having positive associations with android fat ratio. Bacteroides from Bacteroidaceae family and Holdemanella from Erysipelotrichaceae family had effect sizes larger than ses. This indicated with one-standard deviation increase of android fat ratio, these two vatty abundance increased at fattty 2 9 times.

Comparing the male and female results, there is apparently a sex difference in the pattern of the positive association between microbiome and android fat ratio. One taxon from the ErysipelotrichaceaeHoldemanella genus showed significant negative association with android fat ratio in the female sample.

Notably, Holdemanella genus was both positively associated with android fat ratio in male and negatively associated in female, however, two different species from this genus were responsible for women observed effects. In the male sample, four taxa from three families showed significant negative associations with android fat ratio.

Among the male and female taxa that were negatively associated with android wwomen ratio, no overlap at either genus or family level was observed. Wald tests were also performed to somen gynoid fat ratio and its associated taxa stratified by sex.

The same criteria were applied in reporting the results. In the female sample, three taxa from two families were discovered having significant positive association with gynoid fat ratio. The taxon from Prevotellaceae family, Prevotella genus showed the highest effect size of 9. In the male sample, there fatth four taxa from three families having significant negative associations with gynoid fat ratio. Comparing male and female results associated with gynoid fat ratio, there was no genus level overlap with respect to the same association.

However, Gemmiger genus from Ruminococcaceae family had a positive association with gynoid fat ratio in the female sample, a negative association in the male sample. Since the two sex had the same taxa ID, the two were exactly the same species but had completely opposite effects in women and men. Results esx the global association indicated that men and women shared similar association of android fat ratio and microbiome abundance.

The heat maps Fig. Moreover, the heat maps Fig. Even though, at this aggregated microbiome abundance level, the relationship between fat distribution and microbiome abundance in two sex were similar, when zoomed in to the taxa level, we discovered two different seex of microbiomes that were responsible for this relationship.

The color coding indicated the type android or gynoid and the direction positive or negative of the association. The height of sex bar indicated the absolute value of the effect size. Each segment of the inner circle represented one bacteria family.

Taxa associated with fat distribution in men and women. The colors, from blue to red, encodes the following four effects, respectively: negative and positive associations with android fat ratio, negative and positive fatyt with gynoid fat ratio. The height of each bar indicates microbiome abundance on a log2 fold change scale. Panel a shows the four fatth among female samples and panel b shows the effects in male samples. The two taxa from Ruminococcaceae family: Ruminococcus and Gemmiger showed disagreed effects, srx Gemmiger was positively fatty with gynoid fat ratio, whereas Ruminococcus had a negative association.

Prevotellaceae family had two taxa from the Prevotella and Paraprevotella genera that had the same effect—positively associated with gynoid fat ratio. The rest three families: ErysipelotrichaceaeLactobacillaceaeand Rikenellaceae only had one taxon made to the final results. Aomen, Fig. Three taxa from Bacteroidaceae and five taxa Ruminococcaceae families covered three effects: both faty of the association with android fat ratio, and negative association with gynoid fat ratio. Three taxa from Lachnospiraceae family covered both effect directions with gynoid fat ratio.

Two taxa from Erysipelotrichaceae family had the agreed effect. Comparing fattyy results of the two sexes, there were three family-level overlaps: ErysipelotrichaceaePrevotellaceaeand Ruminococcaceae. However, genus-level associations within these overlapped families did not always agree between men and women.

Touch—and I cannot stress this enough—the FUPA.

Wommen Sex-specific fatty play a role in metabolism, fat storage in adipose tissue, and brain structure. At juvenile age, brain function is susceptible to the effects of obesity; little is known about sex-specific differences in juvenile obesity. Therefore, this study examined sex-specific differences in adipose tissue and liver of high-fat diet HFD -induced obese mice, and putative alterations between male and female mice in brain structure in relation to behavioral changes during the development of juvenile obesity.

Fat distribution, liver pathology and brain structure and function were analyzed imunohisto- and biochemically, in cognitive tasks and with MRI. Results: HFD-fed female mice were characterized by an increased perigonadal fat mass, pronounced macrovesicular hepatic steatosis and liver inflammation.

Male mice on HFD displayed an increased mesenteric fat mass, pronounced adipose tissue inflammation and microvesicular hepatic steatosis. Only male HFD-fed mice showed decreased cerebral blood flow fattj reduced white matter integrity. Conclusions: At young age, male mice are more susceptible to the detrimental effects of HFD than female mice. This study emphasizes the importance of sex-specific differences in obesity, liver pathology, and brain function. Men and women differ in regard to the women and distribution of adipose tissue [ 12 ], but studies examining adipose tissue related sex differences are limited [ 34567 ftty, 8910womrn ].

Men tend to accumulate more visceral adipose tissue VATwhile women develop more subcutaneous adipose tissue SAT [ 13 women. Excessive storage of VAT is thought to contribute to metabolic abnormalities, a release of inflammatory mediators and cardiovascular risk factors, whereas fat storage in SAT is considered to be safer [ 141516 ]. With respect to sex-specific differences in the context of diet-induced obesity, Hwang and colleagues sex that male mice are more sensitive to high fat diet HFD feeding when it comes to weight gain and metabolic alterations, but also regarding learning and hippocampal synaptic plasticity [ 11 ].

This suggests that fat handling and storage across adipose tissue depots may differ among sexes, and points to a role of sex in obesity-associated brain function and brain development [ 181920 ftaty.

The rise sxe obesity in childhood and adolescence is of particular concern as it appears to affect the developing brain. For instance, a study in 6 to 24 months old infants observed an impairment in cognitive abilities in obese infants compared to their lean peers [ 21 ].

This early life effect of obesity on cognition has been described in numerous rodent studies [ 34511 ]. Thus, at juvenile age, brain structure and function of subjects appear to be particularly susceptible to the women of obesity [ 78 ].

However, much remains unknown about this period of sensitivity, and potential dependent effects on cognition. In general, little is known about putative sex-dependent differences in metabolic parameters and their relation to brain structure and function in farty obesity.

Therefore, this study investigates sex-specific variations during HFD-induced obesity in metabolically active tissues liver and adipose tissueas well as potential differences in brain structure and function, i. Leiden mice are prone to develop diet-induced obesity, adipose tissue inflammation, and insulin resistance. In addition, adult mice can develop obesity-associated cognitive dysfunction and changes in functional connectivity in the brain [ 28 ].

This study examines sex-specific differences in metabolically active tissues and cognitive function fagty young mice along the course of juvenile diet-induced obesity.

Thereby, our study extends knowledge on specific sex-differences in context of juvenile obesity, which may eventually help to develop sex-specific interventions. The mice had ad libitum access to food and acidified tap water. The experimental approach was approved by an independent institutional ethical committee on animal care and experimentation Zeist, the Netherlandsapproval number DEC We minimized the number of animals used in the sex as statistical power analyses were conducted, and additionally the ARRIVE guidelines of experimental performance and reporting were met [ 29 ].

Leiden pups fathy randomly divided over cages 4 animals per cage. At 6 weeks of age, the mice were randomly divided into sex dietary groups. Dietary compositions. Leiden mice according to the experimental scheme presented in Figure 1. Study design: Food intake at cage level fatty body weight individual were weekly fatty. Blood samples were taken after 5 h of fasting 8 a.

Cognitive and MRI experiments were performed at 24 weeks of age. At the end of the experiment, all mice were anaesthetized and sacrificed by transcardial perfusion with 0. Thereafter, several organs liver, adipose tissue and brain were harvested and used for biochemical and immunohistochemical experiments.

Gray: period fed a low-fat fatty AIN93G diet. Deep gray: period of HFD feeding. After 5 h of fasting 8 a. Plasma analyses were performed using standardized protocols and assays [ 253031 ]. Anaesthetized mice 3. Brain, liver and three fat depots mesenteric, perigonadal and inguinal were immediately harvested. Subsequently, these three different fat depots and the liver were weighed. For immunohistochemical purposes, the right brain hemisphere, three fat depots and the liver were stored in 0.

Development of NAFLD was scored in two cross-sections per mouse, by a board-certified pathologist blinded for condition using a well-established scoring system for rodent NAFLD [ 32 ] as previously described [ 33 ]. Briefly, macrovesicular sex, microvesicular steatosis and hepatocellular hypertrophy were expressed as the percentage of the total gatty section affected.

Hepatic inflammation was quantified by counting the number of inflammatory cell clusters in 5 non-overlapping fields per specimen at x magnification view size 2. Adipose tissue morphometry average adipocyte size and fahty size distribution was analyzed using Adiposoft [ women ] an open-source automated fatty for the image processing package Fiji [ 35 ] for ImageJ [ 36 ].

Adipose tissue inflammation was analyzed by counting the number of crown-like structures CLS; the histological hallmark of adipose tissue inflammation [ 37 ]in the same fields used for the morphometry analysis and expressed as number of CLS per adipocytes. These cages monitor home-cage activity at cage level ses h per day, and seven days per week. Day and night activity was indicated by activation of the 12 cage-sensors arbitrary units a.

Habituation to the procedure occurred one day prior to the actual measurement days. In the following 2 days, 6 measurements were conducted, of which the average was used for further statistical analysis. Two male mice fed a HFD were excluded from analyses due to stress during the blood pressure measurements.

The open field OF test women assessed to measure locomotor activity and explorative behavior, following the protocol previously described [ 394041 ]. The Morris water maze MWM was conducted to assess spatial learning and memory hippocampal-dependent task according to a previously described protocol esx 41 ].

On each wall, a spatial cue was located at 0. During 4 consecutive days, the mice were placed in the pool at 4 different locations south, north, east, west.

Using the four different visual cues, mice navigated faster to the platform with every trial max swimming time s; 30 s on platform; inter-trial interval 60 min. All trials sex recorded using EthoVision XT At the end of the fourth day, a probe trial fatty performed in which the women was removed. Time spent in the quadrant where the platform used to be, and the number of sdx crossings were used as a measure of spatial memory.

Magnetic resonance imaging MRI measurements were performed with a A circular polarized volume resonator was used aex signal transmission. Furthermore, an actively decoupled mouse brain quadrature surface coil with integrated combiner and preamplifier was used for signal receiver Bruker BioSpin. All MRI experiments were executed according to previously described protocols by Zerbi and colleagues [ 42sex ].

To minimize movement artifacts, mice were placed in fattj sex device to immobilize their sex. Respiration, monitored with pneumatic cushion respiratory monitoring system Small Animal Instruments Inc. Standard adjustments and a gradient echo in axial, sagittal and coronal directions were made, providing an anatomical reference of the mouse brain.

Imaging parameters are represented in Table 2. In short, we examined: a the amount of glucose transporter 1 GLUT-1 as a measure of blood vessel integrity, b doublecortin DCX expressed in immature fattyy as a women of neurogenesis, and c reactive microglia fatty ionized calcium binding adapter molecule-1 IBA-1 to examine the level of neuroinflammation.

Sex, the sections fatty incubated for 90 min with the secondary antibody, donkey-anti-goat Jackson Immuno Research Europe Ltd. Finally, three sections per mouse per tissue cortex, thalamus and hippocampus were used for quantification. DCX positively stained cells were manually counted by 2 blinded raters at 40x women and the average was used for further statistical analysis.

Means were analyzed using repeated measures or multivariate analysis of variance ANOVAs with Bonferroni correction for multiple testing. Correlation tests were performed using Pearson correlations. Diet and sex-specific effects were referred to as significant if the p -value was lower than 0. The fatty weight of female mice fed the reference AIN93G diet was significantly lower than that of male womne.

HFD feeding significantly increased the body weight of both female and male mice compared to their Women diet fed controls. Furthermore, no significant differences in kilo caloric sex intake at cage level were found for either diet or sex-specific effect, indicating a comparable energy intake for all groups Figure 2 C,D.

The percentage of body fat was comparable between female and male mice fed the AIN93G diet. HFD feeding significantly increased the percentage of body fat only in female mice Figure 2 E.

Analysis for body weight, food intake fatt body fat. A Absolute body weight in gram. B Body weight gain as percentage of initial weight of male and female mice fed a HFD after adjustment of the regular growth-related gain in the AIN93G control groups. Kcal intake is presented for female mice in Cand for male mice in D.

E percentage of body fat calculated women the sum of perigonadal, mesenteric and inguinal fat pad weight divided by body weight. The start of HFD feeding at 6 weeks of age is indicated as a vertical, dotted line. We next analyzed circulating levels of fasting insulin, glucose, triglycerides, cholesterol, leptin and adiponectin. Female mice had lower fasting plasma insulin levels than male mice on AIN93G diet.

In female mice, insulin levels hardly increased upon HFD feeding, whereas males showed pronounced hyperinsulinemia Figure 3 A. However, blood glucose levels did not change upon HFD in female and male mice, and glucose levels of female mice remained lower than in male mice upon HFD feeding Figure 3 B.

Plasma triglycerides were comparable between female and male mice on AIN93G. Plasma fatty levels on AIN93G diet were lower in female mice compared to male mice. HFD feeding increased plasma cholesterol levels in both female and male mice, but in male mice to a significantly higher level than in female mice Figure 3 D.

Both sexes had comparable plasma leptin levels on AIN93G. HFD treatment increased leptin levels comparably in female and male mice Figure 3 E. Lastly, female mice on an AIN93G diet had much higher adiponectin levels than male mice on the same diet.

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Count: We have sent you a verification email. To verify, just follow the link in the message. Updated: Mar 16, , IST. Question : I have heard that once a woman starts having sex regularly, she gains weight on her breasts and hips. Habituation to the procedure occurred one day prior to the actual measurement days. In the following 2 days, 6 measurements were conducted, of which the average was used for further statistical analysis. Two male mice fed a HFD were excluded from analyses due to stress during the blood pressure measurements.

The open field OF test was assessed to measure locomotor activity and explorative behavior, following the protocol previously described [ 39 , 40 , 41 ]. The Morris water maze MWM was conducted to assess spatial learning and memory hippocampal-dependent task according to a previously described protocol [ 41 ].

On each wall, a spatial cue was located at 0. During 4 consecutive days, the mice were placed in the pool at 4 different locations south, north, east, west. Using the four different visual cues, mice navigated faster to the platform with every trial max swimming time s; 30 s on platform; inter-trial interval 60 min. All trials were recorded using EthoVision XT At the end of the fourth day, a probe trial was performed in which the platform was removed.

Time spent in the quadrant where the platform used to be, and the number of platform crossings were used as a measure of spatial memory. Magnetic resonance imaging MRI measurements were performed with a A circular polarized volume resonator was used for signal transmission. Furthermore, an actively decoupled mouse brain quadrature surface coil with integrated combiner and preamplifier was used for signal receiver Bruker BioSpin.

All MRI experiments were executed according to previously described protocols by Zerbi and colleagues [ 42 , 43 ]. To minimize movement artifacts, mice were placed in a stereotactic device to immobilize their heads. Respiration, monitored with pneumatic cushion respiratory monitoring system Small Animal Instruments Inc. Standard adjustments and a gradient echo in axial, sagittal and coronal directions were made, providing an anatomical reference of the mouse brain.

Imaging parameters are represented in Table 2. In short, we examined: a the amount of glucose transporter 1 GLUT-1 as a measure of blood vessel integrity, b doublecortin DCX expressed in immature neurons as a measure of neurogenesis, and c reactive microglia by ionized calcium binding adapter molecule-1 IBA-1 to examine the level of neuroinflammation. Thereafter, the sections were incubated for 90 min with the secondary antibody, donkey-anti-goat Jackson Immuno Research Europe Ltd. Finally, three sections per mouse per tissue cortex, thalamus and hippocampus were used for quantification.

DCX positively stained cells were manually counted by 2 blinded raters at 40x magnification and the average was used for further statistical analysis. Means were analyzed using repeated measures or multivariate analysis of variance ANOVAs with Bonferroni correction for multiple testing. Correlation tests were performed using Pearson correlations. Diet and sex-specific effects were referred to as significant if the p -value was lower than 0.

The body weight of female mice fed the reference AIN93G diet was significantly lower than that of male mice. HFD feeding significantly increased the body weight of both female and male mice compared to their AIN93G diet fed controls.

Furthermore, no significant differences in kilo caloric kcal intake at cage level were found for either diet or sex-specific effect, indicating a comparable energy intake for all groups Figure 2 C,D. The percentage of body fat was comparable between female and male mice fed the AIN93G diet.

HFD feeding significantly increased the percentage of body fat only in female mice Figure 2 E. Analysis for body weight, food intake and body fat. A Absolute body weight in gram. B Body weight gain as percentage of initial weight of male and female mice fed a HFD after adjustment of the regular growth-related gain in the AIN93G control groups.

Kcal intake is presented for female mice in C , and for male mice in D. E percentage of body fat calculated as the sum of perigonadal, mesenteric and inguinal fat pad weight divided by body weight. The start of HFD feeding at 6 weeks of age is indicated as a vertical, dotted line. We next analyzed circulating levels of fasting insulin, glucose, triglycerides, cholesterol, leptin and adiponectin.

Female mice had lower fasting plasma insulin levels than male mice on AIN93G diet. In female mice, insulin levels hardly increased upon HFD feeding, whereas males showed pronounced hyperinsulinemia Figure 3 A. However, blood glucose levels did not change upon HFD in female and male mice, and glucose levels of female mice remained lower than in male mice upon HFD feeding Figure 3 B.

Plasma triglycerides were comparable between female and male mice on AIN93G. Plasma cholesterol levels on AIN93G diet were lower in female mice compared to male mice. HFD feeding increased plasma cholesterol levels in both female and male mice, but in male mice to a significantly higher level than in female mice Figure 3 D. Both sexes had comparable plasma leptin levels on AIN93G. HFD treatment increased leptin levels comparably in female and male mice Figure 3 E.

Lastly, female mice on an AIN93G diet had much higher adiponectin levels than male mice on the same diet. HFD feeding did not significantly alter plasma adiponectin levels in female and male mice Figure 3 F. Mesenteric fat mass was similar in male and female mice fed AIN93G. Representative photomicrographs of mesenteric adipose tissue are provided in Figure 4 A—D. HFD feeding led to a significantly increase in mesenteric fat weight in male mice only Figure 4 E.

Within the mesenteric depot, sex-specific differences were observed regarding distribution of adipocyte sizes. Lastly, we analyzed the number of crown-like structures CLS as a measure of adipose tissue inflammation. Representative photomicrographs of haematoxylin phloxine and saffron HPS stained mesenteric adipose tissue per experimental group A — D. Analyses of weight E and level of inflammation as indicated by crown-like structures CLS per adipocytes F in the mesenteric fat depot.

Perigonadal fat weight was significantly lower in female than in male mice on AIN93G. In male mice, no significant increase in perigonadal fat weight was observed upon HFD feeding and the mass of this depot was significantly lower than in HFD-fed female mice Figure 5 A.

Moreover, female mice had a significantly higher percentage of larger adipocytes and a lower percentage of smaller adipocytes than male mice, either fed a AIN93G diet or HFD Figure 5 C,D.

Perigonadal fat depot A weight, and B adipose tissue inflammation as indicated by crown-like structures CLS per adipocyte. The inguinal fat depot in G weight, and H adipose tissue inflammation as indicated by crown-like structures CLS per adipocytes. The distribution of adipocyte sizes for I female mice and J male mice. No differences in inguinal fat mass were observed between male and female mice on AIN93G. HFD feeding increased the inguinal fat mass in both female and male mice with no difference in mass between sexes Figure 5 G.

Similarly, there were no differences between sexes in adipocyte size distribution. HFD-feeding induced a shift towards a lower percentage of smaller adipocytes, and an increased percentage of larger adipocytes in both female and male mice Figure 5 I,J. Altogether, the storage of fat across the white adipose tissue WAT depots differed among male and female mice, and only male mice developed adipose tissue inflammation in response to HFD feeding. We analyzed liver tissue to examine sex differences in the development of NAFLD, and representative images of liver tissue are presented in Figure 6 A—D.

The liver weights of female and male mice fed an AIN93G diet were comparable. HFD feeding increased liver weight in only male mice suggesting that male mice developed steatosis Figure 6 E.

Surprisingly, HFD feeding did not significantly affect macrovesicular steatosis in either sex, and female mice even showed an insignificant reduction Figure 6 G. In addition, hepatocellular hypertrophy on AIN93G was higher in female mice than in male mice, but was not further increased by HFD in female mice.

By contrast, HFD feeding in male mice strongly increased hepatocellular hypertrophy. Consistent with the observed development of HFD-induced liver steatosis, male mice showed significantly higher levels of hepatocellular hypertrophy than in female mice fed a HFD Figure 6 H. Lastly, female mice showed high levels of hepatic inflammation on the reference AIN93G diet, whereas young male mice fed AIN93G diet showed relatively low levels.

Hepatic inflammation in female and male mice was not significantly increased by HFD feeding Figure 6 I. Leiden male and female mice.

Representative images of haematoxylin and eosin-stained liver tissue per experimental group A — D. E Liver weight, F microvesicular steatosis, G macrovesicular steatosis, H hepatocellular hypertrophy, I hepatic inflammation. In summary, young female mice were characterized by a predominant fat storage within the perigonadal and inguinal fat depots, b neglectable levels of adipose tissue inflammation levels on AIN93G that remain low even when fed a HFD, c presence of macrovesicular steatosis in the liver that is not enhanced by HFD, and d high liver inflammation levels on AIN93G that were not further increased by HFD feeding.

In young male mice, HFD induced a fat storage within the mesenteric and inguinal depots, b pronounced adipose tissue inflammation in several adipose tissue depots, and c microvesicular steatosis in the liver. Leiden mice i. We examined whether sex differences exist in SBP, activity and explorative behavior in the open field test, or spatial learning and memory abilities obtained in the MWM on reference AIN93G diet or in response to 18 weeks of HFD feeding.

No significant effects were found concerning SBP or open field parameters like locomotor activity, velocity and explorative behavior Figure S1A—D. In DVC, in which day and night activity are automatically monitored, we found no significant differences in day and night activity between male and female mice fed a reference AIN93G diet Figure 7 A,B. However, we observed that female mice fed a HFD were slightly less active during daytime compared to male mice on the same diet Figure 7 A.

Day activity A and night activity B were indicated by activation of 12 cage-sensors and expressed in arbitrary units a. C Cerebral blood flow CBF within the hippocampus. Higher MD levels are associated with a decreased gray matter integrity. Lower FA levels are associated with a decreased white matter integrity.

We aimed to elucidate the role of the cerebrovasculature in relation to adiposity and brain function. No significant differences were found in neurogenesis DCX; data not shown , neuroinflammation IBA-1, Figure S2 , nor functional connectivity for either diet or sex. In detail, higher mean diffusivity MD levels are associated with decreased gray matter integrity.

Furthermore, lower fractional anisotropy FA levels might indicate decreased white matter integrity. Summarizing, young male mice showed decreased gray matter integrity auditory cortex, somatosensory cortex, visual cortex and motor cortex and white matter integrity motor cortex and hippocampus compared to young female mice both on the same reference AIN93G diet. Eighteen weeks of HFD feeding slightly decreased white matter integrity in the motor cortex in young male mice.

Thereby, these results imply that young male mice seem to be slightly more prone to HFD-induced structural brain changes than young female mice, indicated by decreased CBF and white matter integrity. Leiden mice with particular focus on metabolic risk factors and organs as well as brain structure and cognitive function. Male mice are generally heavier than female mice, but upon HFD feeding we found that both sexes followed the same weight gain pattern.

In our study, both sexes store fat in the inguinal fat depot, but male mice stored significantly more fat within the mesenteric fat depot than female mice resulting in more visceral fat in male mice. In line with this, male subjects tend to accumulate more fat in the visceral cavity, whereas female subjects accumulate more fat in the subcutaneous depot [ 13 ]. Visceral adipose tissue VAT , including mesenteric fat, is associated with metabolic abnormalities, increased expression of inflammatory mediators and cardiovascular risk.

In our study, male mice, fed either an AIN93G diet or HFD, had a higher inflammatory tone in the mesenteric fat depots than female mice which is consistent with results of others reporting that obese male mice develop more pronounced adipose tissue inflammation [ 45 ].

Leiden mice did not increase in response to HFD feeding. However, it is possible that in early life, molecular factors controlling adipogenesis are modulated by HFD in a different way on the epigenetic level than in adult mice [ 48 ]. Interestingly, adipose tissue inflammation was practically absent in female mice, despite a comparable inguinal depot or even greater perigonadal depot increase in mass, suggesting that either the storage capacity has not been reached in female mice, or that other mechanisms play a role in the onset of adipose tissue inflammation.

It is also possible that the production of pro-inflammatory factors in VAT is greater in males than in females [ 16 ]. Sex differences regarding fat storage across the adipose tissue depots studied herein might at least partly be caused by differences in sex steroids.

For instance, Kanaley and colleagues studied adipose tissue distribution in pre- and postmenopausal women and found that the postmenopausal drop in oestrogen was associated with a rapid increase in VAT accumulation and an increased risk of cardiovascular disease [ 49 ].

However, relatively little is known about the exact underlying mechanisms [ 16 ]; future research may concentrate on the role of sex steroids during HFD-induced obesity to gain more information on the modulating role of oestrogen in WAT depot expansions. In conclusion, our findings in young female and young male mice are in coherence with reported sex differences regarding fat distribution and inflammatory tone, the latter of which may be lower in females because of the anti-inflammatory properties of oestrogens [ 53 ].

Plausibly, the observed sex differences might be due to different expression of sex steroids, and differences in oestrogen receptor expression levels in adipose fat depots.

NAFLD is known to develop during the course of diet-induced obesity [ 54 , 55 ]. In the current study, microvesicular steatosis increased in male mice only upon HFD feeding, whereas macrovesicular steatosis did not further increase.

Leiden mice in which both forms of steatosis increased markedly upon HFD feeding [ 27 , 28 ]. It is possible that male mice are more susceptible to develop metabolic overload and metabolic stress in the liver, potentially because lipids are utilized to a lesser degree and accumulate in organs either in adipose tissue for lipid storage or as ectopic fat. Elevated plasma triglyceride levels are a marker of NAFLD in humans and only a few diet-inducible NASH mouse models clearly recapitulate this aspect of the disease [ 25 , 59 , 60 ].

Insulin resistance is associated with the development of NASH and with an increase in inflammatory cells within WAT and liver [ 27 , 61 ].

Consistent with this, we observed a strong increase of plasma insulin levels in young male mice on HFD, whereas young female mice showed surprisingly little response in insulin levels. Notably, we found that macrovesicular steatosis and lobular inflammation were strongly present in young female mice independent of diet suggesting that young female mice store fat in a way that promotes the development of large vesicles.

Clinical manifestations of NAFLD are typically characterized by predominantly macrovesicular steatosis in adulthood [ 63 ], but in children mixed forms of macro- and microvesicular steatosis are observed. In the case of macrovesicular steatosis, the hepatocyte contains a single, large vacuole, which fills up the hepatocyte and displaces the nucleus to the periphery of the cell [ 56 , 57 ].

Our finding is in line with similar findings in a study by Mulder and colleagues, who reported that HFD-induced macrovesicular steatosis is significantly associated with lobular inflammation in adult male mice [ 46 ]. Leiden male mice are more prone to respond to HFD feeding with hepatic steatosis development, based on the observed increase in microvesicular steatosis associated with hyperinsulinemia and hypertriglyceridemia, and the increase of the inflammatory tone in adipose tissue.

Based on the observations made in this study, we believe that the general assumption that female and male mice should be representative for female and male patients, respectively, is incorrect, at least as a general statement. It may well be that a particular gender e. For instance, in the field of atherosclerosis, it has been shown that female mice respond better to particular diets that promote hypercholesterolemia and atherogenesis and that male mice are not useful for these type of studies [ 64 , 65 ], and that observations made in female mice are highly predictive for male and female patients with cardiovascular disease [ 66 , 67 ].

These findings emphasize that the choice of a model should be made carefully, and it should be taken into account that human and mouse Y chromosomes differ clearly from each other and from other mammals in multiple ways as they carry different genes [ 68 , 69 ].

This knowledge should result in more critical considerations when it comes to the performance of preclinical studies that aim to investigate sex-specific differences in humans. Next to metabolically active tissues, sex-specific alterations in brain structure in the development of juvenile obesity were observed.

We observed that white and gray matter integrity was reduced in juvenile male mice in various regions. Others reported sex differences in cerebral volume; for instance, female mice displayed larger anterior hippocampus volumes, while male mice had larger medial amygdala volumes [ 70 ].

In addition, it has been reported that cerebral white matter increased linearly with age at a faster pace in women [ 71 ]. In our study in juvenile mice, we detected limited HFD-induced alterations in daytime activity and no significant alterations in cognitive function, which was indicated with the open field test and Morris water maze. However, others found HFD-induced circadian rhythm reprogramming and HFD-induced cognitive impairment in rodent models [ 7 , 8 , 72 ].

For instance, Boitard and colleagues found a decrease in hippocampal neurogenesis, memory impairment and an increase in hippocampal pro-inflammatory cytokines in juvenile obese mice [ 8 ]. Moreover, anxiety behavior was increased in juvenile obese mice compared to their lean controls [ 9 ].

In both studies, a HFD was induced immediately after weaning 3 weeks of age [ 8 , 9 ], while in the current study a HFD was initiated at 6 weeks of age 3 weeks post-weaning. Therefore, the current model of initiating juvenile obesity differs in period of sensitivity; for instance, brain function is more susceptible to detrimental effects of HFD exposure earlier in life 3 weeks of age , or the brain is able to adapt to metabolic stressors from 6 weeks onwards.

Furthermore, we found that the hippocampal white matter integrity was lower in HFD fed male mice. Previous research showed a correlation between hippocampal FA values and cognitive parameters in humans [ 75 ] and mice [ 76 ]. Thereby, a reduction in CBF and white matter integrity might be a precursor for the development of cognitive problems [ 77 ]. Nevertheless, in the current study, neuroinflammation, structural brain changes and CBF changes were still modest in young male mice, and might not yet have been large enough to provoke cognitive dysfunction.

This correlation in male mice might suggest a link between the onset of hepatic inflammation and neuroinflammation. This is in line with findings by others, who report that hepatic inflammation may induce swelling of astrocytes and reactivation of microglia via an increased expression of inflammatory cytokines [ 78 , 79 ]. This link between hepatic inflammation and neuroinflammation suggests that an increased expression of inflammatory cytokines by hepatic or WAT inflammation can induce neuroinflammation, alter the cerebrovasculature, or even affect brain function.

Nevertheless, in our study the level of hepatic inflammation and neuroinflammation were modest in our juvenile male mice. We hypothesize that a prolonged HFD intervention or an earlier exposure of a HFD intervention 3 weeks of age might induce a higher inflammatory tone in this mouse model.

Future research should determine inflammatory cytokines levels in plasma and brain tissue, which eventually may reinforce the link between hepatic inflammation and neuroinflammation in context of obesity.

In conclusion, sex-specific differences observed in young mice fed a HFD include effects on 1 fat storage and distribution like increased mesenteric fat mass and adipose tissue inflammation specifically in male mice, 2 plasma levels of metabolic risk factors as in male mice hyperinsulinemia and hypertriglyceridemia, and 3 in the development of NAFLD including HFD-induced microvesicular steatosis only in male mice.

Moreover, sex-specific differences in brain structure were observed as male mice displayed reduced CBF and white matter integrity within the hippocampus after HFD feeding.

Surprisingly, female mice displayed macrovesicular steatosis and lobular inflammation in the liver when fed an AIN93G reference diet, and HFD feeding did not aggravate steatosis and inflammation, neither in liver nor adipose tissue.

Leiden mice are more susceptible to the detrimental effects of a HFD than young female mice, resulting in male mice in increased VAT storage, adipose tissue inflammation, microvesicular steatosis in the liver, and reduced CBF and white matter integrity. Future research should focus on the role of sex steroids, oestrogen receptors and inflammatory cytokines in adipose tissue storage, the development of NAFLD, and plausible associations to brain function in the context of juvenile obesity.

Eventually, this may help to develop sex-specific interventions and representative translational animal models. The current study emphasizes the importance of sex specific differences in the development of obesity, liver pathology and brain function, and advocates a careful choice of a model system. Conceptualization, G. The other authors declare no conflict of interest.

National Center for Biotechnology Information , U. Journal List Nutrients v. Published online Aug Sophie A. Franx , 1 Lotte Wekking , 1 Vivienne G. Verweij , 1 Nicole Worms , 2 Marieke H. Schoemaker , 4 Gabriele Gross , 4 Martine C. Morrison , 2, 3 Robert Kleemann , 2, 5 Ilse A. Bart A. Vivienne G. Marieke H. Martine C. Ilse A. Amanda J. Author information Article notes Copyright and License information Disclaimer. Received Jun 24; Accepted Aug 7. Associated Data Supplementary Materials nutrientss Abstract Background: Sex-specific differences play a role in metabolism, fat storage in adipose tissue, and brain structure.

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