Sexual dimorphism in intestinal absorption and lymphatic transport of dietary lipids

Liu, Min; Shen, Lei; Yang, Qing; Nauli, Andromeda M.; Bingamon, Madison; Wang, David Q.–H.; Ulrich‐Lai, Yvonne M.; Tso, Patrick

doi:10.1113/jp281621

Cited by 9 publications

(7 citation statements)

References 56 publications

(97 reference statements)

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“…However, only testosterone decreased the intestinal ApoB secretion, resulting in fewer intestinal lipoproteins being produced ( Figures 3B , 4B , 5B ). These results are consistent with our recently published studies that showed ApoB was not affected by the female sex hormones ( Liu et al, 2021 ). It is important to note, however, that our previous mice studies used different concentrations of sex hormones.…”

Section: Discussionsupporting

confidence: 94%

“…As indicated above, earlier studies showed that female rats had higher VLDL protein production than male rats ( Vahouny et al, 1977 ; Vahouny et al, 1980 ). Furthermore, our recently published studies showed that female mice had lower lymphatic TG secretion than male mice, which could partly be due to the estrogen-mediated enhancement of vascular endothelial growth factor A (VEGF-A) signaling ( Liu et al, 2021 ). Enhanced VEGF-A signaling has been shown to prevent the movement of intestinal lipoproteins from the lamina propria of the intestinal villi into their lymphatics ( Zhang et al, 2018 ).…”

Section: Discussionmentioning

confidence: 99%

“…These two time points were selected because they represent the fasting and postprandial lymph, respectively. Based on our extensive experience in lymph fistula mouse model ( Nauli et al, 2006 ; Liu et al, 2021 ), the lymphatic TG transport has usually reached the steady state by the 6 th hour of lipid infusion. Only negligible quantity of infused TGs remains in the lumen of the small intestine and colon at the end of our lipid infusion, indicating that almost all of our infused TGs are hydrolyzed and taken up by the enterocytes.…”

Section: Methodsmentioning

confidence: 99%

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The effects of sex hormones on the size of intestinal lipoproteins

Nauli,

Phan,

Tso

et al. 2023

Front. Physiol.

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Larger intestinal lipoproteins are more likely to be retained longer in the intestinal wall, allowing more time for their fat to be hydrolyzed and subsequently taken up by the abdominal viscera. Since men generally accumulate more abdominal visceral fat than women, we sought to determine if males produce larger intestinal lipoproteins compared to females. Using the conscious lymph fistula mouse model, we discovered that the male mice indeed produced larger intestinal lipoproteins than the female mice when they were intraduodenally infused with lipid emulsion. We then employed our differentiated Caco-2 cell model with semipermeable membrane system to determine the effects of sex hormones on the size of intestinal lipoproteins. Lipoprotein size was quantitatively measured by calculating the ratio of triglycerides (TG)/Apolipoprotein B (ApoB) and by analyzing their transmission electron micrographs. Our studies showed that while there was no dose-dependent effect of estrogen and progesterone, testosterone significantly increased the size of lipoproteins. When these hormones were combined to resemble the physiological concentrations observed in males and the different ovarian cycle phases in premenopausal females, both the male and luteal groups had significantly larger lipoproteins than the ovulatory group; and the male group also had significantly larger lipoproteins than the follicular group. The ovulatory group secreted a significantly lower amount of TG than the male and luteal groups. ApoB was comparable among all these groups. These findings support our hypothesis that, through their testosterone effects, males are more likely to produce larger intestinal lipoproteins. Larger lipoproteins tend to remain longer in the intestinal wall and may facilitate fat uptake preferentially by the abdominal viscera. Our studies may partly explain why men are more prone to accumulating abdominal visceral fat, which is an independent predictor of mortality.

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Section: Discussionsupporting

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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The effects of sex hormones on the size of intestinal lipoproteins

Nauli,

Phan,

Tso

et al. 2023

Front. Physiol.

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“…In general, male rodents transport ingested fat more efficiently than females ( Yang et al, 2014 ). However, analysis of sexual dimorphism in intestinal fat transport ability showed a subset of female rats was able to transport fat at similar rates to males ( Liu et al, 2021 ). Interestingly, ovariectomized female rats displayed fat transport rates similar to males, but lymphatic fat clearance could be reduced by treating the rats with either estradiol alone or an estradiol/progesterone mix, suggesting that ovarian hormones suppress lymphatic fat uptake ( Liu et al, 2021 ).…”

Section: Emerging Topicsmentioning

confidence: 99%

“…However, analysis of sexual dimorphism in intestinal fat transport ability showed a subset of female rats was able to transport fat at similar rates to males ( Liu et al, 2021 ). Interestingly, ovariectomized female rats displayed fat transport rates similar to males, but lymphatic fat clearance could be reduced by treating the rats with either estradiol alone or an estradiol/progesterone mix, suggesting that ovarian hormones suppress lymphatic fat uptake ( Liu et al, 2021 ). As mentioned above, lacteal junction zippering was observed following increased VEGFA signaling ( Zarkada et al, 2023 ; Zhang et al, 2018 ), and ovariectomized rats under estradiol or an estradiol/progesterone treatment significantly enhanced gut Vegfa expression, though lacteal junctions were not analyzed ( Liu et al, 2021 ).…”

Section: Emerging Topicsmentioning

confidence: 99%

Mechanisms and functions of intestinal vascular specialization

Bernier-Latmani,

González-Loyola,

Petrova

2023

Journal of Experimental Medicine

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The intestinal vasculature has been studied for the last 100 years, and its essential role in absorbing and distributing ingested nutrients is well known. Recently, fascinating new insights into the organization, molecular mechanisms, and functions of intestinal vessels have emerged. These include maintenance of intestinal epithelial cell function, coping with microbiota-induced inflammatory pressure, recruiting gut-specific immune cells, and crosstalk with other organs. Intestinal function is also regulated at the systemic and cellular levels, such that the postprandial hyperemic response can direct up to 30% of systemic blood to gut vessels, while micron-sized endothelial cell fenestrations are necessary for nutrient uptake. In this review, we will highlight past discoveries made about intestinal vasculature in the context of new findings of molecular mechanisms underpinning gut function. Such comprehensive understanding of the system will pave the way to breakthroughs in nutrient uptake optimization, drug delivery efficiency, and treatment of human diseases.

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