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Specifically, during short- and long-term settings, oral quercetin generally caused iron depletion and this was evident from the significantly reduced absorption rate of non-haem iron, reduced liver and spleen iron pools and levels of duodenal iron transporters.
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A scrumptious morning smoothy based on the diets of among the healthiest, longest-living hamlet in the world.
Learn More »There is general acceptance of the negative impact of foodstuffs rich in certain polyphenols on non-haem iron bioavailability in vivo. Available data are mainly based on results of isotope absorption studies [7], but there is little information on the precise mechanisms by which specific dietary polyphenols affect non-haem iron absorption in vivo. Our previous study [14] revealed the mechanism of inhibition of non-haem iron absorption by quercetin. We showed that quercetin chelates iron and thus prevents its transport across the enterocyte. Increased apical iron uptake is accompanied by decreased iron release into the blood. However, Lesjak et al. [14] used a protocol where iron and quercetin were introduced into the duodenal lumen together. Proof of an effect of quercetin ingestion on iron absorption is however still missing. The gavage protocol used in the present study was designed to imitate the diet of individuals consuming quercetin both randomly and regularly. Results from our present study indicate that oral quercetin had significant effects on both iron absorption and gene expression of duodenal proteins involved in iron metabolism, as well as iron pools in liver and spleen. Specifically, during short- and long-term settings, oral quercetin generally caused iron depletion and this was evident from the significantly reduced absorption rate of non-haem iron, reduced liver and spleen iron pools and levels of duodenal iron transporters. Uptake studies after short-term single and double quercetin gavage treatments significantly increased of mucosal iron uptake, while there was a notable decrease in iron efflux from enterocytes. For the first time, our results show that orally applied quercetin could decrease iron absorption by inhibiting its basolateral exit. Decreased enterocyte iron transfer might be due to intracellular chelation of iron by quercetin which increases apical uptake of iron, but prevents basolateral exit [14]. However, 18 or 5 h are long periods for quercetin to remain in the lumen or inside the enterocyte and be available to chelate iron due to its fast metabolism [26]. It is certainly possible that towards the end of a 5 h period, levels of quercetin are too low to form an effective complex with iron. In this scenario, the most probable explanation for its effect on iron absorption is to cause changes in the expression of proteins involved in iron metabolism. Our previous study showed that quercetin can mediate knockdown of FPN1 in Caco-2 cells post-transcriptionally, which could be an additional mechanism allowing quercetin to affect efflux of iron from enterocyte in vivo [14]. The possibility that quercetin, or its metabolites, also have direct effects on the expression of other proteins involved in iron absorption and systemic iron balance, and that together with chelation this action modifies iron metabolism, should be further considered. Long-term (10 days) gavage quercetin treatment reduced mRNA levels of duodenal DMT1, Dcytb and FPN, which could be a consequence of a direct effect of quercetin or its metabolites. Even though examined quercetin metabolites were not detected in the serum of treated rats, there is a possibility that other quercetin metabolites affect the expression of iron-related genes. In our study, oral quercetin did not cause a change in liver and spleen hepcidin mRNA expression. These results contrast with the data of Tang et al. [27], who showed in vivo that oral quercetin efficiently supports hepcidin expression by intensification of the BMP6/SMAD4 signalling pathway. In Tang et al. [27], up-regulation of liver hepcidin, on both protein and mRNA levels, was documented after 15 weeks oral treatment with quercetin (100 mg/kg). These conflicting results might reflect the different periods of quercetin treatment. Furthermore, after a 10 days treatment regime with oral quercetin, animals became iron depleted, as both spleen and liver iron pools decreased. Interestingly, Zhang et al. [28] showed that quercetin reduced liver iron content after an induced tissue iron overload. This effect was attributed to the ability of quercetin to combine with non-haem iron in tissue, transport it to the bloodstream and excrete it from the body. We also confirmed this in the study for both liver and spleen, which strongly supports the need for further research on different polyphenols as potential new iron chelating drugs. In addition to observing the effects of oral quercetin on iron uptake and transport, we wanted to inspect the possible therapeutic effect of quercetin on body iron overload. Our data indicate that IP quercetin had a significant effect on systemic iron metabolism by indirectly affecting iron absorption. We shown that IP quercetin induced iron depletion as indicated by significant reductions in serum iron and transferrin saturation levels, as well as an increased hepcidin mRNA and decreased expression of genes involved in duodenal iron absorption.
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Learn More »There are only two reports in the literature that reported a similar effect of quercetin on hepcidin expression in liver. Bayele et al. [18] reported that IP quercetin increased hepcidin expression after 18 h, which might involve the Nrf2 pathway. Bayele et al. [18] also showed that hepcidin induction by quercetin correlated with changes in serum iron levels and transferrin saturation, as well as with reduction in FPN mRNA, which is also in accordance with our present study. Vanhees et al. [29] showed that prenatal exposure to quercetin caused hepcidin induction in adult mice and the authors hypothesized that after birth, when pups were no longer exposed to quercetin, improved bioavailability of dietary iron sensed as body iron overload. Our study shows for the first time that IP quercetin could increase hepcidin levels in both liver and spleen. Increased levels of hepcidin are expected to be followed by reduced FPN levels. This “seesaw” relationship between hepcidin and FPN expression is well-known [6] and our results are in agreement with this notion. After single and double IP quercetin treatment, levels of liver FPN mRNA decreased significantly. This action on FPN, which is believed to be indirectly driven by hepcidin induction, was more pronounced after double quercetin treatment, where FPN mRNA levels declined in both liver and spleen. High hepcidin, as well as the expected reduction in FPN levels, should be accompanied by increased retention of iron in liver and spleen [6]. This pattern was evidenced in the present study. There is a general agreement that increased hepcidin levels decrease intestinal iron absorption [30, 31]. It is proven that hepcidin expression is inversely proportional to expression of intestinal DMT1, Dcytb and FPN expression in vivo [32, 35‒35]. However, this relationship was only partially confirmed in this study. Namely, after single quercetin IP levels of duodenal mRNA DMT1 stayed the same, whilst the levels of Dcytb and FPN were raised. These results were somewhat surprising particularly in the light of detected increased levels of hepcidin and duodenal iron. It would be expected that the levels of DMT1 were down-regulated by the post-transcriptional IRE/IRP control process, such that when iron levels are high, expression of DMT1 is suppressed. Still, FPN mRNA in duodenum could be also partially under IRE/IRP control, which when iron levels in tissue are high, expression of FPN is up-regulated [36]. However, after double IP quercetin treatment, duodenal mRNA levels of DMT1, Dcytb and FPN were significantly down-regulated and lower levels of duodenal iron were recorded. Hepcidin up-regulation is followed by a reduction in serum iron and transferrin saturation [37]. This principle was confirmed in the present study since single and double quercetin IP reduced serum iron and transferrin saturation levels. Surprisingly, IP quercetin treatment did not affect mucosal iron uptake or transfer since a double dose of quercetin up-regulated mRNA hepcidin levels whilst reducing intestinal iron transporter expression. Further studies need to be performed to confirm the actions of IP quercetin on iron absorption in vivo. After IP quercetin administration, quercetin-3-O-glucuronide, quercetin and isorhamnetin were detected with LC-MS/MS in serum, whilst the same analysis did not detect these compounds after long-term oral treatment. This confirms previously known facts that quercetin absorbed in the intestine has a short half-life [26] and that one of the dominant quercetin metabolites in serum is quercetin glucuronide [38]. Bioavailability of quercetin, defined as the portion of an initially administered dose that reaches the systemic circulation unchanged, is very low, mostly due to its extensive metabolism [26]. Quercetin is present in plants mainly in its highly hydrophilic glycosylated forms, primarily as β-glycosides of various sugars which are more bioavailable in humans [39]. There are two main routes for absorption of quercetin glycosides by enterocytes. First, absorption goes via a transporter, followed by deglycosylation within the enterocyte by cytosolic glycosidase. Second, deglycosylation can occur by luminal hydrolases, followed by transport of the aglycone into enterocyte by passive diffusion or transporter-mediated. After absorption, further biotransformation of quercetin aglycone involves glucuronidation, sulfation and methylation of hydroxyl groups, which primarily occurs in enterocytes and hepatocytes [24]. However, by both ways quercetin ends up in the enterocytes as aglycone, which is then able to chelate iron or have direct effect on transcription on iron-related genes. Thus, in this study quercetin aglycone was used instead of quercetin glycoside. However, the possibility that quercetin metabolites could also be involved in the observed effects on iron uptake and metabolism should not be overlooked. It is evident that different routes of quercetin application affect iron metabolism in different ways. Thus, IP treatment mainly affected systemic iron homeostasis, mostly by regulating hepcidin expression and indirectly causing reduction in iron absorption, while oral quercetin directly influenced iron absorption.
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Learn More »Interestingly, previous results of others indicate contradictory results on how different dietary polyphenols affect iron homeostasis. Thus, Mu et al. [19] reported that the polyphenol myricetin inhibits hepcidin expression induction in vivo by the BMP/SMAD signalling pathway. Quercetin and myricetin are very similar in structure, with myricetin having an extra hydroxyl group. The differences in effect of these two similar polyphenols on iron absorption indicate the complexity of responses to polyphenols. Furthermore, Zhen et al. [17] and Patchen et al. [40] showed that genistein, a main polyphenol from soya, and ipriflavone, synthetic analog derived from abundant dietary polyphenol daidzein, respectively, both strongly promote hepcidin expression in vivo. Recent studies by Grillo et al. [41] and Zhang et al. [42] indicate that natural products could have a major role in iron metabolism and may have potential in therapy of iron metabolism disorders. In conclusion, oral and IP treatment with quercetin caused serum and tissue iron depletion in rats by two means—inhibition of iron absorption and altered expression of iron-related genes. Our data confirm that quercetin increases mucosal iron uptake and inhibits iron efflux from duodenal mucosa. Also, oral quercetin treatment decreased mRNA levels of duodenal DMT1, Dcytb and FPN, while IP quercetin induced hepcidin expression, both in liver and spleen. These results also indicate that oral quercetin has a significant inhibitory effect on iron absorption in duodenum, while IP quercetin significantly affects systemic iron regulation leading to iron depletion. However, the precise mechanism of the action of quercetin on iron metabolism remains to be defined. Our study is important in that it could lead to development of new approaches to preventing and treating IDA, as well as alleviating the effects of clinical iron overload. Polyphenols might prove to be a novel therapy for diseases of body iron metabolism.
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