Abstract
Plant-derived secondary metabolites consumed in the diet, especially polyphenolic compounds, are known to have a range of positive health effects. They are present in circulation after ingestion and absorption and can be sequestered into cells within particular organs, but have rarely been investigated systematically in osteological tissues. However, a small number of polyphenols and similar molecules are known to bind to bone. For example alizarin, a plant derived anthraquinone and tetracycline (a naturally occurring antibiotic), are both absorbed into bone from circulation during bone formation and are used to monitor mineralization in osteological studies. Both molecules have also been identified serendipitously in archaeological human bones derived from natural sources in the diet. Whether an analogous mechanism of sequestration extends to additional diet-derived plant-polyphenols has not previously been systematically studied. We investigated whether a range of diet-derived polyphenol-like compounds bind to bone using untargeted metabolomics applied to the analysis of bone extracts from pigs fed an acorn-based diet. We analysed the diet which was rich in ellagitannins, extracts from the pig bones and surrounding tissue, post-mortem. We found direct evidence of multiple polyphenolic compounds in these extracts and matched them to the diet. We also showed that these compounds were present in the bone but not surrounding tissues. We also provide data showing that a range of polyphenolic compounds bind to hydroxyapatite in vitro. The evidence for polyphenol sequestration into physiological bone, and the range and specificity of polyphenols in human and animal diets, raises intriguing questions about potential effects on bone formation and bone health. Further studies are needed to determine the stability of the sequestered molecules post-mortem but there is also potential for (palaeo)dietary reconstruction and forensic applications.
Highlights
Plant-derived secondary metabolites consumed in the diet, especially polyphenolic compounds, are known to have a range of positive health effects
Despite these positive health benefits, polyphenols are treated as xenobiotic molecules by the body and processed via phase 1 & 2 metabolism for removal from the organism
In 1736, Belchier demonstrated that ingestion of root madder resulted in the staining of bones a red colour in vivo, and subsequently this was attributed to alizarin, a red-coloured, hydroxylated anthraquinone found in root madder, which is still used as a bone staining agent in contemporary ossification studies[8,9,10]
Summary
Plant-derived secondary metabolites consumed in the diet, especially polyphenolic compounds, are known to have a range of positive health effects. Polyphenolic compounds, and similar plant-derived secondary metabolites, are found in a wide range of foods including fruits, leaves, roots, and seeds and are an important constituent of the diet of humans and animals They can provide antioxidant effects, scavenge free radicals and consumption is linked to a lower risk of diseases including cancer, cardiovascular disease and chronic inflammation[1,2]. Www.nature.com/scientificreports may provide tissue-specific therapeutic activities such as reducing inflammation or providing anti-tumorigenic effects[5,6,7] It has been known for several hundred years that some polyphenols can bind to bone in vivo, the process is still not well understood. Taken together these serendipitous findings in the archaeological record provide evidence that quite different diet-derived polyphenolic-like compounds can become sequestered into growing bone and survive over archaeological time
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