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The Relationship Between Choline Bioavailability from Diet, Intestinal Microbiota Composition, and Its Modulation of Human Diseases

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The Relationship Between Choline Bioavailability from Diet, Intestinal Microbiota Composition, and Its Modulation of Human Diseases nutrients Review The Relationship between Choline Bioavailability from Diet, Intestinal Microbiota Composition, and Its Modulation of Human Diseases Natalia Arias 1,2,*, Silvia Arboleya 3 , Joseph Allison 2, Aleksandra Kaliszewska 2, Sara G. Higarza 1,4 , Miguel Gueimonde 3 and Jorge L. Arias 1,4 1 Instituto de Neurociencias del Principado de Asturias (INEUROPA), 33003 Oviedo, Asturias, Spain; [email protected] (S.G.H.); [email protected] (J.L.A.) 2 Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, Denmark Hill, London SE5 8AF, UK; [email protected] (J.A.); [email protected] (A.K.) 3 Department of Microbiology and Biochemistry of Dairy Products, Instituto de Productos Lácteos de Asturias (IPLA-CSIC), 33003 Oviedo, Asturias, Spain; [email protected] (S.A.); [email protected] (M.G.) 4 Laboratory of Neuroscience, Department of Psychology, University of Oviedo, Plaza Feijóo, s/n, 33003 Oviedo, Asturias, Spain * Correspondence: [email protected] Received: 14 July 2020; Accepted: 30 July 2020; Published: 5 August 2020 Abstract: Choline is a water-soluble nutrient essential for human life. Gut microbial metabolism of choline results in the production of trimethylamine (TMA), which, upon absorption by the host is converted into trimethylamine-N-oxide (TMAO) in the liver. A high accumulation of both components is related to cardiovascular disease, inflammatory bowel disease, non-alcoholic fatty liver disease, and chronic kidney disease. However, the relationship between the microbiota production of these components and its impact on these diseases still remains unknown. In this review, we will address which microbes contribute to TMA production in the human gut, the extent to which host factors (e.g., the genotype) and diet affect TMA production, and the colonization of these microbes and the reversal of dysbiosis as a therapy for these diseases. Keywords: choline; TMA; TMAO; non-alcoholic steatohepatitis (NASH); cardiovascular disease (CVD); chronic kidney diseases (CKD); probiotics; gut microbiota; polyphenols; fecal microbiota transplantation 1. Introduction Choline is an essential nutrient for humans throughout their life. Although humans can produce choline in small quantities through the hepatic phosphatidylethanolamine N-methyltransferase pathway, most individuals need to increase choline ingestion through their diet, in order to prevent deficiency [1–4]. The main dietary sources of choline include eggs, fish, grains, meat, milk, and their derived products, and to a lesser extent, some vegetables such as soybeans and potatoes [1,3,5,6]. In foods, choline is found as both water-soluble (free choline, phosphocholine, and glycerophosphocholine) and lipid-soluble (phosphatidylcholine and sphingomyelin) forms [7]; however, cooking methods can reduce the amount of choline content in the diet and increase the phosphatidylcholine contribution [8]. Different forms of choline influence the absorption and metabolism of this nutrient throughout development. Indeed, water-soluble forms that are mainly present in human milk enter the portal circulation and reach the liver, while lipid-soluble forms, Nutrients 2020, 12, 2340; doi:10.3390/nu12082340 www.mdpi.com/journal/nutrients Nutrients 2020, 12, 2340 2 of 29 Nutrients 2020, 12, x FOR PEER REVIEW 2 of 30 which can be found in foods, are absorbed and transported through the lymphatic circulation [3,9]. Therefore,which can the be intake found of in choline foods, varies are absorbed in accordance and tr withansported different through stages the of development.lymphatic circulation [3,9]. Therefore,The majority the intake of people of choline do not varies meet in the acco dietaryrdance requirements with different for stages choline, of development. particularly those on vegetarianThe or majority vegan diets of people and pregnant do not meet or lactating the dietary mothers requirements [1]. Lactation for hascholine, been particularly associated with those an on increasedvegetarian choline or vegan demand diets [10 ],and whilst pregnant the maternal or lactating choline mothers intake could[1]. Lactation be linked has to enhancedbeen associated placental with healthan increased [11] and positivecholine demand neurocognitive [10], whilst effects the on maternal the offspring choline [12 intake]. Therefore, could be these linked sub-groups to enhanced of peopleplacental should health be monitored [11] and positive closely inneurocognitive order to ensure effects appropriate on the cholineoffspring intakes [12]. Therefore, [1,13,14]. these sub- groupsCholine of people metabolism should can be be monitored divided into closely four in main order pathways, to ensure which appropriate are involved choline in intakes the synthesis [1,13,14]. of acetylcholine,Choline metabolism betaine, phospholipids, can be divided and into trimethylamine four main pathways, (TMA; overviewed which are in involved Figure1)[ in3 ].the Cholinesynthesis metabolites of acetylcholine, have a wide betaine, range phospholipids, of functions inorganisms and trimethylamine [1,15]. Choline (TMA; is catalyzed overviewed by cholinein Figure acyltransferase1) [3]. Choline into metabolites acetylcholine, have whicha wide is range key in of cholinergic functions in neurotransmission organisms [1,15]. [Choline15,16]. Moreover,is catalyzed cholineby choline can be acyltransferase oxidized to obtain into betaine, acetylcholine, which is which an important is key in osmolyte, cholinergic a methyl neurotransmission donor implicated [15,16]. in theMoreover, epigenetic choline regulation can ofbe DNA oxidized [15,17 to], obtain and a requirementbetaine, which in theis an synthesis important of phosphatidylcholineosmolyte, a methyl donor [3]. Specialimplicated attention in needsthe epigenetic to be given regulation to phosphatidylcholine, of DNA [15,17], the and most a requirement abundant phospholipid in the synthesis in the of body,phosphatidylcholine which is not only a[3]. major Special component attention of cellularneeds to membranes be given andto phosphatidylcholine, needed for cell division the and most growthabundant [18,19 phospholipid], but also plays in the a rolebody, in which cell signaling is not only as a major donor component to synthesize of cellular sphingomyelin membranes from and ceramideneeded [for18,20 cell]. Moreover,division and sphingomyelin growth [18,19], is requiredbut also forplays myelination a role in cell processes signaling in theas a nervous donor to synthesize sphingomyelin from ceramide [18,20]. Moreover, sphingomyelin is required for system [21]. myelination processes in the nervous system [21]. FigureFigure 1. 1.Overview Overview of of choline choline metabolism metabolism from from the the diet. diet. Choline Choline is is taken taken from from the the diet diet and and gut gut microbiotamicrobiota trimethylamine trimethylamine (TMA) (TMA) lyases lyases transform transform it intoit into TMA. TMA. TMA TMA is absorbedis absorbed by by the the intestine intestine andand delivered delivered to theto the liver, liver, where where TMA TMA is metabolized is metabolized into into trimethylamine trimethylamine N-oxide N-oxide (TMAO) (TMAO) by by host host hepatichepatic monooxygenases. monooxygenases. Finally, Finally, TMAO TMAO is distributed is distri tobuted organs, to whereorgans, it canwhere be eliminatedit can be (kidneys)eliminated and(kidneys) accumulated and (tissue).accumulated However, (tissue). it could However, cause impairment it could cause in high impairment concentrations in high (cardiovascular concentrations damage,(cardiovascular for a detailed damage, review for see a detailed Section5 review). see Section 5). Moreover, we want to place a special emphasis on choline metabolism in the large intestine Moreover, we want to place a special emphasis on choline metabolism in the large intestine where it is metabolized to TMA by the gut microbiota prior to absorption [22]. The human microbiota where it is metabolized to TMA by the gut microbiota prior to absorption [22]. The human microbiota harbors trillions of microbes including bacteria, archaea, viruses, phages, yeast, and fungi [23]. harbors trillions of microbes including bacteria, archaea, viruses, phages, yeast, and fungi [23]. It It starts to develop in the perinatal period and becomes diverse and complex in adulthood. Several starts to develop in the perinatal period and becomes diverse and complex in adulthood. Several intrinsic and extrinsic factors may affect the microbiota during infancy such as mode of delivery, intrinsic and extrinsic factors may affect the microbiota during infancy such as mode of delivery, the the gestational age of birth, the infant feeding mode, the maternal diet, environmental factors such gestational age of birth, the infant feeding mode, the maternal diet, environmental factors such as as family lifestyle and geographical location and host genetics, and adulthood such as physiological family lifestyle and geographical location and host genetics, and adulthood such as physiological changes of the digestive tract, the modification of dietary patterns, and the impairment of the immune changes of the digestive tract, the modification of dietary patterns, and the impairment of the immune system [24,25]. These factors may disrupt the microbiota composition, causing so-called dysbiosis [26]. system [24,25]. These factors may disrupt the microbiota composition, causing so-called dysbiosis [26].
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