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Can Xanthophyll-Membrane Interactions Explain Their Selective Presence in the Retina and Brain?

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Can Xanthophyll-Membrane Interactions Explain Their Selective Presence in the Retina and Brain? foods Review Can Xanthophyll-Membrane Interactions Explain Their Selective Presence in the Retina and Brain? Justyna Widomska 1,*, Mariusz Zareba 2 and Witold Karol Subczynski 3 Received: 14 December 2015; Accepted: 5 January 2016; Published: 12 January 2016 Academic Editor: Billy R. Hammond 1 Department of Biophysics, Medical University of Lublin, 20-090 Lublin, Poland 2 Department of Ophthalmology, Medical College of Wisconsin, Milwaukee, WI 53226, USA; [email protected] 3 Department of Biophysics, Medical College of Wisconsin, Milwaukee, WI 53226, USA; [email protected] * Correspondence: [email protected]; Tel.: +48-81-479-7169 Abstract: Epidemiological studies demonstrate that a high dietary intake of carotenoids may offer protection against age-related macular degeneration, cancer and cardiovascular and neurodegenerative diseases. Humans cannot synthesize carotenoids and depend on their dietary intake. Major carotenoids that have been found in human plasma can be divided into two groups, carotenes (nonpolar molecules, such as β-carotene, α-carotene or lycopene) and xanthophylls (polar carotenoids that include an oxygen atom in their structure, such as lutein, zeaxanthin and β-cryptoxanthin). Only two dietary carotenoids, namely lutein and zeaxanthin (macular xanthophylls), are selectively accumulated in the human retina. A third carotenoid, meso-zeaxanthin, is formed directly in the human retina from lutein. Additionally, xanthophylls account for about 70% of total carotenoids in all brain regions. Some specific properties of these polar carotenoids must explain why they, among other available carotenoids, were selected during evolution to protect the retina and brain. It is also likely that the selective uptake and deposition of macular xanthophylls in the retina and brain are enhanced by specific xanthophyll-binding proteins. We hypothesize that the high membrane solubility and preferential transmembrane orientation of macular xanthophylls distinguish them from other dietary carotenoids, enhance their chemical and physical stability in retina and brain membranes and maximize their protective action in these organs. Most importantly, xanthophylls are selectively concentrated in the most vulnerable regions of lipid bilayer membranes enriched in polyunsaturated lipids. This localization is ideal if macular xanthophylls are to act as lipid-soluble antioxidants, which is the most accepted mechanism through which lutein and zeaxanthin protect neural tissue against degenerative diseases. Keywords: carotenoids; macular xanthophylls; zeaxanthin; lutein; neural tissue; lipid antioxidants; age-related macular degeneration (AMD); age-related neurodegenerative diseases 1. Introduction Major carotenoids that are present in the human diet can be divided into two groups, carotenes (nonpolar carotenoids, such as β-carotene, α-carotene and lycopene) and xanthophylls (polar carotenoids, such as lutein, zeaxanthin and β-cryptoxanthin) (see Figure1 for their structures). Xanthophylls form less than 20% of the total carotenoids in the human diet. Already in the blood plasma, the amount of xanthophylls increases to about 40% (Figure2A) [ 1]. It should be noted that the serum xanthophyll-to-carotenoid ratio varies among the population and depends on diet. This preferential intake of xanthophylls is further enhanced at the level of neural tissues. Xanthophylls are preferentially accumulated from circulation into the brain [1,2] and retina [3,4]. Recently, several carotenoids (including lutein, zeaxanthin, β-cryptoxanthin, α-cryptoxanthin, β-carotene, α-carotene Foods 2016, 5, 7; doi:10.3390/foods5010007 www.mdpi.com/journal/foods Foods 20162016,, 55,, 71 22of of 1918 and lycopene) have been identified in the human brain [2]. Surprisingly, xanthophylls are the most andabundant lycopene) carotenoids have been in identifiedthis tissue; in the the evaluation human brain by [2Craft]. Surprisingly, et al. [2] indicates xanthophylls that xanthophylls are the most abundantaccount for carotenoids about 65% in of this total tissue; carotenoids the evaluation in all brain by Craft regions.et al. [ 2Similar] indicates preferential that xanthophylls accumulation account of forup to about 72% 65% of xanthophylls of total carotenoids from circulation in all brain into regions. the brain Similar was reported preferential by Johnson accumulation et al. [1] of. upThus, to 72%brain of tissue, xanthophylls similar fromto the circulation retina, preferentially into the brain accumulates was reported macular by Johnson xanthophyllset al. [1]. Thus,(lutein brain and tissue,zeaxanthin); similar additionally, to the retina, it preferentially accumulates accumulates cryptoxanthin, macular which xanthophylls is not present (lutein in andthe zeaxanthin);retina. This additionally,preferential accumulation it accumulates is maximal cryptoxanthin, in the case which of the is notretina, present where in only the retina.xanthophylls This preferentialare present accumulation[3,4]. Figure 2A is maximalillustrates in the caseenhanced of the tissue retina, preferences where only xanthophyllsand selectivity are for present the accumulation [3,4]. Figure2 Aof illustratesxanthophylls. the enhanced tissue preferences and selectivity for the accumulation of xanthophylls. Only two dietarydietary carotenoids,carotenoids, namely lutein andand zeaxanthinzeaxanthin (macular(macular xanthophylls),xanthophylls), are selectively acc accumulatedumulated in in the the human human retina. retina. The The highest highest concentration concentration of of macular macular xanthophylls xanthophylls is isfound found in inthe the outer outer plexiform plexiform layer, layer, which which is a islayer a layer of neuronal of neuronal synapses synapses between between photoreceptor photoreceptor cells cellsand secondary and secondary neurons neurons [3,5]. Macular [3,5]. xanthophylls Macular xanthophylls are also present are also in the present layer of in rod the outer layer segments of rod outer[6,7] and segments in retinal [6,7 ]pigment and in retinalepithelium pigment cells epithelium[8]. In addition cells [to8]. the In preferential addition to accumulati the preferentialon of accumulationxanthophylls from of xanthophylls food into the from neural food tissue, into thethere neural is a significant tissue, there increase is a significant in the zeaxanthin increase-to in- thelutein zeaxanthin-to-lutein ratio in neural tissue, ratio as incompared neural tissue, to that as in compared the dietary to intake that inof thethese dietary xanthophylls, intake of and these in xanthophylls,blood plasma. andIn human in blood serum, plasma. the zeaxanthin In human-t serum,o-luteinthe ratio zeaxanthin-to-lutein ranges from 1:7 to 1:4 ratio [1,9 ranges–12], which from 1:7is consistent to 1:4 [1,9 with–12], thewhich relatively is consistent high lutein with thecontent relatively in fruits high and lutein vegeta contentbles as in compare fruits andd to vegetables the content as comparedof zeaxanthin. to the content of zeaxanthin. Figure 1. Chemical structures of carotenoids (xanthophylls and carotenes) abundant in food, blood Figure 1. Chemical structures of carotenoids (xanthophylls and carotenes) abundant in food, blood plasma andand neuralneural tissue.tissue. Foods 2016, 5, 7 3 of 19 Foods 2016, 5, 1 3 of 18 Figure 2. (A) Preferential accumulation of xanthophylls in the brain and retina tissues expressed as a percent of xanthophylls in the total carotenoid pool; (B) preferential accumulation of zeaxanthin Figure 2. (A) Preferential accumulation of xanthophylls in the brain and retina tissues expressed as a over lutein in the brain and retina tissues expressed as the zeaxanthin-to-lutein ratio. Data adapted percent of xanthophylls in the total carotenoid pool; (B) preferential accumulation of zeaxanthin over from [1,2,4,9–12]. lutein in the brain and retina tissues expressed as the zeaxanthin-to-lutein ratio. Data adapted from [1,2,4,9–12]. Zeaxanthin is the dominant xanthophyll in only a few food products, such as the goji berry and orangeZeaxanthin pepper [ 13is ,the14]. dominant Thus, the xanthophyll dietary intake in ofonly lutein a few is muchfood products higher than, such that as of the zeaxanthin, goji berry withand ortheange evaluated pepper dietary[13,14]. Thus, zeaxanthin-to-lutein the dietary intake ratio of oflutein 1:12 is to much 1:5 [ 11higher,15,16 than]. As that indicated of zeaxanthin, in Figure with2B, thethis evaluated ratio is increased dietary first zeaxanthin on the level-to-lutein of the ratio serum of and 1:12 next to 1:5 when [11,15,16] macular. As xanthophylls indicated arein Figure selectively 2B, thisaccumulated ratio is increased in the neural first tissue.on the The level zeaxanthin-to-lutein of the serum and rationext inwhen the retina macular increases xanthophylls to the value are selectivelyof 1:2 in the accumulated retina periphery in the neural and 2:1 tissue. in the The central zeaxanthin macula-to [-17lutein]. The ratio significant in the retina part increases of the total to theretina value zeaxanthin of 1:2 in the is represented retina periphery by its and stereoisomer 2:1 in the mesocentral-zeaxanthin macula [17] (see. The Figure significant1 for its part structure), of the totalwhich retina is formed zeaxanthin directly is in represented the retina from by luteinits stereoisomer [17]. The reported meso-zeaxanthin zeaxanthin-to-lutein (see Figure ratio 1 for in theits structure),human brain which ranges is formed from 1:3 directly to 1:1.4 in [ 1the,2]. retina All of from
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