Brain xanthophyll content and exploratory gene expression analysis: subspecies differences in rhesus macaque

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Abstract

Background

The dietary xanthophylls, lutein and zeaxanthin, accumulate in primate retina and brain, and emerging evidence indicates neural lutein content may be beneficial for cognition. Neural xanthophyll content in primates varies greatly among individuals, and genetic factors are likely to be significant contributors. Subspecies of rhesus macaques originating from different geographic locations are known to differ genetically, but the effect of origin on gene expression and carotenoid status has not been determined. The study objective was to determine whether xanthophyll status and expression of carotenoid-related genes, as well as genes with known variants between subspecies, differ between the brains of adult rhesus monkeys of Indian and Chinese origin.

Methods

Samples of prefrontal cortex, cerebellum, and striatum were collected from adult monkeys ( n = 9) fed a standard stock diet containing carotenoids. Serum and brain carotenoids were determined using reverse-phase high-performance liquid chromatography. For each brain region, RNA sequencing and real-time quantitative polymerase chain reaction were used to determine differentially expressed genes between the subspecies.

Results

Indian-origin monkeys had higher xanthophyll levels in brain tissue compared to Chinese-origin monkeys despite consuming similar amounts of dietary carotenoids. In a region-specific manner, four genes related to carotenoid and fatty acid metabolism ( BCO2, RPE65, ELOVL4, FADS2) and four genes involved in the immune response ( CD4, CD74, CXCL12 LTBR) were differentially expressed between Indian- and Chinese-origin monkeys. Expression of all four genes involved in carotenoid and fatty acid metabolism were correlated with brain xanthophyll concentration in a region-specific manner.

Conclusions

These results indicate that origin is related to differences in both gene expression and xanthophyll content in the brain. Findings from this study may have important implications regarding genetic diversity, lutein status, and cognition in primates.

Electronic supplementary material

The online version of this article (doi:10.1186/s12263-017-0557-3) contains supplementary material, which is available to authorized users.

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Most cited references 38

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Dietary Sources of Lutein and Zeaxanthin Carotenoids and Their Role in Eye Health

El-Sayed Abdel-Aal, Humayoun Akhtar, Khalid Zaheer … (2013)

The eye is a major sensory organ that requires special care for a healthy and productive lifestyle. Numerous studies have identified lutein and zeaxanthin to be essential components for eye health. Lutein and zeaxanthin are carotenoid pigments that impart yellow or orange color to various common foods such as cantaloupe, pasta, corn, carrots, orange/yellow peppers, fish, salmon and eggs. Their role in human health, in particular the health of the eye, is well established from epidemiological, clinical and interventional studies. They constitute the main pigments found in the yellow spot of the human retina which protect the macula from damage by blue light, improve visual acuity and scavenge harmful reactive oxygen species. They have also been linked with reduced risk of age-related macular degeneration (AMD) and cataracts. Research over the past decade has focused on the development of carotenoid-rich foods to boost their intake especially in the elderly population. The aim of this article is to review recent scientific evidences supporting the benefits of lutein and zexanthin in preventing the onset of two major age-related eye diseases with diets rich in these carotenoids. The review also lists major dietary sources of lutein and zeaxanthin and refers to newly developed foods, daily intake, bioavailability and physiological effects in relation to eye health. Examples of the newly developed high-lutein functional foods are also underlined.

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Lutein: more than just a filter for blue light.

Aize Kijlstra, Yuan Tian, Elton Kelly … (2012)

Lutein is concentrated in the primate retina, where together with zeaxanthin it forms the macular pigment. Traditionally lutein is characterized by its blue light filtering and anti-oxidant properties. Eliminating lutein from the diet of experimental animals results in early degenerative signs in the retina while patients with an acquired condition of macular pigment loss (Macular Telangiectasia) show serious visual handicap indicating the importance of macular pigment. Whether lutein intake reduces the risk of age related macular degeneration (AMD) or cataract formation is currently a strong matter of debate and abundant research is carried out to unravel the biological properties of the lutein molecule. SR-B1 has recently been identified as a lutein binding protein in the retina and this same receptor plays a role in the selective uptake in the gut. In the blood lutein is transported via high-density lipoproteins (HDL). Genes controlling SR-B1 and HDL levels predispose to AMD which supports the involvement of cholesterol/lutein transport pathways. Apart from beneficial effects of lutein intake on various visual function tests, recent findings show that lutein can affect immune responses and inflammation. Lutein diminishes the expression of various ocular inflammation models including endotoxin induced uveitis, laser induced choroidal neovascularization, streptozotocin induced diabetes and experimental retinal ischemia and reperfusion. In vitro studies show that lutein suppresses NF kappa-B activation as well as the expression of iNOS and COX-2. Since AMD has features of a chronic low-grade systemic inflammatory response, attention to the exact role of lutein in this disease has shifted from a local effect in the eye towards a possible systemic anti-inflammatory function. Copyright © 2012 Elsevier Ltd. All rights reserved.

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Cognitive findings of an exploratory trial of docosahexaenoic acid and lutein supplementation in older women.

Hae-Na Chung, D Snodderly, Dave E. Johnson … (2008)

Low dietary intake of docosahexaenoic acid (DHA) and/or foods rich in lutein may be associated with increased risk of cognitive decline in the elderly. The cognitive benefit of DHA and lutein in unimpaired elder women was explored in the context of a 4-month, double-blind, intervention trial of DHA and lutein supplementation for eye health. Forty-nine women (aged 60-80 years) were randomized to receive DHA (800 mg/day; n = 14), lutein (12 mg/day; n = 11), a combination of DHA and lutein (n = 14) or placebo (n = 10). Subjects underwent cognitive tests measuring verbal fluency, memory, processing speed and accuracy, and self-reports of mood at randomization and upon completion of the trial. Following supplementation, verbal fluency scores improved significantly in the DHA, lutein, and combined treatment groups (P < 0.03). Memory scores and rate of learning improved significantly in the combined treatment group (P < 0.03), who also displayed a trend toward more efficient learning (P = 0.07). Measures of mental processing speed, accuracy and mood were not affected by supplementation. These exploratory findings suggest that DHA and lutein supplementation may have cognitive benefit for older adults.

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Author and article information

Contributors

Emily S. Mohn: Emily.Mohn@tufts.edu

John W. Erdman Jr.: jwerdman@illinois.edu

Martha Neuringer: neuringe@ohsu.edu

Matthew J. Kuchan: Matthew.Kuchan@abbott.com

Elizabeth J. Johnson: Elizabeth.Johnson@tufts.edu

Journal

Journal ID (nlm-ta): Genes Nutr

Journal ID (iso-abbrev): Genes Nutr

Title: Genes & Nutrition

Publisher: BioMed Central (London )

ISSN (Print): 1555-8932

ISSN (Electronic): 1865-3499

Publication date (Electronic): 8 March 2017

Publication date PMC-release: 8 March 2017

Publication date Collection: 2017

Volume: 12

Electronic Location Identifier: 9

Affiliations

[1 ]ISNI 0000 0004 1936 7531, GRID grid.429997.8, Jean Mayer United States Department of Agriculture Human Nutrition Research Center on Aging, , Tufts University, ; Boston, MA USA

[2 ]ISNI 0000 0004 1936 9991, GRID grid.35403.31, Department of Food Science and Human Nutrition, , University of Illinois at Urbana-Champaign, ; Urbana, IL USA

[3 ]ISNI 0000 0000 9758 5690, GRID grid.5288.7, Division of Neuroscience, Oregon National Primate Research Center, , Oregon Health and Science University, ; Beaverton, Oregon USA

[4 ]Abbott Nutrition, Columbus, Ohio USA

[5 ]Antioxidants Research Laboratory, 711 Washington Street, Boston, MA 02111 USA

Article

Publisher ID: 557

DOI: 10.1186/s12263-017-0557-3

PMC ID: 5341479

PubMed ID: 28286579

SO-VID: 70dcc755-10ea-45a3-ba89-65b908976eb3

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 12 December 2016

Date accepted : 17 February 2017

Funding

Funded by: Abbott Nutrition through the Center for Nutrition, Learning and Memory

Funded by: USDA

Award ID: 58-1950-0-014

Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;

Award ID: P51OD011092

Award Recipient : Martha Neuringer

Custom metadata

ScienceOpen disciplines: Nutrition & Dietetics

Keywords: lutein,zeaxanthin,rhesus monkey,subspecies,brain,rna-sequencing

Data availability:

ScienceOpen disciplines: Nutrition & Dietetics

Keywords: lutein, zeaxanthin, rhesus monkey, subspecies, brain, rna-sequencing

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Brain xanthophyll content and exploratory gene expression analysis: subspecies differences in rhesus macaque

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Karger: Endocrinology

Most cited references 38

Dietary Sources of Lutein and Zeaxanthin Carotenoids and Their Role in Eye Health

Lutein: more than just a filter for blue light.

Cognitive findings of an exploratory trial of docosahexaenoic acid and lutein supplementation in older women.

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