Highlights
- •A metabolomics study was done using archived ovarian tissue and serum from midlife cynomolgus monkeys that had been exposed to a prudent diet or a Western diet.
- •Sixty-four metabolites were identified in serum and 47 metabolites were identified in ovarian tissue that differed by diet.
- •Dietary exposure had a significant impact on the serum and ovarian metabolome, and demonstrated perturbation in metabolic pathways.
Abstract
Objective
The objective of this investigation was to determine differences in the profiles of
endogenous metabolites (metabolomics) among ovaries and serum derived from Old World
nonhuman primates fed prudent or Western diets.
Design
A retrospective, observational study was done using archived ovarian tissue and serum
from midlife cynomolgus monkeys (Macaca fasicularis). Targeted and broad spectrum metabolomics analysis was used to compare ovarian tissue
and serum from monkeys that had been exposed to a prudent diet or a Western diet.
Monkeys in the prudent diet group (n = 13) were research naïve and had been exposed only to a commercial monkey chow diet
(low in cholesterol and saturated fats, high in complex carbohydrates). Western diet
monkeys (n = 8) had consumed a diet that was high in cholesterol, saturated animal fats and soluble
carbohydrates for 2 years prior to ovarian tissue and serum collection.
Outcome measures
Metabolomic analyses were done on extracts of homogenized ovary tissue samples, and
extracts of serum. Targeted analysis was conducted using the Biocrates p180 kit and
broad spectrum analysis was conducted using UPLC-TOF-MS, resulting in the detection
of 3500 compound ions.
Results
Using metabolomics methods, which capture thousands of signals for metabolites, 64
metabolites were identified in serum and 47 metabolites were identified in ovarian
tissue that differed by diet. Quantitative targeted analysis revealed 13 amino acids,
6 acrylcarnitines, and 2 biogenic amines that were significantly (p < 0.05) different between the two diet groups for serum extracts, and similar results
were observed for the ovary extracts.
Conclusions
These data demonstrate that dietary exposure had a significant impact on the serum
and ovarian metabolome, and demonstrated perturbation in carnitine, lipids/fatty acid,
and amino acid metabolic pathways.
Abbreviations:
WFPC (wake forest primate center), NHP (nonhuman primate)Keywords
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References
- Roles of reactive oxygen species and antioxidants in ovarian toxicity.Biol. Reprod. 2012; 86: 27
- Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary.Biol. Reprod. 2011; 84: 775-782
- Involvement of the up-regulated FoxO1 expression in follicular granulosa cell apoptosis induced by oxidative stress.J. Biol. Chem. 2012; 287: 25727-25740
- Importance of the omega-6/omega-3 balance in health and disease: evolutionary aspects of diet.World Rev. Nutr. Diet. 2011; 102: 10-21
- Postprandial metabolic events and fruit-derived phenolics: a review of the science.Br. J. Nutr. 2010; 104: S1-14
- Endothelial senescence after high-cholesterol: high-fat diet challenge in baboons.Am. J. Physiol. Heart Circ. Physiol. 2007; 292: H2913-20
- Nutrition and reproduction: is there evidence to support a Fertility Diet to improve mitochondrial function?.Maturitas. 2013; 74: 309-312
- Identification of metabolites in the normal ovary and their transformation in primary and metastatic ovarian cancer.PLoS One. 2011; 6: e19963
- Women with reduced ovarian reserve or advanced maternal age have an altered follicular environment.Fertil. Steril. 2012; 98 (e1-2): 986-994
- The effect of diet and cardiovascular risk on ovarian aging in cynomolgus monkeys (Macaca fascicularis).Menopause. 2010; 17: 741-748
- Physiology and endocrinology of the ovarian cycle in macaques.Toxicol. Pathol. 2008; 36: 7S-23S
- Reproductive aging and risk for chronic disease: insights from studies of nonhuman primates.Maturitas. 2010; 67: 7-14
- DHA-enriched high-oleic acid canola oil improves lipid profile and lowers predicted cardiovascular disease risk in the canola oil multicenter randomized controlled trial.Am. J. Clin. Nutr. 2014; 100: 88-97
- Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry.Nat. Protoc. 2011; 6: 1060-1083
- Chemometrics in metabonomics.J. Proteome Res. 2007; 6: 469-479
- Megavariate analysis of environmental QSAR data. Part I-a basic framework founded on principal component analysis (PCA), partial least squares (PLS), and statistical molecular design (SMD).Mol. Divers. 2006; 10: 169-186
- Extracting meaningful information from metabonomic data using multivariate statistics.Methods Mol. Biol. 2015; 1277: 137-146
- Global urinary metabolic profiling procedures using gas chromatography–mass spectrometry.Nat. Protoc. 2011; 6: 1483-1499
- Procedure for tissue sample preparation and metabolite extraction for high-throughput targeted metabolomics.Metabolomics. 2012; 8: 133-142
- Statistical analysis and modeling of mass spectrometry-based metabolomics data.Methods Mol. Biol. 2014; 1198: 333-353
- Adjusting for multiple testing–when and how?.J. Clin. Epidemiol. 2001; 54: 343-349
- The effects of diet on inflammation: emphasis on the metabolic syndrome.J. Am. Coll. Cardiol. 2006; 48: 677-685
- Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction.Am. J. Clin. Nutr. 2004; 80: 1029-1035
- Arterial stiffness is increased in asymptomatic nondiabetic postmenopausal women with a polycystic ovary syndrome phenotype.J. Hypertens. 2013; 31: 1998-2004
- Maternal high-fat diet impacts endothelial function in nonhuman primate offspring.Int. J. Obes. (Lond.). 2013; 37: 254-262
- Fructose-fed rhesus monkeys: a nonhuman primate model of insulin resistance, metabolic syndrome, and type 2 diabetes.Clin. Transl. Sci. 2011; 4: 243-252
- Fertility of men and women aged 15–44 years in the United States: national survey of family growth, 2006–2010.Natl. Health Stat. Rep. 2016; 2012: 1-28
- Fertility, family planning, and reproductive health of U.S. women: data from the 2002 national survey of family growth.Vital Health Stat. 2005; 23: 1-160
- Fertility and ageing.Hum. Reprod. Update. 2005; 11: 261-276
- High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates.Endocrinology. 2010; 151: 5438-5445
- Prolonging the female reproductive lifespan and improving egg quality with dietary omega-3 fatty acids.Aging Cell. 2012; 11: 1046-1054
- Delay in oocyte aging in mice by the antioxidant N-acetyl-l-cysteine (NAC).Hum. Reprod. 2012; 27: 1411-1420
- Resveratrol protects against age-associated infertility in mice.Hum. Reprod. 2013; 28: 707-717
- Embryo resorptions in mice induced by diterpene resin acids of Pinus ponderosa needles.Cornell Vet. 1981; 71: 34-42
- Urinary hippuric acid after ingestion of edible fruits.Bosn. J. Basic Med. Sci. 2008; 8: 38-43
- Health consequences of catabolic synthesis of hippuric acid in humans.Curr. Clin. Pharmacol. 2010; 5: 67-73
- Metabolomic profiling of human follicular fluid from patients with repeated failure of in vitro fertilization using gas chromatography/mass spectrometry.Int. J. Clin. Exp. Pathol. 2014; 7: 7220-7229
- Fatty acid metabolism during maturation affects glucose uptake and is essential to oocyte competence.Reproduction. 2014; 148: 429-439
Article info
Publication history
Published online: July 13, 2016
Accepted:
July 7,
2016
Received in revised form:
June 25,
2016
Received:
March 21,
2016
Identification
Copyright
Published by Elsevier Ireland Ltd.
