Stachydrine, N-acetylornithine and trimethylamine N-oxide levels as candidate milk biomarkers of maternal consumption of an obesogenic diet during lactation

. 2023 Sep-Oct ; 49 (5) : 1022-1037. [epub] 20230525

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37227188

Grantová podpora
Proyecto PGC2018-097436-B-I00
MCIN/AEI/10.13039/501100011033
FEDER Una manera de hacer Europa
the Instituto de Salud Carlos III
Centro de Investigación Biomédica en Red Fisiopatología de la Obesidad y Nutrición
CIBERobn
LQ200111901 Czech Academy of Sciences
FP6-506360 The European Nutrigenomics Organization, EU

We aimed to evaluate whether improving maternal diet during lactation in diet-induced obese rats reverts the impact of western diet (WD) consumption on the metabolome of milk and offspring plasma, as well as to identify potential biomarkers of these conditions. Three groups of dams were followed: control-dams (CON-dams), fed with standard diet (SD); WD-dams, fed with WD prior and during gestation and lactation; and reversion-dams (REV-dams), fed as WD-dams but moved to SD during lactation. Metabolomic analysis was performed in milk at lactation days 5, 10, and 15, and in plasma from their male and female offspring at postnatal day 15. Milk of WD-dams presented, throughout lactation and compared to CON-dams, altered profiles of amino acids and of the carnitine pool, accompanied by changes in other polar metabolites, being stachydrine, N-acetylornithine, and trimethylamine N-oxide the most relevant and discriminatory metabolites between groups. The plasma metabolome profile was also altered in the offspring of WD-dams in a sex-dependent manner, and stachydrine, ergothioneine and the acylcarnitine C12:1 appeared as the top three most discriminating metabolites in both sexes. Metabolomic changes were largely normalized to control levels both in the milk of REV-dams and in the plasma of their offspring. We have identified a set of polar metabolites in maternal milk and in the plasma of the offspring whose alterations may indicate maternal intake of an unbalanced diet during gestation and lactation. Levels of these metabolites may also reflect the beneficial effects of implementing a healthier diet during lactation.

Zobrazit více v PubMed

World Health Organization. WHO European Regional Obesity Report. Copenhagen: Regional Office for Europe; 2022.

Picó C, Reis F, Egas C, Mathias P, Matafome P. Lactation as a programming window for metabolic syndrome. Eur J Clin Invest. 2021;51:e13482. https://doi.org/10.1111/eci.13482

Erick M. Breast milk is conditionally perfect. Med Hypotheses. 2018;111:82-9. https://doi.org/10.1016/J.MEHY.2017.12.020

Fields DA, Schneider CR, Pavela G. A narrative review of the associations between six bioactive components in breast milk and infant adiposity. Obesity. 2016;24:1213-21. https://doi.org/10.1002/oby.21519

Keikha M, Bahreynian M, Saleki M, Kelishadi R. Macro- and micronutrients of human Milk composition: are they related to maternal diet? A comprehensive systematic review. Breastfeed Med. 2017;12:517-27. https://doi.org/10.1089/BFM.2017.0048

Bravi F, Wiens F, Decarli A, Dal Pont A, Agostoni C, Ferraroni M. Impact of maternal nutrition on breast-milk composition: a systematic review. Am J Clin Nutr. 2016;104:646-62. https://doi.org/10.3945/AJCN.115.120881

Pomar CA, Castro H, Picó C, Serra F, Palou A, Sánchez J. Cafeteria diet consumption during lactation in rats, rather than obesity per Se, alters miR-222, miR-200a, and miR-26a levels in Milk. Mol Nutr Food Res. 2019;63:e1800928. https://doi.org/10.1002/MNFR.201800928

Brandorff NP. The effect of dietary fat on the fatty acid composition of lipids secreted in rats' milk. Lipids. 1980;15:276-8. https://doi.org/10.1007/BF02535840

Priego T, Sánchez J, García AP, Palou A, Picó C. Maternal dietary fat affects milk fatty acid profile and impacts on weight gain and thermogenic capacity of suckling rats. Lipids. 2013;48:481-95. https://doi.org/10.1007/S11745-013-3764-8

Pomar CA, Van Nes R, Sánchez J, Picó C, Keijer J, Palou A. Maternal consumption of a cafeteria diet during lactation in rats leads the offspring to a thin-outside-fat-inside phenotype. Int J Obes (Lond). 2017;41:1279-87. https://doi.org/10.1038/IJO.2017.42

Bayol SA, Farrington SJ, Stickland NC. A maternal “junk food” diet in pregnancy and lactation promotes an exacerbated taste for “junk food” and a greater propensity for obesity in rat offspring. Br J Nutr. 2007;98:843-51. https://doi.org/10.1017/S0007114507812037

Bzikowska-Jura A, Czerwonogrodzka-Senczyna A, Olędzka G, Szostak-Węgierek D, Weker H, Wesołowska A. Maternal nutrition and body composition during breastfeeding: association with human milk composition. Nutrients. 2018;10:1379. https://doi.org/10.3390/NU10101379

Wahlig JL, Bales ES, Jackman MR, Johnson GC, McManaman JL, MacLean PS. Impact of high-fat diet and obesity on energy balance and fuel utilization during the metabolic challenge of lactation. Obesity (Silver Spring). 2012;20:65-75. https://doi.org/10.1038/OBY.2011.196

Pomar CA, Castillo P, Palou M, Palou A, Picó C. Implementation of a healthy diet to lactating rats attenuates the early detrimental programming effects in the offspring born to obese dams. Putative relationship with milk hormone levels. J Nutr Biochem. 2022;107:109043. https://doi.org/10.1016/J.JNUTBIO.2022.109043

Castillo P, Kuda O, Kopecky J, Pomar CA, Palou A, Palou M, et al. Reverting to a healthy diet during lactation normalizes maternal Milk lipid content of diet-induced obese rats and prevents early alterations in the plasma lipidome of the offspring. Mol Nutr Food Res. 2022;66:2200204. https://doi.org/10.1002/MNFR.202200204

Pomar CA, Kuda O, Kopecky J, Rombaldova M, Castro H, Picó C, et al. Maternal diet, rather than obesity itself, has a main influence on milk triacylglycerol profile in dietary obese rats. Biochim Biophys Acta Mol Cell Biol Lipids. 2020;1865:158556. https://doi.org/10.1016/J.BBALIP.2019.158556

Hillesheim E, Brennan L. Metabotyping and its role in nutrition research. Nutr Res rev. 2020;33:33-42. https://doi.org/10.1017/S0954422419000179

Tsugawa H, Ikeda K, Takahashi M, Satoh A, Mori Y, Uchino H, et al. A lipidome atlas in MS-DIAL 4. Nat Biotechnol. 2020;38:1159-63. https://doi.org/10.1038/S41587-020-0531-2

Lopes M, Brejchova K, Riecan M, Novakova M, Rossmeisl M, Cajka T, et al. Metabolomics atlas of oral 13C-glucose tolerance test in mice. Cell Rep. 2021;37:109833. https://doi.org/10.1016/J.CELREP.2021.109833

Pang Z, Chong J, Zhou G, de Lima Morais DA, Chang L, Barrette M, et al. MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021;49:W388-96. https://doi.org/10.1093/NAR/GKAB382

Seibert R, Abbasi F, Hantash FM, Caulfield MP, Reaven G, Kim SH. Relationship between insulin resistance and amino acids in women and men. Physiol Rep. 2015;3:e12392. https://doi.org/10.14814/PHY2.12392

Nakamura H, Jinzu H, Nagao K, Noguchi Y, Shimba N, Miyano H, et al. Plasma amino acid profiles are associated with insulin, C-peptide and adiponectin levels in type 2 diabetic patients. Nutr Diabetes. 2014;4:e133. https://doi.org/10.1038/NUTD.2014.32

Guasch-Ferré M, Hruby A, Toledo E, Clish CB, Martínez-González MA, Salas-Salvadó J, et al. Metabolomics in prediabetes and diabetes: a systematic review and meta-analysis. Diabetes Care. 2016;39:833-46. https://doi.org/10.2337/DC15-2251

Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, Lien LF, et al. A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9:311-26. https://doi.org/10.1016/J.CMET.2009.02.002

Wang TJ, Larson MG, Vasan RS, Cheng S, Rhee EP, McCabe E, et al. Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17:448-53. https://doi.org/10.1038/NM.2307

Siddik MAB, Shin AC. Recent Progress on branched-chain amino acids in obesity, diabetes, and beyond. Endocrinol Metab (Seoul, Korea). 2019;34:234-46. https://doi.org/10.3803/ENM.2019.34.3.234

Estrada-Alcalde I, Tenorio-Guzman MR, Tovar AR, Salinas-Rubio D, Torre-Villalvazo I, Torres N, et al. Metabolic fate of branched-chain amino acids during adipogenesis, in adipocytes from obese mice and C2C12 myotubes. J Cell Biochem. 2017;118:808-18. https://doi.org/10.1002/JCB.25755

Doi M, Yamaoka I, Fukunaga T, Nakayama M. Isoleucine, a potent plasma glucose-lowering amino acid, stimulates glucose uptake in C2C12 myotubes. Biochem Biophys Res Commun. 2003;312:1111-7. https://doi.org/10.1016/J.BBRC.2003.11.039

Newgard CB. Interplay between lipids and branched-chain amino acids in development of insulin resistance. Cell Metab. 2012;15:606-14. https://doi.org/10.1016/J.CMET.2012.01.024

Krzyściak W. Activity of selected aromatic amino acids in biological systems. Acta Biochim pol. 2011;58:461-6. https://doi.org/10.18388/abp.2011_2211

Laterra J, Keep R, Betz LA, Goldstein GW. Blood-brain-cerebrospinal fluid barriers. In: Siegel G, Agranoff B, Albers R, Fisher SK, Uhler MD, editors. Basic Neurochemistry: Molecular, Cellular and Medical Aspects. Raven: Lippincott; 1999. pp. 671-90. https://www.ncbi.nlm.nih.gov/books/NBK28180/

Aquili L. The role of tryptophan and tyrosine in executive function and reward processing. Int J Tryptophan Res. 2020;13:1178646920964825. https://doi.org/10.1177/1178646920964825

Riedel WJ, Sobczak S, Schmitt JAJ. Tryptophan modulation and cognition. Adv Exp Med Biol. 2003;527:207-13. https://doi.org/10.1007/978-1-4615-0135-0_24

Bloemendaal M, Froböse MI, Wegman J, Zandbelt BB, van de Rest O, Cools R, et al. Neuro-cognitive effects of acute tyrosine administration on reactive and proactive response inhibition in healthy older adults. eNeuro. 2018;5:ENEURO.0035-17. https://doi.org/10.1523/ENEURO.0035-17.2018

Fernstrom JD. Large neutral amino acids: dietary effects on brain neurochemistry and function. Amino Acids. 2013;45:419-30. https://doi.org/10.1007/S00726-012-1330-Y

Yamakado M, Tanaka T, Nagao K, Ishizaka Y, Mitushima T, Tani M, et al. Plasma amino acid profile is associated with visceral fat accumulation in obese Japanese subjects. Clin Obes. 2012;2:29-40. https://doi.org/10.1111/J.1758-8111.2012.00039.X

Pomar CA, Kuda O, Kopecky J, Rombaldova M, Castro H, Picó C, et al. Alterations in plasma acylcarnitine and amino acid profiles may indicate poor nutrition during the suckling period due to maternal intake of an unbalanced diet and may predict later metabolic dysfunction. FASEB J. 2019;33:796-807. https://doi.org/10.1096/FJ.201800327RR

Tsan L, Décarie-Spain L, Noble EE, Kanoski SE. Western diet consumption during development: setting the stage for neurocognitive dysfunction. Front Neurosci. 2021;15:632312. https://doi.org/10.3389/FNINS.2021.632312

Sun S, He D, Luo C, Lin X, Wu J, Yin X, et al. Metabolic syndrome and its components are associated with altered amino acid profile in Chinese Han population. Front Endocrinol (Lausanne). 2022;12:795044. https://doi.org/10.3389/FENDO.2021.795044

Holm LJ, Buschard K. L-serine: a neglected amino acid with a potential therapeutic role in diabetes. APMIS. 2019;127:655-9. https://doi.org/10.1111/APM.12987

Arenas J, Rubio JC, Martín MA, Campos Y. Biological roles of L-carnitine in perinatal metabolism. Early Hum Dev. 1998;53:S43-50. https://doi.org/10.1016/S0378-3782(98)00064-4

Peschechera A, Scalibastri M, Russo F, Giarrizzo MG, Carminati P, Giannessi F, et al. Carnitine depletion in rat pups from mothers given mildronate: a model of carnitine deficiency in late fetal and neonatal life. Life Sci. 2005;77:3078-91. https://doi.org/10.1016/J.LFS.2005.03.029

Sánchez C, Franco L, Regal P, Lamas A, Cepeda A, Fente C. Breast Milk: a source of functional compounds with potential application in nutrition and therapy. Nutrients. 2021;13:1-34. https://doi.org/10.3390/NU13031026

Reuter SE, Evans AM. Carnitine and acylcarnitines: pharmacokinetic, pharmacological and clinical aspects. Clin Pharmacokinet. 2012;51:553-72. https://doi.org/10.1007/BF03261931

McCann MR, De la Rosa MVG, Rosania GR, Stringer KA. L-carnitine and Acylcarnitines: mitochondrial biomarkers for precision medicine. Metabolites. 2021;11:1-21. https://doi.org/10.3390/METABO11010051

Gander J, Carrard J, Gallart-Ayala H, Borreggine R, Teav T, Infanger D, et al. Metabolic impairment in coronary artery disease: elevated serum Acylcarnitines under the spotlights. Front Cardiovasc Med. 2021;8:792350. https://doi.org/10.3389/FCVM.2021.792350

Blaak E. Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care. 2001;4:499-502. https://doi.org/10.1097/00075197-200111000-00006

Chenevière X, Borrani F, Sangsue D, Gojanovic B, Malatesta D. Gender differences in whole-body fat oxidation kinetics during exercise. Appl Physiol Nutr Metab. 2011;36:88-95. https://doi.org/10.1139/H10-086

Lamont LS, McCullough AJ, Kalhan SC. Gender differences in leucine, but not lysine, kinetics. J Appl Physiol. 2001;91:357-62. https://doi.org/10.1152/JAPPL.2001.91.1.357

Lamont LS. Gender differences in amino acid use during endurance exercise. Nutr rev. 2005;63:419-22. https://doi.org/10.1301/NR.2005.DEC.419-422

Hamadeh MJ, Devries MC, Tarnopolsky MA. Estrogen supplementation reduces whole body leucine and carbohydrate oxidation and increases lipid oxidation in men during endurance exercise. J Clin Endocrinol Metab. 2005;90:3592-9. https://doi.org/10.1210/JC.2004-1743

Horakova O, Hansikova J, Bardova K, Gardlo A, Rombaldova M, Kuda O, et al. Plasma Acylcarnitines and amino acid levels As an early complex biomarker of propensity to high-fat diet-induced obesity in mice. PLoS One. 2016;11:e0155776. https://doi.org/10.1371/JOURNAL.PONE.0155776

Xie X, Yang C, Cui Q, Ma W, Liu J, Yao Q, et al. Stachydrine mediates rapid vascular relaxation: activation of endothelial nitric oxide synthase involving AMP-activated protein kinase and Akt phosphorylation in vascular endothelial cells. J Agric Food Chem. 2019;67:9942-9. https://doi.org/10.1021/ACS.JAFC.9B03501

Chen HH, Wang SN, Cao TT, Zheng JL, Tian J, Shan XL, et al. Stachydrine hydrochloride alleviates pressure overload-induced heart failure and calcium mishandling on mice. J Ethnopharmacol. 2020;248:112306. https://doi.org/10.1016/J.JEP.2019.112306

Lee E, Kang S, Lee AR, Kim JH, Kim TW, Lee JE, et al. Stachydrine derived from fermented rice prevents diet-induced obesity by regulating adipsin and endoplasmic reticulum homeostasis. J Nutr Biochem. 2022;107:109036. https://doi.org/10.1016/J.JNUTBIO.2022.109036

Smith E, Ottosson F, Hellstrand S, Ericson U, Orho-Melander M, Fernandez C, et al. Ergothioneine is associated with reduced mortality and decreased risk of cardiovascular disease. Heart. 2020;106:691-7. https://doi.org/10.1136/HEARTJNL-2019-315485

Nam HS. Gut microbiota and ischemic stroke: the role of trimethylamine N-oxide. J Stroke. 2019;21:151-9. https://doi.org/10.5853/JOS.2019.00472

Yu ZL, Zhang LY, Jiang XM, Xue CH, Chi N, Zhang TT, et al. Effects of dietary choline, betaine, and L-carnitine on the generation of trimethylamine-N-oxide in healthy mice. J Food Sci. 2020;85:2207-15. https://doi.org/10.1111/1750-3841.15186

Fu TT, Shen L. Ergothioneine as a natural antioxidant against oxidative stress-related diseases. Front Pharmacol. 2022;13:850813. https://doi.org/10.3389/FPHAR.2022.850813

Playdon MC, Moore SC, Derkach A, Reedy J, Subar AF, Sampson JN, et al. Identifying biomarkers of dietary patterns by using metabolomics. Am J Clin Nutr. 2017;105:450-65. https://doi.org/10.3945/AJCN.116.144501

Haikonen R, Kärkkäinen O, Koistinen V, Hanhineva K. Diet- and microbiota-related metabolite, 5-aminovaleric acid betaine (5-AVAB), in health and disease. Trends Endocrinol Metab. 2022;33:463-80. https://doi.org/10.1016/J.TEM.2022.04.004

Koistinen VM, Kärkkäinen O, Borewicz K, Zarei I, Jokkala J, Micard V, et al. Contribution of gut microbiota to metabolism of dietary glycine betaine in mice and in vitro colonic fermentation. Microbiome. 2019;7:103. https://doi.org/10.1186/S40168-019-0718-2

Cheah IK, Lee JZ, Tang RMY, Koh PW, Halliwell B. Does lactobacillus reuteri influence ergothioneine levels in the human body. FEBS Lett. 2022;596:1241-51. https://doi.org/10.1002/1873-3468.14364

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...