Plasma metabolomic profile of adiposity and body composition in childhood: The Genetics of Glucose regulation in Gestation and Growth cohort.

adiposity body composition childhood metabolomics

Journal

Pediatric obesity
ISSN: 2047-6310
Titre abrégé: Pediatr Obes
Pays: England
ID NLM: 101572033

Informations de publication

Date de publication:
03 Jul 2024
Historique:
revised: 21 05 2024
received: 20 12 2023
accepted: 07 06 2024
medline: 3 7 2024
pubmed: 3 7 2024
entrez: 3 7 2024
Statut: aheadofprint

Résumé

This study identified metabolite modules associated with adiposity and body fat distribution in childhood using gold-standard measurements. We used cross-sectional data from 329 children at mid-childhood (age 5.3 ± 0.3 years; BMI 15.7 ± 1.5 kg/m We identified a 'green' module of 120 metabolites, primarily comprised of lipids (mostly sphingomyelins and phosphatidylcholine), that showed positive correlations (all FDR p < 0.05) with DXA estimates of total and truncal fat (ρ A module of metabolites was associated with adiposity measures in childhood.

Identifiants

pubmed: 38958048
doi: 10.1111/ijpo.13149
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13149

Subventions

Organisme : Canadian Institutes of Health Research (CIHR)
ID : MOP 115071
Organisme : Canadian Institutes of Health Research (CIHR)
ID : PJT-152989
Organisme : Fonds de recherche du Québec - Santé (FRQS)
ID : 20697
Organisme : Diabète Québec

Informations de copyright

© 2024 World Obesity Federation.

Références

Hirst JE, Villar J, Papageorghiou AT, Ohuma E, Kennedy SH. Preventing childhood obesity starts during pregnancy. Lancet. 2015;386(9998):1039‐1040. doi:10.1016/S0140‐6736(15)00142‐7
Allcock DM, Gardner MJ, Sowers JR. Relation between childhood obesity and adult cardiovascular risk. Int J Pediatr Endocrinol. 2009;2009:108187. doi:10.1155/2009/108187
McGinty SM, Osganian SK, Feldman HA, Milliren CE, Field AE, Richmond TK. BMI trajectories from birth to young adulthood. Obesity. 2018;26(6):1043‐1049. doi:10.1002/oby.22176
Di Cesare M, Soric M, Bovet P, et al. The epidemiological burden of obesity in childhood: a worldwide epidemic requiring urgent action. BMC Med. 2019;17(1):212. doi:10.1186/s12916‐019‐1449‐8
Nicholson JK, Lindon JC. Systems biology: metabonomics. Nature. 2008;455(7216):1054‐1056. doi:10.1038/4551054a
Anjos S, Feiteira E, Cerveira F, et al. Lipidomics reveals similar changes in serum phospholipid signatures of overweight and obese pediatric subjects. J Proteome Res. 2019;18(8):3174‐3183. doi:10.1021/acs.jproteome.9b00249
Gerl MJ, Klose C, Surma MA, et al. Machine learning of human plasma lipidomes for obesity estimation in a large population cohort. PLoS Biol. 2019;17(10):e3000443. doi:10.1371/journal.pbio.3000443
McClain KM, Friedenreich CM, Matthews CE, et al. Body composition and metabolomics in the alberta physical activity and breast cancer prevention trial. J Nutr. 2022;152(2):419‐428. doi:10.1093/jn/nxab388
Guillemette L, Allard C, Lacroix M, et al. Genetics of Glucose regulation in Gestation and Growth (Gen3G): a prospective prebirth cohort of mother‐child pairs in Sherbrooke, Canada. BMJ Open. 2016;6(2):e010031. doi:10.1136/bmjopen‐2015‐010031
Zaghlool SB, Mook‐Kanamori DO, Kader S, et al. Deep molecular phenotypes link complex disorders and physiological insult to CpG methylation. Hum Mol Genet. 2018;27(6):1106‐1121. doi:10.1093/hmg/ddy006
Evans AM, DeHaven CD, Barrett T, Mitchell M, Milgram E. Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small‐molecule complement of biological systems. Anal Chem. 2009;81(16):6656‐6667. doi:10.1021/ac901536h
Dehaven CD, Evans AM, Dai H, Lawton KA. Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Chem. 2010;2(1):9. doi:10.1186/1758‐2946‐2‐9
Hagenbeek FA, Pool R, van Dongen J, et al. Heritability estimates for 361 blood metabolites across 40 genome‐wide association studies. Nat Commun. 2020;11(1):39. doi:10.1038/s41467‐019‐13770‐6
Wei R, Wang J, Su M, et al. Missing value imputation approach for mass spectrometry‐based metabolomics data. Sci Rep. 2018;8(1):663. doi:10.1038/s41598‐017‐19120‐0
Yang J, Zhao X, Lu X, Lin X, Xu G. A data preprocessing strategy for metabolomics to reduce the mask effect in data analysis. Front Mol Biosci. 2015;2:4. doi:10.3389/fmolb.2015.00004
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinform. 2008;9:559. doi:10.1186/1471‐2105‐9‐559
Pemmaraju S, Skiena S. Computational Discrete Mathematics: Combinatorics and Graph Theory with Mathematica. 1st ed. Cambridge University Press; 1990.
Song L, Langfelder P, Horvath S. Comparison of co‐expression measures: mutual information, correlation, and model based indices. BMC Bioinform. 2012;13:328. doi:10.1186/1471‐2105‐13‐328
Zhang B, Horvath S. A general framework for weighted gene co‐expression network analysis. Stat Appl Genet Mol Biol. 2005;4:17. doi:10.2202/1544‐6115.1128
Yip AM, Horvath S. Gene network interconnectedness and the generalized topological overlap measure. BMC Bioinform. 2007;8:22. doi:10.1186/1471‐2105‐8‐22
Langfelder P, Zhang B, Horvath S. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics. 2008;24(5):719‐720. doi:10.1093/bioinformatics/btm563
Bareinboim E, Barbosa VC. Descents and nodal load in scale‐free networks. Phys Rev E Stat Nonlin Soft Matter Phys. 2008;77(4 Pt 2):046111. doi:10.1103/PhysRevE.77.046111
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol. 2018;57(1):289‐300. doi:10.1111/j.2517‐6161.1995.tb02031.x
Eisinger K, Liebisch G, Schmitz G, Aslanidis C, Krautbauer S, Buechler C. Lipidomic analysis of serum from high fat diet induced obese mice. Int J Mol Sci. 2014;15(2):2991‐3002. doi:10.3390/ijms15022991
Park M, Wu D, Park T, et al. APPL1 transgenic mice are protected from high‐fat diet‐induced cardiac dysfunction. Am J Physiol Endocrinol Metab. 2013;305(7):E795‐E804. doi:10.1152/ajpendo.00257.2013
Turner N, Kowalski GM, Leslie SJ, et al. Distinct patterns of tissue‐specific lipid accumulation during the induction of insulin resistance in mice by high‐fat feeding. Diabetologia. 2013;56(7):1638‐1648. doi:10.1007/s00125‐013‐2913‐1
Li Z, Zhang H, Liu J, et al. Reducing plasma membrane sphingomyelin increases insulin sensitivity. Mol Cell Biol. 2011;31(20):4205‐4218. doi:10.1128/MCB.05893‐11
Hellmuth C, Kirchberg FF, Brandt S, et al. An individual participant data meta‐analysis on metabolomics profiles for obesity and insulin resistance in European children. Sci Rep. 2019;9(1):5053. doi:10.1038/s41598‐019‐41449‐x
Chew WS, Torta F, Ji S, et al. Large‐scale lipidomics identifies associations between plasma sphingolipids and T2DM incidence. JCI Insight. 2019;5(13):e126925. doi:10.1172/jci.insight.126925
Im SS, Park HY, Shon JC, et al. Plasma sphingomyelins increase in pre‐diabetic Korean men with abdominal obesity. PLoS One. 2019;14(3):e0213285. doi:10.1371/journal.pone.0213285
Szczerbinski L, Wojciechowska G, Olichwier A, et al. Untargeted metabolomics analysis of the serum metabolic signature of childhood obesity. Nutrients. 2022;14(1):214. doi:10.3390/nu14010214
Boini KM, Xia M, Koka S, Gehr TW, Li PL. Sphingolipids in obesity and related complications. Front Biosci (Landmark ed). 2017;22(1):96‐116. doi:10.2741/4474
Liu B, Obeid LM, Hannun YA. Sphingomyelinases in cell regulation. Semin Cell Dev Biol. 1997;8(3):311‐322. doi:10.1006/scdb.1997.0153
Rauschert S, Uhl O, Koletzko B, et al. Lipidomics reveals associations of phospholipids with obesity and insulin resistance in Young adults. J Clin Endocrinol Metab. 2016;101(3):871‐879. doi:10.1210/jc.2015‐3525
Candi E, Tesauro M, Cardillo C, et al. Metabolic profiling of visceral adipose tissue from obese subjects with or without metabolic syndrome. Biochem J. 2018;475(5):1019‐1035. doi:10.1042/BCJ20170604
Petkevicius K, Virtue S, Bidault G, et al. Accelerated phosphatidylcholine turnover in macrophages promotes adipose tissue inflammation in obesity. Elife. 2019;8:e47990. doi:10.7554/eLife.47990
Papandreou C, Garcia‐Gavilan J, Camacho‐Barcia L, et al. Circulating metabolites associated with body fat and lean mass in adults with overweight/obesity. Metabolites. 2021;11(5):317. doi:10.3390/metabo11050317
Watanabe K, Wilmanski T, Diener C, et al. Multiomic signatures of body mass index identify heterogeneous health phenotypes and responses to a lifestyle intervention. Nat Med. 2023;29(4):996‐1008. doi:10.1038/s41591‐023‐02248‐0
Yu ZR, Ning Y, Yu H, Tang NJ. A HPLC‐Q‐TOF‐MS‐based urinary metabolomic approach to identification of potential biomarkers of metabolic syndrome. J Huazhong Univ Sci Technolog Med Sci. 2014;34(2):276‐283. doi:10.1007/s11596‐014‐1271‐7
Law KP, Han TL, Mao X, Zhang H. Tryptophan and purine metabolites are consistently upregulated in the urinary metabolome of patients diagnosed with gestational diabetes mellitus throughout pregnancy: a longitudinal metabolomics study of Chinese pregnant women part 2. Clin Chim Acta. 2017;468:126‐139. doi:10.1016/j.cca.2017.02.018
Zheng R, Michaelsson K, Fall T, Elmstahl S, Lind L. The metabolomic profiling of total fat and fat distribution in a multi‐cohort study of women and men. Sci Rep. 2023;13(1):11129. doi:10.1038/s41598‐023‐38318‐z
Lee S, Zhang C, Kilicarslan M, et al. Integrated network analysis reveals an association between plasma mannose levels and insulin resistance. Cell Metab. 2016;24(1):172‐184. doi:10.1016/j.cmet.2016.05.026
Francis EC, Kechris K, Cohen CC, Michelotti G, Dabelea D, Perng W. Metabolomic profiles in childhood and adolescence are associated with fetal overnutrition. Metabolites. 2022;12(3):265. doi:10.3390/metabo12030265
Sharma V, Smolin J, Nayak J, et al. Mannose alters gut microbiome, prevents diet‐induced obesity, and improves host metabolism. Cell Rep. 2018;24(12):3087‐3098. doi:10.1016/j.celrep.2018.08.064
Neeland IJ, Poirier P, Despres JP. Cardiovascular and metabolic heterogeneity of obesity: clinical challenges and implications for management. Circulation. 2018;137(13):1391‐1406. doi:10.1161/CIRCULATIONAHA.117.029617
Visscher TL, Seidell JC, Molarius A, van der Kuip D, Hofman A, Witteman JC. A comparison of body mass index, waist‐hip ratio and waist circumference as predictors of all‐cause mortality among the elderly: the Rotterdam study. Int J Obes Relat Metab Disord. 2001;25(11):1730‐1735. doi:10.1038/sj.ijo.0801787

Auteurs

Zhila Semnani-Azad (Z)

Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA.

Mohammad L Rahman (ML)

Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA.

Melina Arguin (M)

Centre de Recherche du Centre Hospitalier Universitaire de Sherbrooke (CHUS), Sherbrooke, Quebec, Canada.

Myriam Doyon (M)

Centre de Recherche du Centre Hospitalier Universitaire de Sherbrooke (CHUS), Sherbrooke, Quebec, Canada.

Patrice Perron (P)

Centre de Recherche du Centre Hospitalier Universitaire de Sherbrooke (CHUS), Sherbrooke, Quebec, Canada.
Faculty of Medicine and Life Sciences, Department of Medicine, Université de Sherbrooke, Sherbrooke, Quebec, Canada.

Luigi Bouchard (L)

Centre de Recherche du Centre Hospitalier Universitaire de Sherbrooke (CHUS), Sherbrooke, Quebec, Canada.
Faculty of Medicine and Life Sciences, Department of Biochemistry and Functional Genomics, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
Department of Medical Biology, CIUSSS du Saguenay-Lac-Saint- Jean, Saguenay, Quebec, Canada.

Marie-France Hivert (MF)

Centre de Recherche du Centre Hospitalier Universitaire de Sherbrooke (CHUS), Sherbrooke, Quebec, Canada.
Diabetes Unit, Massachusetts General Hospital, Boston, Massachusetts, USA.
Department of Population Medicine, Harvard Medical School, Harvard Pilgrim Health Care Institute, Boston, Massachusetts, USA.

Classifications MeSH