NMR-based metabolic profiling of children with premature adrenarche.


Journal

Metabolomics : Official journal of the Metabolomic Society
ISSN: 1573-3890
Titre abrégé: Metabolomics
Pays: United States
ID NLM: 101274889

Informations de publication

Date de publication:
14 10 2022
Historique:
received: 03 05 2022
accepted: 30 09 2022
entrez: 14 10 2022
pubmed: 15 10 2022
medline: 19 10 2022
Statut: epublish

Résumé

Premature adrenarche (PA) for long time was considered a benign condition but later has been connected to various diseases in childhood and adulthood which remains controversial. To investigate the effect of premature adrenarche on the metabolic phenotype, and correlate the clinical and biochemical data with the metabolic profile of children with PA. Nuclear magnetic resonance (NMR)-based untargeted and targeted metabolomic approach in combination with multivariate and univariate statistical analysis applied to study the metabolic profiles of children with PA. Plasma, serum, and urine samples were collected from fifty-two children with Idiopathic PA and forty-eight age-matched controls from the division of Pediatric Endocrinology of the University Hospital of Patras were enrolled. Metabolomic results showed that plasma and serum glucose, myo-inositol, amino acids, a population of unsaturated lipids, and esterified cholesterol were higher and significantly different in PA children. In the metabolic profiles of children with PA and age-matched control group a gradual increase of glucose and myo-inositol levels was observed in serum and plasma, which was positively correlated their body mass index standard deviation score (BMI SDS) values respectively. Urine This study provides evidence that PA driven metabolic changes begin during the childhood and PA may has an inductive role in a BMI-driven increase of specific metabolites. Finally, urine may be considered as the best biofluid for identification of the PA metabolism as it reflects more clearly the PA metabolic fingerprint.

Identifiants

pubmed: 36239863
doi: 10.1007/s11306-022-01941-4
pii: 10.1007/s11306-022-01941-4
pmc: PMC9568450
doi:

Substances chimiques

Amino Acids 0
Lipids 0
Inositol 4L6452S749
Cholesterol 97C5T2UQ7J
Glucose IY9XDZ35W2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

78

Informations de copyright

© 2022. The Author(s).

Références

Benjamini, Y., & Hochberg, Y. (2000). On the adaptive control of the false discovery rate in multiple testing with independent statistics. Journal of Educational and Behavioral Statistics, 25, 60–83. https://doi.org/10.3102/10769986025001060
doi: 10.3102/10769986025001060
Bernini, P., Bertini, I., Luchinat, C., Nincheri, P., Staderini, S., & Turano, P. (2011). Standard operating procedures for pre-analytical handling of blood and urine for metabolomic studies and biobanks. Journal of Biomolecular NMR, 49, 231–243. https://doi.org/10.1007/s10858-011-9489-1
doi: 10.1007/s10858-011-9489-1 pubmed: 21380509
Bletsa, E., Filippas-Dekouan, S., Kostara, C., Dafopoulos, P., Dimou, A., Pappa, E., Chasapi, S., Spyroulias, G., Koutsovasilis, A., Bairaktari, E., Ferrannini, E., & Tsimihodimos, V. (2021). Effect of dapagliflozin on urine metabolome in patients with type 2 diabetes. The Journal of Clinical Endocrinology & Metabolism, 106, 1269–1283. https://doi.org/10.1210/clinem/dgab086
doi: 10.1210/clinem/dgab086
Boonstra, V. H., Mulder, P. G., De Jong, F. H., & Hokken-Koelega, A. C. (2004). Serum dehydroepiandrosterone sulfate levels and pubarche in short children born small for gestational age before and during growth hormone treatment. The Journal of Clinical Endocrinology & Metabolism, 89, 712–717. https://doi.org/10.1210/jc.2003-031160
doi: 10.1210/jc.2003-031160
Chasapi, S. A., Karagkouni, E., Matzarapi, K., Marousis, K. D., Varvarigou, A., & Spyroulias, G. A. (2019). NMR and Metabolomics. eLS (pp. 1–9). John Wiley & Sons Ltd.
Cho, K., Moon, J., Kang, J. H., Jang, H., Lee, H. J., Park, S., Yu, K. S., & Cho, J. Y. (2017). Combined untargeted and targeted metabolomic profiling reveals urinary biomarkers for discriminating obese from normal-weight adolescents. Pediatric Obesity, 12, 93–101. https://doi.org/10.1111/ijpo.12114
doi: 10.1111/ijpo.12114 pubmed: 26910390
Corvalan, C., Uauy, R., & Mericq, V. (2013). Obesity is positively associated with dehydroepiandrosterone sulfate concentrations at 7 y in Chilean children of normal birth weight. The American Journal of Clinical Nutrition, 97, 318–325. https://doi.org/10.3945/ajcn.112.037325
doi: 10.3945/ajcn.112.037325 pubmed: 23283497 pmcid: 3545681
Cree-Green, M., Carreau, A.-M., Rahat, H., Garcia-Reyes, Y., Bergman, B. C., Pyle, L., & Nadeau, K. J. (2019). Amino acid and fatty acid metabolomic profile during fasting and hyperinsulinemia in girls with polycystic ovarian syndrome. American Journal of Physiology-Endocrinology and Metabolism, 316, 707–718. https://doi.org/10.1152/ajpendo.00532.2018
doi: 10.1152/ajpendo.00532.2018
Croze, M. L., Géloën, A., & Soulage, C. O. (2015). Abnormalities in myo-inositol metabolism associated with type 2 diabetes in mice fed a high-fat diet: Benefits of a dietary myo-inositol supplementation. British Journal of Nutrition, 113, 1862–1875. https://doi.org/10.1017/S000711451500121X
doi: 10.1017/S000711451500121X pubmed: 25990651
D’Adamo, E., Santoro, N., & Caprio, S. (2009). Metabolic syndrome in pediatrics: Old concepts revised, new concepts discussed. Endocrinology and Metabolism Clinics, 38, 549–563. https://doi.org/10.1016/j.ecl.2009.06.002
doi: 10.1016/j.ecl.2009.06.002 pubmed: 19717004
Dahlberg, P. S., Mosdøl, A., Ding, Y., Bleka, Ø., Rolseth, V., Straumann, G. H., Skjerven-Martinsen, M., Delaveris, G. J. M., & Vist, G. E. (2019). A systematic review of the agreement between chronological age and skeletal age based on the Greulich and Pyle atlas. European Radiology, 29, 2936–2948. https://doi.org/10.1007/s00330-018-5718-2
doi: 10.1007/s00330-018-5718-2 pubmed: 30377790
Emmanuel, M., & Bokor, B. (2017). Tanner stages. Treasure Island: StatPearls Publishing.
Gawlik, A., Shmoish, M., Hartmann, M. F., Malecka-Tendera, E., Wudy, S. A., & Hochberg, Z. E. (2016). Steroid metabolomic disease signature of nonsyndromic childhood obesity. The Journal of Clinical Endocrinology & Metabolism, 101, 4329–4337. https://doi.org/10.1210/jc.2016-1754
doi: 10.1210/jc.2016-1754
Georgakopoulou, I., Chasapi, S. A., Bariamis, S. E., Varvarigou, A., Spraul, M., & Spyroulias, G. A. (2020). Metabolic changes in early neonatal life: NMR analysis of the neonatal metabolic profile to monitor postnatal metabolic adaptations. Metabolomics, 16, 1–12. https://doi.org/10.1007/s11306-020-01680-4
doi: 10.1007/s11306-020-01680-4
Georgiopoulou, P. D., Chasapi, S. A., Christopoulou, I., Varvarigou, A., & Spyroulias, G. A. (2022). Untargeted 1H-NMR urine metabolomic analysis of preterm infants with neonatal sepsis. Applied Sciences, 12, 1932. https://doi.org/10.3390/app12041932
doi: 10.3390/app12041932
Gibbs, N. K., Tye, J., & Norval, M. (2008). Recent advances in urocanic acid photochemistry, photobiology and photoimmunology. Photochemical & Photobiological Sciences, 7, 655–667. https://doi.org/10.1039/B717398A
doi: 10.1039/B717398A
Haug, K., Salek, R. M., Conesa, P., Hastings, J., De Matos, P., Rijnbeek, M., Mahendraker, T., Williams, M., Neumann, S., Rocca-Serra, P., Maguire, E., González-Beltrán, A., Sansone, S. A., Griffin, J. L., & Steinbeck, C. (2013). MetaboLights—an open-access general-purpose repository for metabolomics studies and associated meta-data. Nucleic Acids Research, 41, 781–786. https://doi.org/10.1093/nar/gks1004
doi: 10.1093/nar/gks1004
Holeček, M. (2020). Histidine in health and disease: Metabolism, physiological importance, and use as a supplement. Nutrients, 12, 848. https://doi.org/10.3390/nu12030848
doi: 10.3390/nu12030848 pmcid: 7146355
Holmes, E., Wilson, I. D., & Nicholson, J. K. (2008). Metabolic phenotyping in health and disease. Cell, 134, 714–717. https://doi.org/10.1016/j.cell.2008.08.026
doi: 10.1016/j.cell.2008.08.026 pubmed: 18775301
Huang, L., Fonteles, M., Houston, D., Zhang, C., & Larner, J. (1993). Chiroinositol deficiency and insulin resistance. III. Acute glycogenic and hypoglycemic effects of two inositol phosphoglycan insulin mediators in normal and streptozotocin-diabetic rats in vivo. Endocrinology, 132, 652–657. https://doi.org/10.1210/endo.132.2.8425485
doi: 10.1210/endo.132.2.8425485 pubmed: 8425485
Ibáñez, L., Aulesa, C., Potau, N., Ong, K., Dunger, D. B., & De Zegher, F. (2002). Plasminogen activator inhibitor-1 in girls with precocious pubarche: A premenarcheal marker for polycystic ovary syndrome? Pediatric Research, 51, 244–248. https://doi.org/10.1203/00006450-200202000-00019
doi: 10.1203/00006450-200202000-00019 pubmed: 11809921
Ibáñez, L., Potau, N., Francois, I., & de Zegher, F. (1998). Precocious pubarche, hyperinsulinism, and ovarian hyperandrogenism in girls: Relation to reduced fetal growth. The Journal of Clinical Endocrinology & Metabolism, 83, 3558–3562. https://doi.org/10.1210/jcem.83.10.5205
doi: 10.1210/jcem.83.10.5205
Ibáñez, L., Potau, N., Zampolli, M., RiquÉ, S., Saenger, P., & Carrascosa, A. (1997). Hyperinsulinemia and decreased insulin-like growth factor-binding protein-1 are common features in prepubertal and pubertal girls with a history of premature pubarche. The Journal of Clinical Endocrinology & Metabolism, 82, 2283–2288. https://doi.org/10.1210/jcem.82.7.4084
doi: 10.1210/jcem.82.7.4084
Katsila, T., Chasapi, S. A., Gomez Tamayo, J. C., Chalikiopoulou, C., Siapi, E., Moros, G., Zoumpoulakis, P., Spyroulias, G. A., & Kardamakis, D. (2021). Three-dimensional cell metabolomics deciphers the anti-angiogenic properties of the radioprotectant amifostine. Cancers, 13, 2877. https://doi.org/10.3390/cancers13122877
doi: 10.3390/cancers13122877 pubmed: 34207535 pmcid: 8230228
Krzywinski, M., & Altman, N. (2014). Visualizing samples with box plots. Nature Methods, 11, 119–120. https://doi.org/10.1038/nmeth.2813
doi: 10.1038/nmeth.2813 pubmed: 24645192
Kwon, J. H., Lee, H. A., Kim, Y. J., Lee, H., Park, E. A., Cho, S. J., Gwak, H. S., Ha, E., Park, H., & Kim, H. S. (2017). Effects of adrenal androgen levels on bone age advancement in prepubertal children: Using the Ewha birth and growth cohort study. Journal of Korean Medical Science, 32, 968–973. https://doi.org/10.3346/jkms.2017.32.6.968
doi: 10.3346/jkms.2017.32.6.968 pubmed: 28480655 pmcid: 5426240
Martos-Moreno, G. Á., Mastrangelo, A., Barrios, V., Garcia, A., Chowen, J., Rupérez, F., Barbas, C., & Argente, J. (2017). Metabolomics allows the discrimination of the pathophysiological relevance of hyperinsulinism in obese prepubertal children. International Journal of Obesity, 41, 1473–1480. https://doi.org/10.1038/ijo.2017.137
doi: 10.1038/ijo.2017.137 pubmed: 28588306
Matzarapi, K. Giannakopoulos, A. Chasapi, S., Kritikou, D., Efthymiadou, A., Chrysis, D., & Spyroulias, G. A. (2021). MTBLS2387 | NMR-based metabolic profiling of children with premature adrenarche (PA). Metabolights. Accessed May 25, 2021. https://www.ebi.ac.uk/metabolights/editor/study/MTBLS2387/descriptors
Mathew, R. P., Najjar, J. L., Lorenz, R. A., Mayes, D. E., & Russell, W. E. (2002). Premature pubarche in girls is associated with functional adrenal but not ovarian hyperandrogenism. The Journal of Pediatrics, 141, 91–98. https://doi.org/10.1067/mpd.2002.125492
doi: 10.1067/mpd.2002.125492 pubmed: 12091857
Neville, K., & Walker, J. (2005). Precocious pubarche is associated with SGA, prematurity, weight gain, and obesity. Archives of Disease in Childhood, 90, 258–261. https://doi.org/10.1136/adc.2004.053959
doi: 10.1136/adc.2004.053959 pubmed: 15723910 pmcid: 1720316
Niu, Y. C., Feng, R. N., Hou, Y., Li, K., Kang, Z., Wang, J., Sun, C. H., & Li, Y. (2012). Histidine and arginine are associated with inflammation and oxidative stress in obese women. British Journal of Nutrition, 108, 57–61. https://doi.org/10.1017/S0007114511005289
doi: 10.1017/S0007114511005289 pubmed: 21996294
Novello, L., & Speiser, P. W. (2018). Premature adrenarche. Pediatric Annals, 47, 7–11. https://doi.org/10.3928/19382359-20171214-04
doi: 10.3928/19382359-20171214-04
Ortmeyer, H. K., Huang, L. C., Zhang, L., Hansen, B. C., & Larner, J. (1993). Chiroinositol deficiency and insulin resistance. II. Acute effects of D-chiroinositol administration in streptozotocin-diabetic rats, normal rats given a glucose load, and spontaneously insulin-resistant rhesus monkeys. Endocrinology, 132, 646–651. https://doi.org/10.1210/endo.132.2.8425484
doi: 10.1210/endo.132.2.8425484 pubmed: 8425484
Pang, Z., Chong, J., Zhou, G., de Lima Morais, D. A., Chang, L., Barrette, M., Gauthier, C., Jacques, P. E., Li, S., & Xia, J. (2021). MetaboAnalyst 5.0: Narrowing the gap between raw spectra and functional insights. Nucleic Acids Research, 49, 388–396. https://doi.org/10.1093/nar/gkab382
doi: 10.1093/nar/gkab382
Pearce, J. T., Athersuch, T. J., Ebbels, T. M., Lindon, J. C., Nicholson, J. K., & Keun, H. C. (2008). Robust algorithms for automated chemical shift calibration of 1D
doi: 10.1021/ac8011494 pubmed: 18702533
Prieto, R. M. (2008). Response to Demonizing phytate. Nature Biotechnology, 26, 497. https://doi.org/10.1038/nbt0508-497
doi: 10.1038/nbt0508-497
Remer, T., Boye, K. R., Hartmann, M. F., & Wudy, S. A. (2005). Urinary markers of adrenarche: Reference values in healthy subjects, aged 3–18 years. The Journal of Clinical Endocrinology & Metabolism, 90, 2015–2021. https://doi.org/10.1210/jc.2004-1571
doi: 10.1210/jc.2004-1571
Ren, S., Hinzman, A. A., Kang, E. L., Szczesniak, R. D., & Lu, L. J. (2015). Computational and statistical analysis of metabolomics data. Metabolomics, 11, 1492–1513. https://doi.org/10.1007/s11306-015-0823-6
doi: 10.1007/s11306-015-0823-6
Saccenti, E., Hoefsloot, H. C., Smilde, A. K., Westerhuis, J. A., & Hendriks, M. M. (2014). Reflections on univariate and multivariate analysis of metabolomics data. Metabolomics, 10, 361–374. https://doi.org/10.1007/s11306-013-0598-6
doi: 10.1007/s11306-013-0598-6
Salek, R. M., Maguire, M. L., Bentley, E., Rubtsov, D. V., Hough, T., Cheeseman, M., Nunez, D., Sweatman, B. C., Haselden, J. N., Cox, R., Connor, S. C., & Griffin, J. L. (2007). A metabolomic comparison of urinary changes in type 2 diabetes in mouse, rat, and human. Physiological Genomics, 29, 99–108. https://doi.org/10.1152/physiolgenomics.00194.2006
doi: 10.1152/physiolgenomics.00194.2006 pubmed: 17190852
Storbeck, K. H., Schiffer, L., Baranowski, E. S., Chortis, V., Prete, A., Barnard, L., Gilligan, L. C., Taylor, A. E., Idkowiak, J., Arlt, W., & Shackleton, C. H. L. (2019). Steroid metabolome analysis in disorders of adrenal steroid biosynthesis and metabolism. Endocrine Reviews, 40, 1605–1625. https://doi.org/10.1210/er.2018-00262
doi: 10.1210/er.2018-00262 pubmed: 31294783 pmcid: 6858476
Suarez-Diez, M., Adam, J., Adamski, J., Chasapi, S. A., Luchinat, C., Peters, A., Prehn, C., Santucci, C., Spyridonidis, A., Spyroulias, G. A., Tenori, L., Wang-Sattler, R., & Saccenti, E. (2017). Plasma and serum metabolite association networks: Comparability within and between studies using NMR and MS profiling. Journal of Proteome Research, 16, 2547–2559. https://doi.org/10.1021/acs.jproteome.7b00106
doi: 10.1021/acs.jproteome.7b00106 pubmed: 28517934 pmcid: 5645760
Sun, X., Feng, R., Li, Y., Lin, S., Zhang, W., Li, Y., Sun, C., & Li, S. (2014). Histidine supplementation alleviates inflammation in the adipose tissue of high-fat diet-induced obese rats via the NF-κB-and PPARγ-involved pathways. British Journal of Nutrition, 112, 477–485. https://doi.org/10.1017/S0007114514001056
doi: 10.1017/S0007114514001056 pubmed: 24833547
Tsagkarakou, A. S., Chasapi, S. A., Koulas, S. M., Tsialtas, I., Kyriakis, E., Drakou, C. E., Kun, S., Somsák, L., Spyroulias, G. A., Psarra, A.-M.G., & Leonidas D. D. (2021). Structure activity relationship of the binding of p-coumaroyl glucose to glycogen phosphorylase and its effect on hepatic cell metabolic pathways. European Journal of Medicinal Chemistry Reports, 3, 100011. https://doi.org/10.1016/j.ejmcr.2021.100011
doi: 10.1016/j.ejmcr.2021.100011
Utriainen, P., Jääskeläinen, J., Gröhn, O., Kuusisto, J., Pulkki, K., & Voutilainen, R. (2010). Circulating TNF-alpha and IL-6 concentrations and TNF-alpha-308 G> A polymorphism in children with premature adrenarche. Frontiers in Endocrinology, 1, 6. https://doi.org/10.3389/fendo.2010.00006
doi: 10.3389/fendo.2010.00006 pubmed: 22654787 pmcid: 3356042
Utriainen, P., Jääskeläinen, J., Romppanen, J., & Voutilainen, R. (2007). Childhood metabolic syndrome and its components in premature adrenarche. The Journal of Clinical Endocrinology & Metabolism, 92, 4282–4285. https://doi.org/10.1210/jc.2006-2412
doi: 10.1210/jc.2006-2412
Voutilainen, R., & Jääskeläinen, J. (2015). Premature adrenarche: Etiology, clinical findings, and consequences. The Journal of Steroid Biochemistry and Molecular Biology, 145, 226–236. https://doi.org/10.1016/j.jsbmb.2014.06.004
doi: 10.1016/j.jsbmb.2014.06.004 pubmed: 24923732
Wishart, D. S., Tzur, D., Knox, C., Eisner, R., Guo, A. C., Young, N., Cheng, D., Jewell, K., Arndt, D., Sawhney, S., Fung, C., Nikolai, L., Lewis, M., Coutouli, A. M., Forsythe, I., Tang, P., Shrivastava, S., Jeroncic, K., Stothard, P., Amegbey, G., Block, D., Hau, D. D., Wagner, J., Miniaci, J., Clements, M., Gebremedhin, M., Guo, N., Zhang, Y., Duggan, G. E., MacInnis, G. D., Weljie, A. M., Dowlatabadi, R., Bamforth, F., Clive, D., Greiner, R., Li, L., Marrie, T., Sykes, B. D., Vogel, H. J., & Querengesser, L. (2007). HMDB: The human metabolome database. Nucleic Acids Research, 35, 521–526. https://doi.org/10.1093/nar/gkl923
doi: 10.1093/nar/gkl923
Zompra, A. A., Chasapi, S. A., Karagkouni, E. C., Karamouzi, E., Panopoulos, P., & Spyroulias, G. A. (2021). Metabolite and bioactive compounds profiling of Meteora sea buckthorn berries through high-resolution NMR analysis. Metabolites, 11, 822. https://doi.org/10.3390/metabo11120822
doi: 10.3390/metabo11120822 pubmed: 34940580 pmcid: 8705651

Auteurs

Konstantina Matzarapi (K)

Department of Pharmacy, School of Health Sciences, University of Patras, 26504, Rio, Greece.

Aristeidis Giannakopoulos (A)

Division of Endocrinology Department of Pediatrics, Medical School, University of Patras, 26504, Rio, Greece.

Styliani A Chasapi (SA)

Department of Pharmacy, School of Health Sciences, University of Patras, 26504, Rio, Greece.

Dimitra Kritikou (D)

Division of Endocrinology Department of Pediatrics, Medical School, University of Patras, 26504, Rio, Greece.

Alexandra Efthymiadou (A)

Division of Endocrinology Department of Pediatrics, Medical School, University of Patras, 26504, Rio, Greece.

Dionisios Chrysis (D)

Division of Endocrinology Department of Pediatrics, Medical School, University of Patras, 26504, Rio, Greece. dchrysis@upatras.gr.

Georgios A Spyroulias (GA)

Department of Pharmacy, School of Health Sciences, University of Patras, 26504, Rio, Greece. G.A.Spyroulias@upatras.gr.

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