Skip to main content
Top
Published in: Endocrine 3/2017

Open Access 01-12-2017 | Original Article

Specific plasma amino acid disturbances associated with metabolic syndrome

Authors: Marta Siomkajło, Jacek Rybka, Magdalena Mierzchała-Pasierb, Andrzej Gamian, Joanna Stankiewicz-Olczyk, Marek Bolanowski, Jacek Daroszewski

Published in: Endocrine | Issue 3/2017

Login to get access

Abstract

Purpose

The primary objective of the present study was to examine the association between branched chain and aromatic amino acid profiles (BCAA and AAA respectively) and the metabolic syndrome (MS), and to evaluate the clinical utility of these associations in the diagnostic process.

Methods

Two hundred and sixty three healthy men with MS [MS(+): n = 165] and without MS [MS(−): n = 98] were enrolled in the observational study. Anthropometrical, biochemical, and amino acid measurements were performed. The ability of the BCAA and AAA to discriminate subjects with MS and insulin resistance was tested. Based on logistic discrimination, a multivariate early MS diagnostic model was built, and its discrimination properties were evaluated.

Results

Two functionally independent amino acid clusters were identified. BCAA and phenylalanine differed significantly between MS(+) and MS(−) participants (P = 0.003). These factors were also found to be indicators of MS(+) individuals (AUC: 0.66; 95% CI: 0.5757–0.7469), and correlated with cardiometabolic factors. No statistically significant differences in amino acid concentrations between those with and without insulin resistance were noted, and none of the amino groups were indicators of insulin resistance. The proposed MS multivariate diagnostic model consisted of phenylalanine, insulin, leptin, and adiponectin, and had good discrimination properties [AUC 0.79; 95% CI: 0.7239–0.8646].

Conclusions

MS is associated with selective BCAA and AAA profile disturbances, which could be part of cardiometabolic disease pathogenesis and derive neither directly from insulin sensitivity impairment, nor obesity or muscle mass. The MS diagnostic model developed and described herein should be validated in future studies.
Literature
1.
go back to reference E. Pujos-Guillot, M. Brandolini, M. Pétéra, D. Grissa, C. Joly, B. Lyan, É. Herquelot, S. Czernichow, M. Zins, M. Goldberg, B. Comte, Systems metabolomics for prediction of metabolic syndrome. J. Proteome Res. 16, 2262–2272 (2017)CrossRefPubMed E. Pujos-Guillot, M. Brandolini, M. Pétéra, D. Grissa, C. Joly, B. Lyan, É. Herquelot, S. Czernichow, M. Zins, M. Goldberg, B. Comte, Systems metabolomics for prediction of metabolic syndrome. J. Proteome Res. 16, 2262–2272 (2017)CrossRefPubMed
2.
go back to reference S. O’Neill, M. Bohl, S. Gregersen, K. Hermansen, L. O’Driscoll, Blood-based biomarkers for metabolic syndrome. Trends Endocrinol. Metab. 27, 363–374 (2016)CrossRefPubMed S. O’Neill, M. Bohl, S. Gregersen, K. Hermansen, L. O’Driscoll, Blood-based biomarkers for metabolic syndrome. Trends Endocrinol. Metab. 27, 363–374 (2016)CrossRefPubMed
3.
go back to reference O.A.H. Jones (ed), Metabolomics and Systems Biology in Human Health and Medicine. CABI (2014) Roberts, L.D.: Type 2 DIabetes Mellitus and the Metabolic Syndrome, Metabolomics and Systems Biology in Human Health and Medicine (CABI: USA, 2014), pp. 141–153 O.A.H. Jones (ed), Metabolomics and Systems Biology in Human Health and Medicine. CABI (2014) Roberts, L.D.: Type 2 DIabetes Mellitus and the Metabolic Syndrome, Metabolomics and Systems Biology in Human Health and Medicine (CABI: USA, 2014), pp. 141–153
4.
go back to reference B.C. Batch, K. Hyland, L.P. Svetkey, Branch chain amino acids: biomarkers of health and disease. Curr. Opin. Clin. Nutr. Metab. Care 17, 86–89 (2014)PubMed B.C. Batch, K. Hyland, L.P. Svetkey, Branch chain amino acids: biomarkers of health and disease. Curr. Opin. Clin. Nutr. Metab. Care 17, 86–89 (2014)PubMed
5.
go back to reference B.C. Batch, S.H. Shah, C.B. Newgard, C.B. Turer, C. Haynes, J.R. Bain, M. Muehlbauer, M.J. Patel, R.D. Stevens, L.J. Appel, L.K. Newby, L.P. Svetkey, Branched chain amino acids are novel biomarkers for discrimination of metabolic wellness. Metabolism 62, 961–969 (2013)CrossRefPubMedPubMedCentral B.C. Batch, S.H. Shah, C.B. Newgard, C.B. Turer, C. Haynes, J.R. Bain, M. Muehlbauer, M.J. Patel, R.D. Stevens, L.J. Appel, L.K. Newby, L.P. Svetkey, Branched chain amino acids are novel biomarkers for discrimination of metabolic wellness. Metabolism 62, 961–969 (2013)CrossRefPubMedPubMedCentral
6.
go back to reference L. Weng, E. Quinlivan, Y. Gong, A.L. Beitelshees, M.H. Shahin, S.T. Turner, A.B. Chapman, J.G. Gums, J.A. Johnson, R.F. Frye, T.J. Garrett, R.M. Cooper-DeHoff, Association of branched and aromatic amino acids levels with metabolic syndrome and impaired fasting glucose in hypertensive patients. Metab. Syndr. Relat. Disord. 13, 195–202 (2015)CrossRefPubMedPubMedCentral L. Weng, E. Quinlivan, Y. Gong, A.L. Beitelshees, M.H. Shahin, S.T. Turner, A.B. Chapman, J.G. Gums, J.A. Johnson, R.F. Frye, T.J. Garrett, R.M. Cooper-DeHoff, Association of branched and aromatic amino acids levels with metabolic syndrome and impaired fasting glucose in hypertensive patients. Metab. Syndr. Relat. Disord. 13, 195–202 (2015)CrossRefPubMedPubMedCentral
7.
go back to reference K. Nagao, M. Yamakado, The role of amino acid profiles in diabetes risk assessment. [Review]. Curr. Opin. Clin. Nutr. Metab. Care 19, 328–335 (2016)CrossRef K. Nagao, M. Yamakado, The role of amino acid profiles in diabetes risk assessment. [Review]. Curr. Opin. Clin. Nutr. Metab. Care 19, 328–335 (2016)CrossRef
8.
go back to reference C.B. Newgard, J. An, J.R. Bain, M.J. Muehlbauer, R.D. Stevens, L.F. Lien, A.M. Haqq, S.H. Shah, M. Arlotto, C.A. Slentz, J. Rochon, D. Gallup, O. Ilkayeva, B.R. Wenner, W.S. Yancy, H. Eisenson, G. Musante, R.S. Surwit, D.S. Millington, M.D. Butler, L.P. Svetkey, A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 9, 311–326 (2009)CrossRefPubMedPubMedCentral C.B. Newgard, J. An, J.R. Bain, M.J. Muehlbauer, R.D. Stevens, L.F. Lien, A.M. Haqq, S.H. Shah, M. Arlotto, C.A. Slentz, J. Rochon, D. Gallup, O. Ilkayeva, B.R. Wenner, W.S. Yancy, H. Eisenson, G. Musante, R.S. Surwit, D.S. Millington, M.D. Butler, L.P. Svetkey, A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 9, 311–326 (2009)CrossRefPubMedPubMedCentral
10.
go back to reference M.M. Adeva, J. Calviño, G. Souto, C. Donapetry, Insulin resistance and the metabolism of branched-chain amino acids in humans. Amino Acids 43, 171–181 (2011)CrossRefPubMed M.M. Adeva, J. Calviño, G. Souto, C. Donapetry, Insulin resistance and the metabolism of branched-chain amino acids in humans. Amino Acids 43, 171–181 (2011)CrossRefPubMed
11.
go back to reference M. Magnusson, G.D. Lewis, U. Ericson, M. Orho-Melander, B. Hedblad, G. Engström, G. Ostling, C. Clish, T.J. Wang, R.E. Gerszten, O. Melander, A diabetes-predictive amino acid score and future cardiovascular disease. Eur. Heart J. 34, 1982–1989 (2013)CrossRefPubMed M. Magnusson, G.D. Lewis, U. Ericson, M. Orho-Melander, B. Hedblad, G. Engström, G. Ostling, C. Clish, T.J. Wang, R.E. Gerszten, O. Melander, A diabetes-predictive amino acid score and future cardiovascular disease. Eur. Heart J. 34, 1982–1989 (2013)CrossRefPubMed
12.
go back to reference T.J. Wang, M.G. Larson, R.S. Vasan, S. Cheng, E.P. Rhee, E. McCabe, G.D. Lewis, C.S. Fox, P.F. Jacques, C. Fernandez, C.J. O’Donnell, S.A. Carr, V.K. Mootha, J.C. Florez, A. Souza, O. Melander, C.B. Clish, R.E. Gerszten, Metabolite profiles and the risk of developing diabetes. Nat. Med. 17, 448–453 (2011)CrossRefPubMedPubMedCentral T.J. Wang, M.G. Larson, R.S. Vasan, S. Cheng, E.P. Rhee, E. McCabe, G.D. Lewis, C.S. Fox, P.F. Jacques, C. Fernandez, C.J. O’Donnell, S.A. Carr, V.K. Mootha, J.C. Florez, A. Souza, O. Melander, C.B. Clish, R.E. Gerszten, Metabolite profiles and the risk of developing diabetes. Nat. Med. 17, 448–453 (2011)CrossRefPubMedPubMedCentral
13.
go back to reference M. Yamakado, K. Nagao, A. Imaizumi, M. Tani, A. Toda, T. Tanaka, H. Jinzu, H. Miyano, H. Yamamoto, T. Daimon, K. Horimoto, Y. Ishizaka, Plasma free amino acid profiles predict four-year risk of developing diabetes, metabolic syndrome, dyslipidemia, and hypertension in Japanese population. Sci. Rep. 5, 11918 (2015)CrossRefPubMedPubMedCentral M. Yamakado, K. Nagao, A. Imaizumi, M. Tani, A. Toda, T. Tanaka, H. Jinzu, H. Miyano, H. Yamamoto, T. Daimon, K. Horimoto, Y. Ishizaka, Plasma free amino acid profiles predict four-year risk of developing diabetes, metabolic syndrome, dyslipidemia, and hypertension in Japanese population. Sci. Rep. 5, 11918 (2015)CrossRefPubMedPubMedCentral
14.
go back to reference S.E. McCormack, O. Shaham, M.A. McCarthy, A.A. Deik, T.J. Wang, R.E. Gerszten, C.B. Clish, V.K. Mootha, S.K. Grinspoon, A. Fleischman, Circulating branched-chain amino acid concentrations are associated with obesity and future insulin resistance in children and adolescents. Pediatr. Obes. 8, 52–61 (2013)CrossRefPubMed S.E. McCormack, O. Shaham, M.A. McCarthy, A.A. Deik, T.J. Wang, R.E. Gerszten, C.B. Clish, V.K. Mootha, S.K. Grinspoon, A. Fleischman, Circulating branched-chain amino acid concentrations are associated with obesity and future insulin resistance in children and adolescents. Pediatr. Obes. 8, 52–61 (2013)CrossRefPubMed
15.
go back to reference P.K. Wiklund, S. Pekkala, R. Autio, E. Munukka, L. Xu, J. Saltevo, S. Cheng, U.M. Kujala, M. Alen, S. Cheng, Serum metabolic profiles in overweight and obese women with and without metabolic syndrome. Diabetol. Metab. Syndr. 6, 40 (2014)CrossRefPubMedPubMedCentral P.K. Wiklund, S. Pekkala, R. Autio, E. Munukka, L. Xu, J. Saltevo, S. Cheng, U.M. Kujala, M. Alen, S. Cheng, Serum metabolic profiles in overweight and obese women with and without metabolic syndrome. Diabetol. Metab. Syndr. 6, 40 (2014)CrossRefPubMedPubMedCentral
16.
17.
go back to reference H.S. Hundal, P.M. Taylor, Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am. J. Physiol. - Endocrinol. Metab. 296, E603–E613 (2009)CrossRefPubMedPubMedCentral H.S. Hundal, P.M. Taylor, Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am. J. Physiol. - Endocrinol. Metab. 296, E603–E613 (2009)CrossRefPubMedPubMedCentral
18.
go back to reference F. Yoshizawa, New therapeutic strategy for amino acid medicine: notable functions of branched chain amino acids as biological regulators. J. Pharmacol. Sci. 118, 149–155 (2012)CrossRefPubMed F. Yoshizawa, New therapeutic strategy for amino acid medicine: notable functions of branched chain amino acids as biological regulators. J. Pharmacol. Sci. 118, 149–155 (2012)CrossRefPubMed
19.
go back to reference J. Lu, G. Xie, W. Jia, W. Jia, Insulin resistance and the metabolism of branched-chain amino acids. Front. Med. 7, 53–59 (2013)CrossRefPubMed J. Lu, G. Xie, W. Jia, W. Jia, Insulin resistance and the metabolism of branched-chain amino acids. Front. Med. 7, 53–59 (2013)CrossRefPubMed
20.
go back to reference C.X. Wang, F.F. Guo, Branched chain amino acids and metabolic regulation. Chin. Sci. Bull. 58, 1228–1235 (2013) C.X. Wang, F.F. Guo, Branched chain amino acids and metabolic regulation. Chin. Sci. Bull. 58, 1228–1235 (2013)
21.
go back to reference J.D. Fernstrom, Large neutral amino acids: dietary effects on brain neurochemistry and function. Amino Acids 45, 419–430 (2013)CrossRefPubMed J.D. Fernstrom, Large neutral amino acids: dietary effects on brain neurochemistry and function. Amino Acids 45, 419–430 (2013)CrossRefPubMed
22.
go back to reference S. Choi, B. DiSilvio, M.H. Fernstrom, J.D. Fernstrom, Meal ingestion, amino acids and brain neurotransmitters: Effects of dietary protein source on serotonin and catecholamine synthesis rates. Physiol. Behav. 98, 156–162 (2009)CrossRefPubMed S. Choi, B. DiSilvio, M.H. Fernstrom, J.D. Fernstrom, Meal ingestion, amino acids and brain neurotransmitters: Effects of dietary protein source on serotonin and catecholamine synthesis rates. Physiol. Behav. 98, 156–162 (2009)CrossRefPubMed
23.
go back to reference A. Coppola, B.R. Wenner, O. Ilkayeva, R.D. Stevens, M. Maggioni, T.A. Slotkin, E.D. Levin, C.B. Newgard, Branched-chain amino acids alter neurobehavioral function in rats. Am. J. Physiol. Endocrinol. Metab. 304, E405–E413 (2013)CrossRefPubMed A. Coppola, B.R. Wenner, O. Ilkayeva, R.D. Stevens, M. Maggioni, T.A. Slotkin, E.D. Levin, C.B. Newgard, Branched-chain amino acids alter neurobehavioral function in rats. Am. J. Physiol. Endocrinol. Metab. 304, E405–E413 (2013)CrossRefPubMed
24.
go back to reference K.G.M.M. Alberti, R.H. Eckel, S.M. Grundy, P.Z. Zimmet, J.I. Cleeman, K.A. Donato, J.-C. Fruchart, W.P.T. James, C.M. Loria, S.C. Smith, Harmonizing the metabolic syndrome a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation 120, 1640–1645 (2009)CrossRefPubMed K.G.M.M. Alberti, R.H. Eckel, S.M. Grundy, P.Z. Zimmet, J.I. Cleeman, K.A. Donato, J.-C. Fruchart, W.P.T. James, C.M. Loria, S.C. Smith, Harmonizing the metabolic syndrome a joint interim statement of the international diabetes federation task force on epidemiology and prevention; national heart, lung, and blood institute; American heart association; world heart federation; international atherosclerosis society; and international association for the study of obesity. Circulation 120, 1640–1645 (2009)CrossRefPubMed
25.
go back to reference M. Szurkowska, K. Szafraniec, A. Gilis-Januszewska, Z. Szybiński, B. Huszno, [Insulin resistance indices in population-based study and their predictive value in defining metabolic syndrome]. Przegląd Epidemiol. 59, 743–751 (2005) [Article in Polish] M. Szurkowska, K. Szafraniec, A. Gilis-Januszewska, Z. Szybiński, B. Huszno, [Insulin resistance indices in population-based study and their predictive value in defining metabolic syndrome]. Przegląd Epidemiol. 59, 743–751 (2005) [Article in Polish]
27.
go back to reference R. Seibert, F. Abbasi, F.M. Hantash, M.P. Caulfield, G. Reaven, S.H. Kim, Relationship between insulin resistance and amino acids in women and men. Physiol. Rep. 3, e12392 (2015)CrossRefPubMedPubMedCentral R. Seibert, F. Abbasi, F.M. Hantash, M.P. Caulfield, G. Reaven, S.H. Kim, Relationship between insulin resistance and amino acids in women and men. Physiol. Rep. 3, e12392 (2015)CrossRefPubMedPubMedCentral
28.
go back to reference L.A. Cynober, Plasma amino acid levels with a note on membrane transport: characteristics, regulation, and metabolic significance. Nutrition 18, 761–766 (2002)CrossRefPubMed L.A. Cynober, Plasma amino acid levels with a note on membrane transport: characteristics, regulation, and metabolic significance. Nutrition 18, 761–766 (2002)CrossRefPubMed
29.
go back to reference S.H. Adams, Emerging perspectives on essential amino acid metabolism in obesity and the insulin-resistant state. Adv. Nutr. Adv. Nutr. Bethesda Md. 2, 445–456 (2011)CrossRef S.H. Adams, Emerging perspectives on essential amino acid metabolism in obesity and the insulin-resistant state. Adv. Nutr. Adv. Nutr. Bethesda Md. 2, 445–456 (2011)CrossRef
30.
go back to reference M.S. Brown, J.L. Goldstein, Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 7, 95–96 (2008)CrossRefPubMed M.S. Brown, J.L. Goldstein, Selective versus total insulin resistance: a pathogenic paradox. Cell Metab. 7, 95–96 (2008)CrossRefPubMed
31.
go back to reference J.R. Cook, F. Langlet, Y. Kido, D. Accili, Pathogenesis of selective insulin resistance in isolated hepatocytes. J. Biol. Chem. 290, 13972–13980 (2015)CrossRefPubMedPubMedCentral J.R. Cook, F. Langlet, Y. Kido, D. Accili, Pathogenesis of selective insulin resistance in isolated hepatocytes. J. Biol. Chem. 290, 13972–13980 (2015)CrossRefPubMedPubMedCentral
32.
go back to reference S.-X. Tan, K.H. Fisher-Wellman, D.J. Fazakerley, Y. Ng, H. Pant, J. Li, C.C. Meoli, A.C.F. Coster, J. Stöckli, D.E. James, Selective insulin resistance in adipocytes. J. Biol. Chem. 290, 11337–11348 (2015)CrossRefPubMedPubMedCentral S.-X. Tan, K.H. Fisher-Wellman, D.J. Fazakerley, Y. Ng, H. Pant, J. Li, C.C. Meoli, A.C.F. Coster, J. Stöckli, D.E. James, Selective insulin resistance in adipocytes. J. Biol. Chem. 290, 11337–11348 (2015)CrossRefPubMedPubMedCentral
33.
go back to reference P. Würtz, P. Soininen, A.J. Kangas, T. Rönnemaa, T. Lehtimäki, M. Kähönen, J.S. Viikari, O.T. Raitakari, M. Ala-Korpela, Branched-chain and aromatic amino acids are predictors of insulin resistance in young adults. Diabetes Care 36, 648–655 (2013)CrossRefPubMedPubMedCentral P. Würtz, P. Soininen, A.J. Kangas, T. Rönnemaa, T. Lehtimäki, M. Kähönen, J.S. Viikari, O.T. Raitakari, M. Ala-Korpela, Branched-chain and aromatic amino acids are predictors of insulin resistance in young adults. Diabetes Care 36, 648–655 (2013)CrossRefPubMedPubMedCentral
34.
go back to reference P. Giesbertz, H. Daniel, Branched-chain amino acids as biomarkers in diabetes. Curr. Opin. Clin. Nutr. Metab. Care 19, 48–54 (2016)CrossRefPubMed P. Giesbertz, H. Daniel, Branched-chain amino acids as biomarkers in diabetes. Curr. Opin. Clin. Nutr. Metab. Care 19, 48–54 (2016)CrossRefPubMed
35.
go back to reference A. Tom, K.S. Nair, Assessment of branched-chain amino acid status and potential for biomarkers. J. Nutr. 136, 324S–330S (2006)PubMed A. Tom, K.S. Nair, Assessment of branched-chain amino acid status and potential for biomarkers. J. Nutr. 136, 324S–330S (2006)PubMed
36.
go back to reference P. She, C. Van Horn, T. Reid, S.M. Hutson, R.N. Cooney, C.J. Lynch, Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am. J. Physiol. Endocrinol. Metab. 293, E1552–E1563 (2007)CrossRefPubMedPubMedCentral P. She, C. Van Horn, T. Reid, S.M. Hutson, R.N. Cooney, C.J. Lynch, Obesity-related elevations in plasma leucine are associated with alterations in enzymes involved in branched-chain amino acid metabolism. Am. J. Physiol. Endocrinol. Metab. 293, E1552–E1563 (2007)CrossRefPubMedPubMedCentral
37.
go back to reference B. Laferrère, K. Pietiläinen, Y. Boirie, in Weight Loss and Branched Chain Amino Acids and Their Metabolites, ed. by R. Rajendram, V.R. Preedy, V.B. Patel. Branched Chain Amino Acids in Clinical Nutrition: Volume 2 (Humana Press, Springer Science+Business Media, New York: USA, 2015), pp. 251–262 B. Laferrère, K. Pietiläinen, Y. Boirie, in Weight Loss and Branched Chain Amino Acids and Their Metabolites, ed. by R. Rajendram, V.R. Preedy, V.B. Patel. Branched Chain Amino Acids in Clinical Nutrition: Volume 2 (Humana Press, Springer Science+Business Media, New York: USA, 2015), pp. 251–262
38.
go back to reference D.E. Lackey, C.J. Lynch, K.C. Olson, R. Mostaedi, M. Ali, W.H. Smith, F. Karpe, S. Humphreys, D.H. Bedinger, T.N. Dunn, A.P. Thomas, P.J. Oort, D.A. Kieffer, R. Amin, A. Bettaieb, F.G. Haj, P. Permana, T.G. Anthony, S.H. Adams, Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am. J. Physiol. Endocrinol. Metab. 304, E1175–E1187 (2013)CrossRefPubMedPubMedCentral D.E. Lackey, C.J. Lynch, K.C. Olson, R. Mostaedi, M. Ali, W.H. Smith, F. Karpe, S. Humphreys, D.H. Bedinger, T.N. Dunn, A.P. Thomas, P.J. Oort, D.A. Kieffer, R. Amin, A. Bettaieb, F.G. Haj, P. Permana, T.G. Anthony, S.H. Adams, Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am. J. Physiol. Endocrinol. Metab. 304, E1175–E1187 (2013)CrossRefPubMedPubMedCentral
39.
go back to reference M. Yamakado, T. Tanaka, K. Nagao, Y. Ishizaka, T. Mitushima, M. Tani, A. Toda, E. Toda, M. Okada, H. Miyano, H. Yamamoto, Plasma amino acid profile is associated with visceral fat accumulation in obese Japanese subjects. Clin. Obes. 2, 29–40 (2012)CrossRefPubMed M. Yamakado, T. Tanaka, K. Nagao, Y. Ishizaka, T. Mitushima, M. Tani, A. Toda, E. Toda, M. Okada, H. Miyano, H. Yamamoto, Plasma amino acid profile is associated with visceral fat accumulation in obese Japanese subjects. Clin. Obes. 2, 29–40 (2012)CrossRefPubMed
40.
go back to reference M. Cansev, R.J. Wurtman, in 4 Aromatic Amino Acids in the Brain, ed. by A. Lajtha, S.S. Oja, A. Schousboe, P. Saransaari. Handbook of Neurochemistry & Molecular Neurobiology: Amino Acids and Peptides in the Nervous System (Springer US: USA, 2007), pp. 59–97 M. Cansev, R.J. Wurtman, in 4 Aromatic Amino Acids in the Brain, ed. by A. Lajtha, S.S. Oja, A. Schousboe, P. Saransaari. Handbook of Neurochemistry & Molecular Neurobiology: Amino Acids and Peptides in the Nervous System (Springer US: USA, 2007), pp. 59–97
41.
go back to reference T. Skurk, I. Rubio-Aliaga, A. Stamfort, H. Hauner, H. Daniel, New metabolic interdependencies revealed by plasma metabolite profiling after two dietary challenges. Metabolomics 7, 388–399 (2010)CrossRef T. Skurk, I. Rubio-Aliaga, A. Stamfort, H. Hauner, H. Daniel, New metabolic interdependencies revealed by plasma metabolite profiling after two dietary challenges. Metabolomics 7, 388–399 (2010)CrossRef
42.
go back to reference M.S. Koren, J.Q. Purnell, P.A. Breen, C.C. Matthys, H.S. Callahan, K.E. Meeuws, V.R. Burden, D.S. Weigle, Changes in plasma amino acid levels do not predict satiety and weight loss on diets with modified macronutrient composition. Ann. Nutr. Metab. 51, 182–187 (2007)CrossRefPubMed M.S. Koren, J.Q. Purnell, P.A. Breen, C.C. Matthys, H.S. Callahan, K.E. Meeuws, V.R. Burden, D.S. Weigle, Changes in plasma amino acid levels do not predict satiety and weight loss on diets with modified macronutrient composition. Ann. Nutr. Metab. 51, 182–187 (2007)CrossRefPubMed
43.
go back to reference J.D. Fernstrom, K.A. Langham, L.M. Marcelino, Z.L.E. Irvine, M.H. Fernstrom, W.H. Kaye, The ingestion of different dietary proteins by humans induces large changes in the plasma tryptophan ratio, a predictor of brain tryptophan uptake and serotonin synthesis. Clin. Nutr. 32, 1073–1076 (2013)CrossRefPubMed J.D. Fernstrom, K.A. Langham, L.M. Marcelino, Z.L.E. Irvine, M.H. Fernstrom, W.H. Kaye, The ingestion of different dietary proteins by humans induces large changes in the plasma tryptophan ratio, a predictor of brain tryptophan uptake and serotonin synthesis. Clin. Nutr. 32, 1073–1076 (2013)CrossRefPubMed
44.
go back to reference R.J. Wurtman, J.J. Wurtman, Brain serotonin, carbohydrate-craving, obesity and depression. Obes. Res 3(Suppl 4), 477S–480S (1995)CrossRefPubMed R.J. Wurtman, J.J. Wurtman, Brain serotonin, carbohydrate-craving, obesity and depression. Obes. Res 3(Suppl 4), 477S–480S (1995)CrossRefPubMed
45.
go back to reference C. Blouet, Y.-H. Jo, X. Li, G.J. Schwartz, Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus–brainstem circuit. J. Neurosci. 29, 8302–8311 (2009)CrossRefPubMedPubMedCentral C. Blouet, Y.-H. Jo, X. Li, G.J. Schwartz, Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus–brainstem circuit. J. Neurosci. 29, 8302–8311 (2009)CrossRefPubMedPubMedCentral
46.
go back to reference A.L. Carreiro, J. Dhillon, S. Gordon, A.G. Jacobs, K.A. Higgins, B.M. McArthur, B.W. Redan, R.L. Rivera, L.R. Schmidt, R.D. Mattes, The macronutrients, appetite and energy intake. Annu. Rev. Nutr. 36, 73–103 (2016)CrossRefPubMedPubMedCentral A.L. Carreiro, J. Dhillon, S. Gordon, A.G. Jacobs, K.A. Higgins, B.M. McArthur, B.W. Redan, R.L. Rivera, L.R. Schmidt, R.D. Mattes, The macronutrients, appetite and energy intake. Annu. Rev. Nutr. 36, 73–103 (2016)CrossRefPubMedPubMedCentral
48.
go back to reference E. Maury, S.M. Brichard, Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol. Cell. Endocrinol. 314, 1–16 (2010)CrossRefPubMed E. Maury, S.M. Brichard, Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome. Mol. Cell. Endocrinol. 314, 1–16 (2010)CrossRefPubMed
49.
go back to reference R.H. Eckel, S.M. Grundy, P.Z. Zimmet, The metabolic syndrome. The Lancet 365, 1415–1428 (2005)CrossRef R.H. Eckel, S.M. Grundy, P.Z. Zimmet, The metabolic syndrome. The Lancet 365, 1415–1428 (2005)CrossRef
50.
go back to reference S. Mirza, H.-Q. Qu, Li. Quan, P.J. Martinez, A.R. Rentfro, J.B. McCormick, S.P. Fisher-Hoch, Adiponectin/leptin, ratio and metabolic syndrome in a Mexican American population. Clin. Invest. Med. 34, E290–E297 (2011)CrossRefPubMedPubMedCentral S. Mirza, H.-Q. Qu, Li. Quan, P.J. Martinez, A.R. Rentfro, J.B. McCormick, S.P. Fisher-Hoch, Adiponectin/leptin, ratio and metabolic syndrome in a Mexican American population. Clin. Invest. Med. 34, E290–E297 (2011)CrossRefPubMedPubMedCentral
51.
go back to reference Q. Zhuo, Z. Wang, P. Fu, J. Piao, Y. Tian, J. Xu, X. Yang, Comparison of adiponectin, leptin and leptin to adiponectin ratio as diagnostic marker for metabolic syndrome in older adults of Chinese major cities. Diabetes Res. Clin. Pract. 84, 27–33 (2009)CrossRefPubMed Q. Zhuo, Z. Wang, P. Fu, J. Piao, Y. Tian, J. Xu, X. Yang, Comparison of adiponectin, leptin and leptin to adiponectin ratio as diagnostic marker for metabolic syndrome in older adults of Chinese major cities. Diabetes Res. Clin. Pract. 84, 27–33 (2009)CrossRefPubMed
52.
go back to reference R. Fujikawa, C. Ito, A. Tsuboi, Is the screening of metabolic syndrome using adiponectin possible? Diabetol. Int. 6, 313–320 (2015)CrossRef R. Fujikawa, C. Ito, A. Tsuboi, Is the screening of metabolic syndrome using adiponectin possible? Diabetol. Int. 6, 313–320 (2015)CrossRef
53.
go back to reference K. Hara, M. Horikoshi, T. Yamauchi, H. Yago, O. Miyazaki, H. Ebinuma, Y. Imai, R. Nagai, T. Kadowaki, Measurement of the high-molecular weight form of adiponectin in plasma is useful for the prediction of insulin resistance and metabolic syndrome. Diabetes Care 29, 1357–1362 (2006)CrossRefPubMed K. Hara, M. Horikoshi, T. Yamauchi, H. Yago, O. Miyazaki, H. Ebinuma, Y. Imai, R. Nagai, T. Kadowaki, Measurement of the high-molecular weight form of adiponectin in plasma is useful for the prediction of insulin resistance and metabolic syndrome. Diabetes Care 29, 1357–1362 (2006)CrossRefPubMed
54.
go back to reference P. Gayoso-Diz, A. Otero-González, M.X. Rodriguez-Alvarez, F. Gude, F. García, A.D. Francisco, A.G. Quintela, Insulin resistance (HOMA-IR) cut-off values and the metabolic syndrome in a general adult population: effect of gender and age: EPIRCE cross-sectional study. BMC Endocr. Disord. 13, 1–10 (2013)CrossRef P. Gayoso-Diz, A. Otero-González, M.X. Rodriguez-Alvarez, F. Gude, F. García, A.D. Francisco, A.G. Quintela, Insulin resistance (HOMA-IR) cut-off values and the metabolic syndrome in a general adult population: effect of gender and age: EPIRCE cross-sectional study. BMC Endocr. Disord. 13, 1–10 (2013)CrossRef
55.
go back to reference A. Esteghamati, H. Ashraf, O. Khalilzadeh, A. Zandieh, M. Nakhjavani, A. Rashidi, M. Haghazali, F. Asgari, Optimal cut-off of homeostasis model assessment of insulin resistance (HOMA-IR) for the diagnosis of metabolic syndrome: third national surveillance of risk factors of non-communicable diseases in Iran (SuRFNCD-2007). Nutr. Metab. 7, 26 (2010)CrossRef A. Esteghamati, H. Ashraf, O. Khalilzadeh, A. Zandieh, M. Nakhjavani, A. Rashidi, M. Haghazali, F. Asgari, Optimal cut-off of homeostasis model assessment of insulin resistance (HOMA-IR) for the diagnosis of metabolic syndrome: third national surveillance of risk factors of non-communicable diseases in Iran (SuRFNCD-2007). Nutr. Metab. 7, 26 (2010)CrossRef
56.
go back to reference M.J. Patel, B.C. Batch, L.P. Svetkey, J.R. Bain, C.B. Turer, C. Haynes, M.J. Muehlbauer, R.D. Stevens, C.B. Newgard, S.H. Shah, Race and sex differences in small-molecule metabolites and metabolic hormones in overweight and obese adults. OMICS J. Integr. Biol. 17, 627–635 (2013)CrossRef M.J. Patel, B.C. Batch, L.P. Svetkey, J.R. Bain, C.B. Turer, C. Haynes, M.J. Muehlbauer, R.D. Stevens, C.B. Newgard, S.H. Shah, Race and sex differences in small-molecule metabolites and metabolic hormones in overweight and obese adults. OMICS J. Integr. Biol. 17, 627–635 (2013)CrossRef
57.
go back to reference D. Newbern, P. Gumus Balikcioglu, M. Balikcioglu, J. Bain, M. Muehlbauer, R. Stevens, O. Ilkayeva, D. Dolinsky, S. Armstrong, K. Irizarry, M. Freemark, Sex differences in biomarkers associated with insulin resistance in obese adolescents: metabolomic profiling and principal components analysis. J. Clin. Endocrinol. Metab. 99, 4730–4739 (2014)CrossRefPubMedPubMedCentral D. Newbern, P. Gumus Balikcioglu, M. Balikcioglu, J. Bain, M. Muehlbauer, R. Stevens, O. Ilkayeva, D. Dolinsky, S. Armstrong, K. Irizarry, M. Freemark, Sex differences in biomarkers associated with insulin resistance in obese adolescents: metabolomic profiling and principal components analysis. J. Clin. Endocrinol. Metab. 99, 4730–4739 (2014)CrossRefPubMedPubMedCentral
58.
go back to reference A. Tchernof, J.-P. Després, Pathophysiology of human visceral obesity: an update. Physiol. Rev. 93, 359–404 (2013)CrossRefPubMed A. Tchernof, J.-P. Després, Pathophysiology of human visceral obesity: an update. Physiol. Rev. 93, 359–404 (2013)CrossRefPubMed
59.
go back to reference U.M. Kujala, V.-P. Mäkinen, I. Heinonen, P. Soininen, A.J. Kangas, T.H. Leskinen, P. Rahkila, P. Würtz, V. Kovanen, S. Cheng, S. Sipilä, M. Hirvensalo, R. Telama, T. Tammelin, M.J. Savolainen, A. Pouta, P.F. O’Reilly, P. Mäntyselkä, J. Viikari, M. Kähönen, T. Lehtimäki, P. Elliott, M.J. Vanhala, O.T. Raitakari, M.-R. Järvelin, J. Kaprio, H. Kainulainen, M. Ala-Korpela, Long-term leisure-time physical activity and serum metabolome. Circulation 127, 340–348 (2013)CrossRefPubMed U.M. Kujala, V.-P. Mäkinen, I. Heinonen, P. Soininen, A.J. Kangas, T.H. Leskinen, P. Rahkila, P. Würtz, V. Kovanen, S. Cheng, S. Sipilä, M. Hirvensalo, R. Telama, T. Tammelin, M.J. Savolainen, A. Pouta, P.F. O’Reilly, P. Mäntyselkä, J. Viikari, M. Kähönen, T. Lehtimäki, P. Elliott, M.J. Vanhala, O.T. Raitakari, M.-R. Järvelin, J. Kaprio, H. Kainulainen, M. Ala-Korpela, Long-term leisure-time physical activity and serum metabolome. Circulation 127, 340–348 (2013)CrossRefPubMed
60.
go back to reference R. Elango, R.O. Ball, P.B. Pencharz. Tolerability of Leucine in Humans. In: Branched Chain Amino Acids in Clinical Nutrition. (Springer Science+Business Media, New York, NY, (2015)CrossRef R. Elango, R.O. Ball, P.B. Pencharz. Tolerability of Leucine in Humans. In: Branched Chain Amino Acids in Clinical Nutrition. (Springer Science+Business Media, New York, NY, (2015)CrossRef
61.
go back to reference Y. Noguchi, Q.-W. Zhang, T. Sugimoto, Y. Furuhata, R. Sakai, M. Mori, M. Takahashi, T. Kimura, Network analysis of plasma and tissue amino acids and the generation of an amino index for potential diagnostic use. Am. J. Clin. Nutr. 83, 513S–519S (2006)PubMed Y. Noguchi, Q.-W. Zhang, T. Sugimoto, Y. Furuhata, R. Sakai, M. Mori, M. Takahashi, T. Kimura, Network analysis of plasma and tissue amino acids and the generation of an amino index for potential diagnostic use. Am. J. Clin. Nutr. 83, 513S–519S (2006)PubMed
Metadata
Title
Specific plasma amino acid disturbances associated with metabolic syndrome
Authors
Marta Siomkajło
Jacek Rybka
Magdalena Mierzchała-Pasierb
Andrzej Gamian
Joanna Stankiewicz-Olczyk
Marek Bolanowski
Jacek Daroszewski
Publication date
01-12-2017
Publisher
Springer US
Published in
Endocrine / Issue 3/2017
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-017-1460-9

Other articles of this Issue 3/2017

Endocrine 3/2017 Go to the issue

Clinical Management of Endocrine Diseases

Bilateral Tolosa-Hunt syndrome mimicking pituitary adenoma