Plasma Metabolomics Reveal Alterations of Sphingo- and Glycerophospholipid Levels in Non-Diabetic Carriers of the Transcription Factor 7-Like 2 Polymorphism rs7903146

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Then, Cornelia ^a,b   Wahl, Simone ^c   Kirchhofer, Anna ^a   Grallert, Harald ^b,c   Krug, Susanne ^d   Kastenmüller, Gabi ^c   Römisch Margl, Werner ^c   Claussnitzer, Melina ^d   Illig, Thomas ^e   Heier, Margit ^c   Meisinger, Christa ^c   Adamski, Jerzy ^c   Thorand, Barbara ^c,f   Huth, Cornelia ^c,f   Peters, Annette ^c   Prehn, Cornelia ^c   Heukamp, Ina ^a   Laumen, Helmut ^d   Lechner, Andreas ^a,b   Hauner, Hans ^d   Seissler, Jochen ^a,b   more..

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e HANNOVER MEDICAL SCHOOL   (Germany)

^f GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCEROPHOSPHOLIPID; HYDROXYSPHINGOMYELIN; INSULIN; LYSOPHOSPHATIDYLCHOLINE; PHOSPHATIDYLCHOLINE; SPHINGOLIPID; SPHINGOMYELIN; TRANSCRIPTION FACTOR 7 LIKE 2; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL; TCF7L2 PROTEIN, HUMAN;

ALLELE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HUMAN; INSULIN RESPONSE; INSULIN SENSITIVITY; INTRAVENOUS GLUCOSE TOLERANCE TEST; LIPID BLOOD LEVEL; MALE; METABOLITE; METABOLOMICS; NORMAL HUMAN; PHOSPHOLIPID METABOLISM; TCF7L2 GENE; BLOOD; GENETICS; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE TEST; METABOLOME; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; PROCEDURES;

ALLELES; BLOOD GLUCOSE; DIABETES MELLITUS, TYPE 2; GENOTYPE; GLUCOSE TOLERANCE TEST; GLYCEROPHOSPHOLIPIDS; HUMANS; INSULIN; MALE; METABOLOME; METABOLOMICS; MIDDLE AGED; PHOSPHATIDYLCHOLINES; POLYMORPHISM, GENETIC; SPHINGOMYELINS; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN;

EID: 84886256198     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0078430     Document Type: Article

References (48)

1. Morris AP, Voight BF, Teslovich TM, Ferreira T, Segrè AV, et al. (2012) Large-scale association analysis provides insights into the genetic architecture and pathophysiology of type 2 diabetes. Nat Genet 44: 981-990. doi:10.1038/ng.2383. PubMed: 22885922.
2. Voight BF, Scott LJ, Steinthorsdottir V, Morris AP, Dina C, et al. (2010) Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat Genet 42: 579-589. doi:10.1038/ng.609. PubMed: 20581827.
3. Lyssenko V, Lupi R, Marchetti P, Del Guerra S, Orho-Melander M, et al. (2007) Mechanisms by which common variants in the TCF7L2 gene increase risk of type 2 diabetes. J Clin Invest 117: 2155-2163. doi:10.1172/JCI30706. PubMed: 17671651.
4. Alibegovic AC, Sonne MP, Højbjerre L, Hansen T, Pedersen O, et al. (2010) The T-allele of TCF7L2 rs7903146 associates with a reduced compensation of insulin secretion for insulin resistance induced by 9 days of bed rest. Diabetes 59: 836-843. doi:10.2337/db09-0918. PubMed: 20107109.
5. Schäfer SA, Tschritter O, Machicao F, Thamer C, Stefan N, et al. (2007) Impaired glucagon-like peptide-1-induced insulin secretion in carriers of transcription factor 7-like 2 (TCF7L2) gene polymorphisms. Diabetologia 50: 2443-2450. doi:10.1007/s00125-007-0753-6. PubMed: 17661009.
6. Villareal DT, Robertson H, Bell GI, Patterson BW, Tran H, et al. (2010) TCF7L2 variant rs7903146 affects the risk of type 2 diabetes by modulating incretin action. Diabetes 59: 479-485. doi:10.2337/db09-1169. PubMed: 19934000.
7. Pilgaard K, Jensen CB, Schou JH, Lyssenko V, Wegner L, et al. (2009) The T allele of rs7903146 TCF7L2 is associated with impaired insulinotropic action of incretin hormones, reduced 24 h profiles of plasma insulin and glucagon, and increased hepatic glucose production in young healthy men. Diabetologia 52: 1298-1307. doi:10.1007/s00125-009-1307-x. PubMed: 19288077.
8. Shu L, Sauter NS, Schulthess FT, Matveyenko AV, Oberholzer J, et al. (2008) Transcription factor 7-like 2 regulates beta-cell survival and function in human pancreatic islets. Diabetes 57: 645-653. doi:10.2337/db07-0847. PubMed: 18071026.
9. Kaminska D, Kuulasmaa T, Venesmaa S, Käkelä P, Vaittinen M, et al. (2012) Adipose tissue TCF7L2 splicing is regulated by weight loss and associates with glucose and fatty acid metabolism. Diabetes 61: 2807-2813. doi:10.2337/db12-0239. PubMed: 23086040.
10. Ip W, Shao W, Chiang YT, Jin T, (2012) The Wnt signaling pathway effector TCF7L2 is upregulated by insulin and represses hepatic gluconeogenesis. Am J Physiol Endocrinol Metab 303: E1166-E1176. doi:10.1152/ajpendo.00249.2012. PubMed: 22967502.
11. Boj SF, van Es JH, Huch M, Li VS, José A, et al. (2012) Diabetes risk gene and Wnt effector Tcf7l2/TCF4 controls hepatic response to perinatal and adult metabolic demand. Cell 151: 1595-1607. doi:10.1016/j.cell.2012.10.053. PubMed: 23260145.
12. Zhang X, Wang Y, Hao F, Zhou X, Han X, et al. (2009) Human serum metabonomic analysis reveals progression axes for glucose intolerance and insulin resistance statuses. J Proteome Res 8: 5188-5195. doi:10.1021/pr900524z. PubMed: 19697961.
13. Zhu C, Liang QL, Hu P, Wang YM, Luo GA, (2011) Phospholipidomic identification of potential plasma biomarkers associated with type 2 diabetes mellitus and diabetic nephropathy. Talanta 85: 1711-1720. doi:10.1016/j.talanta.2011.05.036. PubMed: 21872008.
14. Floegel A, Stefan N, Yu Z, Mühlenbruch K, Drogan D, et al. (2012) Identification of Serum Metabolites Associated With Risk of Type 2 Diabetes Using a Targeted Metabolomic Approach. Diabetes, 62: 639-48. PubMed: 23043162.
15. Suhre K, Meisinger C, Döring A, Altmaier E, Belcredi P, et al. (2010) Metabolic footprint of diabetes: a multiplatform metabolomics study in an epidemiological setting. PLOS ONE 5: e13953. doi:10.1371/journal.pone.0013953. PubMed: 21085649.
16. Shaham O, Wei R, Wang TJ, Ricciardi C, Lewis GD, et al. (2008) Metabolic profiling of the human response to a glucose challenge reveals distinct axes of insulin sensitivity. Mol Syst Biol 4: 214. PubMed: 18682704.
17. Rathmann W, Strassburger K, Heier M, Holle R, Thorand B, et al. (2009) Incidence of Type 2 diabetes in the elderly German population and the effect of clinical and lifestyle risk factors: KORA S4/F4 cohort study. Diabet Med 26: 1212-1219. doi:10.1111/j.1464-5491.2009.02863.x. PubMed: 20002472.
18. Marzi C, Huth C, Kolz M, Grallert H, Meisinger C, et al. (2007) Variants of the transcription factor 7-like 2 gene (TCF7L2) are strongly associated with type 2 diabetes but not with the metabolic syndrome in the MONICA/KORA surveys. Horm Metab Res 39: 46-52. doi:10.1055/s-2007-957345. PubMed: 17226113.
19. Anzeneder L, Kircher F, Feghelm N, Fischer R, Seissler J, (2011) Kinetics of insulin secretion and glucose intolerance in adult patients with cystic fibrosis. Horm Metab Res 43: 355-360. doi:10.1055/s-0031-1275270. PubMed: 21448848.
20. Römisch-Margl W, Bogumil R, Röhring C, Suhre K, Adamski J, (2012) Procedure for tissue sample preparation and metabolite extraction for high-throughput targeted metabolomics. Metabolomics 8: 133-142. doi:10.1007/s11306-011-0293-4.
21. Illig T, Gieger C, Zhai G, Römisch-Margl W, Wang-Sattler R, et al. (2010) A genome-wide perspective of genetic variation in human metabolism. Nat Genet 42: 137-141. doi:10.1038/ng.507. PubMed: 20037589.
22. Laird NM, Ware JH, (1982) Random-effects models for longitudinal data. Biometrics 38: 963-974. doi:10.2307/2529876. PubMed: 7168798.
23. Benjamini YHY, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57: 289-300.
24. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, et al. (2009) A branched-chain amino acid-related metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab 9: 311-326. doi:10.1016/j.cmet.2009.02.002. PubMed: 19356713.
25. Fiehn O, Garvey WT, Newman JW, Lok KH, Hoppel CL, et al. (2010) Plasma metabolomic profiles reflective of glucose homeostasis in non-diabetic and type 2 diabetic obese African-American women. PLOS ONE 5: e15234. doi:10.1371/journal.pone.0015234. PubMed: 21170321.
26. Gall WE, Beebe K, Lawton KA, Adam KP, Mitchell MW, et al. (2010) alpha-hydroxybutyrate is an early biomarker of insulin resistance and glucose intolerance in a nondiabetic population. PLOS ONE 5: e10883. doi:10.1371/journal.pone.0010883. PubMed: 20526369.
27. Wang TJ, Larson MG, Vasan RS, Cheng S, Rhee EP, et al. (2011) Metabolite profiles and the risk of developing diabetes. Nat Med 17: 448-453. doi:10.1038/nm.2307. PubMed: 21423183.
28. González-Sánchez JL, Martínez-Larrad MT, Zabena C, Pérez-Barba M, Serrano-Ríos M, (2008) Association of variants of the TCF7L2 gene with increases in the risk of type 2 diabetes and the proinsulin:insulin ratio in the Spanish population. Diabetologia 51: 1993-1997. doi:10.1007/s00125-008-1129-2. PubMed: 18712344.
29. Gault CR, Obeid LM, Hannun YA, (2010) An overview of sphingolipid metabolism: from synthesis to breakdown. Adv Exp Med Biol 688: 1-23. doi:10.1007/978-1-4419-6741-1_1. PubMed: 20919643.
30. Nelson JC, Jiang XC, Tabas I, Tall A, Shea S, (2006) Plasma sphingomyelin and subclinical atherosclerosis: findings from the multi-ethnic study of atherosclerosis. Am J Epidemiol 163: 903-912. doi:10.1093/aje/kwj140. PubMed: 16611667.
31. Chen X, Sun A, Zou Y, Ge J, Lazar JM, et al. (2011) Impact of sphingomyelin levels on coronary heart disease and left ventricular systolic function in humans. Nutr Metab (Lond) 8: 25. doi:10.1186/1743-7075-8-25. PubMed: 21521522.
32. Samad F, Hester KD, Yang G, Hannun YA, Bielawski J, (2006) Altered adipose and plasma sphingolipid metabolism in obesity: a potential mechanism for cardiovascular and metabolic risk. Diabetes 55: 2579-2587. doi:10.2337/db06-0330. PubMed: 16936207.
33. Li Z, Zhang H, Liu J, Liang CP, Li Y, et al. (2011) Reducing plasma membrane sphingomyelin increases insulin sensitivity. Mol Cell Biol 31: 4205-4218. doi:10.1128/MCB.05893-11. PubMed: 21844222.
34. Mitsutake S, Zama K, Yokota H, Yoshida T, Tanaka M, et al. (2011) Dynamic modification of sphingomyelin in lipid microdomains controls development of obesity, fatty liver, and type 2 diabetes. J Biol Chem 286: 28544-28555. doi:10.1074/jbc.M111.255646. PubMed: 21669879.
35. Yano M, Watanabe K, Yamamoto T, Ikeda K, Senokuchi T, et al. (2011) Mitochondrial dysfunction and increased reactive oxygen species impair insulin secretion in sphingomyelin synthase 1-null mice. J Biol Chem 286: 3992-4002. doi:10.1074/jbc.M110.179176. PubMed: 21115496.
36. Zhang Y, Ranta F, Tang C, Shumilina E, Mahmud H, et al. (2009) Sphingomyelinase dependent apoptosis following treatment of pancreatic beta-cells with amyloid peptides Abeta(1-42) or IAPP. Apoptosis 14: 878-889. doi:10.1007/s10495-009-0364-4. PubMed: 19488858.
37. Boslem E, MacIntosh G, Preston AM, Bartley C, Busch AK, et al. (2011) A lipidomic screen of palmitate-treated MIN6 beta-cells links sphingolipid metabolites with endoplasmic reticulum (ER) stress and impaired protein trafficking. Biochem J 435: 267-276. doi:10.1042/BJ20101867. PubMed: 21265737.
38. Ha CY, Kim JY, Paik JK, Kim OY, Paik YH, et al. (2012) The association of specific metabolites of lipid metabolism with markers of oxidative stress, inflammation and arterial stiffness in men with newly diagnosed type 2 diabetes. Clin Endocrinol (Oxf) 76: 674-682. doi:10.1111/j.1365-2265.2011.04244.x. PubMed: 21958081.
39. Wang-Sattler R, Yu Z, Herder C, Messias AC, Floegel A, et al. (2012) Novel biomarkers for pre-diabetes identified by metabolomics. Mol Syst Biol 8: 615. PubMed: 23010998.
40. Pietiläinen KH, Kannisto K, Korsheninnikova E, Rissanen A, Kaprio J, et al. (2006) Acquired obesity increases CD68 and tumor necrosis factor-alpha and decreases adiponectin gene expression in adipose tissue: a study in monozygotic twins. J Clin Endocrinol Metab 91: 2776-2781. doi:10.1210/jc.2005-2848. PubMed: 16608891.
41. Kougias P, Chai H, Lin PH, Lumsden AB, Yao Q, et al. (2006) Lysophosphatidylcholine and secretory phospholipase A2 in vascular disease: mediators of endothelial dysfunction and atherosclerosis. Med Sci Monit 12: RA5-16. PubMed: 16369478.
42. Dohi T, Miyauchi K, Ohkawa R, Nakamura K, Kishimoto T, et al. (2012) Increased circulating plasma lysophosphatidic acid in patients with acute coronary syndrome. Clin Chim Acta 413: 207-212. doi:10.1016/j.cca.2011.09.027. PubMed: 21983165.
43. Huo T, Cai S, Lu X, Sha Y, Yu M, et al. (2009) Metabonomic study of biochemical changes in the serum of type 2 diabetes mellitus patients after the treatment of metformin hydrochloride. J Pharm Biomed Anal 49: 976-982. doi:10.1016/j.jpba.2009.01.008. PubMed: 19249171.
44. Han MS, Lim YM, Quan W, Kim JR, Chung KW, et al. (2011) Lysophosphatidylcholine as an effector of fatty acid-induced insulin resistance. J Lipid Res 52: 1234-1246. doi:10.1194/jlr.M014787. PubMed: 21447485.
45. Yea K, Kim J, Yoon JH, Kwon T, Kim JH, et al. (2009) Lysophosphatidylcholine activates adipocyte glucose uptake and lowers blood glucose levels in murine models of diabetes. J Biol Chem 284: 33833-33840. doi:10.1074/jbc.M109.024869. PubMed: 19815546.
46. Ishida-Oku M, Iwase M, Sonoki K, Sasaki N, Imoto H, et al. (2010) Expression of secretory phospholipase A 2 in insulitis of human transplanted pancreas and its insulinotropic effect on isolated rat islets. Islets 2: 274-277. doi:10.4161/isl.2.5.12728. PubMed: 21099324.
47. Xu F, Tavintharan S, Sum CF, Woon K, Lim SC, et al. (2013) Metabolic signature shift in type 2 diabetes mellitus revealed by mass spectrometry-based metabolomics. J Clin Endocrinol Metab 98: E1060-E1065. doi:10.1210/jc.2012-4132. PubMed: 23633210.
48. Pietiläinen KH, Naukkarinen J, Rissanen A, Saharinen J, Ellonen P, et al. (2008) Global transcript profiles of fat in monozygotic twins discordant for BMI: pathways behind acquired obesity. PLOS Med 5: e51. doi:10.1371/journal.pmed.0050051. PubMed: 18336063.