Adipose tissue dysfunction and altered systemic amino acid metabolism are associated with non-alcoholic fatty liver disease

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Cheng, Sulin ^a,b   Wiklund, Petri ^b   Autio, Reija ^c   Borra, Ronald ^d   Ojanen, Xiaowei ^e   Xu, Leiting ^a,f   Törmäkangas, Timo ^b   Alen, Markku ^b,g  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d TURKU UNIVERSITY HOSPITAL   (Finland)

^e UNIVERSITY OF EASTERN FINLAND   (Finland)

^f NINGBO UNIVERSITY   (China)

^g OULU UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BRANCHED CHAIN AMINO ACID; OROSOMUCOID; AMINO ACID; FATTY ACID;

ADIPOSE TISSUE; AMINO ACID METABOLISM; ARTICLE; BLOOD ANALYSIS; BLOOD SAMPLING; CATABOLISM; CONTROLLED STUDY; DOWN REGULATION; ENERGY METABOLISM; FAT CONTENT; FEMALE; GENE EXPRESSION REGULATION; HUMAN; INSULIN RESISTANCE; LIFESTYLE; LIPID STORAGE; MAJOR CLINICAL STUDY; MALE; METABOLIC DISORDER; MICROARRAY ANALYSIS; NONALCOHOLIC FATTY LIVER; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OBESITY; PATHOGENESIS; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTON NUCLEAR MAGNETIC RESONANCE; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; WESTERN BLOTTING; LIVER; METABOLISM; MIDDLE AGED; PATHOLOGY; PATHOPHYSIOLOGY;

ADIPOSE TISSUE; AMINO ACIDS; FATTY ACIDS; FEMALE; HUMANS; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; OBESITY;

EID: 84947935205     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138889     Document Type: Article

References (56)

1. Smith BW, Adams LA (2011) Non-alcoholic fatty liver disease. Crit Rev Clin Lab Sci 48: 97-113. doi: 10.3109/10408363.2011.596521 PMID: 21875310
2. Tilg H, Moschen AR (2010) Evolution of inflammation in nonalcoholic fatty liver disease: the multiple parallel hits hypothesis. Hepatology 52: 1836-1846. doi: 10.1002/hep.24001 PMID: 21038418
3. Cano A, Alonso C (2014) Deciphering non-alcoholic fatty liver disease through metabolomics. Biochem Soc Trans 42: 1447-1452. doi: 10.1042/BST20140138 PMID: 25233430
4. Beyoglu D, Idle JR (2013) The metabolomic window into hepatobiliary disease. J Hepatol 59: 842-858. doi: 10.1016/j.jhep.2013.05.030 PMID: 23714158
5. Hyysalo J, Gopalacharyulu P, Bian H, Hyotylainen T, Leivonen M, Jaser N, et al. (2013) Circulating triacylglycerol signatures in nonalcoholic fatty liver disease associated with the I148M variant in PNPLA3 and with obesity. Diabetes 63: 312-322. doi: 10.2337/db13-0774 PMID: 24009255
6. Lehmann R, Franken H, Dammeier S, Rosenbaum L, Kantartzis K, Peter A, et al. (2013) Circulating lysophosphatidylcholines are markers of a metabolically benign nonalcoholic fatty liver. Diabetes Care 36: 2331-2338. doi: 10.2337/dc12-1760 PMID: 23514731
7. Iwasa M, Ishihara T, Mifuji-Moroka R, Fujita N, Kobayashi Y, Hasegawa H, et al. (2015) Elevation of branched-chain amino acid levels in diabetes and NAFL and changes with antidiabetic drug treatment. Obes Res Clin Pract.
8. Lehmann R, Franken H, Dammeier S, Rosenbaum L, Kantartzis K, Peter A, et al. Circulating lysophosphatidylcholines are markers of a metabolically benign nonalcoholic fatty liver. Diabetes Care 36: 2331-2338. doi: 10.2337/dc12-1760 PMID: 23514731
9. Rodriguez-Gallego E, Guirro M, Riera-Borrull M, Hernandez-Aguilera A, Marine-Casado R, Fernandez-Arroyo S, et al. (2015) Mapping of the circulating metabolome reveals alpha-ketoglutarate as a predictor of morbid obesity-associated non-alcoholic fatty liver disease. Int J Obes (Lond) 39: 279-287.
10. Lake AD, Novak P, Shipkova P, Aranibar N, Robertson DG, Reily MD, et al. (2014) Branched chain amino acid metabolism profiles in progressive human nonalcoholic fatty liver disease. Amino Acids 47: 603-615. doi: 10.1007/s00726-014-1894-9 PMID: 25534430
11. Stefan N, Kantartzis K, Haring HU (2008) Causes and metabolic consequences of Fatty liver. Endocr Rev 29: 939-960. doi: 10.1210/er.2008-0009 PMID: 18723451
12. Yki-Jarvinen H (2014) Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. doi: 10.1016/S2213-8587(14)70032-4 PMID: 24731669
13. Gastaldelli A, Natali A, Vettor R, Corradini SG (2010) Insulin resistance, adipose depots and gut: interactions and pathological implications. Dig Liver Dis 42: 310-319. doi: 10.1016/j.dld.2010.01.013 PMID: 20194050
14. Tsochatzis EA, Papatheodoridis GV, Archimandritis AJ (2009) Adipokines in nonalcoholic steatohepatitis: from pathogenesis to implications in diagnosis and therapy. Mediators Inflamm 2009: 831670. doi: 10.1155/2009/831670 PMID: 19753129
15. Duval C, Thissen U, Keshtkar S, Accart B, Stienstra R, Boekschoten MV, et al. (2010) Adipose tissue dysfunction signals progression of hepatic steatosis towards nonalcoholic steatohepatitis in C57BL/6 mice. Diabetes 59: 3181-3191. doi: 10.2337/db10-0224 PMID: 20858684
16. Flannery C, Dufour S, Rabol R, Shulman GI, Petersen KF (2012) Skeletal muscle insulin resistance promotes increased hepatic de novo lipogenesis, hyperlipidemia, and hepatic steatosis in the elderly. Diabetes 61: 2711-2717. doi: 10.2337/db12-0206 PMID: 22829450
17. Argiles JM, Lopez-Soriano J, Almendro V, Busquets S, Lopez-Soriano FJ (2005) Cross-talk between skeletal muscle and adipose tissue: a link with obesity? Med Res Rev 25: 49-65. PMID: 15389734
18. Liu WY, Lu da J, Du XM, Sun JQ, Ge J, Wang RW, et al. (2014) Effect of aerobic exercise and low carbohydrate diet on pre-diabetic non-alcoholic fatty liver disease in postmenopausal women and middle aged men - the role of gut microbiota composition: study protocol for the AELC randomized controlled trial. BMC Public Health 14: 48. doi: 10.1186/1471-2458-14-48 PMID: 24438438
19. Choi ES, Kim MK, Song MK, Kim JM, Kim ES, Chung WJ, et al. (2014) Association between serum irisin levels and non-alcoholic fatty liver disease in health screen examinees. PLoS One 9: e110680. doi: 10.1371/journal.pone.0110680 PMID: 25343462
20. Brosnan JT, Brosnan ME (2006) Branched-chain amino acids: enzyme and substrate regulation. J Nutr 136: 207S-211S. PMID: 16365084
21. Herman MA, She P, Peroni OD, Lynch CJ, Kahn BB (2010) Adipose tissue branched chain amino acid (BCAA) metabolism modulates circulating BCAA levels. J Biol Chem 285: 11348-11356. doi: 10.1074/jbc.M109.075184 PMID: 20093359
22. Pietilainen KH, Naukkarinen J, Rissanen A, Saharinen J, Ellonen P, Keranen H, 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 PMID: 18336063
23. Cheng S, Volgyi E, Tylavsky FA, Lyytikainen A, Tormakangas T, Xu L, et al. (2009) Trait-specific tracking and determinants of body composition: a 7-year follow-up study of pubertal growth in girls. BMC Med 7: 5. doi: 10.1186/1741-7015-7-5 PMID: 19171028
24. Wang Q, Xu L, Chen D, Tian H, Lu C, Cheng S, et al. (2011) Is bone loss the reversal of bone accrual? Evidence from a cross-sectional study in daughter-mother-grandmother trios. J Bone Miner Res 26: 934-940. doi: 10.1002/jbmr.291 PMID: 21541995
25. Szczepaniak LS, Nurenberg P, Leonard D, Browning JD, Reingold JS, Grundy S, et al. (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288: E462-468. PMID: 15339742
26. Lu C, Ivaska KK, Alen M, Wang Q, Tormakangas T, Xu L, et al. (2012) Serum osteocalcin is not associated with glucose but is inversely associated with leptin across generations of nondiabetic women. J Clin Endocrinol Metab 97: 4106-4114. doi: 10.1210/jc.2012-2045 PMID: 22948754
27. Cheng S, Lyytikainen A, Kroger H, Lamberg-Allardt C, Alen M, Koistinen A, et al. (2005) Effects of calcium, dairy product, and vitamin D supplementation on bone mass accrual and body composition in 10-12-y-old girls: a 2-y randomized trial. Am J Clin Nutr 82: 1115-1126; quiz 1147-1118. PMID: 16280447
28. Volgyi E, Lyytikainen A, Tylavsky FA, Nicholson PH, Suominen H, Alen M, et al. (2010) Long-term leisure-time physical activity has a positive effect on bone mass gain in girls. J Bone Miner Res 25: 1034-1041. doi: 10.1359/jbmr.091115 PMID: 19929440
29. Provencher SW (2001) Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14: 260-264. PMID: 11410943
30. Borra RJ, Salo S, Dean K, Lautamaki R, Nuutila P, Komu M, et al. (2009) Nonalcoholic fatty liver disease: rapid evaluation of liver fat content with in-phase and out-of-phase MR imaging. Radiology 250: 130-136. doi: 10.1148/radiol.2501071934 PMID: 19017926
31. Munukka E, Pekkala S, Wiklund P, Rasool O, Borra R, Kong L, et al. (2014) Gut-adipose tissue axis in hepatic fat accumulation in humans. J Hepatol. doi: 10.1016/j.jhep.2014.02.020 PMID: 24613361
32. Furuyama JK, Nagarajan R, Roberts CK, Lee CC, Hahn TJ, Thomas MA (2014) A pilot validation of multi-echo based echo-planar correlated spectroscopic imaging in human calf muscles. NMR Biomed 27: 1176-1183. doi: 10.1002/nbm.3171 PMID: 25132520
33. Soininen P, Kangas AJ, Wurtz P, Tukiainen T, Tynkkynen T, Laatikainen R, et al. (2009) High-throughput serum NMR metabonomics for cost-effective holistic studies on systemic metabolism. Analyst 134: 1781-1785. doi: 10.1039/b910205a PMID: 19684899
34. Wiklund PK, Pekkala S, Autio R, Munukka E, Xu L, Saltevo J, et al. (2014) Serum metabolic profiles in overweight and obese women with and without metabolic syndrome. Diabetol Metab Syndr 6: 40. doi: 10.1186/1758-5996-6-40 PMID: 24650495
35. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273. PMID: 12808457
36. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B 57: 289-300.
37. Emilsson V, Thorleifsson G, Zhang B, Leonardson AS, Zink F, Zhu J, et al. (2008) Genetics of gene expression and its effect on disease. Nature 452: 423-428. doi: 10.1038/nature06758 PMID: 18344981
38. Trayhurn P (2013) Hypoxia and adipose tissue function and dysfunction in obesity. Physiol Rev 93: 1-21. doi: 10.1152/physrev.00017.2012 PMID: 23303904
39. Masoodi M, Kuda O, Rossmeisl M, Flachs P, Kopecky J (2014) Lipid signaling in adipose tissue: Connecting inflammation & metabolism. Biochim Biophys Acta 1851: 503-518. doi: 10.1016/j.bbalip.2014.09.023 PMID: 25311170
40. Chen G, Xu R, Zhang S, Wang Y, Wang P, Edin ML, et al. (2015) CYP2J2 overexpression attenuates nonalcoholic fatty liver disease induced by high-fat diet in mice. Am J Physiol Endocrinol Metab 308: E97-E110. doi: 10.1152/ajpendo.00366.2014 PMID: 25389366
41. Stefan N, Haring HU (2011) The metabolically benign and malignant fatty liver. Diabetes 60: 2011-2017. doi: 10.2337/db11-0231 PMID: 21788578
42. Charakida M, Masi S, Deanfield JE (2013) The Year in Cardiology 2012: focus on cardiovascular disease prevention. Eur Heart J 34: 314-317. doi: 10.1093/eurheartj/ehs429 PMID: 23284098
43. Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F (2009) Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol 51: 433-445. doi: 10.1016/j.jhep.2009.05.023 PMID: 19604596
44. Kalhan SC, Guo L, Edmison J, Dasarathy S, McCullough AJ, Hanson RW, et al. (2011) Plasma metabolomic profile in nonalcoholic fatty liver disease. Metabolism 60: 404-413. doi: 10.1016/j.metabol.2010.03.006 PMID: 20423748
45. Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. (2005) Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology 128: 1898-1906. PMID: 15940625
46. MacCallum RC, Zhang S, Preacher KJ, Rucker DD (2002) On the practice of dichotomization of quantitative variables. Psychol Methods 7: 19-40. PMID: 11928888
47. Batch BC, Shah SH, Newgard CB, Turer CB, Haynes C, Bain JR, et al. (2013) Branched chain amino acids are novel biomarkers for discrimination of metabolic wellness. Metabolism 62: 961-969. doi: 10.1016/j.metabol.2013.01.007 PMID: 23375209
48. Huffman KM, Shah SH, Stevens RD, Bain JR, Muehlbauer M, Slentz CA, et al. (2009) Relationships between circulating metabolic intermediates and insulin action in overweight to obese, inactive men and women. Diabetes Care 32: 1678-1683. doi: 10.2337/dc08-2075 PMID: 19502541
49. Wurtz P, Makinen VP, Soininen P, Kangas AJ, Tukiainen T, Kettunen J, et al. (2012) Metabolic signatures of insulin resistance in 7,098 young adults. Diabetes 61: 1372-1380. doi: 10.2337/db11-1355 PMID: 22511205
50. Sunny NE, Kalavalapalli S, Bril F, Garrett TJ, Nautiyal M, Mathew JT, et al. (2015) Crosstalk between branched chain amino acids and hepatic mitochondria is compromised in nonalcoholic fatty liver disease. Am J Physiol Endocrinol Metab: ajpendo 00161 02015.
51. Heilbronn L, Smith SR, Ravussin E (2004) Failure of fat cell proliferation, mitochondrial function and fat oxidation results in ectopic fat storage, insulin resistance and type II diabetes mellitus. Int J Obes Relat Metab Disord 28 Suppl 4: S12-21. PMID: 15592481
52. Goossens GH (2008) The role of adipose tissue dysfunction in the pathogenesis of obesity-related insulin resistance. Physiol Behav 94: 206-218. PMID: 18037457
53. Burrill JS, Long EK, Reilly B, Deng Y, Armitage IM, Scherer PE, et al. (2015) Inflammation and ER Stress Regulate Branched Chain Amino Acid Uptake and Metabolism in Adipocytes. Mol Endocrinol: me20141275. doi: 10.1210/me.2014-1275 PMID: 25635940
54. Libreros S, Garcia-Areas R, Shibata Y, Carrio R, Torroella-Kouri M, Iragavarapu-Charyulu V (2011) Induction of proinflammatory mediators by CHI3L1 is reduced by chitin treatment: decreased tumor metastasis in a breast cancer model. Int J Cancer 131: 377-386. doi: 10.1002/ijc.26379 PMID: 21866546
55. Petersen KF, Dufour S, Savage DB, Bilz S, Solomon G, Yonemitsu S, et al. (2007) The role of skeletal muscle insulin resistance in the pathogenesis of the metabolic syndrome. Proc Natl Acad Sci U S A 104: 12587-12594. PMID: 17640906
56. Szendroedi J, Kaul K, Kloock L, Strassburger K, Schmid AI, Chmelik M, et al. (2013) Lower fasting muscle mitochondrial activity relates to hepatic steatosis in humans. Diabetes Care 37: 468-474. doi: 10.2337/dc13-1359 PMID: 24026561