The ratio of dihomo-γ-linolenic acid to deoxycholic acid species is a potential biomarker for the metabolic abnormalities in obesity

FASEB Journal

Volumn 31, Issue 9, 2017, Pages 3904-3912

  Lei, Sha ^a   Huang, Fengjie ^a   Zhao, Aihua ^a   Chen, Tianlu ^a   Chen, Wenlian ^b   Xie, Guoxiang ^b   Zheng, Xiaojiao ^a   Zhang, Yunjing ^a   Yu, Haoyong ^a   Zhang, Pin ^a   Rajani, Cynthia ^b   Bao, Yuqian ^a   Jia, Weiping ^a   Jia, Wei ^a,b  

^a SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

^b UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

Bile acid; Free fatty acid; Targeted metabolomics; Type 2 diabetes

Indexed keywords

BILE ACID; BIOLOGICAL MARKER; CARNITINE PALMITOYLTRANSFERASE I; CARNITINE PALMITOYLTRANSFERASE IA; DEOXYCHOLIC ACID; DIHOMO GAMMA LINOLENIC ACID; FATTY ACID; FATTY ACID TRANSPORTER; FATTY ACID TRANSPORTER 5; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE ACID METABOLISM; BLOOD LEVEL; BODY MASS; BODY WEIGHT; CASE CONTROL STUDY; COHORT ANALYSIS; CONTROLLED STUDY; DIET INDUCED OBESITY; FATTY ACID ANALYSIS; FATTY ACID METABOLISM; FEMALE; FOLLOW UP; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IMPAIRED GLUCOSE TOLERANCE; IN VITRO STUDY; LIPID METABOLISM; LIVER; LIVER CELL LINE; LIVER LEVEL; MAJOR CLINICAL STUDY; MALE; METABOLIC DISORDER; METABOLOMICS; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PRIORITY JOURNAL; QUADRUPOLE MASS SPECTROMETRY; REMISSION; ROUX-EN-Y GASTRIC BYPASS; SERUM; TARGETED METABOLOMICS; TIME OF FLIGHT MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; WEIGHT REDUCTION; ADULT; ADVERSE EFFECTS; ANIMAL; BLOOD; CELL LINE; CHEMISTRY; GLUCOSE TOLERANCE TEST; INSULIN RESISTANCE; LIPID DIET; LIVER CELL; METABOLISM;

8,11,14-EICOSATRIENOIC ACID; ADULT; ANIMALS; BIOMARKERS; CELL LINE; DEOXYCHOLIC ACID; DIET, HIGH-FAT; FEMALE; GLUCOSE TOLERANCE TEST; HEPATOCYTES; HUMANS; INSULIN RESISTANCE; MALE; MICE; OBESITY;

EID: 85028947750     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.201700055R     Document Type: Article

References (47)

1. Zhou, J., Febbraio, M., Wada, T., Zhai, Y., Kuruba, R., He, J., Lee, J. H., Khadem, S., Ren, S., Li, S., Silverstein, R. L., and Xie, W. (2008) Hepatic fatty acid transporter Cd36 is a common target of LXR, PXR, and PPARgamma in promoting steatosis. Gastroenterology 134, 556–567
2. Li, T., and Chiang, J. Y. (2014) Bile acid signaling in metabolic disease and drug therapy. Pharmacol. Rev. 66, 948–983
3. Ma, H., and Patti, M. E. (2014) Bile acids, obesity, and the metabolic syndrome. Best Pract. Res. Clin. Gastroenterol. 28, 573–583
4. Boden, G. (2011) Obesity, insulin resistance and free fatty acids. Curr. Opin. Endocrinol. Diabetes Obes. 18, 139–143
5. Ni, Y., Zhao, L., Yu, H., Ma, X., Bao, Y., Rajani, C., Loo, L. W., Shvetsov, Y. B., Yu, H., Chen, T., Zhang, Y., Wang, C., Hu, C., Su, M., Xie, G., Zhao, A., Jia, W., and Jia, W. (2015) Circulating unsaturated fatty acids delineate the metabolic status of obese individuals. EBioMedicine 2, 1513–1522
6. Yary, T., Voutilainen, S., Tuomainen, T. P., Ruusunen, A., Nurmi, T., and Virtanen, J. K. (2016) Serum n-6 polyunsaturated fatty acids, D5- and D6-desaturase activities, and risk of incident type 2 diabetes in men: the Kuopio Ischaemic Heart Disease Risk Factor Study. Am. J. Clin. Nutr. 103, 1337–1343
7. Alhazmi, A., Stojanovski, E., Garg, M. L., and McEvoy, M. (2014) Fasting whole blood fatty acid profile and risk of type 2 diabetes in adults: a nested case control study. PLoS One 9, e97001
8. Matsuda, M., Kawamoto, T., and Tamura, R. (2017) Predictive value of serum dihomo-g-linolenic acid level and estimated D-5 desaturase activity in patients with hepatic steatosis. Obes. Res. Clin. Pract. 11, 34–43
9. Penney, N. C., Kinross, J., Newton, R. C., and Purkayastha, S. (2015) The role of bile acids in reducing the metabolic complications of obesity after bariatric surgery: a systematic review. Int. J. Obes. 39, 1565–1574
10. Nie, B., Park, H. M., Kazantzis, M., Lin, M., Henkin, A., Ng, S., Song, S., Chen, Y., Tran, H., Lai, R., Her, C., Maher, J. J., Forman, B. M., and Stahl, A. (2012) Specific bile acids inhibit hepatic fatty acid uptake in mice. Hepatology 56, 1300–1310
11. Wang, X., Xie, G., Zhao, A., Zheng, X., Huang, F., Wang, Y., Yao, C., Jia, W., and Liu, P. (2016) Serum bile acids are associated with pathological progression of hepatitis B-induced cirrhosis. J. Proteome Res. 15, 1126–1134
12. Yu, H., Di, J., Bao, Y., Zhang, P., Zhang, L., Tu, Y., Han, X., and Jia, W. (2015) Visceral fat area as a new predictor of short-term diabetes remission after Roux-en-Y gastric bypass surgery in Chinese patients with a body mass index less than 35 kg/m2. Surg. Obes. Relat. Dis. 11, 6–11
13. Alberti, K. G. M. M., and Zimmet, P. Z. (1998) Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet. Med. 15, 539–553
14. Zhou, B. F. (2002) Effect of body mass index on all-cause mortality and incidence of cardiovascular diseases–report for meta-analysis of prospective studies open optimal cut-off points of body mass index in Chinese adults. Biomed. Environ. Sci. 15, 245–252
15. Buse, J. B., Caprio, S., Cefalu, W. T., Ceriello, A., Del Prato, S., Inzucchi, S. E., McLaughlin, S., Phillips G. L. II, Robertson, R. P., Rubino, F., Kahn, R., and Kirkman, M. S. (2009) How do we define cure of diabetes? Diabetes Care 32, 2133–2135
16. Xie, G., Wang, X., Huang, F., Zhao, A., Chen, W., Yan, J., Zhang, Y., Lei, S., Ge, K., Zheng, X., Liu, J., Su, M., Liu, P., and Jia, W. (2016) Dysregulated hepatic bile acids collaboratively promote liver carcinogenesis. Int. J. Cancer 139, 1764–1775
17. Chen, W. L., Wang, J. H., Zhao, A. H., Xu, X., Wang, Y. H., Chen, T. L., Li, J. M., Mi, J. Q., Zhu, Y. M., Liu, Y. F., Wang, Y. Y., Jin, J., Huang, H., Wu, D. P., Li, Y., Yan, X. J., Yan, J. S., Li, J. Y., Wang, S., Huang, X. J., Wang, B. S., Chen, Z., Chen, S. J., and Jia, W. (2014) A distinct glucose metabolism signature of acute myeloid leukemia with prognostic value. Blood 124, 1645–1654
18. Xie, G., Wang, Y., Wang, X., Zhao, A., Chen, T., Ni, Y., Wong, L., Zhang, H., Zhang, J., Liu, C., Liu, P., and Jia, W. (2015) Profiling of serum bile acids in a healthy Chinese population using UPLC-MS/ MS. J. Proteome Res. 14, 850–859
19. Xie, G., Zhong, W., Li, H., Li, Q., Qiu, Y., Zheng, X., Chen, H., Zhao, X., Zhang, S., Zhou, Z., Zeisel, S. H., and Jia, W. (2013) Alteration of bile acid metabolism in the rat induced by chronic ethanol consumption. FASEB J. 27, 3583–3593
20. Gerhard, G. S., Styer, A. M., Wood, G. C., Roesch, S. L., Petrick, A. T., Gabrielsen, J., Strodel, W. E., Still, C. D., and Argyropoulos, G. (2013) A role for fibroblast growth factor 19 and bile acids in diabetes remission after Roux-en-Y gastric bypass. Diabetes Care 36, 1859–1864
21. Jørgensen, N. B., Dirksen, C., Bojsen-Møller, K. N., Kristiansen, V. B., Wulff, B. S., Rainteau, D., Humbert, L., Rehfeld, J. F., Holst, J. J., Madsbad, S., and Clausen, T. R. (2015) Improvements in glucose metabolism early after gastric bypass surgery are not explained by increases in total bile acids and fibroblast growth factor 19 concentrations. J. Clin. Endocrinol. Metab. 100, E396–E406
22. Steinert, R. E., Peterli, R., Keller, S., Meyer-Gerspach, A. C., Drewe, J., Peters, T., and Beglinger, C. (2013) Bile acids and gut peptide secretion after bariatric surgery: a 1-year prospective randomized pilot trial. Obesity (Silver Spring) 21, E660–E668
23. Park, W. H., and Pak, Y. K. (2011) Insulin-dependent suppression of cholesterol 7a-hydroxylase is a possible link between glucose and cholesterol metabolisms. Exp. Mol. Med. 43, 571–579
24. Kohli, R., Bradley, D., Setchell, K. D., Eagon, J. C., Abumrad, N., and Klein, S. (2013) Weight loss induced by Roux-en-Y gastric bypass but not laparoscopic adjustable gastric banding increases circulating bile acids. J. Clin. Endocrinol. Metab. 98, E708–E712
25. Patti, M. E., Houten, S. M., Bianco, A. C., Bernier, R., Larsen, P. R., Holst, J. J., Badman, M. K., Maratos-Flier, E., Mun, E. C., Pihlajamaki, J., Auwerx, J., and Goldfine, A. B. (2009) Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring) 17, 1671–1677
26. Albaugh, V. L., Flynn, C. R., Cai, S., Xiao, Y., Tamboli, R. A., and Abumrad, N. N. (2015) Early increases in bile acids post Roux-en-Y gastric bypass are driven by insulin-sensitizing, secondary bile acids. J. Clin. Endocrinol. Metab. 100, E1225–E1233
27. Larsen, N., Vogensen, F. K., van den Berg, F. W., Nielsen, D. S., Andreasen, A. S., Pedersen, B. K., Al-Soud, W. A., Sørensen, S. J., Hansen, L. H., and Jakobsen, M. (2010) Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5, e9085
28. Jump, D. B. (2002) The biochemistry of n-3 polyunsaturated fatty acids. J. Biol. Chem. 277, 8755–8758
29. Wall, R., Ross, R. P., Fitzgerald, G. F., and Stanton, C. (2010) Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr. Rev. 68, 280–289
30. Forouhi, N. G., Imamura, F., Sharp, S. J., Koulman, A., Schulze, M. B., Zheng, J., Ye, Z., Sluijs, I., Guevara, M., Huerta, J. M., Kröger, J., Wang, L. Y., Summerhill, K., Griffin, J. L., Feskens, E. J., Affret, A., Amiano, P., Boeing, H., Dow, C., Fagherazzi, G., Franks, P. W., Gonzalez, C., Kaaks, R., Key, T. J., Khaw, K. T., Kühn, T., Mortensen, L. M., Nilsson, P. M., Overvad, K., Pala, V., Palli, D., Panico, S., Quirós, J. R., Rodriguez-Barranco, M., Rolandsson, O., Sacerdote, C., Scalbert, A., Slimani, N., Spijkerman, A. M., Tjonneland, A., Tormo, M. J., Tumino, R., van der A, D. L., van der Schouw, Y. T., Langenberg, C., Riboli, E., and Wareham, N. J. (2016) Association of plasma phospholipid n-3 and n-6 polyunsaturated fatty acids with type 2 diabetes: the EPIC-InterAct Case-Cohort Study. PLoS Med. 13, e1002094
31. Molendi-Coste, O., Legry, V., and Leclercq, I. A. (2011) Why and how meet n-3 PUFA dietary recommendations? Gastroenterol. Res. Pract. 2011, 364040
32. Steffen, B. T., Steffen, L. M., Tracy, R., Siscovick, D., Hanson, N. Q., Nettleton, J., and Tsai, M. Y. (2012) Obesity modifies the association between plasma phospholipid polyunsaturated fatty acids and markers of inflammation: the Multi-Ethnic Study of Atherosclerosis. Int. J. Obes. 36, 797–804
33. Cho, J. S., Baek, S. H., Kim, J. Y., Lee, J. H., and Kim, O. Y. (2014) Serum phospholipid monounsaturated fatty acid composition and D-9-desaturase activity are associated with early alteration of fasting glycemic status. Nutr. Res. 34, 733–741
34. Netto, B. D., Bettini, S. C., Clemente, A. P., Ferreira, J. P., Boritza, K., Souza, Sde. F., Von der Heyde, M. E., Earthman, C. P., and Dâmaso, A. R. (2015) Roux-en-Y gastric bypass decreases pro-inflammatory and thrombotic biomarkers in individuals with extreme obesity. Obes. Surg. 25, 1010–1018
35. Hubbard, B., Doege, H., Punreddy, S., Wu, H., Huang, X., Kaushik, V. K., Mozell, R. L., Byrnes, J. J., Stricker-Krongrad, A., Chou, C. J., Tartaglia, L. A., Lodish, H. F., Stahl, A., and Gimeno, R. E. (2006) Mice deleted for fatty acid transport protein 5 have defective bile acid conjugation and are protected from obesity. Gastroenterology 130, 1259–1269
36. Doege, H., Baillie, R. A., Ortegon, A. M., Tsang, B., Wu, Q., Punreddy, S., Hirsch, D., Watson, N., Gimeno, R. E., and Stahl, A. (2006) Targeted deletion of FATP5 reveals multiple functions in liver metabolism: alterations in hepatic lipid homeostasis. Gastroenterology 130, 1245–1258
37. Kawamata, Y., Fujii, R., Hosoya, M., Harada, M., Yoshida, H., Miwa, M., Fukusumi, S., Habata, Y., Itoh, T., Shintani, Y., Hinuma, S., Fujisawa, Y., and Fujino, M. (2003) A G protein-coupled receptor responsive to bile acids. J. Biol. Chem. 278, 9435–9440
38. Guo, C., Xie, S., Chi, Z., Zhang, J., Liu, Y., Zhang, L., Zheng, M., Zhang, X., Xia, D., Ke, Y., Lu, L., and Wang, D. (2016) Bile acids control inflammation and metabolic disorder through inhibition of NLRP3 inflammasome. Immunity 45, 802–816
39. Nausheen, S., Shah, I. H., Pezeshki, A., Sigalet, D. L., and Chelikani, P. K. (2013) Effects of sleeve gastrectomy and ileal transposition, alone and in combination, on food intake, body weight, gut hormones, and glucose metabolism in rats. Am. J. Physiol. Endocrinol. Metab. 305, E507–E518
40. Kashihara, H., Shimada, M., Kurita, N., Sato, H., Yoshikawa, K., Higashijima, J., Chikakiyo, M., Nishi, M., and Takasu, C. (2015) Duodenal-jejunal bypass improves diabetes and liver steatosis via enhanced glucagon-like peptide-1 elicited by bile acids. J. Gastroenterol. Hepatol. 30, 308–315
41. Shao, Y., Yuan, G., Zhang, J., and Guo, X. (2015) Liraglutide reduces lipogenetic signals in visceral adipose of db/db mice with AMPK activation and Akt suppression. Drug Des. Devel. Ther. 9, 1177–1184
42. Decara, J., Arrabal, S., Beiroa, D., Rivera, P., Vargas, A., Serrano, A., Pavón, F. J., Ballesteros, J., Dieguez, C., Nogueiras, R., Rodríguez de Fonseca, F., and Suárez, J. (2016) Antiobesity efficacy of GLP-1 receptor agonist lir-aglutide is associated with peripheral tissue-specific modulation of lipid metabolic regulators. Biofactors 42, 600–611
43. Yabe, D., and Seino, Y. (2011) Two incretin hormones GLP-1 and GIP: comparison of their actions in insulin secretion and b cell preservation. Prog. Biophys. Mol. Biol. 107, 248–256
44. Hao, Z., Mumphrey, M. B., Townsend, R. L., Morrison, C. D., Münzberg, H., Ye, J., and Berthoud, H.-R. (2016) Body composition, food intake, and energy expenditure in a murine model of Roux-en-Y gastric bypass surgery. Obes. Surg. 26, 2173–2182
45. Hao, Z., Zhao, Z., Berthoud, H. R., and Ye, J. (2013) Development and verification of a mouse model for Roux-en-Y gastric bypass surgery with a small gastric pouch. PLoS One 8, e52922
46. Watanabe, M., Houten, S. M., Mataki, C., Christoffolete, M. A., Kim, B. W., Sato, H., Messaddeq, N., Harney, J. W., Ezaki, O., Kodama, T., Schoonjans, K., Bianco, A. C., and Auwerx, J. (2006) Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 439, 484–489
47. Simonen, M., Dali-Youcef, N., Kaminska, D., Venesmaa, S., Käkelä, P., Pääkkönen, M., Hallikainen, M., Kolehmainen, M., Uusitupa, M., Moilanen, L., Laakso, M., Gylling, H., Patti, M. E., Auwerx, J., and Pihlajamäki, J. (2012) Conjugated bile acids associate with altered rates of glucose and lipid oxidation after Roux-en-Y gastric bypass. Obes. Surg. 22, 1473–1480