The beneficial effects of betaine on dysfunctional adipose tissue and N6-methyladenosine mRNA methylation requires the AMP-activated protein kinase α1 subunit

Journal of Nutritional Biochemistry

Volumn 26, Issue 12, 2015, Pages 1678-1684

  Zhou, Xihong ^a,b   Chen, Jingqing ^a   Chen, Jin ^a   Wu, Weiche ^a   Wang, Xinxia ^a   Wang, Yizhen ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Adipose tissue; AMP activated protein kinase; Betaine; Fatty acid oxidation; N6 methyladenosine methylation

Indexed keywords

6 N METHYLADENOSINE; ADIPOCYTOKINE; BETAINE; DRINKING WATER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA 1; MESSENGER RNA; UNCLASSIFIED DRUG; ADENOSINE; AMPK ALPHA1 SUBUNIT, MOUSE; GASTROINTESTINAL AGENT; INSULIN; N(6)-METHYLADENOSINE;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FATTY ACID OXIDATION; GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; LIPID DIET; LIPID METABOLISM; LIPID OXIDATION; LIPOLYSIS; LOW FAT DIET; MALE; MITOCHONDRIAL GENE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RNA METHYLATION; WEIGHT GAIN; ANALOGS AND DERIVATIVES; ANIMAL; BODY WEIGHT; C57BL MOUSE; CHEMISTRY; CYTOLOGY; DNA METHYLATION; GENETICS; GLUCOSE TOLERANCE TEST; KNOCKOUT MOUSE; METABOLISM; METHYLATION; PHOSPHORYLATION;

ADENOSINE; ADIPOCYTES; ADIPOSE TISSUE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BETAINE; BODY WEIGHT; DIET, HIGH-FAT; DNA METHYLATION; GASTROINTESTINAL AGENTS; GLUCOSE TOLERANCE TEST; INSULIN; LIPID METABOLISM; MALE; METHYLATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; RNA, MESSENGER;

EID: 84983132810     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.08.014     Document Type: Article

References (36)

1. Lewis J.R., Mohanty S.R. Nonalcoholic fatty liver disease: a review and update. Dig Dis Sci 2010, 55:560-578.
2. Jou J., Choi S.S., Diehl A.M. Mechanisms of disease progression in nonalcoholic fatty liver disease. Semin Liver Dis 2008, 28:370-379.
3. Tuncman G., Hirosumi J., Solinas G., Chang L., Karin M., Hotamisligil G.S. Functional in vivo interactions between JNK1 and JNK2 isoforms in obesity and insulin resistance. Proc Natl Acad Sci U S A 2006, 103:10741-10746.
4. Sanyal A.J. Mechanisms of disease: pathogenesis of nonalcoholic fatty liver disease. Nat Clin Pract Gastroenterol Hepatol 2005, 2:46-53.
5. Donnelly K.L., Smith C.I., Schwarzenberg S.J., Jessurun J., Boldt M.D., Parks E.J. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005, 115:1343-1351.
6. Ji C., Kaplowitz N. Betaine decreases hyperhomocysteinemia, endoplasmic reticulum stress, and liver injury in alcohol-fed mice. Gastroenterology 2003, 124:1488-1499.
7. Kharbanda K.K., Rogers D.D., Mailliard M.E., Siford G.L., Barak A.J., Beckenhauer H.C., et al. Role of elevated S-adenosylhomocysteine in rat hepatocyte apoptosis: protection by betaine. Biochem Pharmacol 2005, 70:1883-1890.
8. Wang L.J., Zhang H.W., Zhou J.Y., Liu Y., Yang Y., Chen X.L., et al. Betaine attenuates hepatic steatosis by reducing methylation of the MTTP promoter and elevating genomic methylation in mice fed a high-fat diet. J Nutr Biochem 2014, 25:329-336.
9. Wang Z., Yao T., Pini M., Zhou Z., Fantuzzi G., Song Z. Betaine improved adipose tissue function in mice fed a high-fat diet: a mechanism for hepatoprotective effect of betaine in nonalcoholic fatty liver disease. Am J Physiol Gastrointest Liver Physiol 2010, 298:G634-G642.
10. Dou X., Xia Y., Chen J., Qian Y., Li S., Zhang X., et al. Rectification of impaired adipose tissue methylation status and lipolytic response contributes to hepatoprotective effect of betaine in a mouse model of alcoholic liver disease. Br J Pharmacol 2014, 171:4073-4086.
11. Zhao X., Yang Y., Sun B.F., Shi Y., Yang X., Xiao W., et al. FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis. Cell Res 2014, 24:1403-1419.
12. Chen J., Zhou X., Wu W., Wang X., Wang Y. FTO-dependent function of N6-methyladenosine is involved in the hepatoprotective effects of betaine on adolescent mice. J Physiol Biochem 2015, 71:405-413.
13. Ceddia R.B. The role of AMP-activated protein kinase in regulating white adipose tissue metabolism. Mol Cell Endocrinol 2013, 366:194-203.
14. Daval M., Diot-Dupuy F., Bazin R., Hainault I., Viollet B., Vaulont S., et al. Anti-lipolytic action of AMP-activated protein kinase in rodent adipocytes. J Biol Chem 2005, 280:25250-25257.
15. Mulligan J.D., Gonzalez A.A., Stewart A.M., Carey H.V., Saupe K.W. Upregulation of AMPK during cold exposure occurs via distinct mechanisms in brown and white adipose tissue of the mouse. J Physiol 2007, 580:677-684.
16. Lihn A.S., Jessen N., Pedersen S.B., Lund S., Richelsen B. AICAR stimulates adiponectin and inhibits cytokines in adipose tissue. Biochem Biophys Res Commun 2004, 316:853-858.
17. Dahlhoff C., Worsch S., Sailer M., Hummel B.A., Fiamoncini J., Uebel K., et al. Methyl-donor supplementation in obese mice prevents the progression of NAFLD, activates AMPK and decreases acyl-carnitine levels. Mol Metab 2014, 3:565-580.
18. Song Z., Deaciuc I., Zhou Z., Song M., Chen T., Hill D., et al. Involvement of AMP-activated protein kinase in beneficial effects of betaine on high-sucrose diet-induced hepatic steatosis. Am J Physiol Gastrointest Liver Physiol 2007, 293:G894-G902.
19. Pitman R.T., Fong J.T., Billman P., Puri N. Knockdown of the fat mass and obesity gene disrupts cellular energy balance in a cell-type specific manner. PLoS One 2012, 7:e38444.
20. Jia G., Fu Y., Zhao X., Dai Q., Zheng G., Yang Y., et al. N6-methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nat Chem Biol 2011, 7:885-887.
21. Shan T., Liang X., Bi P., Kuang S. Myostatin knockout drives browning of white adipose tissue through activating the AMPK-PGC1alpha-Fndc5 pathway in muscle. FASEB J 2013, 27:1981-1989.
22. Cholewa J.M., Wyszczelska-Rokiel M., Glowacki R., Jakubowski H., Matthews T., Wood R., et al. Effects of betaine on body composition, performance, and homocysteine thiolactone. J Int Soc Sports Nutr 2013, 10:39-50.
23. Rojas-Cano M.L., Lara L., Lachica M., Aguilera J.F., Fernandez-Figares I. Influence of betaine and conjugated linoleic acid on development of carcass cuts of Iberian pigs growing from 20 to 50kg body weight. Meat Sci 2011, 88:525-530.
24. Cholewa J.M., Guimaraes-Ferreira L., Zanchi N.E. Effects of betaine on performance and body composition: a review of recent findings and potential mechanisms. Amino Acids 2014, 46:1785-1793.
25. Jang A., Kim D., Sung K.S., Jung S., Kim H.J., Jo C. The effect of dietary alpha-lipoic acid, betaine, l-carnitine, and swimming on the obesity of mice induced by a high-fat diet. Food Funct 2014, 5:1966-1974.
26. Pooya S., Blaise S., Moreno Garcia M., Giudicelli J., Alberto J.M., Gueant-Rodriguez R.M., et al. Methyl donor deficiency impairs fatty acid oxidation through PGC-1alpha hypomethylation and decreased ER-alpha, ERR-alpha, and HNF-4alpha in the rat liver. J Hepatol 2012, 57:344-351.
27. Gaidhu M.P., Perry R.L., Noor F., Ceddia R.B. Disruption of AMPKalpha1 signaling prevents AICAR-induced inhibition of AS160/TBC1D4 phosphorylation and glucose uptake in primary rat adipocytes. Mol Endocrinol 2010, 24:1434-1440.
28. Ruderman N.B., Saha A.K., Kraegen E.W. Minireview: malonyl CoA, AMP-activated protein kinase, and adiposity. Endocrinology 2003, 144:5166-5171.
29. Greenberg A.S., Obin M.S. Obesity and the role of adipose tissue in inflammation and metabolism. Am J Clin Nutr 2006, 83:461S-465S.
30. Ruderman N., Prentki M. AMP kinase and malonyl-CoA: targets for therapy of the metabolic syndrome. Nat Rev Drug Discov 2004, 3:340-351.
31. Meyer K.D., Saletore Y., Zumbo P., Elemento O., Mason C.E., Jaffrey S.R. Comprehensive analysis of mRNA methylation reveals enrichment in 3' UTRs and near stop codons. Cell 2012, 149:1635-1646.
32. Cui G.Z., Hong W., Zhang J., Li W.L., Feng Y., Liu Y.J., et al. Targeted gene engineering in Clostridium cellulolyticum H10 without methylation. J Microbiol Methods 2012, 89:201-208.
33. Church C., Moir L., McMurray F., Girard C., Banks G.T., Teboul L., et al. Overexpression of Fto leads to increased food intake and results in obesity. Nat Genet 2010, 42:1086-1092.
34. Fischer J., Koch L., Emmerling C., Vierkotten J., Peters T., Bruning J.C., et al. Inactivation of the Fto gene protects from obesity. Nature 2009, 458:894-898.
35. Olszewski P.K., Fredriksson R., Olszewska A.M., Stephansson O., Alsio J., Radomska K.J., et al. Hypothalamic FTO is associated with the regulation of energy intake not feeding reward. BMC Neurosci 2009, 10:129-140.
36. Bravard A., Lefai E., Meugnier E., Pesenti S., Disse E., Vouillarmet J., et al. FTO is increased in muscle during type 2 diabetes, and its overexpression in myotubes alters insulin signaling, enhances lipogenesis and ROS production, and induces mitochondrial dysfunction. Diabetes 2011, 60:258-268.