Liver MicroRNA-291b-3p promotes hepatic lipogenesis through negative regulation of adenosine 5′-monophosphate (AMP)-activated protein kinase α1

Journal of Biological Chemistry

Volumn 291, Issue 20, 2016, Pages 10625-10634

  Meng, Xiangyu ^a,b   Guo, Jun ^a,b   Fang, Weiwei ^a   Dou, Lin ^a   Li, Meng ^a   Huang, Xiuqing ^a   Zhou, Shutong ^a   Man, Yong ^a   Tang, Weiqing ^a,c   Yu, Liqing ^c   Li, Jian ^a  

^a BEIJING HOSPITAL   (China)

^b INSTITUTE OF BIOPHYSICS   (China)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME ACTIVITY; FATTY ACIDS; GENE EXPRESSION;

ACTIVATED PROTEINS; AMP-ACTIVATED PROTEIN KINASE; FATTY ACID SYNTHASE; FATTY LIVER DISEASE; LIPID ACCUMULATIONS; LIPID METABOLISMS; STEROL REGULATORY ELEMENT-BINDING PROTEINS; THERAPEUTIC POTENTIALS;

MAMMALS;

FATTY ACID SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIPID; METFORMIN; MICRORNA; OLEIC ACID; PALMITIC ACID; PROTEIN AMPKALPHA1; PROTEIN MIR 291B 3P; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; AMPK ALPHA1 SUBUNIT, MOUSE; FAT INTAKE; MIRN-291 MICRORNA, MOUSE; SREBF1 PROTEIN, MOUSE;

ADENOVIRIDAE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FATTY LIVER; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; IN VITRO STUDY; LIPID ANALYSIS; LIPID DIET; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID STORAGE; LIPOGENESIS; LOSS OF FUNCTION MUTATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; WILD TYPE MOUSE; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; CHEMICALLY INDUCED; DRUG EFFECTS; ENZYME ACTIVATION; EXPERIMENTAL DIABETES MELLITUS; FAT INTAKE; GENETICS; LIVER; METABOLISM; PATHOLOGY; PHARMACOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIETARY FATS; ENZYME ACTIVATION; FATTY ACID SYNTHASE, TYPE I; FATTY LIVER; LIPOGENESIS; LIVER; METFORMIN; MICE; MICRORNAS; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 84969264034     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.713768     Document Type: Article

References (50)

1. Younossi, Z. M., Stepanova, M., Afendy, M., Fang, Y., Younossi, Y., Mir, H., and Srishord, M. (2011) Changes in the prevalence of the most common causes of chronic liver diseases in the United States from 1988 to 2008. Clin. Gastroenterol. Hepatol. 9, 524-530
2. Ajmal, M. R., Yaccha, M., Malik, M. A., Rabbani, M. U., Ahmad, I., Isalm, N., and Abdali, N. (2014) Prevalence of nonalcoholic fatty liver disease (NAFLD) in patients of cardiovascular diseases and its association with hs-CRP and TNF-alpha. Indian Heart J. 66, 574-579
3. Targher, G., Bertolini, L., Poli, F., Rodella, S., Scala, L., Tessari, R., Zenari, L., and Falezza, G. (2005) Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes 54, 3541-3546
4. Adams, L. A., Lymp, J. F., St Sauver, J., Sanderson, S. O., Lindor, K. D., Feldstein, A., and Angulo, P. (2005) The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 129, 113-121
5. Harrison, S. A., Torgerson, S., and Hayashi, P. H. (2003) The natural history of nonalcoholic fatty liver disease: a clinical histopathological study. Am. J. Gastroenterol. 98, 2042-2047
6. Foretz, M., Carling, D., Guichard, C., Ferré, P., and Foufelle, F. (1998) AMP-activated protein kinase inhibits the glucose-activated expression of fatty acid synthase gene in rat hepatocytes. J. Biol. Chem. 273, 14767-14771
7. An, Z., Wang, H., Song, P., Zhang, M., Geng, X., and Zou, M. H. (2007) Nicotine-induced activation of AMP-activated protein kinase inhibits fatty acid synthase in 3T3L1 adipocytes: a role for oxidant stress. J. Biol. Chem. 282, 26793-26801
8. Zhou, W., Han, W. F., Landree, L. E., Thupari, J. N., Pinn, M. L., Bililign, T., Kim, E. K., Vadlamudi, A., Medghalchi, S. M., El Meskini, R., Ronnett, G. V., Townsend, C. A., and Kuhajda, F. P. (2007) Fatty acid synthase inhibition activates AMP-activated protein kinase in SKOV3 human ovarian cancer cells. Cancer Res. 67, 2964-2971
9. Stapleton, D., Mitchelhill, K. I., Gao, G., Widmer, J., Michell, B. J., Teh, T., House, C. M., Fernandez, C. S., Cox, T., Witters, L. A., and Kemp, B. E. (1996) Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271, 611-614
10. Chen, Z., Heierhorst, J., Mann, R. J., Mitchelhill, K. I., Michell, B. J., Witters, L. A., Lynch, G. S., Kemp, B. E., and Stapleton, D. (1999) Expression of the AMP-activated protein kinase β1 and β2 subunits in skeletal muscle. FEBS Lett. 460, 343-348
11. Cheung, P. C., Salt, I. P., Davies, S. P., Hardie, D. G., and Carling, D. (2000) Characterization of AMP-activated protein kinase γ-subunit isoforms and their role in AMP binding. Biochem. J. 346, 659-669
12. Tangeman, L., Wyatt, C. N., and Brown, T. L. (2012) Knockdown of AMPactivated protein kinase α1 and α2 catalytic subunits. J. RNAi. Gene. Silencing 8, 470-478
13. Li, Y., Xu, S., Mihaylova, M. M., Zheng, B., Hou, X., Jiang, B., Park, O., Luo, Z., Lefai, E., Shyy, J. Y., Gao, B., Wierzbicki, M., Verbeuren, T. J., Shaw, R. J., Cohen, R. A., and Zang, M. (2011) AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in dietinduced insulin-resistant mice. Cell Metab. 13, 376-388
14. Horton, J. D., Goldstein, J. L., and Brown, M. S. (2002) SREBPs: transcriptional mediators of lipid homeostasis. Cold Spring Harb. Symp. Quant. Biol. 67, 491-498
15. Kong, Y., and Han, J. H. (2005) MicroRNA: biological and computational perspective. Genomics, Proteomics Bioinformatics 3, 62-72
16. Lee, R. C., Feinbaum, R. L., and Ambros, V. (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854
17. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
18. Xiao, F., Yu, J., Liu, B., Guo, Y., Li, K., Deng, J., Zhang, J., Wang, C., Chen, S., Du, Y., Lu, Y., Xiao, Y., Zhang, Z., and Guo, F. (2014) A novel function of microRNA 130a-3p in hepatic insulin sensitivity and liver steatosis. Diabetes 63, 2631-2642
19. Ng, R., Wu, H., Xiao, H., Chen, X., Willenbring, H., Steer, C. J., and Song, G. (2014) Inhibition of microRNA-24 expression in liver prevents hepatic lipid accumulation and hyperlipidemia. Hepatology 60, 554-564
20. Soh, J., Iqbal, J., Queiroz, J., Fernandez-Hernando, C., and Hussain, M. M. (2013) MicroRNA-30c reduces hyperlipidemia and atherosclerosis in mice by decreasing lipid synthesis and lipoprotein secretion. Nat. Med. 19, 892-900
21. Ramírez, C. M., Goedeke, L., Rotllan, N., Yoon, J. H., Cirera-Salinas, D., Mattison, J. A., Suárez, Y., de Cabo, R., Gorospe, M., and Fernández-Hernando, C. (2013) MicroRNA 33 regulates glucose metabolism. Mol. Cell. Biol. 33, 2891-2902
22. Wen, J., and Friedman, J. R. (2012) miR-122 regulates hepatic lipid metabolism and tumor suppression. J. Clin. Invest. 122, 2773-2776
23. Guo, J., Li, M., Meng, X., Sui, J., Dou, L., Tang, W., Huang, X., Man, Y., Wang, S., and Li, J. (2014) MiR-291b-3p induces apoptosis in liver cell line NCTC1469 by reducing the level of RNA-binding protein HuR. Cell. Physiol. Biochem. 33, 810-822
24. Kaspi, H., Chapnik, E., Levy, M., Beck, G., Hornstein, E., and Soen, Y. (2013) Brief report: miR-290-295 regulate embryonic stem cell differentiation propensities by repressing Pax6. Stem cells 31, 2266-2272
25. Lichner, Z., Páll, E., Kerekes, A., Pállinger, E., Maraghechi, P., Bosze, Z., and Gócza, E. (2011) The miR-290-295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells. Differentiation 81, 11-24
26. Zovoilis, A., Smorag, L., Pantazi, A., and Engel, W. (2009) Members of the miR-290 cluster modulate in vitro differentiation of mouse embryonic stem cells. Differentiation. 78, 69-78
27. Lee, K. H., Song, J. L., Park, E. S., Ju, J., Kim, H. Y., and Park, K. Y. (2015) Anti-obesity effects of starter fermented Kimchi on 3T3-L1 adipocytes. Prev. Nutr. Food. Sci. 20, 298-302
28. Kleiner, D. E., Brunt, E. M., Van Natta, M., Behling, C., Contos, M. J., Cummings, O. W., Ferrell, L. D., Liu, Y. C., Torbenson, M. S., Unalp-Arida, A., Yeh, M., McCullough, A. J., Sanyal, A. J., and Nonalcoholic Steatohepatitis Clinical Research, N. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41, 1313-1321
29. Ricchi, M., Odoardi, M. R., Carulli, L., Anzivino, C., Ballestri, S., Pinetti, A., Fantoni, L. I., Marra, F., Bertolotti, M., Banni, S., Lonardo, A., Carulli, N., and Loria, P. (2009) Differential effect of oleic and palmitic acid on lipid accumulation and apoptosis in cultured hepatocytes. J. Gastroenterol. Hepatol. 24, 830-840
30. Hsu, S. H., Wang, B., Kota, J., Yu, J., Costinean, S., Kutay, H., Yu, L., Bai, S., La Perle, K., Chivukula, R. R., Mao, H., Wei, M., Clark, K. R., Mendell, J. R., Caligiuri, M. A., Jacob, S. T., Mendell, J. T., and Ghoshal, K. (2012) Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J. Clin. Invest. 122, 2871-2883
31. Rottiers, V., Najafi-Shoushtari, S. H., Kristo, F., Gurumurthy, S., Zhong, L., Li, Y., Cohen, D. E., Gerszten, R. E., Bardeesy, N., Mostoslavsky, R., and Näär, A. M. (2011) MicroRNAs in metabolism and metabolic diseases. Cold Spring Harb. Symp. Quant. Biol. 76, 225-233
32. Chu, B., Wu, T., Miao, L., Mei, Y., and Wu, M. (2015) MiR-181a regulates lipid metabolism via IDH1. Sci. Rep. 5, 8801
33. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M., Lin, C., Socci, N. D., Hermida, L., Fulci, V., Chiaretti, S., Foà, R., Schliwka, J., Fuchs, U., Novosel, A., Müller, R. U., Schermer, B., Bissels, U., Inman, J., Phan, Q., Chien, M., Weir, D. B., Choksi, R., De Vita, G., Frezzetti, D., Trompeter, H. I., Hornung, V., Teng, G., Hartmann, G., Palkovits, M., Di Lauro, R., Wernet, P., Macino, G., Rogler, C. E., Nagle, J. W., Ju, J., Papavasiliou, F. N., Benzing, T., Lichter, P., Tam, W., Brownstein, M. J., Bosio, A., Borkhardt, A., Russo, J. J., Sander, C., Zavolan, M., and Tuschl, T. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401-1414
34. Medeiros, L. A., Dennis, L. M., Gill, M. E., Houbaviy, H., Markoulaki, S., Fu, D., White, A. C., Kirak, O., Sharp, P. A., Page, D. C., and Jaenisch, R. (2011) Mir-290-295 deficiency in mice results in partially penetrant embryonic lethality and germ cell defects. Proc. Natl. Acad. Sci. U.S.A. 108, 14163-14168
35. Sinkkonen, L., Hugenschmidt, T., Berninger, P., Gaidatzis, D., Mohn, F., Artus-Revel, C. G., Zavolan, M., Svoboda, P., and Filipowicz, W. (2008) MicroRNAs control de novo DNA methylation through regulation of transcriptional repressors in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 15, 259-267
36. Wang, Y., Baskerville, S., Shenoy, A., Babiarz, J. E., Baehner, L., and Blelloch, R. (2008) Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat. Genet. 40, 1478-1483
37. Zheng, G. X., Ravi, A., Calabrese, J. M., Medeiros, L. A., Kirak, O., Dennis, L. M., Jaenisch, R., Burge, C. B., and Sharp, P. A. (2011) A latent prosurvival function for the mir-290-295 cluster in mouse embryonic stem cells. PLoS Genet. 7, e1002054
38. Lüningschröor, P., Stöcker, B., Kaltschmidt, B., and Kaltschmidt, C. (2012) miR-290 cluster modulates pluripotency by repressing canonical NF-κB signaling. Stem cells. 30, 655-664
39. Cao, Y., Guo, W. T., Tian, S., He, X., Wang, X. W., Liu, X., Gu, K. L., Ma, X., Huang, D., Hu, L., Cai, Y., Zhang, H., Wang, Y., and Gao, P. (2015) miR-290/371-Mbd2-Myc circuit regulates glycolytic metabolism to promote pluripotency. EMBO J. 34, 609-623
40. Hu, M., Wang, F., Li, X., Rogers, C. Q., Liang, X., Finck, B. N., Mitra, M. S., Zhang, R., Mitchell, D. A., and You, M. (2012) Regulation of hepatic lipin-1 by ethanol: role of AMP-activated protein kinase/sterol regulatory element-binding protein 1 signaling in mice. Hepatology 55, 437-446
41. Shimano, H., Horton, J. D., Hammer, R. E., Shimomura, I., Brown, M. S., and Goldstein, J. L. (1996) Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a. J. Clin. Invest. 98, 1575-1584
42. Yang, J., Craddock, L., Hong, S., and Liu, Z. M. (2009) AMP-activated protein kinase suppresses LXR-dependent sterol regulatory elementbinding protein-1c transcription in rat hepatoma McA-RH7777 cells. J. Cell. Biochem. 106, 414-426
43. Horton, J. D., Goldstein, J. L., and Brown, M. S. (2002) SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 109, 1125-1131
44. Cho, K., Kim, S. J., Park, S. H., Kim, S., and Park, T. (2009) Protective effect of Codonopsis lanceolata root extract against alcoholic fatty liver in the rat. J. Med. Food. 12, 1293-1301
45. Ha, J., Daniel, S., Broyles, S. S., and Kim, K. H. (1994) Critical phosphorylation sites for acetyl-CoA carboxylase activity. J. Biol. Chem. 269, 22162-22168
46. Aljada, A., and Mousa, S. A. (2012) Metformin and neoplasia: implications and indications. Pharmacol. Therap. 133, 108-115
47. Ford, R. J., Fullerton, M. D., Pinkosky, S. L., Day, E. A., Scott, J. W., Oakhill, J. S., Bujak, A. L., Smith, B. K., Crane, J. D., Blümer, R. M., Marcinko, K., Kemp, B. E., Gerstein, H. C., and Steinberg, G. R. (2015) Metformin and salicylate synergistically activate liver AMPK, inhibit lipogenesis and improve insulin sensitivity. Biochem. J. 468, 125-132
48. Nangia-Makker, P., Yu, Y., Vasudevan, A., Farhana, L., Rajendra, S. G., Levi, E., and Majumdar, A. P. (2014) Metformin: a potential therapeutic agent for recurrent colon cancer. PLoS ONE 9, e84369
49. Bao, B., Wang, Z., Ali, S., Ahmad, A., Azmi, A. S., Sarkar, S. H., Banerjee, S., Kong, D., Li, Y., Thakur, S., and Sarkar, F. H. (2012) Metformin inhibits cell proliferation, migration and invasion by attenuating CSC function mediated by deregulating miRNAs in pancreatic cancer cells. Cancer Prev. Res. 5, 355-364
50. Zaiss, A. K., Liu, Q., Bowen, G. P., Wong, N. C., Bartlett, J. S., and Muruve, D. A. (2002) Differential activation of innate immune responses by adenovirus and adeno-associated virus vectors. J. Virol. 76, 4580-4590