An SREBP-responsive microRNA operon contributes to a regulatory loop for intracellular lipid homeostasis

Cell Metabolism

Volumn 18, Issue 1, 2013, Pages 51-61

  Jeon, Tae Il ^a,b   Esquejo, Ryan M ^a   Roqueta Rivera, Manuel ^a   Phelan, Peter E ^a   Moon, Young Ah ^c   Govindarajan, Subramaniam S ^a   Esau, Christine C ^d   Osborne, Timothy F ^a  

^a BURNHAM INSTITUTE   (United States)

^b Chonnam National University   (South Korea)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

^d REGULUS THERAPEUTICS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; EZETIMIBE; MEVINOLIN; MICRORNA; MICRORNA 182; STEROL REGULATORY ELEMENT BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DIET; EXPRESSION VECTOR; GENE EXPRESSION PROFILING; GENETIC REGULATION; GENETIC TRANSFECTION; HELA CELL; HOMEOSTASIS; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LIPID METABOLISM; LIPOGENESIS; LIVER; MOUSE; NONHUMAN; OPERON; PRIORITY JOURNAL; RNA ISOLATION;

ANIMALS; CELLS, CULTURED; F-BOX PROTEINS; GENES, REGULATOR; HOMEOSTASIS; LIPID METABOLISM; LIVER; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICRORNAS; MODELS, ANIMAL; OPERON; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; UBIQUITIN-PROTEIN LIGASES;

BACTERIA (MICROORGANISMS);

EID: 84879852051     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2013.06.010     Document Type: Article

References (47)

1. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
2. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
3. M.K. Bennett, Y.K. Seo, S. Datta, D.J. Shin, and T.F. Osborne Selective binding of sterol regulatory element-binding protein isoforms and co-regulatory proteins to promoters for lipid metabolic genes in liver J. Biol. Chem. 283 2008 15628 15637
4. M.S. Brown, and J.L. Goldstein A receptor-mediated pathway for cholesterol homeostasis Science 232 1986 34 47
5. M.S. Brown, and J.L. Goldstein A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood Proc. Natl. Acad. Sci. USA 96 1999 11041 11048
6. M.S. Brown, and J.L. Goldstein Cholesterol feedback: from Schoenheimer's bottle to Scap's MELADL J. Lipid Res. 50 Suppl 2009 S15 S27
7. C.H. Chien, Y.M. Sun, W.C. Chang, P.Y. Chiang-Hsieh, T.Y. Lee, W.C. Tsai, J.T. Horng, A.P. Tsou, and H.D. Huang Identifying transcriptional start sites of human microRNAs based on high-throughput sequencing data Nucleic Acids Res. 39 2011 9345 9356
8. K.A. Dooley, S. Millinder, and T.F. Osborne Sterol regulation of 3-hydroxy-3-methylglutaryl-coenzyme A synthase gene through a direct interaction between sterol regulatory element binding protein and the trimeric CCAAT-binding factor/nuclear factor Y J. Biol. Chem. 273 1998 1349 1356
9. C. Fernández-Hernando, and K.J. Moore MicroRNA modulation of cholesterol homeostasis Arterioscler. Thromb. Vasc. Biol. 31 2011 2378 2382
10. M.P. Gantier, C.E. McCoy, I. Rusinova, D. Saulep, D. Wang, D. Xu, A.T. Irving, M.A. Behlke, P.J. Hertzog, F. Mackay, and B.R. Williams Analysis of microRNA turnover in mammalian cells following Dicer1 ablation Nucleic Acids Res. 39 2011 5692 5703
11. I. Gerin, L.A. Clerbaux, O. Haumont, N. Lanthier, A.K. Das, C.F. Burant, I.A. Leclercq, O.A. MacDougald, and G.T. Bommer Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation J. Biol. Chem. 285 2010 33652 33661
12. J.L. Goldstein, and M.S. Brown Regulation of the mevalonate pathway Nature 343 1990 425 430
13. R.G. Gould Lipid metabolism and atherosclerosis Am. J. Med. 11 1951 209 227
14. T. Horie, K. Ono, M. Horiguchi, H. Nishi, T. Nakamura, K. Nagao, M. Kinoshita, Y. Kuwabara, H. Marusawa, and Y. Iwanaga MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo Proc. Natl. Acad. Sci. USA 107 2010 17321 17326
15. J.D. Horton, H. Shimano, R.L. Hamilton, M.S. Brown, and J.L. Goldstein Disruption of LDL receptor gene in transgenic SREBP-1a mice unmasks hyperlipidemia resulting from production of lipid-rich VLDL J. Clin. Invest. 103 1999 1067 1076
16. J.D. Horton, N.A. Shah, J.A. Warrington, N.N. Anderson, S.W. Park, M.S. Brown, and J.L. Goldstein Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes Proc. Natl. Acad. Sci. USA 100 2003 12027 12032
17. C. Huynh, M.F. Segura, A. Gaziel-Sovran, S. Menendez, F. Darvishian, L. Chiriboga, B. Levin, D. Meruelo, I. Osman, and J. Zavadil Efficient in vivo microRNA targeting of liver metastasis Oncogene 30 2011 1481 1488
18. F. Jacob, and J. Monod Genetic regulatory mechanisms in the synthesis of proteins J. Mol. Biol. 3 1961 318 356
19. T.I. Jeon, and T.F. Osborne SREBPs: metabolic integrators in physiology and metabolism Trends Endocrinol. Metab. 23 2012 65 72
20. D.M. Koepp, L.K. Schaefer, X. Ye, K. Keyomarsi, C. Chu, J.W. Harper, and S.J. Elledge Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase Science 294 2001 173 177
21. J. Krol, V. Busskamp, I. Markiewicz, M.B. Stadler, S. Ribi, J. Richter, J. Duebel, S. Bicker, H.J. Fehling, and D. Schübeler Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs Cell 141 2010 618 631
22. R.G. Langdon, and K. Bloch The effect of some dietary additions on the synthesis of cholesterol from acetate in vitro J. Biol. Chem. 202 1953 77 81
23. L. Liscum, K.L. Luskey, D.J. Chin, Y.K. Ho, J.L. Goldstein, and M.S. Brown Regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase and its mRNA in rat liver as studied with a monoclonal antibody and a cDNA probe J. Biol. Chem. 258 1983 8450 8455
24. T.J. Marquart, R.M. Allen, D.S. Ory, and A. Baldán miR-33 links SREBP-2 induction to repression of sterol transporters Proc. Natl. Acad. Sci. USA 107 2010 12228 12232
25. J. Monod, J.P. Changeux, and F. Jacob Allosteric proteins and cellular control systems J. Mol. Biol. 6 1963 306 329
26. J. Monod, J. Wyman, and J.P. Changeux On the Nature of Allosteric Transitions: A Plausible Model J. Mol. Biol. 12 1965 88 118
27. S.H. Najafi-Shoushtari, F. Kristo, Y. Li, T. Shioda, D.E. Cohen, R.E. Gerszten, and A.M. Näär MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis Science 328 2010 1566 1569
28. A.S. Nateri, L. Riera-Sans, C. Da Costa, and A. Behrens The ubiquitin ligase SCFFbw7 antagonizes apoptotic JNK signaling Science 303 2004 1374 1378
29. I. Onoyama, A. Suzuki, A. Matsumoto, K. Tomita, H. Katagiri, Y. Oike, K. Nakayama, and K.I. Nakayama Fbxw7 regulates lipid metabolism and cell fate decisions in the mouse liver J. Clin. Invest. 121 2011 342 354
30. T.F. Osborne, and P.J. Espenshade Evolutionary conservation and adaptation in the mechanism that regulates SREBP action: what a long, strange tRIP it's been Genes Dev. 23 2009 2578 2591
31. K.J. Rayner, Y. Suárez, A. Dávalos, S. Parathath, M.L. Fitzgerald, N. Tamehiro, E.A. Fisher, K.J. Moore, and C. Fernández- Hernando MiR-33 contributes to the regulation of cholesterol homeostasis Science 328 2010 1570 1573
32. B.D. Reed, A.E. Charos, A.M. Szekely, S.M. Weissman, and M. Snyder Genome-wide occupancy of SREBP1 and its partners NFY and SP1 reveals novel functional roles and combinatorial regulation of distinct classes of genes PLoS Genet. 4 2008 e1000133
33. V. Rottiers, S.H. Najafi-Shoushtari, F. Kristo, S. Gurumurthy, L. Zhong, Y. Li, D.E. Cohen, R.E. Gerszten, N. Bardeesy, R. Mostoslavsky, and A.M. Näär MicroRNAs in metabolism and metabolic diseases Cold Spring Harb. Symp. Quant. Biol. 76 2011 225 233
34. J. Sakai, A. Nohturfft, D. Cheng, Y.K. Ho, M.S. Brown, and J.L. Goldstein Identification of complexes between the COOH-terminal domains of sterol regulatory element-binding proteins (SREBPs) and SREBP cleavage-activating protein J. Biol. Chem. 272 1997 20213 20221
35. Y.K. Seo, H.K. Chong, A.M. Infante, S.S. Im, X. Xie, and T.F. Osborne Genome-wide analysis of SREBP-1 binding in mouse liver chromatin reveals a preference for promoter proximal binding to a new motif Proc. Natl. Acad. Sci. USA 106 2009 13765 13769
36. Y.K. Seo, T.I. Jeon, H.K. Chong, J. Biesinger, X. Xie, and T.F. Osborne Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy Cell Metab. 13 2011 367 375
37. N. Sever, T. Yang, M.S. Brown, J.L. Goldstein, and R.A. DeBose-Boyd Accelerated degradation of HMG CoA reductase mediated by binding of insig-1 to its sterol-sensing domain Mol. Cell 11 2003 25 33
38. Z. Sheng, H. Otani, M.S. Brown, and J.L. Goldstein Independent regulation of sterol regulatory element-binding proteins 1 and 2 in hamster liver Proc. Natl. Acad. Sci. USA 92 1995 935 938
39. E.M. Small, and E.N. Olson Pervasive roles of microRNAs in cardiovascular biology Nature 469 2011 336 342
40. A.B. Stittrich, C. Haftmann, E. Sgouroudis, A.A. Kühl, A.N. Hegazy, I. Panse, R. Riedel, M. Flossdorf, J. Dong, and F. Fuhrmann The microRNA miR-182 is induced by IL-2 and promotes clonal expansion of activated helper T lymphocytes Nat. Immunol. 11 2010 1057 1062
41. L.P. Sun, J. Seemann, J.L. Goldstein, and M.S. Brown Sterol-regulated transport of SREBPs from endoplasmic reticulum to Golgi: Insig renders sorting signal in Scap inaccessible to COPII proteins Proc. Natl. Acad. Sci. USA 104 2007 6519 6526
42. A. Sundqvist, M.T. Bengoechea-Alonso, X. Ye, V. Lukiyanchuk, J. Jin, J.W. Harper, and J. Ericsson Control of lipid metabolism by phosphorylation- dependent degradation of the SREBP family of transcription factors by SCF(Fbw7) Cell Metab. 1 2005 379 391
43. S. Xu, P.D. Witmer, S. Lumayag, B. Kovacs, and D. Valle MicroRNA (miRNA) transcriptome of mouse retina and identification of a sensory organ-specific miRNA cluster J. Biol. Chem. 282 2007 25053 25066
44. D. Yabe, M.S. Brown, and J.L. Goldstein Insig-2, a second endoplasmic reticulum protein that binds SCAP and blocks export of sterol regulatory element-binding proteins Proc. Natl. Acad. Sci. USA 99 2002 12753 12758
45. M. Yada, S. Hatakeyama, T. Kamura, M. Nishiyama, R. Tsunematsu, H. Imaki, N. Ishida, F. Okumura, K. Nakayama, and K.I. Nakayama Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7 EMBO J. 23 2004 2116 2125
46. T. Yang, P.J. Espenshade, M.E. Wright, D. Yabe, Y. Gong, R. Aebersold, J.L. Goldstein, and M.S. Brown Crucial step in cholesterol homeostasis: sterols promote binding of SCAP to INSIG-1, a membrane protein that facilitates retention of SREBPs in ER Cell 110 2002 489 500
47. C. Yokoyama, X. Wang, M.R. Briggs, A. Admon, J. Wu, X. Hua, J.L. Goldstein, and M.S. Brown SREBP-1, a basic-helix-loop-helix-zipper protein that controls transcription of the low density receptor gene Cell 75 1993 185 197