MicroRNA 34a inhibits beige and brown fat formation in obesity in part by suppressing adipocyte fibroblast growth factor 21 signaling and SIRT1 function

Molecular and Cellular Biology

Volumn 34, Issue 22, 2014, Pages 4130-4142

  Fu, Ting ^a   Seok, Sunmi ^a   Choi, Sunge ^a   Huang, Zhang ^a   Suino Powell, Kelly ^b   Eric Xu, H ^b   Kemper, Byron ^a   Kemper, Jongsook Kim ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CD37 ANTIGEN; FIBROBLAST GROWTH FACTOR 21; LENTIVIRUS VECTOR; MICRORNA 34A; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SIRTUIN 1; UNCOUPLING PROTEIN 1; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 1; MICRORNA; MIRN34 MICRORNA, MOUSE; SIRT1 PROTEIN, MOUSE;

ADIPOSE TISSUE; ARTICLE; BAGG ALBINO MOUSE; BEIGE ADIPOSE TISSUE; BROWN ADIPOSE TISSUE; C57BL 6 MOUSE; CONTROLLED STUDY; DIET; DOWN REGULATION; GENE DOSAGE; INTRAABDOMINAL FAT; MALE; MOUSE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WHITE ADIPOSE TISSUE; 3T3 CELL LINE; ANIMAL; C57BL MOUSE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY;

3T3-L1 CELLS; ADIPOSE TISSUE, BROWN; ADIPOSITY; ANIMALS; DOWN-REGULATION; FIBROBLAST GROWTH FACTORS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICRORNAS; OBESITY; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 1; SIGNAL TRANSDUCTION; SIRTUIN 1;

EID: 84908868680     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00596-14     Document Type: Article

References (44)

1. Rosen ED, Spiegelman BM. 2006. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444:847-853. http://dx.doi.org/10.1038/nature05483.
2. Cannon B, Nedergaard J. 2004. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84:277-359. http://dx.doi.org/10.1152/physrev.00015.2003.
3. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR. 2009. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 360:1509-1517. http://dx.doi.org/10.1056/NEJMoa0810780.
4. Kajimura S, Seale P, Spiegelman BM. 2010. Transcriptional control of brown fat development. Cell Metab. 11:257-262. http://dx.doi.org/10.1016/j.cmet.2010.03.005.
5. Harms M, Seale P. 2013. Brown and beige fat: development, function and therapeutic potential. Nat. Med. 19:1252-1263. http://dx.doi.org/10.1038/nm.3361.
6. Wu J, Bostrom P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerback S, Schrauwen P, Spiegelman BM. 2012. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150:366-376. http://dx.doi.org/10.1016/j.cell.2012.05.016.
7. Vijgen GH, Bouvy ND, Teule GJ, Brans B, Schrauwen P, van Marken Lichtenbelt WD. 2011. Brown adipose tissue in morbidly obese subjects. PLoS One 6:e17247. http://dx.doi.org/10.1371/journal.pone.0017247.
8. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J, Cohen P, Cinti S, Spiegelman BM. 2011. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J. Clin. Invest. 121:96-105. http://dx.doi.org/10.1172/JCI44271.
9. Ohno H, Shinoda K, Spiegelman BM, Kajimura S. 2012. PPARgamma agonists induce a white-to-brown fat conversion through stabilization of PRDM16 protein. Cell Metab. 15:395-404. http://dx.doi.org/10.1016/j.cmet.2012.01.019.
10. Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Hojlund K, Gygi SP, Spiegelman BM. 2012. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:463-468. http://dx.doi.org/10.1038/nature10777.
11. Qiang L, Wang L, Kon N, Zhao W, Lee S, Zhang Y, Rosenbaum M, Zhao Y, Gu W, Farmer SR, Accili D. 2012. Brown remodeling of white adipose tissue by SirT1-dependent deacetylation of Ppargamma. Cell 150: 620-632. http://dx.doi.org/10.1016/j.cell.2012.06.027.
12. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V, Li Y, Goetz R, Mohammadi M, Esser V, Elmquist JK, Gerard RD, Burgess SC, Hammer RE, Mangelsdorf DJ, Kliewer SA. 2007. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 5:415-425. http://dx.doi.org/10.1016/j.cmet.2007.05.003.
13. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E. 2007. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab. 5:426-437. http://dx.doi.org/10.1016/j.cmet.2007.05.002.
14. Fisher FM, Kleiner S, Douris N, Fox EC, Mepani RJ, Verdeguer F, Wu J, Kharitonenkov A, Flier JS, Maratos-Flier E, Spiegelman BM. 2012. FGF21 regulates PGC-1alpha and browning of white adipose tissues in adaptive thermogenesis. Genes Dev. 26:271-281. http://dx.doi.org/10.1101/gad.177857.111.
15. Dutchak PA, Katafuchi T, Bookout AL, Choi JH, Yu RT, Mangelsdorf DJ, Kliewer SA. 2012. Fibroblast growth factor-21 regulates PPARgamma activity and the antidiabetic actions of thiazolidinediones. Cell 148:556-567. http://dx.doi.org/10.1016/j.cell.2011.11.062.
16. Canto C, Auwerx J. 2012. Cell biology. FGF21 takes a fat bite. Science 336:675-676. http://dx.doi.org/10.1126/science.1222646.
17. Lee P, Linderman JD, Smith S, Brychta RJ, Wang J, Idelson C, Perron RM, Werner CD, Phan GQ, Kammula US, Kebebew E, Pacak K, Chen KY, Celi FS. 2014. Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metab. 19:302-309. http://dx.doi.org/10.1016/j.cmet.2013.12.017.
18. Trajkovski M, Ahmed K, Esau CC, Stoffel M. 2012. MyomiR-133 regulates brown fat differentiation through Prdm16. Nat. Cell Biol. 14:1330-1335. http://dx.doi.org/10.1038/ncb2612.
19. Yin H, Pasut A, Soleimani VD, Bentzinger CF, Antoun G, Thorn S, Seale P, Fernando P, van Ijcken W, Grosveld F, Dekemp RA, Boushel R, Harper ME, Rudnicki MA. 2013. MicroRNA-133 controls brown adipose determination in skeletal muscle satellite cells by targeting Prdm16. Cell Metab. 17:210-224. http://dx.doi.org/10.1016/j.cmet.2013.01.004.
20. Chen Y, Siegel F, Kipschull S, Haas B, Frohlich H, Meister G, Pfeifer A. 2013. miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nat. Commun. 4:1769. http://dx.doi.org/10.1038/ncomms2742.
21. Ortega FJ, Moreno-Navarrete JM, Pardo G, Sabater M, Hummel M, Ferrer A, Rodriguez-Hermosa JI, Ruiz B, Ricart W, Peral B, Fernandez-Real JM. 2010. MiRNA expression profile of human subcutaneous adipose and during adipocyte differentiation. PLoS One 5:e9022. http://dx.doi.org/10.1371/journal.pone.0009022.
22. Fu T, Choi SE, Kim DH, Seok S, Suino-Powell KM, Xu HE, Kemper JK. 2012. Aberrantly elevated microRNA-34a in obesity attenuates hepatic responses to FGF19 by targeting a membrane coreceptor beta-Klotho. Proc. Natl. Acad. Sci. U. S. A. 109:16137-16142. http://dx.doi.org/10.1073/pnas.1205951109.
23. Choi SE, Fu T, Seok S, Kim DH, Yu E, Lee KW, Kang Y, Li X, Kemper B, Kemper JK. 2013. Elevated microRNA-34a in obesity reduces NAD levels and SIRT1 activity by directly targeting NAMPT. Aging Cell 12: 1062-1072. http://dx.doi.org/10.1111/acel.12135.
24. Kemper JK, Xiao Z, Ponugoti B, Miao J, Fang S, Kanamaluru D, Tsang S, Wu S, Chiang CM, Veenstra TD. 2009. FXR acetylation is normally dynamically regulated by p300 and SIRT1 but constitutively elevated in metabolic disease states. Cell Metab. 10:392-404. http://dx.doi.org/10.1016/j.cmet.2009.09.009.
25. Lee J, Padhye A, Sharma A, Song G, Miao J, Mo YY, Wang L, Kemper JK. 2010. A pathway involving farnesoid X receptor and small heterodimer partner positively regulates hepatic sirtuin 1 levels via microRNA-34a inhibition. J. Biol. Chem. 285:12604-12611. http://dx.doi.org/10.1074/jbc.M109.094524.
26. Villanueva CJ, Vergnes L, Wang J, Drew BG, Hong C, Tu Y, Hu Y, Peng X, Xu F, Saez E, Wroblewski K, Hevener AL, Reue K, Fong LG, Young SG, Tontonoz P. 2013. Adipose subtype-selective recruitment of TLE3 or Prdm16 by PPARgamma specifies lipid storage versus thermogenic gene programs. Cell Metab. 17:423-435. http://dx.doi.org/10.1016/j.cmet.2013.01.016.
27. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. 1988. Diet-induced type II diabetes in C57BL/6J mice. Diabetes 37:1163-1167.
28. Montgomery MK, Hallahan NL, Brown SH, Liu M, Mitchell TW, Cooney GJ, Turner N. 2013. Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia 56:1129-1139. http://dx.doi.org/10.1007/s00125-013-2846-8.
29. Wu J, Cohen P, Spiegelman BM. 2013. Adaptive thermogenesis in adipocytes: is beige the new brown? Genes Dev. 27:234-250. http://dx.doi.org/10.1101/gad.211649.112.
30. Kajimura S, Seale P, Tomaru T, Erdjument-Bromage H, Cooper MP, Ruas JL, Chin S, Tempst P, Lazar MA, Spiegelman BM. 2008. Regulation of the brown and white fat gene programs through a PRDM16/CtBP transcriptional complex. Genes Dev. 22:1397-1409. http://dx.doi.org/10.1101/gad.1666108.
31. Kurosu H, Choi M, Ogawa Y, Dickson AS, Goetz R, Eliseenkova AV, Mohammadi M, Rosenblatt KP, Kliewer SA, Kuro-o M. 2007. Tissuespecific expression of betaKlotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J. Biol. Chem. 282:26687-26695. http://dx.doi.org/10.1074/jbc.M704165200.
32. Fisher FM, Chui PC, Antonellis PJ, Bina HA, Kharitonenkov A, Flier JS, Maratos-Flier E. 2010. Obesity is a fibroblast growth factor 21 (FGF21)-resistant state. Diabetes 59:2781-2789. http://dx.doi.org/10.2337/db10-0193.
33. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839. http://dx.doi.org/10.1016/S0092-8674 (00)81410-5.
34. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. 2005. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434:113-118. http://dx.doi.org/10.1038/nature03354.
35. Chau MD, Gao J, Yang Q, Wu Z, Gromada J. 2010. Fibroblast growth factor 21 regulates energy metabolism by activating the AMPK-SIRT1-PGC-1alpha pathway. Proc. Natl. Acad. Sci. U. S. A. 107:12553-12558. http://dx.doi.org/10.1073/pnas.1006962107.
36. Choi SE, Kemper JK. 2013. Regulation of SIRT1 by microRNAs. Mol. Cells 36:385-392. http://dx.doi.org/10.1007/s10059-013-0297-1.
37. Mraz M, Bartlova M, Lacinova Z, Michalsky D, Kasalicky M, Haluzikova D, Matoulek M, Dostalova I, Humenanska V, Haluzik M. 2009. Serum concentrations and tissue expression of a novel endocrine regulator fibroblast growth factor-21 in patients with type 2 diabetes and obesity. Clin. Endocrinol. (Oxford) 71:369-375. http://dx.doi.org/10.1111/j.1365-2265.2008.03502.x.
38. Hale C, Chen MM, Stanislaus S, Chinookoswong N, Hager T, Wang M, Veniant MM, Xu J. 2012. Lack of overt FGF21 resistance in two mouse models of obesity and insulin resistance. Endocrinology 153:69-80. http://dx.doi.org/10.1210/en.2010-1262.
39. Diaz-Delfin J, Hondares E, Iglesias R, Giralt M, Caelles C, Villarroya F. 2012. TNF-alpha represses beta-Klotho expression and impairs FGF21 action in adipose cells: involvement of JNK1 in the FGF21 pathway. Endocrinology 153:4238-4245. http://dx.doi.org/10.1210/en.2012-1193.
40. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J. 2006. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127: 1109-1122. http://dx.doi.org/10.1016/j.cell.2006.11.013.
41. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J. 2009. AMPK regulates energy expenditure by modulating NAD+metabolism and SIRT1 activity. Nature 458: 1056-1060. http://dx.doi.org/10.1038/nature07813.
42. Frontini A, Cinti S. 2010. Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab. 11:253-256. http://dx.doi.org/10.1016/j.cmet.2010.03.004.
43. Lidell ME, Betz MJ, Dahlqvist Leinhard O, Heglind M, Elander L, Slawik M, Mussack T, Nilsson D, Romu T, Nuutila P, Virtanen KA, Beuschlein F, Persson A, Borga M, Enerback S. 2013. Evidence for two types of brown adipose tissue in humans. Nat. Med. 19:631-634. http://dx.doi.org/10.1038/nm.3017.
44. Despres JP, Lemieux I, Bergeron J, Pibarot P, Mathieu P, Larose E, Rodes-Cabau J, Bertrand OF, Poirier P. 2008. Abdominal obesity and the metabolic syndrome: contribution to global cardiometabolic risk. Arterioscler. Thromb. Vasc. Biol. 28:1039-1049. http://dx.doi.org/10.1161/ATVBAHA.107.159228.