Reducing Smad3/ATF4 was essential for Sirt1 inhibiting ER stress-induced apoptosis in mice brown adipose tissue

Oncotarget

Volumn 8, Issue 6, 2017, Pages 9267-9279

  Liu, Zhenjiang ^a   Gu, Huihui ^a   Gan, Lu ^a   Xu, Yatao ^a   Feng, Fei ^a   Saeed, Muhammad ^a   Sun, Chao ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Apoptosis; ATF; Brown adipocytes; Sirt; Smad

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ADENOSINE TRIPHOSPHATE; CALCIUM ION; CASPASE 12; CASPASE 3; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MESSENGER RNA; PROTEIN BAX; PROTEIN BCL 2; SIRTUIN 1; SMAD3 PROTEIN; UNCOUPLING PROTEIN 1; ATF4 PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE; TUNICAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BROWN ADIPOCYTE; CALCIUM CELL LEVEL; CELL VIABILITY; COLD EXPOSURE; COLD TOLERANCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; INTERSCAPULAR BROWN ADIPOSE TISSUE; MALE; MITOCHONDRION; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THERMOGENESIS; TRANSCRIPTION REGULATION; ANIMAL; BINDING SITE; BROWN ADIPOSE TISSUE; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; GENETICS; HYPOTHERMIA; LIPID DIET; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RNA INTERFERENCE; TIME FACTOR; TRANSCRIPTION INITIATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ADIPOCYTES, BROWN; ADIPOSE TISSUE, BROWN; ANIMALS; APOPTOSIS; BINDING SITES; CELLS, CULTURED; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; HYPOTHERMIA; MALE; MICE, INBRED C57BL; OBESITY; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SIRTUIN 1; SMAD3 PROTEIN; THERMOGENESIS; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; TUNICAMYCIN;

EID: 85012014504     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14035     Document Type: Article

References (42)

1. Odgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature. 2005; 434:113-118.
2. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, Leid M, McBurney MW, Guarente L. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature. 2004; 429:771-776.
3. Yoshizaki T, Milne JC, Imamura T, Schenk S, Sonoda N, Babendure JL, Lu JC, Smith JJ, Jirousek MR, Olefsky JM. SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol Cell Biol. 2009; 29:1363-1374.
4. Mayoral R, Osborn O, McNelis J, Johnson AM, Oh DY, Izquierdo CL, Chung H, Li P, Traves PG, Bandyopadhyay G, Pessentheiner AR, Ofrecio JM, Cook JR, et al. Adipocyte SIRT1 knockout promotes PPARgamma activity, adipogenesis and insulin sensitivity in chronic-HFD and obesity. Mol Metab. 2015; 4:378-391.
5. Liu Z, Gan L, Liu G, Chen Y, Wu T, Feng F, Sun C. Sirt1 decreased adipose inflammation by interacting with Akt2 and inhibiting mTOR/S6K1 pathway in mice. J Lipid Res. 2016; 57:1373-1381.
6. Xu C, Bai B, Fan P, Cai Y, Huang B, Law IK, Liu L, Xu A, Tung C, Li X, Siu FM, Che CM, Vanhoutte PM, et al. Selective overexpression of human SIRT1 in adipose tissue enhances energy homeostasis and prevents the deterioration of insulin sensitivity with ageing in mice. Am J Transl Res. 2013; 5:412-426.
7. Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, Kaul MG, Tromsdorf UI, Weller H, Waurisch C, Eychmuller A, Gordts PL, Rinninger F, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011; 17:200-205.
8. Sidossis L, Kajimura S. Brown and beige fat in humans: thermogenic adipocytes that control energy and glucose homeostasis. J Clin Invest. 2015; 125:478-486.
9. Xu F, Lin B, Zheng X, Chen Z, Cao H, Xu H, Liang H, Weng J. GLP-1 receptor agonist promotes brown remodelling in mouse white adipose tissue through SIRT1. Diabetologia. 2016; 59:1059-1069.
10. Wang L, Teng R, Di L, Rogers H, Wu H, Kopp JB, Noguchi CT. PPARalpha and Sirt1 mediate erythropoietin action in increasing metabolic activity and browning of white adipocytes to protect against obesity and metabolic disorders. Diabetes. 2013; 62:4122-4131.
11. Fu T, Seok S, Choi S, Huang Z, Suino-Powell K, Xu HE, Kemper B, Kemper JK. MicroRNA 34a inhibits beige and brown fat formation in obesity in part by suppressing adipocyte fibroblast growth factor 21 signaling and SIRT1 function. Mol Cell Biol. 2014; 34:4130-4142.
12. Xu F, Zheng X, Lin B, Liang H, Cai M, Cao H, Ye J, Weng J. Diet-induced obesity and insulin resistance are associated with brown fat degeneration in SIRT1-deficient mice. Obesity (Silver Spring, Md). 2016; 24:634-642.
13. Boutant M, Joffraud M, Kulkarni SS, Garcia-Casarrubios E, Garcia-Roves PM, Ratajczak J, Fernandez-Marcos PJ, Valverde AM, Serrano M, Canto C. Mol Metab. Molecular metabolism. 2015; 4:118-131.
14. Boutant M, Canto C. SIRT1: A novel guardian of brown fat against metabolic damage. Obesity (Silver Spring, Md). 2016; 24:554.
15. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004; 306:457-461.
16. Li Y, Xu S, Giles A, Nakamura K, Lee JW, Hou X, Donmez G, Li J, Luo Z, Walsh K, Guarente L, Zang M. Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J. 2011; 25:1664-1679.
17. Contreras C, Gonzalez-Garcia I, Martinez-Sanchez N, Seoane-Collazo P, Jacas J, Morgan DA, Serra D, Gallego R, Gonzalez F, Casals N, Nogueiras R, Rahmouni K, Dieguez C, et al. Central ceramide-induced hypothalamic lipotoxicity and ER stress regulate energy balance. Cell reports. 2014; 9:366-377.
18. Okla M, Wang W, Kang I, Pashaj A, Carr T, Chung S. Activation of Toll-like receptor 4 (TLR4) attenuates adaptive thermogenesis via endoplasmic reticulum stress. J Biol Chem. 2015; 290:26476-26490.
19. Cnop M, Foufelle F, Velloso LA. Endoplasmic reticulum stress, obesity and diabetes. Trends Mol Med. 2012; 18:59-68.
20. van der Kallen CJ, van Greevenbroek MM, Stehouwer CD, Schalkwijk CG. Endoplasmic reticulum stress-induced apoptosis in the development of diabetes: is there a role for adipose tissue and liver? Apoptosi. 2009; 14:1424-1434.
21. Kozak LP. Brown fat and the myth of diet-induced thermogenesis. Cell Metab. 2010; 11:263-267.
22. Rajan S, Shankar K, Beg M, Varshney S, Gupta A, Srivastava A, Kumar D, Mishra RK, Hussain Z, Gayen JR, Gaikwad AN. Chronic hyperinsulinemia reduces insulin sensitivity and metabolic functions of brown adipocyte. J Endocrinol. 2016; 230:275-290.
23. Williams KW, Liu T, Kong X, Fukuda M, Deng Y, Berglund ED, Deng Z, Gao Y, Liu T, Sohn JW, Jia L, Fujikawa T, Kohno D, et al. Xbp1s in Pomc neurons connects ER stress with energy balance and glucose homeostasis. Cell Metab. 2014; 20:471-482.
24. Asada R, Kanemoto S, Matsuhisa K, Hino K, Cui M, Cui X, Kaneko M, Imaizumi K. IRE1alpha-XBP1 is a novel branch in the transcriptional regulation of Ucp1 in brown adipocytes. Sci Rep. 2015; 5:16580.
25. Gan L, Liu Z, Jin W, Zhou Z, Sun C. Foxc2 enhances proliferation and inhibits apoptosis through activating Akt/mTORC1 signaling pathway in mouse preadipocytes. J Lipid Res. 2015; 56:1471-1480.
26. Liu Z, Gan L, Chen Y, Luo D, Zhang Z, Cao W, Zhou Z, Lin X, Sun C. Mark4 promotes oxidative stress and inflammation via binding to PPARgamma and activating NF-kappaB pathway in mice adipocytes. Sci Rep. 2016; 6:21382.
27. Liu Z, Gan L, Zhou Z, Jin W, Sun C. SOCS3 promotes inflammation and apoptosis via inhibiting JAK2/STAT3 signaling pathway in 3T3-L1 adipocyte. Immunobiology. 2015; 220:947-953.
28. Gan L, Yan J, Liu Z, Feng M, Sun C. Adiponectin prevents reduction of lipid-induced mitochondrial biogenesis via AMPK/ACC2 pathway in chicken adipocyte. J Cell Biochem. 2015; 116:1090-1100.
29. Koga T, Suico MA, Shimasaki S, Watanabe E, Kai Y, Koyama K, Omachi K, Morino-Koga S, Sato T, Shuto T, Mori K, Hino S, Nakao M, et al. Endoplasmic Reticulum (ER) Stress Induces Sirtuin 1 (SIRT1) Expression via the PI3K-Akt-GSK3beta Signaling Pathway and Promotes Hepatocellular Injury. J Biol Chem. 2015; 290:30366-30374.
30. Coppari R. Metabolic actions of hypothalamic SIRT1. Trends Endocrinol Metab. 2012; 23:179-185.
31. Arruda AP, Hotamisligil GS. Calcium Homeostasis and Organelle Function in the Pathogenesis of Obesity and Diabetes. Cell Metab. 2015; 22:381-397.
32. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell. 2010; 140:900-917.
33. Zhu G, Ye R, Jung DY, Barron E, Friedline RH, Benoit VM, Hinton DR, Kim JK, Lee AS. GRP78 plays an essential role in adipogenesis and postnatal growth in mice. FASEB J. 2013; 27:955-964.
34. Huang XZ, Wen D, Zhang M, Xie Q, Ma L, Guan Y, Ren Y, Chen J, Hao CM. Sirt1 activation ameliorates renal fibrosis by inhibiting the TGF-beta/Smad3 pathway. FASEB J. 2014; 115:996-1005.
35. Sun L, Fan Z, Chen J, Tian W, Li M, Xu H, Wu X, Shao J, Bian Y, Fang M, Xu Y. Transcriptional repression of SIRT1 by protein inhibitor of activated STAT 4 (PIAS4) in hepatic stellate cells contributes to liver fibrosis. Sci Rep. 2016; 6:28432.
36. Li J, Qu X, Ricardo SD, Bertram JF, Nikolic-Paterson DJ. Resveratrol inhibits renal fibrosis in the obstructed kidney: potential role in deacetylation of Smad3. Am J Pathol. 2010; 177:1065-1071.
37. Xu B, Chen H, Xu W, Zhang W, Buckley S, Zheng SG, Warburton D, Kolb M, Gauldie J, Shi W. Molecular mechanisms of MMP9 overexpression and its role in emphysema pathogenesis of Smad3-deficient mice. Am J Physiol Lung Cell Mol Physiol. 2012; 303:L89-96.
38. Lian N, Lin T, Liu W, Wang W, Li L, Sun S, Nyman JS, Yang X. Transforming growth factor beta suppresses osteoblast differentiation via the vimentin activating transcription factor 4 (ATF4) axis. J Biol Chem. 2012; 287:35975-35984.
39. Liu SH, Yang CC, Chan DC, Wu CT, Chen LP, Huang JW, Hung KY, Chiang CK. Chemical chaperon 4-phenylbutyrate protects against the endoplasmic reticulum stress-mediated renal fibrosis in vivo and in vitro. Oncotarget. 2016; 7:22116-22127. doi: 10.18632/oncotarget.7904.
40. Qing G, Li B, Vu A, Skuli N, Walton ZE, Liu X, Mayes PA, Wise DR, Thompson CB, Maris JM, Hogarty MD, Simon MC. ATF4 regulates MYC-mediated neuroblastoma cell death upon glutamine deprivation. Cancer cell. 2012; 22:631-644.
41. Armstrong JL, Flockhart R, Veal GJ, Lovat PE, Redfern CP. Regulation of endoplasmic reticulum stress-induced cell death by ATF4 in neuroectodermal tumor cells. J Biol Chem. 2010; 285:6091-6100.
42. Beck D, Niessner H, Smalley KS, Flaherty K, Paraiso KH, Busch C, Sinnberg T, Vasseur S, Iovanna JL, Driessen S, Stork B, Wesselborg S, Schaller M, et al. Vemurafenib potently induces endoplasmic reticulum stress-mediated apoptosis in BRAFV600E melanoma cells. Sci Signal. 2013; 6:ra7.