Effects of a high fat diet and voluntary wheel running exercise on cidea and cidec expression in liver and adipose tissue of mice

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Reynolds, Thomas H ^a   Banerjee, Sayani ^b   Sharma, Vishva Mitra ^b   Donohue, Jacob ^a   Couldwell, Sandrine ^a   Sosinsky, Alexandra ^a   Frulla, Ashton ^a   Robinson, Allegra ^a   Puri, Vishwajeet ^b  

^a SKIDMORE COLLEGE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIDEA PROTEIN; CIDEC PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; RNA; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CIDEA PROTEIN, MOUSE; FAT-SPECIFIC PROTEIN 27, MOUSE; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PPARGC1A PROTEIN, MOUSE; PROTEIN; TRANSCRIPTION FACTOR;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; EPIDIDYMIS FAT; FATTY LIVER; GENE EXPRESSION; IN VIVO STUDY; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIVER PARENCHYMA; LOW FAT DIET; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RUNNING; VOLUNTARY MOVEMENT; WILD TYPE MOUSE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LIVER; METABOLISM;

ADIPOSE TISSUE; ADIPOSITY; ANIMALS; APOPTOSIS REGULATORY PROTEINS; DIET, HIGH-FAT; GENE EXPRESSION REGULATION; INSULIN; LIVER; MALE; MICE; MICE, INBRED C57BL; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PHYSICAL CONDITIONING, ANIMAL; PPAR GAMMA; PROTEINS; RNA, MESSENGER; RUNNING; TRANSCRIPTION FACTORS;

EID: 84941366577     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130259     Document Type: Article

References (46)

1. Centers for Disease Control and Prevention: National diabetes fact sheet:national estimates and general information on diabetes and prediabetes in the United States, Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, 2011.
2. American Diabetes Association: Economic costs of diabetes in the U.S. in 2012. Diabetes Care 2013, 36(4):1033-1046. doi: 10.2337/dc12-2625 PMID: 23468086
3. Ogden CL, Carroll MD, Kit BK, Flegal KM: Prevalence of obesity in the United States, 2009-2010. NCHS Data Brief 2012, (82: ):1-8. PMID: 22617494
4. Boden G: Obesity, insulin resistance and free fatty acids. Curr Opin Endocrinol Diabetes Obes 2011, 18(2):139-143. doi: 10.1097/MED.0b013e3283444b09 PMID: 21297467
5. Bickel PE, Tansey JT, Welte MA: PAT proteins, an ancient family of lipid droplet proteins that regulate cellular lipid stores. Biochim Biophys Acta 2009, 1791(6):419-440. doi: 10.1016/j.bbalip.2009.04.002 PMID: 19375517
6. Larigauderie G, Cuaz-Pérolin C, Younes AB, Furman C, Lasselin C, Copin C, Jaye M, Fruchart J, Rouis M: Adipophilin increases triglyceride storage in human macrophages by stimulation of biosynthesis and inhibition of beta-oxidation. FEBS J 2006, 273(15):3498-3510. PMID: 16884492
7. Sun Z, Gong J, Wu H, Xu W, Wu L, Xu D, Gao J, Wu J, Yang H, Yang M, Li P: Perilipin1 promotes unilocular lipid droplet formation through the activation of Fsp27 in adipocytes. Nat Commun 2013, 4:1594-1594. doi: 10.1038/ncomms2581 PMID: 23481402
8. Liu K, Zhou S, Kim J, Tillison K, Majors D, Rearick D, Lee JH, Fernandez-Boyanapalli R, Barricklow K, Houston MS, Smas CM: Functional analysis of FSP27 protein regions for lipid droplet localization, caspase-dependent apoptosis, and dimerization with CIDEA. Am J Physiol Endocrinol Metab 2009, 297 (6):E1395-E1413. doi: 10.1152/ajpendo.00188.2009 PMID: 19843876
9. Jambunathan S, Yin J, Khan W, Tamori Y, Puri V: FSP27 promotes lipid droplet clustering and then fusion to regulate triglyceride accumulation. PLoS One 2011, 6(12):e28614-e28614. doi: 10.1371/journal.pone.0028614 PMID: 22194867
10. Christianson JL, Boutet E, Puri V, Chawla A, Czech MP: Identification of the lipid droplet targeting domain of the Cidea protein. J Lipid Res 2010, 51(12):3455-3462. doi: 10.1194/jlr.M009498 PMID: 20810722
11. Gong J, Sun Z, Wu L, Xu W, Schieber N, Xu D, Shui G, Yang H, Parton RG, Li P: Fsp27 promotes lipid droplet growth by lipid exchange and transfer at lipid droplet contact sites. J Cell Biol 2011, 195 (6):953-963. doi: 10.1083/jcb.201104142 PMID: 22144693
12. Tansey JT, Sztalryd C, Gruia-Gray J, Roush DL, Zee JV, Gavrilova O, Reitman ML, Deng CX, Li C, Kimmel AR, Londos C: Perilipin ablation results in a lean mouse with aberrant adipocyte lipolysis, enhanced leptin production, and resistance to diet-induced obesity. Proc Natl Acad Sci U S A 2001, 98 (11):6494-6499. PMID: 11371650
13. Zhou Z, Yon Toh S, Chen Z, Guo K, Ng CP, Ponniah S, Lin S, Hong W, Li P: Cidea-deficient mice have lean phenotype and are resistant to obesity. Nat Genet 2003, 35(1):49-56. PMID: 12910269
14. Nishino N, Tamori Y, Tateya S, Kawaguchi T, Shibakusa T, Mizunoya W, Inoue K, Kitazawa R, Kitazawa S, Matsuki Y, Hiramatsu R, Masubuchi S, Omachi A, Kimura K, Saito M, Amo T, Ohta S, Yamaguchi T, Osumi T, Cheng J, Fujimoto T, Nakao H, Nakao K, Aiba A, Okamura H, Fushiki T, Kasuga M: FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J Clin Invest 2008, 118(8):2808-2821. doi: 10.1172/JCI34090 PMID: 18654663
15. Reynolds TH 4th, Cinquino N, Anthony M, Phelps CB, Zachary Berk E: Insulin resistance without elevated mammalian target of rapamycin complex 1 activity in muscles of mice fed a high-fat diet. J Appl Physiol 2009, 107(5):1479-1485. doi: 10.1152/japplphysiol.00574.2009 PMID: 19729590
16. Puri V, Ranjit S, Konda S, Nicoloro SMC, Straubhaar J, Chawla A, Chouinard M, Lin C, Burkart A, Corvera S, Perugini RA, Czech MP: Cidea is associated with lipid droplets and insulin sensitivity in humans. Proc Natl Acad Sci U S A 2008, 105(22):7833-7838. doi: 10.1073/pnas.0802063105 PMID: 18509062
17. Nordström EA, Rydén M, Backlund EC, Dahlman I, Kaaman M, Blomqvist L, Cannon B, Nedergaard J, Arner P: A human-specific role of cell death-inducing DFFA (DNA fragmentation factor-Alpha)-like effector A (CIDEA) in adipocyte lipolysis and obesity. Diabetes 2005, 54(6):1726-1734. PMID: 15919794
18. Kim Y, Cho SY, Yun CH, Moon YS, Lee TR, Kim SH: Transcriptional activation of Cidec by PPARgamma2 in adipocyte. Biochem Biophys Res Commun 2008, 377(1):297-302. doi: 10.1016/j.bbrc. 2008.09.129 PMID: 18845124
19. Baar K: Involvement of PPAR gamma co-Activator-1, nuclear respiratory factors 1 and 2, and PPAR alpha in the adaptive response to endurance exercise. Proc Nutr Soc 2004, 63(2):269-273. PMID: 15294042
20. Pilegaard H, Saltin B, Neufer PD: Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 2003, 546:851-858. PMID: 12563009
21. Hallberg M, Morganstein DL, Kiskinis E, Shah K, Kralli A, Dilworth SM, White R, Parker MG, Christian M: A functional interaction between RIP140 and PGC-1alpha regulates the expression of the lipid droplet protein CIDEA. Mol Cell Biol 2008, 28(22):6785-6795. doi: 10.1128/MCB.00504-08 PMID: 18794372
22. Reynolds,Thomas H. 4th, Merrell E, Cinquino N, Gaugler M, Ng L: Disassociation of insulin action and Akt/FOXO signaling in skeletal muscle of older Akt-deficient mice. Am J Physiol Regul Integr Comp Physiol 2012, 303(11):R1186-R1194. doi: 10.1152/ajpregu.00358.2012 PMID: 23100026
23. Grahn THM, Kaur R, Yin J, Schweiger M, Sharma VM, Lee M, Ido Y, Smas CM, Zechner R, Lass A, Puri V: Fat-specific protein 27 (FSP27) interacts with adipose triglyceride lipase (ATGL) to regulate lipolysis and insulin sensitivity in human adipocytes. J Biol Chem 2014, 289(17):12029-12039. doi: 10. 1074/jbc.M113.539890 PMID: 24627478
24. Rubio-Cabezas O, Puri V, Murano I, Saudek V, Semple RK, Dash S, Hyden CSS, Bottomley W, Vigouroux C, Magré J, Raymond-Barker P, Murgatroyd PR, Chawla A, Skepper JN, Chatterjee VK, Suliman S, Patch A, Agarwal AK, Garg A, Barroso I, Cinti S, Czech MP, Argente J, O'Rahilly S, Savage DB: Partial lipodystrophy and insulin resistant diabetes in a patient with a homozygous nonsense mutation in CIDEC. EMBO Mol Med 2009, 1(5):280-287. doi: 10.1002/emmm.200900037 PMID: 20049731
25. Singh M, Kaur R, Lee M, Pickering RT, Sharma VM, Puri V, Kandror KV: Fat-specific protein 27 inhibits lipolysis by facilitating the inhibitory effect of transcription factor Egr1 on transcription of adipose triglyceride lipase. J Biol Chem 2014, 289(21):14481-14487. doi: 10.1074/jbc.C114.563080 PMID: 24742676
26. Yonezawa T, Haga S, Kobayashi Y, Katoh K, Obara Y: Saturated fatty acids stimulate and insulin suppresses CIDE-A expression in bovine mammary epithelial cells. Biochem Biophys Res Commun 2009, 384(4):535-539. doi: 10.1016/j.bbrc.2009.05.012 PMID: 19427838
27. Sahlin K, Harris RC: Control of lipid oxidation during exercise: role of energy state and mitochondrial factors. Acta Physiol (Oxf) 2008, 194(4):283-291.
28. Jeppesen J, Kiens B: Regulation and limitations to fatty acid oxidation during exercise. J Physiol 2012, 590:1059-1068. doi: 10.1113/jphysiol.2011.225011 PMID: 22271865
29. Ranjit S, Boutet E, Gandhi P, Prot M, Tamori Y, Chawla A, Greenberg AS, Puri V, Czech MP: Regulation of fat specific protein 27 by isoproterenol and TNF-? to control lipolysis in murine adipocytes. J Lipid Res 2011, 52(2):221-236.
30. Zhang X, Heckmann BL, Xie X, Saarinen AM, Liu J: Regulation of FSP27 protein stability by AMPK and HSC70. Am J Physiol Endocrinol Metab 2014, 307(11):E1047-E1056. doi: 10.1152/ajpendo.00125. 2014 PMID: 25315694
31. Nian Z, Sun Z, Yu L, Toh SY, Sang J, Li P: Fat-specific protein 27 undergoes ubiquitin-dependent degradation regulated by triacylglycerol synthesis and lipid droplet formation. J Biol Chem 2010, 285 (13):9604-9615. doi: 10.1074/jbc.M109.043786 PMID: 20089860
32. Viswakarma N, Yu S, Naik S, Kashireddy P, Matsumoto K, Sarkar J, Surapureddi S, Jia Y, Rao MS, Reddy JK: Transcriptional regulation of Cidea, mitochondrial cell death-inducing DNA fragmentation factor alpha-like effector A, in mouse liver by peroxisome proliferator-Activated receptor alpha and gamma. J Biol Chem 2007, 282(25):18613-18624. PMID: 17462989
33. Zhou L, Xu L, Ye J, Li D, Wang W, Li X, Wu L, Wang H, Guan F, Li P: Cidea promotes hepatic steatosis by sensing dietary fatty acids. Hepatology 2012, 56(1):95-107. doi: 10.1002/hep.25611 PMID: 22278400
34. Matsusue K, Kusakabe T, Noguchi T, Takiguchi S, Suzuki T, Yamano S, Gonzalez FJ: Hepatic steatosis in leptin-deficient mice is promoted by the PPARgamma target gene Fsp27. Cell Metab 2008, 7 (4):302-311. doi: 10.1016/j.cmet.2008.03.003 PMID: 18396136
35. Sato W, Horie Y, Kataoka E, Ohshima S, Dohmen T, Iizuka M, Sasaki J, Sasaki T, Hamada K, Kishimoto H, Suzuki A, Watanabe S: Hepatic gene expression in hepatocyte-specific Pten deficient mice showing steatohepatitis without ethanol challenge. Hepatol Res 2006, 34(4):256-265. PMID: 16490391
36. Scarpulla RC: Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 2008, 88(2):611-638. doi: 10.1152/physrev.00025.2007 PMID: 18391175
37. Lira VA, Benton CR, Yan Z, Bonen A: PGC-1alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am J Physiol Endocrinol Metab 2010, 299(2):E145-E161. doi: 10.1152/ajpendo.00755.2009 PMID: 20371735
38. Hancock CR, Han D, Chen M, Terada S, Yasuda T, Wright DC, Holloszy JO: High-fat diets cause insulin resistance despite an increase in muscle mitochondria. Proc Natl Acad Sci U S A 2008, 105 (22):7815-7820. doi: 10.1073/pnas.0802057105 PMID: 18509063
39. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM: Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 2001, 413(6852):131-138. PMID: 11557972
40. Matiello R, Fukui RT, Silva ME, Rocha DM, Wajchenberg BL, Azhar S, Santos RF: Differential regulation of PGC-1alpha expression in rat liver and skeletal muscle in response to voluntary running. Nutr Metab (Lond) 2010, 7:36-36.
41. Souza Pauli LS, Ropelle ECC, de Souza CT, Cintra DE, da Silva A,Sanchez Ramos, de AR, de Moura LP, Marinho R, de Oliveira V, Katashima CK, Pauli JR, Ropelle ER: Exercise training decreases mitogen-Activated protein kinase phosphatase-3 expression and suppresses hepatic gluconeogenesis in obese mice. J Physiol 2014, 592:1325-1340. doi: 10.1113/jphysiol.2013.264002 PMID: 24396063
42. Semple RK, Crowley VC, Sewter CP, Laudes M, Christodoulides C, Considine RV, Vidal-Puig A, O'Rahilly S: Expression of the thermogenic nuclear hormone receptor coactivator PGC-1alpha is reduced in the adipose tissue of morbidly obese subjects. Int J Obes Relat Metab Disord 2004, 28(1):176-179. PMID: 14557831
43. Hammarstedt A, Jansson P, Wesslau C, Yang X, Smith U: Reduced expression of PGC-1 and insulinsignaling molecules in adipose tissue is associated with insulin resistance. Biochem Biophys Res Commun 2003, 301(2):578-582. PMID: 12565902
44. 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: Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012, 150 (2):366-376. doi: 10.1016/j.cell.2012.05.016 PMID: 22796012
45. Puigserver P,Wu Z, Park CW, Graves R, Wright M, Spiegelman BM: A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92(6):829-839. PMID: 9529258
46. Sutherland LN, Bomhof MR, Capozzi LC, Basaraba SAU, Wright DC: Exercise and adrenaline increase PGC-1{alpha} mRNA expression in rat adipose tissue. J Physiol 2009, 587:1607-1617. doi: 10.1113/jphysiol.2008.165464 PMID: 19221126