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Molecular Characterization of PGC-1β (PPAR Gamma Coactivator 1β) and its Roles in Mitochondrial Biogenesis in Blunt Snout Bream (Megalobrama amblycephala)

. 2020 Mar 12 ; 21 (6) : . [epub] 20200312

Language English Country Switzerland Media electronic

Document type Journal Article

Grant support
B17162 Outstanding Young Scientific Research Talents Program of Fujian province
31801969 National Nature Science Foundation of China
LM2018099 Ministry of Education, Youth and Sports of the Czech Republic, project CENAKVA
QK1710310 Ministry of Agriculture of the Czech Republic, project NAZV

This study aimed at achieving the molecular characterization of peroxisome proliferator-activated receptor-gamma coactivator 1β (PGC-1β) and exploring its modulatory roles in mitochondria biogenesis in blunt snout bream (Megalobrama amblycephala). A full-length cDNA of PGC-1β was cloned from liver which covered 3110 bp encoding 859 amino acids. The conserved motifs of PGC-1β family proteins were gained by MEME software, and the phylogenetic analyses showed motif loss and rearrangement of PGC-1β in fish. The function of PGC-1β was evaluated through overexpression and knockdown of PGC-1β in primary hepatocytes of blunt snout bream. We observed overexpression of PGC-1β along with enhanced mitochondrial transcription factor A (TFAM) expression and mtDNA copies in hepatocytes, and its knockdown led to slightly reduced NRF1 expression. However, knockdown of PGC-1β did not significantly influence TFAM expression or mtDNA copies. The alterations in mitochondria biogenesis were assessed following high-fat intake, and the results showed that it induces downregulation of PGC-1β. Furthermore, significant decreases in mitochondrial respiratory chain activities and mitochondria biogenesis were observed by high-fat intake. Our findings demonstrated that overexpression of PGC-1β induces the enhancement of TFAM expression and mtDNA amount but not NRF-1. Therefore, it could be concluded that PGC-1β is involved in mitochondrial biogenesis in blunt snout bream but not through PGC-1β/NRF-1 pathway.

See more in PubMed

Scarpulla R.C. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim. Biophys. Acta Mol. Cell Res. 2011;1813:1269–1278. doi: 10.1016/j.bbamcr.2010.09.019. PubMed DOI PMC

Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis. Cell. 1998;92:829–839. doi: 10.1016/S0092-8674(00)81410-5. PubMed DOI

Andersson U., Scarpulla R.C. PGC-1-Related Coactivator, a Novel, Serum-Inducible Coactivator of Nuclear Respiratory Factor 1-Dependent Transcription in Mammalian Cells. Mol. Cell. Biol. 2001;21:3738–3749. doi: 10.1128/MCB.21.11.3738-3749.2001. PubMed DOI PMC

Puigserver P., Spiegelman B.M. Peroxisome Proliferator-Activated Receptor-γ Coactivator 1α (PGC-1α): Transcriptional Coactivator and Metabolic Regulator. Endocr. Rev. 2003;24:78–90. doi: 10.1210/er.2002-0012. PubMed DOI

Northam C., LeMoine C.M.R. Metabolic regulation by the PGC-1α and PGC-1β coactivators in larval zebrafish (Danio rerio) Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2019;234:60–67. doi: 10.1016/j.cbpa.2019.04.011. PubMed DOI

LeMoine C.M.R., Genge C.E., Moyes C.D. Role of the PGC-1 family in the metabolic adaptation of goldfish to diet and temperature. J. Exp. Biol. 2008;211:1448–1455. doi: 10.1242/jeb.014951. PubMed DOI

Bremer K., Moyes C.D. Origins of variation in muscle cytochrome C oxidase activity within and between fish species. J. Exp. Biol. 2011;214:1888–1895. doi: 10.1242/jeb.053330. PubMed DOI

Bremer K., Kocha K.M., Snider T., Moyes C.D. Sensing and responding to energetic stress: The role of the AMPK-PGC1α-NRF1 axis in control of mitochondrial biogenesis in fish. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2016;199:4–12. doi: 10.1016/j.cbpb.2015.09.005. PubMed DOI

Song X., Rahimnejad S., Zhou W., Cai L., Lu K. Molecular Characterization of Peroxisome Proliferator-Activated Receptor-Gamma Coactivator-1α (PGC1α) and Its Role in Mitochondrial Biogenesis in Blunt Snout Bream (Megalobrama amblycephala) Front. Physiol. 2019;9:1957. doi: 10.3389/fphys.2018.01957. PubMed DOI PMC

Goto M., Terada S., Kato M., Katoh M., Yokozeki T., Tabata I., Shimokawa T. cDNA Cloning and mRNA Analysis of PGC-1 in Epitrochlearis Muscle in Swimming-Exercised Rats. Biochem. Biophys. Res. Commun. 2000;274:350–354. doi: 10.1006/bbrc.2000.3134. PubMed DOI

Mortensen O.H., Frandsen L., Schjerling P., Nishimura E., Grunnet N. PGC-1α and PGC-1β have both similar and distinct effects on myofiber switching toward an oxidative phenotype. Am. J. Physiol. Metab. 2006;291:E807–E816. doi: 10.1152/ajpendo.00591.2005. PubMed DOI

Uldry M., Yang W., St-Pierre J., Lin J., Seale P., Spiegelman B.M. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 2006;3:333–341. doi: 10.1016/j.cmet.2006.04.002. PubMed DOI

St-Pierre J., Lin J., Krauss S., Tarr P.T., Yang R., Newgard C.B., Spiegelman B.M. Bioenergetic Analysis of Peroxisome Proliferator-activated Receptor γ Coactivators 1α and 1β (PGC-1α and PGC-1β) in Muscle Cells. J. Biol. Chem. 2003;278:26597–26603. doi: 10.1074/jbc.M301850200. PubMed DOI

Frier B.C., Williams D.B., Wright D.C. The effects of apelin treatment on skeletal muscle mitochondrial content. Am. J. Physiol. Integr. Comp. Physiol. 2009;297:R1761–R1768. doi: 10.1152/ajpregu.00422.2009. PubMed DOI

LeMoine C.M.R., Lougheed S.C., Moyes C.D. Modular Evolution of PGC-1α in Vertebrates. J. Mol. Evol. 2010;70:492–505. doi: 10.1007/s00239-010-9347-x. PubMed DOI

Handschin C., Spiegelman B.M. Peroxisome Proliferator-Activated Receptor γ Coactivator 1 Coactivators, Energy Homeostasis, and Metabolism. Endocr. Rev. 2006;27:728–735. doi: 10.1210/er.2006-0037. PubMed DOI

Meirhaeghe A., Crowley V., Lenaghan C., Lelliott C., Green K., Stewart A., Hart K., Schinner S., Sethi J.K., Yeo G., et al. Characterization of the human, mouse and rat PGC1 beta (peroxisome-proliferator-activated receptor-gamma co-activator 1 beta) gene in vitro and in vivo. Biochem. J. 2003;373:155–165. doi: 10.1042/bj20030200. PubMed DOI PMC

Vercauteren K., Gleyzer N., Scarpulla R.C. PGC-1-related coactivator complexes with HCF-1 and NRF-2beta in mediating NRF-2(GABP)-dependent respiratory gene expression. J. Biol. Chem. 2008;283:12102–12111. doi: 10.1074/jbc.M710150200. PubMed DOI PMC

Choi S., editor. 14-3-3alpha BT-Encyclopedia of Signaling Molecules. Springer International Publishing; Cham, Switzerland: 2018. p. 11.

Wilson-Fritch L., Burkart A., Bell G., Mendelson K., Leszyk J., Nicoloro S., Czech M., Corvera S. Mitochondrial Biogenesis and Remodeling during Adipogenesis and in Response to the Insulin Sensitizer Rosiglitazone. Mol. Cell. Biol. 2003;23:1085–1094. doi: 10.1128/MCB.23.3.1085-1094.2003. PubMed DOI PMC

Nagai Y., Yonemitsu S., Erion D.M., Iwasaki T., Stark R., Weismann D., Dong J., Zhang D., Jurczak M.J., Löffler M.G., et al. The role of peroxisome proliferator-activated receptor gamma coactivator-1 beta in the pathogenesis of fructose-induced insulin resistance. Cell Metab. 2009;9:252–264. doi: 10.1016/j.cmet.2009.01.011. PubMed DOI PMC

Lu R., Ji H., Chang Z., Su S., Yang G. Mitochondrial development and the influence of its dysfunction during rat adipocyte differentiation. Mol. Biol. Rep. 2010;37:2173–2182. doi: 10.1007/s11033-009-9695-z. PubMed DOI

Bremer K., Monk C.T., Gurd B.J., Moyes C.D. Transcriptional regulation of temperature-induced remodeling of muscle bioenergetics in goldfish. Am. J. Physiol. Integr. Comp. Physiol. 2012;303:R150–R158. doi: 10.1152/ajpregu.00603.2011. PubMed DOI

Gao C.-L., Liu G.-L., Liu S., Chen X.-H., Ji C.-B., Zhang C.-M., Xia Z.-K., Guo X. Overexpression of PGC-1β improves insulin sensitivity and mitochondrial function in 3T3-L1 adipocytes. Mol. Cell. Biochem. 2011;353:215–223. doi: 10.1007/s11010-011-0789-2. PubMed DOI

Picca A., Lezza A.M.S. Regulation of mitochondrial biogenesis through TFAM–mitochondrial DNA interactions: Useful insights from aging and calorie restriction studies. Mitochondrion. 2015;25:67–75. doi: 10.1016/j.mito.2015.10.001. PubMed DOI

Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., et al. Mechanisms Controlling Mitochondrial Biogenesis and Respiration through the Thermogenic Coactivator PGC-1. Cell. 1999;98:115–124. doi: 10.1016/S0092-8674(00)80611-X. PubMed DOI

Shao D., Liu Y., Liu X., Zhu L., Cui Y., Cui A., Qiao A., Kong X., Liu Y., Chen Q., et al. PGC-1β-Regulated mitochondrial biogenesis and function in myotubes is mediated by NRF-1 and ERRα. Mitochondrion. 2010;10:516–527. doi: 10.1016/j.mito.2010.05.012. PubMed DOI

Gacias M., Pérez-Martí A., Pujol-Vidal M., Marrero P.F., Haro D., Relat J. PGC-1β regulates mouse carnitine–acylcarnitine translocase through estrogen-related receptor α. Biochem. Biophys. Res. Commun. 2012;423:838–843. doi: 10.1016/j.bbrc.2012.06.051. PubMed DOI

Hood D., Takahashi M., Connor M., Freyssenet D. Assembly of the cellular powerhouse: Current issues in muscle mitochondrial biogenesis. Exerc. Sport Sci. Rev. 2000;28:68–73. PubMed

Raftery T.D., Jayasundara N., Di Giulio R.T. A bioenergetics assay for studying the effects of environmental stressors on mitochondrial function in vivo in zebrafish larvae. Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 2017;192:23–32. doi: 10.1016/j.cbpc.2016.12.001. PubMed DOI PMC

Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., et al. Resveratrol Improves Mitochondrial Function and Protects against Metabolic Disease by Activating SIRT1 and PGC-1α. Cell. 2006;127:1109–1122. doi: 10.1016/j.cell.2006.11.013. PubMed DOI

Csiszar A., Labinskyy N., Pinto J.T., Ballabh P., Zhang H., Losonczy G., Pearson K., de Cabo R., Pacher P., Zhang C., et al. Resveratrol induces mitochondrial biogenesis in endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 2009;297:H13–H20. doi: 10.1152/ajpheart.00368.2009. PubMed DOI PMC

García-Ruiz I., Solís-Muñoz P., Fernández-Moreira D., Muñoz-Yagüe T., Solís-Herruzo J.A. In vitro treatment of HepG2 cells with saturated fatty acids reproduces mitochondrial dysfunction found in nonalcoholic steatohepatitis. Dis. Model. Mech. 2015;8:183–191. doi: 10.1242/dmm.018234. PubMed DOI PMC

Lee M.-S., Kim I.-H., Kim Y. Effects of Eicosapentaenoic Acid and Docosahexaenoic Acid on Uncoupling Protein 3 Gene Expression in C2C12 Muscle Cells. Nutrients. 2013;5:1660–1671. doi: 10.3390/nu5051660. PubMed DOI PMC

Verdin E., Hirschey M.D., Finley L.W.S., Haigis M.C. Sirtuin regulation of mitochondria: Energy production, apoptosis, and signaling. Trends Biochem. Sci. 2010;35:669–675. doi: 10.1016/j.tibs.2010.07.003. PubMed DOI PMC

Paradies G., Petrosillo G., Paradies V., Ruggiero F.M. Oxidative stress, mitochondrial bioenergetics, and cardiolipin in aging. Free Radic. Biol. Med. 2010;48:1286–1295. doi: 10.1016/j.freeradbiomed.2010.02.020. PubMed DOI

Rato L., Duarte A.I., Tomás G.D., Santos M.S., Moreira P.I., Socorro S., Cavaco J.E., Alves M.G., Oliveira P.F. Pre-diabetes alters testicular PGC1-α/SIRT3 axis modulating mitochondrial bioenergetics and oxidative stress. Biochim. Biophys. Acta Bioenerg. 2014;1837:335–344. doi: 10.1016/j.bbabio.2013.12.008. PubMed DOI

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Höhna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space. Syst. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC

Livak K.J., Schmittgen T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

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