Transcriptional regulation of adipogenic marker genes for the improvement of intramuscular fat in Qinchuan beef cattle

References

• Kazala EC, Lozeman FJ, Mir PS, Laroche A, Bailey DR, Weselake RJ. Relationship of fatty acid composition to intramuscular fat content in beef from crossbred Wagyu cattle. J Anim Sci. 1999;77(7):1717–1725.
   PubMed Web of Science ®Google Scholar
• Mannen H. Identification and utilization of genes associated with beef qualities. Anim Sci J. 2011;82(1):1–7.
   PubMed Web of Science ®Google Scholar
• Khan R, Raza SHA, Junjvlieke Z, et al. RNA-seq reveal role of bovine TORC2 in the regulation of adipogenesis. Arch Biochem Biophys. 2020;680:108236.
   PubMed Web of Science ®Google Scholar
• Guo H, Raza SHA, Schreurs NM, et al. Genetic variants in the promoter region of the KLF3 gene associated with fat deposition in Qinchuan cattle. Gene. 2018;672:50–55.
   PubMed Web of Science ®Google Scholar
• Feve B. Adipogenesis: cellular and molecular aspects. Best Pract Res Clin Endocrinol Metab. 2005;19:483–499.
   PubMed Web of Science ®Google Scholar
• Taniguchi M, Guan LL, Zhang B, Dodson MV, Okine E, Moore SS. Adipogenesis of bovine perimuscular preadipocytes. Biochem Biophys Res Commun. 2008;366(1):54–59.
   PubMed Web of Science ®Google Scholar
• Nuttall ME, Gimble JM. Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol. 2004;4(3):290–294.
   PubMedGoogle Scholar
• Zhuang H, Zhang X, Zhu C, et al. Molecular mechanisms of PPAR-γ governing MSC osteogenic and adipogenic differentiation. Curr Stem Cell Res Ther. 2016;11(3):255–264.
   PubMed Web of Science ®Google Scholar
• Ambele MA, Dessels C, Durandt C, Pepper MS. Genome-wide analysis of gene expression during adipogenesis in human adipose-derived stromal cells reveals novel patterns of gene expression during adipocyte differentiation. Stem Cell Res. 2016;16(3):725–734.
   PubMed Web of Science ®Google Scholar
• Yu WH, Li FG, Chen XY, et al. PPARγ suppression inhibits adipogenesis but does not promote osteogenesis of human mesenchymal stem cells. Int J Biochem Cell Biol. 2012;44(2):377–384.
   PubMed Web of Science ®Google Scholar
• McKnight SL, Lane MD, Gluecksohn-Waelsch S. Is CCAAT/enhancer-binding protein a central regulator of energy metabolism? Genes Dev. 1989;3(12B):2021–2024.
   PubMed Web of Science ®Google Scholar
• Cao Z, Umek RM, McKnight SL. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 1991;5(9):1538–1552.
   PubMed Web of Science ®Google Scholar
• Wang ND, Finegold MJ, Bradley A, et al. Impaired energy homeostasis in C/EBP alpha knockout mice. Science. 1995;269(5227):1108–1112.
   PubMed Web of Science ®Google Scholar
• Linhart HG, Ishimura-Oka K, DeMayo F, et al. C/EBPalpha is required for differentiation of white, but not brown, adipose tissue. Proc Natl Acad Sci USA. 2001;98(22):12532–12537.
   PubMed Web of Science ®Google Scholar
• Rosen ED, MacDougald OA. Adipocyte differentiation from the inside out. Nat Rev Mol Cell Biol. 2006;7(12):885–896.
   PubMed Web of Science ®Google Scholar
• Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature. 2006;444(7121):847–853.
   PubMed Web of Science ®Google Scholar
• Braun K, Oeckl J, Westermeier J, Li Y, Klingenspor M. Non-adrenergic control of lipolysis and thermogenesis in adipose tissues. J Exp Biol. 2018;221(Suppl 1):jeb165381.
   PubMedGoogle Scholar
• Albalat A, Gutierrez J, Navarro I. Regulation of lipolysis in isolated adipocytes of rainbow trout (Oncorhynchus mykiss): the role of insulin and glucagon, comparative biochemistry and physiology. Comp Biochem Physiol A Mol Integr Physiol. 2005;142(3):347–354.
   PubMedGoogle Scholar
• Albalat A, Sánchez-Gurmaches J, Gutiérrez J, Navarro I. Regulation of lipoprotein lipase activity in rainbow trout (Oncorhynchus mykiss) tissues. Gen Comp Endocrinol. 2006;146(3):226–235.
   PubMed Web of Science ®Google Scholar
• Todorcevic M, Vegusdal A, Gjoen T, et al. Changes in fatty acids metabolism during differentiation of Atlantic salmon preadipocytes; effects of n-3 and n-9 fatty acids. Biochim Biophys Acta. 2008;1781(6–7):326–335.
   PubMed Web of Science ®Google Scholar
• Todorcević M, Kjaer MA, Djaković N, Vegusdal A, Torstensen BE, Ruyter B. N-3 HUFAs affect fat deposition, susceptibility to oxidative stress, and apoptosis in Atlantic salmon visceral adipose tissue. Comp Biochem Physiol B Biochem Mol Biol. 2009;152(2):135–143.
   PubMed Web of Science ®Google Scholar
• Blüher M, Mantzoros CS. From leptin to other adipokines in health and disease: facts and expectations at the beginning of the 21st century. Metabolism. 2015;64(1):131–145.
   PubMed Web of Science ®Google Scholar
• Schoettl T, Fischer IP, Ussar S. Heterogeneity of adipose tissue in development and metabolic function. J Exp Biol. 2018;221(Suppl 1):jeb162958.
   PubMedGoogle Scholar
• Deck CA, Honeycutt JL, Cheung E, Reynolds HM, Borski RJ. Assessing the functional role of leptin in energy homeostasis and the stress response in vertebrates. Front Endocrinol (Lausanne). 2017;8:63.
   PubMedGoogle Scholar
• Maffei á, Halaas J, Ravussin E, et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med. 1995;1(11):1155–1161.
   PubMed Web of Science ®Google Scholar
• Paul DS, Grevengoed TJ, Pascual F, Ellis JM, Willis MS, Coleman RA. Deficiency of cardiac Acyl-CoA synthetase-1 induces diastolic dysfunction, but pathologic hypertrophy is reversed by rapamycin. Biochimica et Biophysica Acta. 1841(6):880–887.
   Google Scholar
• Ellis JM, Li LO, Wu P-C, et al. Adipose acyl-CoA synthetase-1 directs fatty acids toward beta-oxidation and is required for cold thermogenesis. Cell Metab. 2010;12(1):53–64.
   PubMed Web of Science ®Google Scholar
• Jensen-Urstad APL, Semenkovich CF. Fatty acid synthase and liver triglyceride metabolism: housekeeper or messenger? Biochim Biophys Acta. 2012;1821(5):747–753.
   PubMed Web of Science ®Google Scholar
• Swierczynski J, Sledzinski T. Metabolic and regulatory function of fatty acid synthase. Postepy Biochem. 2012;58:175–185.
   PubMedGoogle Scholar
• Brownsey RW, Boone AN, Elliott JE, Kulpa JE, Lee WM. Regulation of acetyl-CoA carboxylase. Biochem Soc Trans. 2006;34(Pt 2):223–227.
   PubMedGoogle Scholar
• Li LO, Klett EL, Coleman RA. Acyl-CoA synthesis, lipid metabolism and lipotoxicity. Biochim Biophys Acta. 2010;1801(3):246–251.
   PubMed Web of Science ®Google Scholar
• Watkins PA. Very-long-chain acyl-CoA synthetases. J Biol Chem. 2008;283(4):1773–1777.
   PubMed Web of Science ®Google Scholar
• Zimmerman AW, Veerkamp JH. Members of the fatty acid-binding protein family inhibit cell-free protein synthesis. FEBS Lett. 1998;437(3):183–186.
   PubMed Web of Science ®Google Scholar
• Chmurzynska A. The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet. 2006;47:39–48.
   PubMed Web of Science ®Google Scholar
• Floresta G, Pistara V, Amata E, et al. Adipocyte fatty acid binding protein 4 (FABP4) inhibitors. A comprehensive systematic review. Eur J Med Chem. 2017;138:854–873.
   PubMed Web of Science ®Google Scholar
• Cho KH, Kim MJ, Jeon GJ, Chung HY. Association of genetic variants for FABP3 gene with back fat thickness and intramuscular fat content in pig. Mol Biol Rep. 2011;38(3):2161–2166.
   PubMed Web of Science ®Google Scholar
• Cho S, Park TS, Yoon DH, et al. Identification of genetic polymorphisms in FABP3 and FABP4 and putative association with back fat thickness in Korean native cattle. BMB Rep. 2008;41(1):29–34.
   PubMed Web of Science ®Google Scholar
• Hoashi S, Hinenoya T, Tanaka A, et al. Association between fatty acid compositions and genotypes of FABP4 and LXR-alpha in Japanese black cattle. BMC Genet. 2008;9(1):84.
   PubMedGoogle Scholar
• Zhang L, Zhao Y, Ning Y, Wang H, Zan L. Ectopical expression of FABP4 gene can induce bovine muscle-derived stem cells adipogenesis. Biochem Biophys Res Commun. 2017;482(2):352–358.
   PubMed Web of Science ®Google Scholar
• Martins TS, Sanglard LMP, Silva W, et al. Molecular factors underlying the deposition of intramuscular fat and collagen in skeletal muscle of Nellore and Angus cattle. PLOS One. 2015;10(10):e0139943.
   PubMed Web of Science ®Google Scholar
• Duarte MS, Paulino PV, Das AK, et al. Enhancement of adipogenesis and fibrogenesis in skeletal muscle of Wagyu compared with Angus cattle. J Anim Sci. 2013;91(6):2938–2946.
   PubMed Web of Science ®Google Scholar
• Gregory KE, Cundiff LV, Koch RM, Dikeman ME, Koohmaraie M. Breed effects, retained heterosis, and estimates of genetic and phenotypic parameters for carcass and meat traits of beef cattle. J Anim Sci. 1994;72(5):1174–1183.
   PubMed Web of Science ®Google Scholar
• Grigoletto L, Ferraz JBS, Oliveira HR, et al. Genetic architecture of carcass and meat quality traits in Montana Tropical® composite beef cattle. Front Genet. 2020;11:123–123.
   PubMed Web of Science ®Google Scholar
• Park B, Choi T, Kim S, Oh SH. National genetic evaluation (system) of hanwoo (korean native cattle). Asian-Australas J Anim Sci. 2013;26(2):151–156.
   PubMed Web of Science ®Google Scholar
• Lim D, Choi BH, Cho YM, et al. Analysis of extended haplotype in Korean cattle (Hanwoo) population. BMB Rep. 2016;49(9):514–519.
   PubMed Web of Science ®Google Scholar
• Bedhane M, van der Werf J, Gondro C, et al. Genome-wide association study of meat quality traits in Hanwoo beef cattle using imputed whole-genome sequence data. Front Genet. 2019;10:1235.
   PubMed Web of Science ®Google Scholar
• Pino LMD, Arana A, Alfonso L, Mendizábal JA, Soret B. Adiposity and adipogenic gene expression in four different muscles in beef cattle. PLOS One. 2017;12(6):e0179604.
   PubMed Web of Science ®Google Scholar
• Mei C, Wang H, Liao Q, et al. Genome-wide analysis reveals the effects of artificial selection on production and meat quality traits in Qinchuan cattle. Genomics. 2019;111(6):1201–1208.
   PubMed Web of Science ®Google Scholar
• Wei D, Raza SHA, Zhang J, et al. Polymorphism in promoter of SIX4 gene shows association with its transcription and body measurement traits in Qinchuan cattle. Gene. 2018;656:9–16.
   PubMed Web of Science ®Google Scholar
• Chen N, Huang J, Zulfiqar A, et al. Population structure and ancestry of Qinchuan cattle. Anim Genet. 2018;49(3):246–248.
   PubMed Web of Science ®Google Scholar
• Khan R, Raza SHA, Junjvlieke Z, et al. Function and transcriptional regulation of bovine TORC2 gene in adipocytes: roles of C/EBP, XBP1, INSM1 and ZNF263. Int J Mol Sci. 2019;20.
   Web of Science ®Google Scholar
• Han RH, Zan LS, Yang DP, Hao RC. SNPs detection of IGF2 gene and its relationship with carcass and meat quality traits in Qinchuan cattle. Yi Chuan Hereditas. 2009;30(12):1579–1584.
   Google Scholar
•  LM, Cai H, Sun X, Plath M, et al. Global transcriptome analysis during adipogenic differentiation and involvement of transthyretin gene in adipogenesis in cattle. Front. Genet. 2018;9:13.
   PubMed Web of Science ®Google Scholar
• Folch Fau - Lees MJ, Lees G, Fau - Sloane Stanley HM, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem. 1957;226(1):497–509. PMID: 13428781
   Google Scholar
• Hassen A, Wilson De Fau-Amin VR, Amin Vr Fau-Rouse GH, Rouse Gh Fau-Hays CL, Hays CL. Predicting percentage of intramuscular fat using two types of real-time ultrasound equipment. J Anim Sci. 2001;9(1):11–18.
   Google Scholar
• Boesch C, Slotboom J, Hoppeler H, Kreis R. In vivo determination of intra-myocellular lipids in human muscle by means of localized 1H-MR-spectroscopy. Magn Reson Med. 1997;37(4):484–493.
   PubMed Web of Science ®Google Scholar
• Essen-Gustavsson B, Karlsson A, Lundstrom K, Enfalt AC. Intramuscular fat and muscle fibre lipid contents in halothane-gene-free pigs fed high or low protein diets and its relation to meat quality. Meat Sci. 1994;38(2):269–277.
   PubMed Web of Science ®Google Scholar
• Albrecht E, Teuscher F, Ender K, Wegner J. Growth- and breed-related changes of marbling characteristics in cattle. J Anim Sci. 2006;84(5):1067–1075.
   PubMed Web of Science ®Google Scholar
• Gao Y, Zhang R, Hu X, Li N. Application of genomic technologies to the improvement of meat quality of farm animals. Meat Sci. 2007;77(1):36–45.
   PubMed Web of Science ®Google Scholar
• Allais S, Journaux L, Leveziel H, et al. Effects of polymorphisms in the calpastatin and μ-calpain genes on meat tenderness in 3 French beef breeds. J Anim Sci. 2011;89(1):1–11.
   PubMed Web of Science ®Google Scholar
• Reardon W, Mullen AM, Sweeney T, Hamill RM. Association of polymorphisms in candidate genes with colour, water-holding capacity, and composition traits in bovine M. longissimus and M. semimembranosus. Meat Sci. 2010;86(2):270–275.
   PubMed Web of Science ®Google Scholar
• Albrecht E, Gotoh T, Ebara F, et al. Cellular conditions for intramuscular fat deposition in Japanese Black and Holstein steers. Meat Sci. 2011;89(1):13–20.
   PubMed Web of Science ®Google Scholar
• Lee S-H, Gondro C, van der Werf J, et al. Use of a bovine genome array to identify new biological pathways for beef marbling in Hanwoo (Korean Cattle). BMC Genomics. 2010;11(1):623–623.
   PubMedGoogle Scholar
• Sasaki Y, Nagai K, Nagata Y, et al. Exploration of genes showing intramuscular fat deposition-associated expression changes in musculus longissimus muscle. Animal Genetics. 2006;37(1):40–46.
   PubMed Web of Science ®Google Scholar
• Farmer SR. Transcriptional control of adipocyte formation. Cell Metab. 2006;4(4):263–273.
   PubMed Web of Science ®Google Scholar
• Rosen ED, Walkey CJ, Puigserver P, Spiegelman BM. Transcriptional regulation of adipogenesis. Genes Dev. 2000;14(11):1293–1307.
   PubMed Web of Science ®Google Scholar
• Wei DW, Gui LS, Raza SHA, et al. NRF1 and ZSCAN10 bind to the promoter region of the SIX1 gene and their effects body measurements in Qinchuan cattle. Sci Rep. 2017;7(1):7867.
   PubMedGoogle Scholar
• Liang C, Li A, Raza SHA, et al. The molecular characteristics of the FAM13A gene and the role of transcription factors ACSL1 and ASCL2 in its core promoter region. Genes. 2019;10(12):981.
   Web of Science ®Google Scholar
• Wei Y, Chhiba K, Zhang F, et al. Transcriptional regulation by CpG sites methylation in the core promoter region of the bovine SIX1 gene: roles of histone H4 and E2F2. IJMS. 2018;20(1):19.
   Google Scholar
• Dekkers JC. Commercial application of marker- and gene-assisted selection in livestock: strategies and lessons. J Anim Sci. 2004;82(E-Suppl):E313–328.
   PubMedGoogle Scholar
• Gui LS, Hao RJ, Zhang YR, Zhao XL, Zan LS. Haplotype distribution in the class I sirtuin genes and their associations with ultrasound carcass traits in Qinchuan cattle (Bos taurus). Mol Cell Probes. 2015;29(3):167–171.
   PubMed Web of Science ®Google Scholar
• Yang WC, Wang YN, Fu CZ, Zan LS. Association study and expression analysis of MTNR1A as a candidate gene for body measurement and meat quality traits in Qinchuan cattle. Gene. 2015;570(2):199–204.
   PubMed Web of Science ®Google Scholar
• Wang G, Zhang S, Wei S, et al. Novel polymorphisms of SIX4 gene and their association with body measurement traits in Qinchuan cattle. Gene. 2014;539(1):107–110.
   PubMed Web of Science ®Google Scholar
• Liu H, Tian W, Zan L, Wang H, Cui H. Mutations of MC4R gene and its association with economic traits in Qinchuan cattle. Mol Biol Rep. 2010;37(1):535–540.
   PubMed Web of Science ®Google Scholar
• Fontanesi L, Scotti E, Buttazzoni L, et al. Confirmed association between a single nucleotide polymorphism in the FTO gene and obesity-related traits in heavy pigs. Mol Biol Rep. 2010;37(1):461–466.
   PubMed Web of Science ®Google Scholar
• Wang X, Khan R, Raza SHA, et al. Molecular characterization of ABHD5 gene promoter in intramuscular preadipocytes of Qinchuan cattle: roles of Evi1 and C/EBPα. Gene. 2019;690:38–47.
   PubMed Web of Science ®Google Scholar
• Raza SHA, Khan R, Schreurs NM, et al. Expression of the bovine KLF6 gene polymorphisms and their association with carcass and body measures in Qinchuan cattle (Bos taurus). Genomics. 2020;112(1):423–431.
   PubMed Web of Science ®Google Scholar
• Raza SHA, Khan R, Abdelnour SA, et al. Advances of molecular markers and their application for body variables and carcass traits in Qinchuan cattle. Genes. 2019;10(9):717.
   PubMed Web of Science ®Google Scholar
• Junjvlieke Z, Mei C-G, Khan R, et al. Transcriptional regulation of bovine elongation of very long chain fatty acids protein 6 in lipid metabolism and adipocyte proliferation. J Cell Biochem. 2019;120(8):13932–13943.
   PubMed Web of Science ®Google Scholar
• Gui L-s, Raza SHA, Sun Y-g, Khan R, Ullah I, Han Y-c. Detection of polymorphisms in the promoter of bovine SIRT1 gene 'and their effects on intramuscular fat content in Chinese indigenous cattle. Gene. 2019;700:47–51.
   PubMed Web of Science ®Google Scholar
• Wu S, Wang Y, Ning Y, et al. Genetic variants in STAT3 promoter regions and their application in molecular breeding for body size traits in Qinchuan cattle. IJMS. 2018;19(4):1035.
   Google Scholar
• Raza SHA, Gui L, Khan R, et al. Association between FASN gene polymorphisms ultrasound carcass traits and intramuscular fat in Qinchuan cattle. Gene. 2018;645:55–59.
   PubMed Web of Science ®Google Scholar
• Wei D-W, Gui L-S, Raza SHA, et al. NRF1 and ZSCAN10 bind to the promoter region of the SIX1 gene and their effects body measurements in Qinchuan cattle. Sci Rep. 2017;7(1).
   Google Scholar
• Mi X, Ning Y, Wang X, et al. GR and Foxa1 promote the transcription of ANGPTL4 in bovine adipocytes. Mol Cell Probes. 2019;48:101443.
   PubMed Web of Science ®Google Scholar
• Khan R, Raza SHA, Schreurs N, et al. Bioinformatics analysis and transcriptional regulation of TORC1 gene through transcription factors NRF1 and Smad3 in bovine preadipocytes. Genomics. 2020;112(2):1575–1587.
   PubMed Web of Science ®Google Scholar
• Zhao ZD, Zan LS, Li AN, et al. Characterization of the promoter region of the bovine long-chain acyl-CoA synthetase 1 gene: Roles of E2F1, Sp1, KLF15, and E2F4. Sci Rep. 2016;6:19661.
   PubMed Web of Science ®Google Scholar
• Zhang L, Ning Y, Li P, Guo H, Zan L. Tissue expression analysis and characterization of Smad3 promoter in bovine myoblasts and preadipocytes. DNA Cell Biol. 2018;37(6):551–559.
   PubMed Web of Science ®Google Scholar
• Hong J, Mei C, Wang X, Cheng G, Zan L. Bioinformatics analysis and competitive regulation by transcription factors of SIRT5 at the core promoter region using bovine adipocytes. DNA Cell Biol. 2018;37(12):1003–1015.
   PubMed Web of Science ®Google Scholar
• Hong JY, Mei CG, Li SJ, Wang HB, Zhao CP, Zan LS. Coordinate regulation by transcription factors and DNA methylation in the core promoter region of SIRT6 in bovine adipocytes. Arch Biochem Biophys. 2018;659:1–12.
   PubMed Web of Science ®Google Scholar
• Hong J, Li S, Wang X, Mei C, Zan L. Study of expression analysis of SIRT4 and the coordinate regulation of bovine adipocyte differentiation by SIRT4 and its transcription factors. Biosci Rep. 2018;38(6).
   Google Scholar
• Hong J, Wang X, Mei C, Zan L. Competitive regulation by transcription factors and DNA methylation in the bovine SIRT5 promoter: Roles of E2F4 and KLF6. Gene. 2019;684:39–46.
   PubMed Web of Science ®Google Scholar
• Guo H, Khan R, Raza SHA, et al. KLF15 promotes transcription of KLF3 gene in bovine adipocytes. Gene. 2018;659:77–83.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang Y, Su X, Wang H, Yang W, Zan L. Cooperative and independent functions of the miR-23a∼27a∼24-2 cluster in bovine adipocyte adipogenesis. IJMS. 2018;19(12):3957.
   Google Scholar
• Senyilmaz D, Virtue S, Xu XJ, et al. Regulation of mitochondrial morphology and function by stearoylation of TFR1. Nature. 2015;525(7567):124–128.
   PubMed Web of Science ®Google Scholar
• Chen S, He H, Liu XL. Tissue expression profiles and transcriptional regulation of elongase of very long chain fatty acid 6 in bovine mammary epithelial cells. PLOS One. 2017;12(4):e0175777.
   PubMed Web of Science ®Google Scholar
• Mei cg. Research on the genetic characteristics of QinChuan cattle, Japanese Black cattle, Angus cattle and Gayal based on multi-omics analysis. Thesis submitted to college of animal science and technology. Northwest Agriculture and Forestry University, 2017.
   Google Scholar
• Junjvlieke Z, Khan R, Mei C, et al. Effect of ELOVL6 on the lipid metabolism of bovine adipocytes. Genomics. 2020;112(3):2282–2290.
   PubMed Web of Science ®Google Scholar
• Hashmi S, Zhang J, Siddiqui SS, Parhar RS, Bakheet R, Al-Mohanna F. Partner in fat metabolism: role of KLFs in fat burning and reproductive behavior. 3 Biotech. 2011;1(2):59–72.
   PubMedGoogle Scholar
• Wang F, Tong Q. Transcription factor PU.1 is expressed in white adipose and inhibits adipocyte differentiation. Am J Physiol Cell Physiol. 2008;295(1):C213–C220.
   PubMed Web of Science ®Google Scholar
• Lane JM, Doyle JR, Fortin JP, Kopin AS, Ordovas JM. Development of an OP9 derived cell line as a robust model to rapidly study adipocyte differentiation. PLOS One. 2014;9(11):e112123.
   PubMed Web of Science ®Google Scholar
• DiSpirito JR, Fang B, Wang FF, Lazar MA. Pruning of the adipocyte peroxisome proliferator-activated receptor γ cistrome by hematopoietic master regulator PU.1. Mol Cell Biol. 2013;33(16):3354–3364.
   PubMed Web of Science ®Google Scholar
• Wei N, Wang Y, Xu RX, et al. PU.1 antisense lncRNA against its mRNA translation promotes adipogenesis in porcine preadipocytes. Anim Genet. 2015;46(2):133–140.
   PubMed Web of Science ®Google Scholar
• Ahn J, Li X, Choi YM, et al. Differential expressions of G0/G1 switch gene 2 and comparative gene identification-58 are associated with fat content in bovine muscle. Lipids. 2014;49(1):1–14.
   PubMed Web of Science ®Google Scholar
• Jin JB, Jin YJ, Rajasekar P, et al. Differential expression of genes associated with lipid metabolism in longissimus dorsi of Korean bulls and steers. Meat Sci. 2012;91(3):284–293.
   PubMed Web of Science ®Google Scholar
• Zhao SM, Ren LJ, Chen L, et al. Differential expression of lipid metabolism related genes in porcine muscle tissue leading to different intramuscular fat deposition. Lipids. 2009;44(11):1029–1037.
   PubMed Web of Science ®Google Scholar
• Haemmerle G, Lass A, Zimmermann R, et al. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science. 2006;312(5774):734–737.
   PubMed Web of Science ®Google Scholar
• Lass A, Zimmermann R, Haemmerle G, et al. Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin-Dorfman syndrome. Cell Metab. 2006;3(5):309–319.
   PubMed Web of Science ®Google Scholar
• Yang X, Lu X, Lombès M, et al. The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab. 2010;11(3):194–205.
   PubMed Web of Science ®Google Scholar
• Lu X, Yang X, Liu J. Differential control of ATGL-mediated lipid droplet degradation by CGI-58 and G0S2. Cell Cycle. 2010;9(14):2719–2725.
   PubMed Web of Science ®Google Scholar
• An Q, Wu D, Ma Y, Zhou B, Liu Q. Suppression of Evi1 promotes the osteogenic differentiation and inhibits the adipogenic differentiation of bone marrow-derived mesenchymal stem cells in vitro. Int J Mol Med. 2015;36(6):1615–1622.
   PubMed Web of Science ®Google Scholar
• Ishibashi J, Firtina Z, Rajakumari S, et al. An evi1-C/EBPβ complex controls peroxisome proliferator-activated receptor γ2 gene expression to initiate white fat cell differentiation. Mol Cell Biol. 2012;32(12):2289–2299.
   PubMed Web of Science ®Google Scholar
• Hwang CS, Mandrup S, Macdougald OA, Geiman DE, Lane MD. Transcriptional activation of the mouse obese (ob) gene by CCAAT/enhancer binding protein alpha. Proc Natl Acad Sci USA. 1996;93(2):873–877.
   PubMed Web of Science ®Google Scholar
• MacDougald OA, Lane MD. Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem. 1995;64:345–373.
   PubMed Web of Science ®Google Scholar
• Lin FT, Lane MD. Antisense CCAAT/enhancer-binding protein RNA suppresses coordinate gene expression and triglyceride accumulation during differentiation of 3T3-L1 preadipocytes. Genes Dev. 1992;6(4):533–544.
   PubMed Web of Science ®Google Scholar
• Black AR, Black JD, Azizkhan-Clifford J. Sp1 and krüppel-like factor family of transcription factors in cell growth regulation and cancer. J Cell Physiol. 2001;188(2):143–160.
   PubMed Web of Science ®Google Scholar
• Dang DT, Pevsner J, Yang VW. The biology of the mammalian Kruppel-like family of transcription factors. Int J Biochem Cell Biol. 2000;32(11–12):1103–1121.
   PubMed Web of Science ®Google Scholar
• Banerjee SS, Feinberg MW, Watanabe M, et al. The Kruppel-like factor KLF2 inhibits peroxisome proliferator-activated receptor-gamma expression and adipogenesis. J Biol Chem. 2003;278(4):2581–2584.
   PubMed Web of Science ®Google Scholar
• Kawamura Y, Tanaka Y, Kawamori R, Maeda S. Overexpression of Kruppel-like factor 7 regulates adipocytokine gene expressions in human adipocytes and inhibits glucose-induced insulin secretion in pancreatic beta-cell line. Mol Endocrinol. 2006;20(4):844–856.
   PubMedGoogle Scholar
• Sue N, Jack BH, Eaton SA, et al. Targeted disruption of the basic Krüppel-like factor gene (Klf3) reveals a role in adipogenesis. Mol Cell Biol. 2008;28(12):3967–3978.
   PubMed Web of Science ®Google Scholar
• Birsoy K, Chen Z, Friedman J. Transcriptional regulation of adipogenesis by KLF4. Cell Metab. 2008;7(4):339–347.
   PubMed Web of Science ®Google Scholar
• Li D, Yea S, Li S, et al. Krüppel-like factor-6 promotes preadipocyte differentiation through histone deacetylase 3-dependent repression of DLK1. J Biol Chem. 2005;280(29):26941–26952.
   PubMed Web of Science ®Google Scholar
• Small KS, Hedman AK, Grundberg E, MuTHER Consortium, et al. Identification of an imprinted master trans regulator at the KLF14 locus related to multiple metabolic phenotypes. Nat Genet. 2011;43(6):561–564.
   PubMed Web of Science ®Google Scholar
• Mori T, Sakaue H, Iguchi H, et al. Role of Krüppel-like factor 15 (KLF15) in transcriptional regulation of adipogenesis. J Biol Chem. 2005;280(13):12867–12875.
   PubMed Web of Science ®Google Scholar
• Bell-Anderson KS, Funnell AP, Williams H, et al. Loss of Krüppel-like factor 3 (KLF3/BKLF) leads to upregulation of the insulin-sensitizing factor adipolin (FAM132A/CTRP12/C1qdc2)). Diabetes. 2013;62(8):2728–2737.
   PubMed Web of Science ®Google Scholar
• Eaton SA, Funnell AP, Sue N, Nicholas H, Pearson RC, Crossley M. A network of Krüppel-like factors (Klfs). Klf8 is repressed by Klf3 and activated by Klf1 in vivo. J Biol Chem. 2008;283(40):26937–26947.
   PubMed Web of Science ®Google Scholar
• Zhang J, Bakheet R, Parhar RS, et al. Regulation of fat storage and reproduction by Krüppel-like transcription factor KLF3 and fat-associated genes in Caenorhabditis elegans. J Mol Biol. 2011;411(3):537–553.
   PubMed Web of Science ®Google Scholar
• Zhang J, Hashmi S, Cheema F, et al. Regulation of lipoprotein assembly, secretion and fatty acid β-oxidation by Krüppel-like transcription factor, klf-3. J Mol Biol. 2013;425(15):2641–2655.
   PubMed Web of Science ®Google Scholar
• Pearson RC, Funnell AP, Crossley M. The mammalian zinc finger transcription factor Krüppel-like factor 3 (KLF3/BKLF) ). IUBMB Life. 2011;63(2):86–93.
   PubMed Web of Science ®Google Scholar
• Zhang ZW, Wu CY, Li H, Wang N. Expression and functional analyses of Krüppel-like factor 3 in chicken adipose tissue. Biosci Biotechnol Biochem. 2014;78(4):614–623.
   PubMed Web of Science ®Google Scholar
• Gray S, Feinberg MW, Hull S, et al. The Kruppel-like factor KLF15 regulates the insulin-sensitive glucose transporter GLUT4. J Biol Chem. 2002;277(37):34322–34328.
   PubMed Web of Science ®Google Scholar
• Funnell AP, Maloney CA, Thompson LJ, et al. Erythroid Krüppel-like factor directly activates the basic Krüppel-like factor gene in erythroid cells. Mol Cell Biol. 2007;27(7):2777–2790.
   PubMed Web of Science ®Google Scholar
• McConnell BB, Yang VW. Mammalian Krüppel-like factors in health and diseases. Physiol Rev. 2010;90(4):1337–1381.
   PubMed Web of Science ®Google Scholar
• Pearson R, Fleetwood J, Eaton S, Crossley M, Bao S. Krüppel-like transcription factors: a functional family. Int J Biochem Cell Biol. 2008;40(10):1996–2001.
   PubMed Web of Science ®Google Scholar
• Nagare T, Sakaue H, Takashima M, et al. The Krüppel-like factor KLF15 inhibits transcription of the adrenomedullin gene in adipocytes. Biochem Biophys Res Commun. 2009;379(1):98–103.
   PubMed Web of Science ®Google Scholar
• Pei H, Yao Y, Yang Y, Liao K, Wu JR. Krüppel-like factor KLF9 regulates PPARγ transactivation at the middle stage of adipogenesis. Cell Death Differ. 2011;18(2):315–327.
   PubMed Web of Science ®Google Scholar
• Turner J, Crossley M. Cloning and characterization of mCtBP2, a co-repressor that associates with basic Krüppel-like factor and other mammalian transcriptional regulators. Embo J. 1998;17(17):5129–5140.
   PubMed Web of Science ®Google Scholar
• Sheetal G, Caroline LD, William B, et al. B. Inês, Perilipin deficiency and autosomal dominant partial lipodystrophy. N Engl J Med. 2011;364:740–748.
   PubMed Web of Science ®Google Scholar
• Maurizi G, Poloni A, Mattiucci D, et al. Human white adipocytes convert into "rainbow" adipocytes in vitro. J Cell Physiol. 2017;232(10):2887–2899.
   PubMed Web of Science ®Google Scholar
• Maurizi G, Petäistö T, Maurizi A, Guardia LD. Key-genes regulating the liposecretion process of mature adipocytes. J Cell Physiol. 2018;233(5):3784–3793.
   PubMed Web of Science ®Google Scholar
• Sun Z, Gong J, Wu H, et al. Perilipin1 promotes unilocular lipid droplet formation through the activation of Fsp27 in adipocytes. Nat Commun. 2013;4:1594.
   PubMed Web of Science ®Google Scholar
• Castro-Chavez F, Yechoor VK, Saha PK, et al. Coordinated upregulation of oxidative pathways and downregulation of lipid biosynthesis underlie obesity resistance in perilipin knockout mice: a microarray gene expression profile. Diabetes. 2003;52(11):2666–2674.
   PubMed Web of Science ®Google Scholar
• Martinez-Botas J, Anderson JB, Tessier D, et al. Absence of perilipin results in leanness and reverses obesity in Lepr(db/db) mice. Nat Genet. 2000;26(4):474–479.
   PubMed Web of Science ®Google Scholar
• Temprano A, Sembongi H, Han GS, et al. Redundant roles of the phosphatidate phosphatase family in triacylglycerol synthesis in human adipocytes. Diabetologia. 2016;59(9):1985–1994.
   PubMed Web of Science ®Google Scholar
• Lee B, Zhu J, Wolins NE, Cheng J-X, Buhman KK. Differential association of adipophilin and TIP47 proteins with cytoplasmic lipid droplets in mouse enterocytes during dietary fat absorption. Biochim Biphys Acta. 2009;1791;1180.
   Web of Science ®Google Scholar
• Shijun L, Khan R, Raza SHA, et al. Function and characterization of the promoter region of perilipin 1 (PLIN1): Roles of E2F1, PLAG1, C/EBPbeta, and SMAD3 in bovine adipocytes. Genomics. 2020;112(3):2400–2409.
   PubMed Web of Science ®Google Scholar
• Laurent G, de Boer VC, Finley LW, et al. SIRT4 represses peroxisome proliferator-activated receptor α activity to suppress hepatic fat oxidation. Mol Cell Biol. 2013;33(22):4552–4561.
   PubMed Web of Science ®Google Scholar
• Ho L, Titus AS, Banerjee KK, et al. SIRT4 regulates ATP homeostasis and mediates a retrograde signaling via AMPK. Aging (Albany NY)). 2013;5(11):835–849.
   PubMedGoogle Scholar
• Laurent G, German NJ, Saha AK, et al. SIRT4 controls the balance between lipid synthesis and catabolism by repressing malonyl-CoA decarboxylase. In: BMC proceedings, Springer; 2012: 30.
   Google Scholar
• Laurent G, German NJ, Saha AK, et al. SIRT4 coordinates the balance between lipid synthesis and catabolism by repressing malonyl CoA decarboxylase. Mol Cell. 2013;50(5):686–698.
   PubMed Web of Science ®Google Scholar
• Saberi M, Bjelica D, Schenk S, et al. Novel liver-specific TORC2 siRNA corrects hyperglycemia in rodent models of type 2 diabetes. Am J Physiol Endocrinol Metab. 2009;297:E1137–E1146.
   Google Scholar
• Hill MJ, Suzuki S, Segars JH, Kino T. corresponding author, CRTC2 is a coactivator of GR and couples GR and CREB in the regulation of hepatic gluconeogenesis. Mol Endocrinol. 2016;30(1):104–117.
   PubMedGoogle Scholar
• Canettieri G, Koo SH, Berdeaux R, et al. Dual role of the coactivator TORC2 in modulating hepatic glucose output and insulin signaling. Cell Metab. 2005;2(5):331–338.
   PubMed Web of Science ®Google Scholar
• Dentin R, Hedrick S, Xie J, Yates J, Montminy M. Hepatic glucose sensing via the CREB coactivator CRTC2. Science. 2008;319(5868):1402–1405.
   PubMed Web of Science ®Google Scholar
• Dentin R, Liu Y, Koo SH, et al. Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2. Nature. 2007;449(7160):366–369.
   PubMed Web of Science ®Google Scholar
• Koo SH, Flechner L, Qi L, et al. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature. 2005;437(7062):1109–1111.
   PubMed Web of Science ®Google Scholar
• Perry RJ, Samuel VT, Petersen KF, Shulman GI. The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature. 2014;510(7503):84–91.
   PubMed Web of Science ®Google Scholar
• Rahnert JA, Zheng B, Hudson MB, Woodworth-Hobbs ME, Price SR. Glucocorticoids alter CRTC-CREB signaling in muscle cells: impact on PGC-1α expression and atrophy markers. PLOS One. 2016;11(7):e0159181.
   PubMed Web of Science ®Google Scholar
• Wang Y, Inoue H, Ravnskjaer K, et al. Targeted disruption of the CREB coactivator Crtc2 increases insulin sensitivity. Proc Natl Acad Sci USA. 2010;107(7):3087–3092.
   PubMed Web of Science ®Google Scholar
•  TG, Le Lay J, White P, Dhir R, Ahima RS, Kaestner KH. CRTC2(TORC2) contributes to the transcriptional response to fasting in the liver but is not required for the maintenance of glucose homeostasis. Cell Metab. 2009;10:7.
   PubMed Web of Science ®Google Scholar
• Samarajeewa NU, Docanto MM, Simpson ER, Brown KA. CREB-regulated transcription co-activator family stimulates promoter II-driven aromatase expression in preadipocytes. Horm Canc. 2013;4(4):233–241.
   PubMed Web of Science ®Google Scholar
• Han J, Li E, Chen L, et al. The CREB coactivator CRTC2 controls hepatic lipid metabolism by regulating SREBP1. Nature. 2015;524(7564):243–246.
   PubMed Web of Science ®Google Scholar