Abstract
Adipose triglyceride lipase (ATGL), catalyzing the initial step of hydrolysis of triacylglycerol (TAG) in adipocytes, has been known to be inhibited by G0/G1 switch gene 2 (G0S2). In this study, we report the porcine G0S2 cDNA and amino acid sequences as well as the expression level of porcine G0S2. The porcine G0S2 mRNA was abundantly expressed in adipose tissue and liver among various tissues. In adipose tissue, porcine G0S2 expression was 16-fold higher in the fat cell fraction than the stromal vascular fraction. The G0S2 level increased significantly during adipogenesis in vitro and in vivo. These data indicate that G0S2 expression is closely associated with lipid accumulation and adipogenesis. Considering G0S2 as an inhibitor of cell proliferation, the relatively low levels of G0S2 in preadipocytes and adipose tissues of fetal and neonatal pigs compared to adipocytes and adipose tissues of adult pigs may allow the fast cell proliferation rates. Further studies showed that a short-term 24-h fast down-regulated G0S2 expression and increased ATGL expression in adipose tissue; however, a long-term calorie restriction for 8 days had no influence on the level of G0S2 but increased ATGL expression. Therefore, porcine G0S2, which is both a negative regulator of ATGL-mediated lipolysis and cell proliferation in adipose tissue, can be down-regulated in vivo by a short-term 24-h fast followed by increased ATGL-mediated lipolysis.
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Abbreviations
- AA:
-
Amino acid
- ATGL:
-
Adipose triglyceride lipase
- DAG:
-
Diacylglycerol
- DLK1:
-
Delta-like 1 homolog
- FBS:
-
Fetal bovine serum
- FFA:
-
Free fatty acids
- G0S2:
-
G0/G1 switch gene 2
- HSL:
-
Hormone sensitive lipase
- LPL:
-
Lipoprotein lipase
- MAG:
-
Monoacylglycerol
- NEFA:
-
Nonesterified fatty acids
- PPARγ:
-
Peroxisome proliferator-activated receptor gamma
- RT-PCR:
-
Reverse transcription polymerase chain reaction
- SV:
-
Stromal vascular
- TAG:
-
Triacylglycerol
References
Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS (2007) Regulation of lipolysis in adipocytes. Annu Rev Nutr 27:79–101
Newsom SA, Schenk S, Thomas KM, Harber MP, Knuth ND, Goldenberg N, Horowitz JF (2010) Energy deficit after exercise augments lipid mobilization but does not contribute to the exercise-induced increase in insulin sensitivity. J Appl Physiol 108:554–560
Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, Riederer M, Lass A, Neuberger G, Eisenhaber F, Hermetter A, Zechner R (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306:1383–1386
Wang SP, Laurin N, Himms-Hagen J, Rudnicki MA, Levy E, Robert MF, Pan L, Oligny L, Mitchell GA (2001) The adipose tissue phenotype of hormone-sensitive lipase deficiency in mice. Obes Res 9:119–128
Yang X, Lu X, Lombes M, Rha GB, Chi YI, Guerin TM, Smart EJ, Liu J (2010) The G0/G1 switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab 11:194–205
Lass A, Zimmermann R, Haemmerle G, Riederer M, Schoiswohl G, Schweiger M, Kienesberger P, Strauss JG, Gorkiewicz G, Zechner R (2006) Adipose triglyceride lipase-mediated lipolysis of cellular fat stores is activated by CGI-58 and defective in Chanarin–Dorfman syndrome. Cell Metab 3:309–319
Cornaciu I, Boeszoermenyi A, Lindermuth H, Nagy HM, Cerk IK, Ebner C, Salzburger B, Gruber A, Schweiger M, Zechner R, Lass A, Zimmermann R, Oberer M (2011) The minimal domain of adipose triglyceride lipase (ATGL) ranges until leucine 254 and can be activated and inhibited by CGI-58 and G0S2, respectively. PLoS ONE 6(10):1–11
Russell L, Forsdyke DR (1991) A human putative lymphocyte G0/G1 switch gene containing a CpG-rich island encodes a small basic protein with the potential to be phosphorylated. DNA and Cell Biol 10(8):581–591
Zandbergen F, Mandard S, Escher P, Tan NS, Patsouris D, Jatkoe T, Pojas-Caro S, Madore S, Wahli W, Tafuri S, Muller M, Kersten S (2005) The G0/G2 switch gene 2 is a novel PPAR target gene. Biochem J 392:313–324
Yamada T, Park CS, Burns A, Nakada D, Lacorazza HD (2012) The cytosolic protein G0S2 maintains quiescence in hematopoietic stem cells. PLoS ONE 7(5):e38280
Oh SA, Suh Y, Pang MG, Lee K (2011) Cloning of avian G(0)/G(1) switch gene 2 genes and developmental and nutritional regulation of G(0)/G(1) switch gene 2 in chicken adipose tissue. J Anim Sci 89:367–375
Nielsen TS, Vendelbo MH, Jessen N, Pedersen SB, Jorgensen JO, Lund S, Moller N (2011) Fasting, but not exercise, increases adipose triglyceride lipase (ATGL) protein and reduces G(0)/G(1) switch gene 2 (G0S2) protein and mRNA content in human adipose tissue. J Clin Endocrinol Metab 96(8):E1293–E1297
Hart HA, Azain MJ, Hausman GJ, Reeves DE, Barb CR (2007) Failure of short-term feed restriction to affect luteinizing hormone and leptin secretion or subcutaneous adipose tissue expression of leptin in the prepubertal gilt. Can J Anim Sci 87:191–197
Deiuliis J, Shin J, Bae D, Azain MJ, Barb R, Lee K (2008) Developmental, hormonal, and nutritional regulation of porcine adipose triglyceride lipase (ATGL). Lipids 43:215–225
Hausman GJ, Poulos S (2004) Recruitment and differentiation of intramuscular preadipocytes in stromal-vascular cell cultures derived from neonatal pig semitendinosus muscles. J Anim Sci 82:429–437
Li B, Zerby HN, Lee K (2007) Heart fatty acid binding protein is up-regulated during porcine adipocyte development. J Anim Sci 85:1651–1659
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Gronke S, Mildner A, Fellert S, Tennagels N, Petry S, Muller G, Jackle H, Kuhnlein RP (2005) Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab 1(5):323–330
Narbonne P, Roy R (2009) Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457:210–214
Grisart B, Coppieters W, Farnir F, Karim L, Ford C, Berzi P, Cambisano N, Mni M, Reig S, Simon P, Spelman R, Georges M, Snell R (2002) Positional candidate cloning of a QTL in dairy cattle: identification of a missense mutation in the bovine DGAT1 gene with major effect on milk yield and composition. Genome Res 12:222–231
Ong KT, Mashek MT, Bu SY, Greenberg AS, Mashek DG (2011) Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 53(1):116–126
Li X, Suh Y, Kim E, Moeller J, Lee K (2012) Alternative splicing and developmental and hormonal regulation of porcine comparative gene identification-58 (CGI-58) mRNA. J Anim Sci 90:4346–4354
Filipak M, Estervig DN, Tzen C-Y, Minoo P, Hoerl BJ, Maercklein PB, Zschunke MA, Edens M, Scott RE (1989) Integrated control of proliferation and differentiation of mesenchymal stem cells. Environ Health Perspect 80:117–125
Gregoire FM (2001) Adipocyte differentiation: from fibroblast to endocrine cells. Exp Biol Med 226:997–1002
Kershaw EE, Schupp M, Guan H-P, Gardner NP, Lazar MA, Flier JS (2007) PPARγ regulates adipose triglyceride lipase in adipocytes in vitro and in vivo. Am J Physiol Endocrinol Metab 293:E1736–E1745
Liu L-F, Purushotham A, Wendel AA, Koba K, DeIuiis J, Lee K, Belury MA (2009) Regulation of adipose triglyceride lipase by rosiglitazone. Diabetes Obes Metab 11:131–142
Acknowledgments
This work was supported by the National Research Foundation of Korea Grant funded by the Korean government (KRF-2009-220-F00006) and the Ohio Agricultural Research and Development Center Director’s Associateship Program.
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11745_2013_3756_MOESM1_ESM.pdf
Multiple alignments of complete coding sequences of G0S2 from Human (GenBank accession NM_015714), Mouse (GenBank accession NM_008059) Berkshire (GenBank accession JQ_013998), Landrace (GenBank accession JQ_013999), and Duroc (GenBank accession JQ_014000). Identities to the human G0S2 nucleotide sequence are denoted by a period, and nucleotide differences among porcine species were indicated by an open box (PDF 83 kb)
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Ahn, J., Oh, SA., Suh, Y. et al. Porcine G0/G1 Switch Gene 2 (G0S2) Expression is Regulated During Adipogenesis and Short-Term In-Vivo Nutritional Interventions. Lipids 48, 209–218 (2013). https://doi.org/10.1007/s11745-013-3756-8
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DOI: https://doi.org/10.1007/s11745-013-3756-8