Skip to main content
SpringerLink
Log in

Differential Expressions of G0/G1 Switch Gene 2 and Comparative Gene Identification-58 are Associated with Fat Content in Bovine Muscle

  • Original Article
  • Published:
Lipids

Abstract

Regulation of lipolysis in muscle is a potential mechanism affecting marbling in beef carcasses and fat accumulation in muscles of humans, which is a known risk factor for type 2 diabetes. Adipose triglyceride lipase-mediated lipolysis is inhibited by G0/G1 switch gene 2 (G0S2) and co-activated by comparative gene identification-58 (CGI-58). In this study, bovine G0S2 and CGI-58 were sequenced, and expressions of these genes were compared among various tissues and in muscles between bulls and steers with different degrees of marbling. The protein coding sequences of bovine G0S2 and CGI-58 revealed breed-specific SNPs, causing two amino acid variations for each protein. Bovine CGI-58 mRNA showed two isoforms from alternative splicing. The G0S2 gene was preferentially expressed in fat and, to a lesser degree, in the liver; whereas, CGI-58 was highly expressed in the muscle and fat (P < 0.05), suggesting their association with lipid metabolism in those tissues. The longissimus dorsi muscle (LM) of steers showed higher FABP4, G0S2 and CGI-58 mRNA expression levels than the LM of bulls, implying the roles of those genes more in marbling of steers than in that of bulls. The G0S2 expression was markedly higher in the intramuscular fat (IMF) (P < 0.001); whereas, the CGI-58 expression was significantly higher in the pure muscle portion of the LM of steers (P < 0.01), suggesting that G0S2 and CGI-58 may regulate IMF and intramyocellular triglycerides, respectively. Taken together, our data suggest that G0S2 and CGI-58 are associated with fat content in bovine species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AA:

Amino acid

ABHD5:

α/β Hydrolase domain-containing protein 5

ATGL:

Adipose triglyceride lipase

CGI-58:

Comparative gene identification-58

cDNA:

Complementary DNA

G0S2:

G0/G1 switch gene 2

HSL:

Hormone-sensitive lipase

IMF:

Intramuscular fat

IMTGs:

Intramyocellular triglycerides

LM:

Longissimus dorsi muscle

PCR:

Polymerase chain reaction

qPCR:

Quantitative real-time polymerase chain reaction

RT:

Reverse transcription

TAG:

Triacylglycerol

References

  1. Smith GC, Carpenter ZL, Cross HL, Murphey CE, Abraham HC, Savell JW, Davis GW, Berry BW, Parrish FC Jr (1984) Relationship of USDA marbling groups to palatability of cooked beef. J Food Qual 7:289–308

    Article  Google Scholar 

  2. Bennett GL, Williams CB (1994) Implications of genetic changes in body composition on beef production systems. J Anim Sci 72:2756–2763

    CAS  PubMed  Google Scholar 

  3. Wertz AE, Berger LL, Walker PM, Faulkner DB, McKeith FK, Rodriguez-Zas SL (2002) Early-weaning and postweaning nutritional management affect feedlot performance, carcass merit, and the relationship of 12th-rib fat, marbling score, and feed efficiency among Angus and Wagyu heifers. J Anim Sci 80:28–37

    CAS  PubMed  Google Scholar 

  4. Jeremiah LE (1996) The influence of subcutaneous fat thickness and marbling on beef. Palatability and consumer acceptability. Food Res Int 29:513–520

    Article  Google Scholar 

  5. Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, Hughes SI, Whittington FM (2008) Fat deposition, fatty acid composition and meat quality: a review. Meat Sci 78:343–358

    Article  CAS  PubMed  Google Scholar 

  6. Yang KX, Ma JW, Guo YM, Guo TF, Zhao YG, Ding NS, Betti M, Plastow GS, Huang LS (2010) Correlations between fat depot traits and fatty acid composition in abdominal subcutaneous adipose tissue and longissimus muscle: results from a white Duroc × Erhualian intercross F2 population. J Anim Sci 88:3538–3545

    Article  CAS  PubMed  Google Scholar 

  7. Lee SH, Cho YM, Lee SH, Kim BS, Kim NK, Choy YH, Kim KH, Yoon D, Im SK, Oh SJ, Park EW (2008) Identification of marbling-related candidate genes in M. longissimus dorsi of high- and low marbled Hanwoo (Korean Native Cattle) steers. BMB Reports 41:846–851

    Article  CAS  PubMed  Google Scholar 

  8. Krssak M, Falk Petersen K, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M, Shulman GI (1999) Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia 42:113–116

    Article  CAS  PubMed  Google Scholar 

  9. Virkamäki A, Korsheninnikova E, Seppälä-Lindroos A, Vehkavaara S, Goto T, Halavaara J, Häkkinen AM, Yki-Järvinen H (2001) Intramyocellular lipid is associated with resistance to in vivo insulin actions on glucose uptake, anti-lipolysis, and early insulin signaling pathways in human skeletal muscle. Diabetes 50:2337–2343

    Article  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. Jenkins CM, Mancuso DJ, Yan W, Sims HF, Gibson B, Gross RW (2004) Identification, cloning, expression, and purification of three novel human calcium-independent phospholipase A2 family members possessing triacylglycerol lipase and acylglycerol transacylase activities. J Biol Chem 279:48968–48975

    Article  CAS  PubMed  Google Scholar 

  12. Villena JA, Roy S, Sarkadi-Nagy E, Kim KH, Sul HS (2004) Desnutrin, an adipocyte gene encoding a novel patatin domain-containing protein, is induced by fasting and glucocorticoids: ectopic expression of desnutrin increases triglyceride hydrolysis. J Biol Chem 279:47066–47075

    Article  CAS  PubMed  Google Scholar 

  13. Kershaw EE, Hamm JK, Verhagen LA, Peroni O, Katic M, Flier JS (2006) Adipose triglyceride lipase: function, regulation by insulin, and comparison with adiponutrin. Diabetes 55:148–157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Kim JY, Tillison K, Lee JH, Rearick DA, Smas CM (2006) The adipose tissue triglyceride lipase ATGL/PNPLA2 is downregulated by insulin and TNF-alpha in 3T3-L1 adipocytes and is a target for transactivation by PPAR gamma. Am J Physiol Endocrinol Metab 291:E115–E127

    Article  CAS  PubMed  Google Scholar 

  15. Deiuliis J, Shin J, Murphy E, Kronberg SL, Eastridge ML, Suh Y, Yoon JT, Lee K (2010) Bovine adipose triglyceride lipase is not altered and adipocyte fatty acid-binding protein is increased by dietary flaxseed. Lipids 4:963–973

    Article  Google Scholar 

  16. Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J, Heldmaier G, Maier R, Theussl C, Eder S, Kratky D, Wagner EF, Klingenspor M, Hoefler G, Zechner R (2006) Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312:734–737

    Article  CAS  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed  Google Scholar 

  18. Yang X, Lu X, Lombès M, Rha GB, Chi YI, Guerin TM, Smart EJ, Liu J (2010) The G(0)/G(1) switch gene 2 regulates adipose lipolysis through association with adipose triglyceride lipase. Cell Metab 11:194–205

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  Google Scholar 

  20. Ahn J, Oh SA, Suh Y, Moeller SJ, Lee K (2013) Porcine G0/G1 switch gene 2 (G0S2) expression is regulated during adipogenesis and short-term in vivo nutritional interventions. Lipids 48:209–218

    Article  CAS  PubMed  Google Scholar 

  21. Bong JJ, Jeong JY, Rajasekar P, Cho YM, Kwon EG, Kim HC, Paek BH, Baik M (2012) Differential expression of genes associated with lipid metabolism in longissimus dorsi of Korean bulls and steers. Meat Sci 91:284–293

    Article  CAS  PubMed  Google Scholar 

  22. Ghinis-Hozumi Y, González-Gallardo A, González-Dávalos L, Antaramian A, Villarroya F, Shimada A, Varela-Echavarría A, Mora O (2011) Bovine sirtuins: initial characterization and expression of sirtuins 1 and 3 in liver, muscle, and adipose tissue. J Anim Sci 89:2529–2536

    Article  CAS  PubMed  Google Scholar 

  23. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  24. Jeong JY, Kim JS, Nguyen TH, Lee H-J, Baik M (2013) Wnt/beta-catenin signaling and adipogenic genes are associated with intramuscular fat content in the longissimus dorsi muscle of Korean cattle. Anim Genet 44:627–635

    Article  CAS  PubMed  Google Scholar 

  25. Thompson JD, Higgins DG, Gibson TJ, Clustal W (1994) 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Schweiger M, Lass A, Zimmermann R, Eichmann TO, Zechner R (2009) Neutral lipid storage disease: genetic disorders caused by mutations in adipose triglyceride lipase/PNPLA2 or CGI-58/ABHD5. Am J Physiol Endocrinol Metab 297:E289–E296

    Article  CAS  PubMed  Google Scholar 

  27. Gruber A, Cornaciu I, Lass A, Schweiger M, Poeschl M, Eder C, Kumari M, Schoiswohl G, Wolinski H, Kohlwein SD, Zechner R, Zimmermann R, Oberer M (2010) The N-terminal region of comparative gene identification-58 (CGI-58) is important for lipid droplet binding and activation of adipose triglyceride lipase. J Biol Chem 285:12289–12298

    Article  CAS  PubMed  Google Scholar 

  28. Serr J, Suh Y, Lee K (2011) Cloning of comparative gene identification-58 gene in avian species and investigation of its developmental and nutritional regulation in chicken adipose tissue. J Anim Sci 89:3490–3500

    Article  CAS  PubMed  Google Scholar 

  29. Li X, Suh Y, Kim E, Moeller SJ, 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

    Article  CAS  PubMed  Google Scholar 

  30. Yang X, Lu X, Liu J (2010) Identification of a novel splicing isoform of murine CGI-58. FEBS Lett 584:903–910

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Montero-Moran G, Caviglia JM, McMahon D, Rothenberg A, Subramanian V, Xu Z, Lara-Gonzalez S, Storch J, Carman GM, Brasaemle DL (2010) CGI-58/ABHD5 is a coenzyme a-dependent lysophosphatidic acid acyltransferase. J Lipid Res 51:709–719

    Article  CAS  PubMed  Google Scholar 

  32. Estellé J, Pérez-Enciso M, Mercadé A, Varona L, Alves E, Sánchez A, Folch JM (2006) Characterization of the porcine FABP5 gene and its association with the FAT1 QTL in an Iberian by Landrace cross. Anim Genet 37:589–591

    Article  PubMed  Google Scholar 

  33. Wibowo TA, Gaskins CT, Newberry RC, Thorgaard GH, Michal JJ, Jiang Z (2008) Genome assembly anchored QTL map of bovine chromosome 14. Int J Bio Sci 4:406–414

    Article  CAS  Google Scholar 

  34. Lee SH, van der Werf JH, Lee SH, Park EW, Oh SJ, Gibson JP, Thompson JM (2010) Genetic polymorphisms of the bovine fatty acid binding protein 4 gene are significantly associated with marbling and carcass weight in Hanwoo (Korean Cattle). Anim Genet 41:442–444

    CAS  PubMed  Google Scholar 

  35. Shin J, Li B, Davis ME, Suh Y, Lee K (2009) Comparative analysis of fatty acid-binding protein 4 promoters: conservation of peroxisome proliferator-activated receptor binding sites. J Anim Sci 87:3923–3934

    Article  CAS  PubMed  Google Scholar 

  36. Jurie C, Cassar-Malek I, Bonnet M, Leroux C, Bauchart D, Boulesteix P, Pethick DW, Hocquette JF (2007) Adipocyte fatty acid-binding protein and mitochondrial enzyme activities in muscles as relevant indicators of marbling in cattle. J Anim Sci 85:2660–2669

    Article  CAS  PubMed  Google Scholar 

  37. Saez G, Davail S, Gente`s G, Hocquette JF, Jourdan T, Degrace P, Bae’za E (2009) Gene expression and protein content in relation to intramuscular fat content in Muscovy and Peking ducks. Poult Sci 88:2382–2391

    Article  CAS  PubMed  Google Scholar 

  38. Li WJ, Li HB, Chen JL, Zhao GP, Zheng MQ, Wen J (2008) Gene expression of heart-and adipocyte-fatty acid-binding protein and correlation with intramuscular fat in Chinese chickens. Anim Biotechnol 19:189–193

    Article  CAS  PubMed  Google Scholar 

  39. Ye MH, Chen JL, Zhao GP, Zheng MQ, Wen J (2010) Associations of A-FABP and H-FABP markers with the content of intramuscular fat in Beijing-You chicken. Anim Biotechnol 21:14–24

    Article  CAS  PubMed  Google Scholar 

  40. Gardan D, Louveau I, Gondret F (2007) Adipocyte- and heart-type fatty acid binding proteins are both expressed in subcutaneous and intramuscular porcine (Sus scrofa) adipocytes. Comp Biochem Physiol B 148:14–19

    Article  PubMed  Google Scholar 

  41. Zhao SM, Ren LJ, Chen L, Zhang X, Cheng ML, Li WZ, Zhang YY, Gao SZ (2009) Differential expression of lipid metabolism related genes in porcine muscle tissue leading to different intramuscular fat deposition. Lipids 44:1029–1037

    Article  CAS  PubMed  Google Scholar 

  42. Fischer J, Lefèvre C, Morava E, Mussini JM, Laforêt P, Negre-Salvayre A, Lathrop M, Salvayre R (2007) The gene encoding adipose triglyceride lipase (PNPLA2) is mutated in neutral lipid storage disease with myopathy. Nat Genet 39:28–30

    Article  CAS  PubMed  Google Scholar 

  43. Wu JW, Wang SP, Alvarez F, Casavant S, Gauthier N, Abed L, Soni KG, Yang G, Mitchell GA (2011) Deficiency of liver adipose triglyceride lipase in mice causes progressive hepatic steatosis. Hepatology 54:122–132

    Article  CAS  PubMed  Google Scholar 

  44. Nunes PM, van de Weijer T, Veltien A, Arnts H, Hesselink MK, Glatz JF, Schrauwen P, Tack CJ, Heerschap A (2012) Increased intramyocellular lipids but unaltered in vivo mitochondrial oxidative phosphorylation in skeletal muscle of adipose triglyceride lipase-deficient mice. Am J Physiol Endocrinol Metab 303:E71–E81

    Article  CAS  PubMed  Google Scholar 

  45. Reilich P, Horvath R, Krause S, Schramm N, Turnbull DM, Trenell M, Hollingsworth KG, Gorman GS, Hans VH, Reimann J, MacMillan A, Turner L, Schollen A, Witte G, Czermin B, Holinski-Feder E, Walter MC, Schoser B, Lochmüller H (2011) The phenotypic spectrum of neutral lipid storage myopathy due to mutations in the PNPLA2 gene. J Neurol 258:1987–1997

    Article  CAS  PubMed  Google Scholar 

  46. 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 53:116–126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Badin PM, Loubière C, Coonen M, Louche K, Tavernier G, Bourlier V, Mairal A, Rustan AC, Smith SR, Langin D, Moro C (2012) Regulation of skeletal muscle lipolysis and oxidative metabolism by the co-lipase CGI-58. J Lipid Res 53:839–848

    Article  CAS  PubMed  Google Scholar 

  48. Lefèvre C, Jobard F, Caux F, Bouadjar B, Karaduman A, Heilig R, Lakhdar H, Wollenberg A, Verret JL, Weissenbach J, Ozgüc M, Lathrop M, Prud’homme JF, Fischer J (2001) Mutations in CGI-58, the gene encoding a new protein of the esterase/lipase/thioesterase subfamily, in Chanarin-Dorfman syndrome. Am J Hum Genet 69:1002–1012

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Ohio Agricultural Research and Development Center Director’s Associateship Program and two Grants from the Next-Generation BioGreen 21 Program (No. PJ008191 and PJ009457), Rural Development Administration, Republic of Korea.

Author information

Authors and Affiliations

  1. Department of Animal Sciences, The Ohio State University, Columbus, OH, 43210, USA

    Jinsoo Ahn, Xiang Li, Young Min Choi, Sangsu Shin, Shin-Ae Oh, Yeunsu Suh & Kichoon Lee

  2. The Ohio State University Interdisciplinary Ph.D. Program in Nutrition, The Ohio State University, Columbus, OH, 43210, USA

    Jinsoo Ahn & Kichoon Lee

  3. Department of Molecular Biotechnology, Chonnam National University, Gwangju, 500-757, Republic of Korea

    Trang Hoa Nguyen

  4. Department of Agricultural Biotechnology and Research Institute for Agriculture and Life Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul, 151-921, Republic of Korea

    Myunggi Baik

  5. Animal Biotechnology Division, National Institute of Animal Science, RDA, Seosuwon-ro 143-13, Gyeonggi, Suwon, 441-706, Republic of Korea

    Seongsoo Hwang

Authors
  1. Jinsoo Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Young Min Choi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sangsu Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shin-Ae Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yeunsu Suh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Trang Hoa Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Myunggi Baik
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Seongsoo Hwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kichoon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kichoon Lee.

About this article

Cite this article

Ahn, J., Li, X., Choi, Y.M. et al. Differential Expressions of G0/G1 Switch Gene 2 and Comparative Gene Identification-58 are Associated with Fat Content in Bovine Muscle. Lipids 49, 1–14 (2014). https://doi.org/10.1007/s11745-013-3866-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-013-3866-3

Keywords

Search

Navigation