Skip to main content
Log in

Loss of Fat with Increased Adipose Triglyceride Lipase-Mediated Lipolysis in Adipose Tissue During Laying Stages in Quail

  • Original Article
  • Published:
Lipids

Abstract

The goal of the current study was to investigate regulation of key genes involved in lipid metabolism in adipose and liver to relate lipolytic and lipogenic capacities with physiological changes at the pre-laying, onset of laying, and actively laying stages of quail. Followed by a 50 % increase from pre-laying to onset of laying, adipose to body weight ratio was significantly reduced by 60 % from the onset of laying to the actively laying stage (P < 0.05), mainly resulting from the significantly increased adipocyte size from the pre-laying stage to the onset of laying and reduction of adipocyte size from the onset of laying to the actively laying stage (P < 0.05). In the adipose tissue of actively laying quail, increased protein expression and phosphorylation of adipose triglyceride lipase (ATGL) together with an elevated mRNA expression of comparative gene identification-58, an activator of ATGL, contributes to increased lipolytic activity, as proved by increased amounts of plasma non-esterified fatty acid (P < 0.05). In addition, decreased mRNA expression of fatty acid transport protein in the actively laying quail could contribute to the adipocyte hypotrophy (P < 0.05). In the liver, relative mRNA expression of apo-very low density lipoprotein (VLDL)-II increased significantly from the pre-laying to actively laying stages (P < 0.05), indicating increased apoVLDL-II actively facilitated VLDL secretion in the actively laying quail. These results suggest that the laying birds undergo active lipolysis in the adipocyte, and increase VLDL secretion from the liver in order to secure a lipid supply for yolk maturation.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ACC:

Acetyl-CoA carboxylase

AP:

Alkaline phosphatase

ATGL:

Adipose triglyceride lipase

CGI-58:

Comparative gene identification-58

CSA:

Cross sectional area

FATP1:

Fatty acid transporter protein 1

FAS:

Fatty acid synthase

GPAT:

Glycerol-3-phosphate O-acyltransferase

LPL:

Lipoprotein lipase

NEFA:

Non-esterified fatty acids

RPS13:

Ribosomal protein 13

TAG:

Triacylglycerol

VLDL:

Very low density lipoprotein(s)

References

  1. King JW, List GR (1996) Supercritical fluid technology in oil and lipid chemistry. AOCS Press, Champaign, Illinois

    Google Scholar 

  2. Noble RC, Cocchi M (1990) Lipid metabolism and the neonatal chicken. Prog Lipid Res 29:107–140

    Article  PubMed  CAS  Google Scholar 

  3. Saadoun A, Leclercq B (1983) Comparison of in vivo fatty acid synthesis of the genetically lean and fat chickens. Comp Biochem Physiol Part B Biochem Mol Biol 75:641–644

    CAS  Google Scholar 

  4. Pageaux JF, Joulain C, Fayard JM, Lagarde M, Laugier C (1992) Changes in fatty acid composition of plasma and oviduct lipids during sexual maturation of Japanese quail. Lipids 27:518–521

    Article  CAS  Google Scholar 

  5. Lien T, Lu J, Jan D (2001) Alterations in lipid metabolism between the growing and the laying periods of white leghorn layers. Asian-Aust J Anim Sci 14:1460–1464

    CAS  Google Scholar 

  6. 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  PubMed  CAS  Google Scholar 

  7. Ahmadian M, Abbott MJ, Tang TY, Hudak CSS, Kim Y, Bruss M, Hellerstein MK, Lee HY, Samuel VT, Shulman GI, Wang Y, Duncan RE, Kang C, Sul HK (2001) Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab 13:739–774

    Article  Google Scholar 

  8. Duan W, Fuerst PA (2001) Isolation of a sex-linked DNA sequence in cranes. J Hered 92:392–397

    Article  PubMed  CAS  Google Scholar 

  9. 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  PubMed  CAS  Google Scholar 

  10. Lee K, Shin J, Latshaw JD, Suh Y, Serr J (2009) Cloning of adipose triglyceride lipase complementary deoxyribonucleic acid in poultry and expression of adipose triglyceride lipase during development of adipose in chickens. Poult Sci 88:620–630

    Article  PubMed  CAS  Google Scholar 

  11. Ahmadian M, Duncan RE, Varady KA, Frasson D, Hellerstein MK, Birkenfeld AL, Samuel VT, Shulman GI, Wang YH, Kang CH, Sul HS (2009) Adipose overexpression of desnutrin promotes fatty acid use and attenuates diet-induced obesity. Diabetes 58:855–866

    Article  PubMed  CAS  Google Scholar 

  12. 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  PubMed  CAS  Google Scholar 

  13. Ahmadian M, Duncan RE, Sul HS (2009) The skinny on fat: lipolysis and fatty acid utilization in adipocytes. Trends Endocrinol Metab 20:424–428

    Article  PubMed  CAS  Google Scholar 

  14. 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  PubMed  CAS  Google Scholar 

  15. Ehehalt R, Fullekrug J, Pohl J, Ring A, Herrmann T, Stremmel W (2006) Translocation of long chain fatty acids across the plasma membrane—lipid rafts and fatty acid transport proteins. Mol Cell Biochem 284:135–140

    Article  PubMed  CAS  Google Scholar 

  16. Cunningham MJ, Clifton DK, Steiner RA (1999) Leptin’s actions on the reproductive axis: perspectives and mechanisms. Biol Reprod 60:216–222

    Article  PubMed  CAS  Google Scholar 

  17. Garcia MR, Amstalden M, Morrison CD, Keisler DH, Williams GL (2003) Age at puberty, total fat and conjugated linoleic acid content of carcass, and circulating metabolic hormones in beef heifers fed a diet high in linoleic acid beginning at 4 months of age. J Anim Sci 81:261–268

    PubMed  CAS  Google Scholar 

  18. Euling SY, Selevan SG, Pescovitz OH, Skakkebaek NE (2008) Role of environmental factors in the timing of puberty. Pediatrics 3:S167–S171

    Article  Google Scholar 

  19. Burt SCM, McCartney CR (2010) Obesity and the pubertal transition in girls and boys. Reproduction 140:399–410

    Article  Google Scholar 

  20. Gasser CL, Burke CR, Mussard ML, Behlke EJ, Grum DE, Kinder JE, Day ML (2006) Induction of precocious puberty in heifers II: advanced ovarian follicular development. J Anim Sci 84:2042–2049

    Article  PubMed  CAS  Google Scholar 

  21. Sul HS, Wang D (1998) Nutritional and hormonal regulation of enzymes in fat synthesis: studies of fatty acid synthase and mitochondrial glycerol-3-phosphate acyltransferase gene transcription. Annu Rev Nutr 18:331–351

    Article  PubMed  CAS  Google Scholar 

  22. Tong L (2005) Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell Mol Life Sci 62:1784–1803

    Article  PubMed  CAS  Google Scholar 

  23. Glatz JF, Borchers T, van der Spener F, Vusse GJ (1995) Fatty acids in cell signalling: modulation by lipid binding proteins. Prostag Leukotr Ess 52:121–127

    Article  CAS  Google Scholar 

  24. Luxon BA, Milliano MT, Weisiger RA (2000) Induction of hepatic cytosolic fatty acid binding protein with clofibrate accelerates both membrane and cytoplasmic transport of palmitate. Biochim Biophys Acta 1487:309–318

    Article  PubMed  CAS  Google Scholar 

  25. Wolfrum C, Buhlmann C, Rolf B, Borchers T, Spener F (1999) Variation of liver-type fatty acid binding protein content in the human hepatoma cell line HepG2 by peroxisome proliferators and antisense RNA affects the rate of fatty acid uptake. Biochim Biophys Acta 1437:194–201

    Article  PubMed  CAS  Google Scholar 

  26. Newberry EP, Xie Y, Kennedy S, Han X, Buhman KK, Luo J, Gross RW, Davidson NO (2003) Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J Bio Chem 278:51664–51672

    Article  CAS  Google Scholar 

  27. Sato K, Suzuki K, Akiba Y (2009) Characterisation of chicken portomicron remnant and very low density lipoprotein remnant. J Poult Sci 46:35–39

    Article  CAS  Google Scholar 

  28. Wiskocil R, Bensky P, Dower W, Goldberger RF, Gordon JI, Deeley RG (1980) Coordinate regulation of two estrogen-dependent genes in avian liver. Proc Natl Acad Sci USA 77:4474–4478

    Article  PubMed  CAS  Google Scholar 

  29. Wiskocil R, Goldman P, Deeley RG (1981) Cloning and structural characterization of an estrogen-dependent apolipoprotein gene. J Bio Chem 256:9662–9667

    CAS  Google Scholar 

  30. Schneider WJ, Carroll R, Severson DL, Nimpf J (1990) Apolipoprotein VLDL-II inhibits lipolysis of triglyceride-rich lipoproteins in the laying hen. J Lipid Res 31:507–513

    PubMed  CAS  Google Scholar 

  31. Ding ST, Yen CF, Wang PH, Lin HW, Hsu JC, Shen TF (2007) The differential expression of hepatic genes between prelaying and laying geese. Poult Sci 86:1206–1212

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a National Research Foundation of Korea Grant funded by the Korean government (KRF-2009-220-F00006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kichoon Lee.

About this article

Cite this article

Yang, S., Suh, Y., Choi, Y.M. et al. Loss of Fat with Increased Adipose Triglyceride Lipase-Mediated Lipolysis in Adipose Tissue During Laying Stages in Quail. Lipids 48, 13–21 (2013). https://doi.org/10.1007/s11745-012-3742-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-012-3742-6

Keywords

Navigation