Skip to main content
Log in

Seasonal changes in critical enzymes of lipogenesis and triacylglycerol synthesis in the marmot (Marmota flaviventris)

  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Fatty acid metabolism and triacylglycerol synthesis are critical processes for the survival of hibernating mammals that undergo a prolonged fasting period. Fatty acid synthase, fatty-acid-CoA ligase, diacylglycerol acyltransferase, and monoacylglycerol acyltransferase activities were measured in liver and in white and brown adipose tissue, in order to determine whether enzymes of lipogenesis and triacylglycerol synthesis vary seasonally during hibernation in the yellow-bellied marmot (Marmota flaviventris). Compared with mid-winter hibernation, fatty acid synthase activity was higher in all three tissues during early spring when marmots emerged from hibernation and in mid-summer when they were feeding, consistent with the synthesis of fatty acids from the carbohydrate-rich summer diet. Fatty-acid-CoA ligase and diacylglycerol acyltransferase activities were highest in summer in white adipose tissue when triacylglycerol synthesis would be expected to be high; diacylglycerol acyltransferase activity was also high in brown adipose tissue during spring and summer. In liver, however, diacylglycerol acyltransferase specific activity was highest during hibernation, suggesting that triacylglycerol synthesis may be prominent in liver in winter. Monoacylglycerol acyltransferase activity, which may aid in the retention of essential fatty-acids, was 80-fold higher in liver than in white or brown adipose tissue, but did not vary seasonally. Its dependence on palmitoyl-CoA suggests that a divalent cation might play a role in enzyme activation. The high hepatic diacylglycerol acyltransferase activity during hibernation suggests that the metabolism of very low density lipoprotein may be important in the movement of adipose fatty acids to brown adipose tissue and muscle during the rewarming that occurs periodically during hibernation. These studies suggest that enzymes of lipid metabolism vary seasonally in the marmot, consistent with requirements of this hibernator for triacylglycerol synthesis and metabolism.

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.

Similar content being viewed by others

Abbreviations

BAT:

brown adipose tissue

DGAT:

diacylglycerol acyltransferase

FAS:

fatty acid synthase

K m :

Michaelis constant

MGAT:

monoacylglycerol acyltransferase

RQ:

respiratory quotiant

VLDL:

very low density lipoprotein

WAT:

white adipose tissue

References

  • Andersen BO, Turner JJ, Bintz GL (1989) Fatty acid synthetase in control starved, and refed Richardson's ground squirrels. Comp Biochem Physiol 93A:613–616

    Google Scholar 

  • Bell RM, Coleman RA (1983) Enzymes of triacylglycerol formation in mammals. In: Boyer PD (ed) The enzymes, vol XVI. Academic Press, New York, pp 87–112

    Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Google Scholar 

  • Carneheim C, Cannon B, Nedergaard J (1989) Rare fatty acids in brown fat are substrates for thermogenesis during arousal from hibernation. Am J Physiol 256:R146-R154

    Google Scholar 

  • Coleman RA, Haynes EB (1983) Selective changes in microsomal enzymes of triacylglycerol and phosphatidylcholine synthesis in fetal and postnatal rat liver: induction of microsomal snglycerol 3-P and dihydroxyacetone-P acyltransferase activities. J Biol Chem 258:450–465

    Google Scholar 

  • Coleman RA, Haynes EB (1984) Hepatic monoacylglycerol acyltransferase: characterization of an activity associated with the suckling period in rats. J Biol Chem 259:8934–8938

    Google Scholar 

  • Coleman RA, Haynes EB (1986) Monoacylglycerol acyltransferase. Evidence that the activities from rat intestine and suckling liver are tissue-specific isoenzymes. J Biol Chem 261:224–228

    Google Scholar 

  • Coleman RA, Walsh JP, Millington DS, Maltby DA (1986) Stereospecificity of monoacylglycerol acyltransferase activity from rat intestine and suckling rat liver. J Lipid Res 27:158–165

    Google Scholar 

  • Coleman RA, Haynes EB, Coats CD (1987) Ontogeny of microsomal activities of triacylglycerol synthesis in guinea pig liver. J Lipid Res 28:320–325

    Google Scholar 

  • Cooney G, Curi R, Mitchelson A, Newsholme P, Simpson M, Newsholme E (1986) Activities of some key enzymes of carbohydrate, ketone body, adenosine and glutamine metabolism in liver, and brown and white adipose tissue of the rat. Biochem Biophys Res Comm 138:687–692

    Google Scholar 

  • Denyes A, Carter JD (1961) Utilization of acetate-1-14C by hepatic tissue from cold exposed and hibernating hamsters. Am J Physiol 200:1043–1046

    Google Scholar 

  • Fischer PWF, Goodridge AG (1978) Coordinate regulation of acetyl coenzyme A carboxylase and fatty acid synthetase in liver cells of the developing chick in vivo and in culture. Arch Biochem Biophys 190:332–344

    Google Scholar 

  • Florant GLL, Nuttle C, Mullinex DE, Rintoul DA (1990) Plasma and white adipose tissue lipid composition in marmots. Am J Physiol 258:R1123-R1131

    Google Scholar 

  • Florant GL, Hester L, Ameenuddin S, Rintoul DA (1993) The effect of low essential fatty acid diet on hibernation in marmots. Am J Physiol 264:R747–753

    Google Scholar 

  • Geiser F (1990) Influence of polyunsaturated and saturated dietary lipids on adipose tissue, brain and mitochondrial membrane fatty acid composition of a mammalian hibernator. Biochim Biophys Acta 1046:159–166

    Google Scholar 

  • Gurr MI, James AT (1980) Lipid biochemistry: an introduction. Chapman and Hall, London

    Google Scholar 

  • Himms-Hagen J (1989) Brown adipose tissue thermogenesis and obesity. Prog Lipid Res 28:67–115

    Google Scholar 

  • Hsu RY, Yun SL (1970) Stabilization and physiochemical properties of the fatty acid synthetase of chicken liver. Biochem 9:239–245

    Google Scholar 

  • Leibel RL, Hirsch JA (1985) Radioisotopic technique for analysis of free fatty acid reesterification in human adipose tissue. Am J Physiol 248:E140-E147

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr RA Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Google Scholar 

  • MacDonald JIS, Sprecher H (1991) Phospholipid fatty acid remodeling in mammalian cells. Biochim Biophys Acta 1084:105–121

    Google Scholar 

  • McCormack JG (1982) The regulation of fatty acid synthesis in brown adipose tissue by insulin. Prog Lipid Res 21:195–223

    Google Scholar 

  • Merrill AH Jr, Gidwitz S, Bell RM (1982) Facile enzymatic synthesis of fatty acyl-coenzyme A thioesters. J Lipid Res 23:1368–1373

    Google Scholar 

  • Neuringer M, Anderson GK, Connor WE (1988) The essentiality of N-3 fatty acids for the development and function of the retina and brain. Annu Rev Nutr 8:517–541

    Google Scholar 

  • Sansbury D, Millington DS, Coleman RA (1989) Hepatic monoacylglycerol acyltransferase: ontogeny and characterization of an activity associated with the chick embryo. J Lipid Res 30:1251–1258

    Google Scholar 

  • Segal IH (1975) Enzyme kinetics. Wiley, New York

    Google Scholar 

  • Slakey SPM, Lands WEM (1967) The structure of rat liver triglycerides. Lipids 3:30–36

    Google Scholar 

  • South FE, House WA (1967) Energy metabolism in hibernation. In: Fisher KC et al (eds) Mammalian hibernation vol III. Elsevier, New York, pp 305–324

    Google Scholar 

  • Trayhurn P (1980) Fatty acid synthesis in brown adipose tissue in relation to whole body synthesis in the cold-acclimated golden hamster (Mesocricetus auratus). Biochim Biophys Acta 620:10–17

    Google Scholar 

  • Trayhurn P (1981) Fatty acid synthesis in mouse brown adipose tissue: the influence of environmental temperature on the proportion of whole-body fatty acid synthesis in brown adipose tissue and liver. Biochim Biophys Acta 664:549–560

    Google Scholar 

  • Trayhurn P, Douglas JB (1984) Fatty acid synthesis in brown adipose tissue of the Mongolian gerbil (Meriones unguiculatus): influence of acclimation temperature on synthesis in brown adipose tissue and liver in relation to whole body synthesis. Comp Biochem Physiol 78B:601–607

    Google Scholar 

  • Turner JJ, Anderson BO, Bintz GL (1989) Whole-body lipids and fatty acid synthase activity in Richardson's ground squirrels, Spermophilus richardsonii. Physiol Zool 62:1383–1397

    Google Scholar 

  • Wang LCH (1989) Ecological, physiological and biochemical aspects of torpor in mammals and birds. In: Wang LCH (ed) Advances in comparative and environmental physiology. Springer, Berlin, pp 361–401

    Google Scholar 

  • Willis JS (1982) Intermediary metabolism in hibernation. In: Lyman CP et al (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 124–139

    Google Scholar 

  • Xia T, Mostafa N, Bhat BG, Florant GL, Coleman RA (1993) Selective retention of essential fatty acids: the role of hepatic monoacylglycerol acyltransferase. Am J Physiol 265:414–419

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. 2nd edn. Prentice-Hall, Englewood Cliffs, NJ, pp 185–190

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mostafa, N., Everett, D.C., Chou, S.C. et al. Seasonal changes in critical enzymes of lipogenesis and triacylglycerol synthesis in the marmot (Marmota flaviventris). J Comp Physiol B 163, 463–469 (1993). https://doi.org/10.1007/BF00346930

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00346930

Key words

Navigation