Skip to main content
SpringerLink
Log in

Selective Seasonal Fatty Acid Accumulation and Mobilization in the Wild Raccoon Dog (Nyctereutes procyonoides)

  • Original Article
  • Published:
Lipids

Abstract

Previous studies on laboratory rodents, rabbits and humans have demonstrated that fatty acid (FA) mobilization from white adipose tissue (WAT) is selective and its efficiency is related to FA structure. Selective FA mobilization was also documented in a carnivore, the farmed raccoon dog (Nyctereutes procyonoides), fasted for 8 weeks. The present study explored whether similar selectivity of FA mobilization was manifested in wild mammals experiencing seasonal food scarcity and abundance. Fractional mobilization from and incorporation into WAT of a wide spectrum of FA were studied by gas–liquid chromatography from the subcutaneous WAT of free-ranging raccoon dogs with the same individuals sampled in consecutive seasons. The wintertime FA mobilization was selective and mostly confirmed the patterns of FA release in captivity. Mobilization correlated inversely with the FA chain length but increased with unsaturation and when the first double bond was located closer to the methyl end. 18–20C n-3 polyunsaturated FA (PUFA) and 14–17C monounsaturated FA (MUFA) were preferentially mobilized while 19–24C saturated FA and MUFA were preserved during wintering. The summertime FA incorporation correlated inversely with the chain length and increased with unsaturation and in MUFA and PUFA with double bonds closer to the methyl end. The principles of selective FA mobilization were valid in wild mammals. FA incorporation was also selective and reversed the wintertime losses of the preferably mobilized FA.

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
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Bełtowski J (2003) Adiponectin and resistin—new hormones of white adipose tissue. Med Sci Monitor 9:RA55–RA61

    Google Scholar 

  2. Ackman RG, Cunnane SC (1992) Long-chain polyunsaturated fatty acids: sources, biochemistry and nutritional/clinical applications. In: Padley FB (ed) Advances in applied lipid research, vol 1. JAI, London

    Google Scholar 

  3. Pond CM, Mattacks CA (1998) In vivo evidence for the involvement of the adipose tissue surrounding lymph nodes in immune responses. Immunol Lett 63:159–167

    Article  PubMed  CAS  Google Scholar 

  4. Raclot T, Groscolas R (1995) Selective mobilization of adipose tissue fatty acids during energy depletion in the rat. J Lipid Res 36:2164–2173

    PubMed  CAS  Google Scholar 

  5. Spitzer JJ, Nakamura H, Gold M, Altschuler H, Lieberson M (1966) Correlation between release of individual free fatty acids and fatty acid composition of adipose tissue. Proc Soc Exp Biol Med 122:1276–1279

    PubMed  CAS  Google Scholar 

  6. Hunter JD, Buchanan H, Nye ER (1970) The mobilization of free fatty acids in relation to adipose tissue triglyceride fatty acids in the rat. J Lipid Res 11:259–265

    PubMed  CAS  Google Scholar 

  7. Connor WE, Lin DS, Colvis C (1996) Differential mobilization of fatty acids from adipose tissue. J Lipid Res 37:290–298

    CAS  Google Scholar 

  8. Halliwell KJ, Fielding BA, Samra JS, Humphreys SM, Frayn KN (1996) Release of individual fatty acids from human adipose tissue in vivo after an overnight fast. J Lipid Res 37:1842–1848

    PubMed  CAS  Google Scholar 

  9. Raclot T, Groscolas R (1993) Differential mobilization of white adipose tissue fatty acids according to chain length, unsaturation, and positional isomerism. J Lipid Res 34:1515–1526

    PubMed  CAS  Google Scholar 

  10. Mustonen A-M, Käkelä R, Käkelä A, Pyykönen T, Aho J, Nieminen P (2007) Lipid metabolism in the adipose tissues of a carnivore, the raccoon dog, during prolonged fasting. Exp Biol Med 232:58–69

    CAS  Google Scholar 

  11. Asikainen J, Mustonen A-M, Hyvärinen H, Nieminen P (2004) Seasonal physiology of the wild raccoon dog (Nyctereutes procyonoides). Zool Sci 21:385–391

    Article  PubMed  Google Scholar 

  12. Viro P (1983) The raccoon dog (in Finnish). In: Koivisto I (ed) Animals in Finland 1. Weilin+Göös, Espoo

    Google Scholar 

  13. Mustonen A-M, Nieminen P, Puukka M, Asikainen J, Saarela S, Karonen S-L, Kukkonen JVK, Hyvärinen H (2004) Physiological adaptations of the raccoon dog (Nyctereutes procyonoides) to seasonal fasting-fat and nitrogen metabolism and influence of continuous melatonin treatment. J Comp Physiol B 174:1–12

    Article  PubMed  CAS  Google Scholar 

  14. Käkelä R, Hyvärinen H (1996) Site-specific fatty acid composition in adipose tissues of several northern aquatic and terrestrial mammals. Comp Biochem Physiol B 115:501–514

    Article  Google Scholar 

  15. Siivonen L (1972) The raccoon dog (in Finnish). In: Siivonen L (ed) Mammals in Finland II. Otava, Keuruu

  16. Wijendran V, Hayes KC (2004) Dietary n-6 and n-3 fatty acid balance and cardiovascular health. Annu Rev Nutr 24:597–615

    Article  PubMed  CAS  Google Scholar 

  17. Iverson SJ, Frost KJ, Lowry LF (1997) Fatty acid signatures reveal fine scale structure of foraging distribution of harbor seals and their prey in Prince William Sound, Alaska. Mar Ecol Prog Ser 151:255–271

    Article  CAS  Google Scholar 

  18. Kauhala K (1992) Ecological characteristics of the raccoon dog in Finland. Ph.D. dissertation. University of Helsinki, Helsinki

  19. Nieminen P, Saarela S, Pyykönen T, Asikainen J, Mononen J, Mustonen A-M (2004) Endocrine response to fasting in the overwintering captive raccoon dog (Nyctereutes procyonoides). J Exp Zool A 301:919–929

    Article  CAS  Google Scholar 

  20. Christie WW (1993) Preparation of ester derivatives of fatty acids for chromatographic analysis. In: Christie WW (ed) Advances in lipid methodology—two. Oily, Dundee

    Google Scholar 

  21. Nieminen P, Käkelä R, Pyykönen T, Mustonen A-M (2006) Selective fatty acid mobilization in the American mink (Mustela vison) during food deprivation. Comp Biochem Physiol B 145:81–93

    Article  PubMed  CAS  Google Scholar 

  22. Ackman RG (1992) Application of gas–liquid chromatography to lipid separation and analysis: qualitative and quantitative analysis. In: Chow CK (ed) Fatty acids in foods and their health implications. Marcel Dekker, NY

    Google Scholar 

  23. Kates M (1986) Techniques of lipidology: isolation, analysis and identification of lipids, 2nd edn. Elsevier, Amsterdam

    Google Scholar 

  24. Kvalheim OM, Karstang TV (1987) A general-purpose program for multivariate data analysis. Chemometr Intell Lab 2:235–237

    Article  CAS  Google Scholar 

  25. Groscolas R (1990) Metabolic adaptations to fasting in emperor and king penguins. In: Davis LS, Darby JT (eds) Penguin biology. Academic, San Diego

    Google Scholar 

  26. Raclot T (1997) Selective mobilization of fatty acids from white fat cells: evidence for a relationship to the polarity of triacylglycerols. Biochem J 322:483–489

    PubMed  CAS  Google Scholar 

  27. Raclot T, Holm C, Langin D (2001) A role for hormone-sensitive lipase in the selective mobilization of adipose tissue fatty acids. Biochim Biophys Acta 1532:88–96

    PubMed  CAS  Google Scholar 

  28. Hazel JR, Sidell BD (2004) The substrate specificity of hormone-sensitive lipase from adipose tissue of the Antarctic fish Trematomus newnesi. J Exp Biol 207:897–903

    Article  PubMed  CAS  Google Scholar 

  29. Raclot T, Oudart H (2000) Net release of individual fatty acids from white adipose tissue during lipolysis in vitro: evidence for selective fatty acid re-uptake. Biochem J 348:129–136

    Article  PubMed  CAS  Google Scholar 

  30. Leyton J, Drury PJ, Crawford MA (1987) Differential oxidation of saturated and unsaturated fatty acids in vivo in the rat. Br J Nutr 57:383–393

    Article  PubMed  CAS  Google Scholar 

  31. Hovik R, Osmundsen H (1987) Peroxisomal β-oxidation of long-chain fatty acids possessing different extents of unsaturation. Biochem J 247:531–535

    PubMed  CAS  Google Scholar 

  32. Raclot T, Leray C, Bach AC, Groscolas R (1995) The selective mobilization of fatty acids is not based on their positional distribution in white-fat-cell triacylglycerols. Biochem J 311:911–916

    PubMed  CAS  Google Scholar 

  33. Raclot T, Holm C, Langin D (2001) Fatty acid specificity of hormone-sensitive lipase: implication in the selective hydrolysis of triacylglycerols. J Lipid Res 42:2049–2057

    PubMed  CAS  Google Scholar 

  34. Nieminen P, Rouvinen-Watt K, Collins D, Grant J, Mustonen A-M (2006) Fatty acid profiles and relative mobilization during fasting in adipose tissue depots of the American marten (Martes americana). Lipids 41:231–240

    Article  PubMed  CAS  Google Scholar 

  35. Soppela P, Nieminen M (2002) Effect of moderate wintertime undernutrition on fatty acid composition of adipose tissues of reindeer (Rangifer tarandus tarandus L.). Comp Biochem Physiol A 132:403–409

    Article  Google Scholar 

  36. Raclot T, Groscolas R (1994) Individual fish-oil n-3 polyunsaturated fatty acid deposition and mobilization rates for adipose tissue of rats in a nutritional steady state. Am J Clin Nutr 60:72–78

    PubMed  CAS  Google Scholar 

  37. Raclot T (2003) Selective mobilization of fatty acids from adipose tissue triacylglycerols. Prog Lipid Res 42:257–288

    Article  PubMed  CAS  Google Scholar 

  38. Sinclair AJ, Attar-Bashi NM, Li D (2002) What is the role of α-linolenic acid for mammals? Lipids 37:1113–1123

    Article  PubMed  CAS  Google Scholar 

  39. Ågren J, Muje P, Hänninen O, Herranen J, Penttilä I (1987) Seasonal variations of lipid fatty acids of boreal freshwater fish species. Comp Biochem Physiol B 88:905–909

    Article  PubMed  Google Scholar 

  40. Żmijewski T, Kujawa R, Jankowska B, Kwiatkowska A, Mamcarz A (2006) Slaughter yield, proximate and fatty acid composition and sensory properties of rapfen (Aspius aspius L) with tissue of bream (Abramis brama L) and pike (Esox lucius L). J Food Compos Anal 19:176–181

    Article  CAS  Google Scholar 

  41. Bernard A, Carlier H (1991) Absorption and intestinal catabolism of fatty acids in the rat: effect of chain length and unsaturation. Exp Physiol 76:445–455

    PubMed  CAS  Google Scholar 

  42. Herzberg GR, Skinner C (1997) Differential accumulation and release of long-chain n-3 fatty acids from liver, muscle, and adipose tissue triacylglycerols. Can J Physiol Pharmacol 75:945–951

    Article  PubMed  CAS  Google Scholar 

  43. Leaf DA, Connor WE, Barstad L, Sexton G (1995) Incorporation of dietary n-3 fatty acids into the fatty acids of human adipose tissue and plasma lipid classes. Am J Clin Nutr 62:68–73

    PubMed  CAS  Google Scholar 

  44. Lhuillery C, Mebarki S, Lecourtier M-J, Demarne Y (1988) Influence of different dietary fats on the incorporation of exogenous fatty acids into rat adipose glycerides. J Nutr 118:1447–1454

    PubMed  CAS  Google Scholar 

  45. Lin DS, Connor WE (1990) Are the n-3 fatty acids from dietary fish oil deposited in the triglyceride stores of adipose tissue? Am J Clin Nutr 51:535–539

    PubMed  CAS  Google Scholar 

  46. Lin DS, Connor WE, Spenler CW (1993) Are dietary saturated, monounsaturated, and polyunsaturated fatty acids deposited to the same extent in adipose tissue of rabbits? Am J Clin Nutr 58:174–179

    PubMed  CAS  Google Scholar 

  47. Perona JS, Portillo MP, Macarulla MT, Tueros AI, Ruiz-Gutiérrez V (2000) Influence of different dietary fats on triacylglycerol deposition in rat adipose tissue. Br J Nutr 84:765–774

    PubMed  CAS  Google Scholar 

  48. Summers LKM, Barnes SC, Fielding BA, Beysen C, Ilic V, Humphreys SM, Frayn KN (2000) Uptake of individual fatty acids into adipose tissue in relation to their presence in the diet. Am J Clin Nutr 71:1470–1477

    PubMed  CAS  Google Scholar 

  49. Cochet N, Georges B, Meister R, Florant GL, Barré H (1999) White adipose tissue fatty acids of alpine marmots during their yearly cycle. Lipids 34:275–281

    Article  PubMed  CAS  Google Scholar 

  50. Frank CL (1991) Adaptations for hibernation in the depot fats of a ground squirrel (Spermophilus beldingi). Can J Zool 69:2707–2711

    Article  Google Scholar 

  51. Melin T, Qi C, Bengtsson-Olivecrona G, Åkesson B, Nilsson A (1991) Hydrolysis of chylomicron polyenoic fatty acid esters with lipoprotein lipase and hepatic lipase. Biochim Biophys Acta 1075:259–266

    PubMed  CAS  Google Scholar 

  52. Wang C-S, Bass H, Whitmer R, McConathy WJ (1993) Effects of albumin and apolipoprotein C-II on the acyl-chain specificity of lipoprotein lipase catalysis. J Lipid Res 34:2091–2098

    PubMed  CAS  Google Scholar 

  53. Sato K, Suzuki K, Akiba Y (1998) Species differences in substrate specificity of lipoprotein lipase purified from chickens and rats. Comp Biochem Physiol A 119:569–573

    Article  CAS  Google Scholar 

  54. Lin K-C, Cross HR, Smith SB (1992) Esterification of fatty acids by bovine intramuscular and subcutaneous adipose tissues. Lipids 27:111–116

    Article  PubMed  CAS  Google Scholar 

  55. Chen Z-Y, Menard CR, Cunnane SC (1995) Moderate, selective depletion of linoleate and α-linolenate in weight-cycled rats. Am J Physiol 268:R498–R505

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the Academy of Finland, the Alfred Kordelin Foundation and the Finnish Game Management Fund. The technical help of Rauni Kojo, Tommi Paakkonen and Kasper Heikkilä is greatly acknowledged.

Author information

Authors and Affiliations

  1. Faculty of Biosciences, University of Joensuu, P.O. Box 111, 80101, Joensuu, Finland

    Anne-Mari Mustonen, Juha Asikainen & Petteri Nieminen

  2. Municipal Veterinary Clinic of Joensuu, Jokikatu 7, 80220, Joensuu, Finland

    Jari Aho

Authors
  1. Anne-Mari Mustonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juha Asikainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jari Aho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Petteri Nieminen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne-Mari Mustonen.

About this article

Cite this article

Mustonen, AM., Asikainen, J., Aho, J. et al. Selective Seasonal Fatty Acid Accumulation and Mobilization in the Wild Raccoon Dog (Nyctereutes procyonoides). Lipids 42, 1155–1167 (2007). https://doi.org/10.1007/s11745-007-3118-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-007-3118-5

Keywords

Search

Navigation