Skip to main content
SpringerLink
Log in

Natural abundance stable carbon isotope evidence for the routing and de novo synthesis of bone FA and cholesterol

  • Articles
  • Published:
Lipids

Abstract

This research reported in this paper investigated the relationship between diet and bone FA and cholesterol in rats raised on a variety of isotopically controlled diets comprising 20% C3 or C4 protein (casein) and C3 and/or C4 nonprotein or energy (sucrose, starch, and oil) macronutrients. Compoundspecific stable carbon isotope analysis (δ13C) was performed on the FA (16∶0, 18∶0, 18∶1, and 18∶2) and cholesterol isolated from the diet (n=4) and bone (n=8) of these animals. The dietary signals reflected by the bone lipids were investigated using linear regression analysis. δ13C values of bone cholesterol and stearic (18∶0) acid were shown to reflect whole-diet δ13C values. whereas the δ13C values of bone palmitic (16∶0), oleic (18∶1), and linoleic (18∶2) acids reflected dietary FA δ13C values. Dietary signal differences are a result of the balance between direct incorporation (or routing) and de novo synthesis of each of these bone lipids. Estimates of the degree of routing of these bone lipids gleaned from correlations between Δ13C dlipid-wdiet (δ13Cdiet lipid-δ13Cwhole diet) spacings and Δ13C blipid-wdiet (δ13Cbone lipid-δ13Cwhole diet fractionations demonstrated that the extent of routing, where 18∶2>16∶0>18∶1>18∶0>cholesterol, reflected the relative abundances of these lipids in the diet. These findings provide the basis for more accurate insights into diet when the δ13C analysis of bone fatty FA or cholesterol is employed.

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

Similar content being viewed by others

Abbreviations

BSTFA:

bis(trimethylsilyl)trifluoroacetamide

GC/C/IRMS:

gas chromatography/combustion/isotope ratio mass spectrometry

TLE:

total lipid extract

TMS:

trimethylsilyl

References

  1. van der Merwe, N.J. (1982) Carbon Isotopes, Photosynthesis and Archaeology, Am. Sci. 70, 596–606.

    Google Scholar 

  2. Chisholm, B.S. (1989) Variation in Diet Reconstructions Based on Stable Carbon Isotopic Evidence, in The Chemistry of Prehistoric Human Bone (Price, T.D., ed.), pp. 10–37, Cambridge University Press, Cambridge.

    Google Scholar 

  3. Lee-Thorp, J.A., Sealy, J.C., and van der Merwe, N.J. (1989) Stable Carbon Isotope Ratio Differences Between Bone Collagen and Bone Apatite, and Their Relationship to Diet, J. Archaeol. Sci. 16, 585–599.

    Article  Google Scholar 

  4. Schwarcz, H.P. (1991) Some Theoretical Aspects of Isotope Paleodiet Studies, J. Archaeol. Sci. 18, 261–275.

    Article  Google Scholar 

  5. Schwarcz, H.P. (2000) Some Biochemical Aspects of Carbon Isotopic Paleodiet Studies, in Biogeochemical Approaches to Paleodietary Analysis (Ambrose, S.H., and Katzenberg, M.A., eds.), pp. 189–209, Kluwer Academic/Plenum New York.

    Google Scholar 

  6. Koch, P.L., Fogel, M.L., and Tuross, N. (1994) Tracing the Diets of Fossil Animals Using Stable Isotopes, in Methods in Ecology, Stable Isotopes in Ecology and Environmental Science (Lajtha, K., and Michener, R.H., eds.), pp. 63–92, Blackwell Scientific Publications, Oxford.

    Google Scholar 

  7. DeNiro, M.J., and Epstein, S. (1978) Influence of Diet on the Distribution of Carbon Isotopes in Animals, Geochim. Cosmochim. Acta 42, 495–506.

    Article  CAS  Google Scholar 

  8. DeNiro, M.J., and Epstein, S. (1981) Influence of Diet on the Distribution of Nitrogen Isotopes in Animals, Geochim. Cosmochim. Acta 45, 341–351.

    Article  CAS  Google Scholar 

  9. Hare, P.E., Fogel, M.L., Stafford, T.W., Jr., Mitchell, A.D., and Hoering, T.C. (1991) The Isotopic Composition of Carbon and Nitrogen in Individual Amino Acids Isolated from Modern and Fossil Proteins, J. Archaeol. Sci. 18, 277–292.

    Article  Google Scholar 

  10. Ambrose, S.H., and Norr, L. (1993) Experimental Evidence for the Relationship of the Carbon Isotope Ratios of Whole Diet and Dietary Protein to Those of Bone Collagen and Carbonate, in Prehistoric Human Bone—Archaeology at the Molecular Level (Lambert, J.B., and Grupe, G., eds.), pp. 1–37, Springer-Verlag, Berlin.

    Google Scholar 

  11. Tieszen, L.L., and Fagre, T. (1993) Effect of Diet Quality and Composition on the Isotopic Composition of Respiratory CO2, Bone Collagen, Bioapatite and Soft Tissues, in Prehistoric Human Bone—Archaeology at the Molecular Level (Lambert, J.B., and Grupe, G., eds.), pp. 121–155, Springer-Verlag, Berlin.

    Google Scholar 

  12. Matthews, D.E., and Hayes, J.M. (1978) Isotope-Ratio-Monitoring Gas Chromatography-Mass Spectrometry, Anal. Chem. 50, 1465–1473.

    Article  CAS  Google Scholar 

  13. Fantle, M.S., Dittel, A.I., Schwalm, S.M., Epifanio, C.E., and Fogel, M.L. (1999) A Food Web Analysis of the Juvenile Crab, Callinectes sapidus, Using Stable Isotopes in Whole Animals and Individual Amino Acids, Oecologia 120, 416–426.

    Article  Google Scholar 

  14. O’Brien, D.M., Fogel, M.L., and Boggs, C.L. (2002) Renewable and Nonrenewable Resources: Amino Acid Turnover and Allocation to Reproduction in Lepidoptera, Proc. Nat. Acad. Sci. USA 99, 4413–4418.

    Article  PubMed  CAS  Google Scholar 

  15. Pond, C.M., and Gilmour, I. (1997) Stable Isotopes in Adipose Tissue Fatty Acids as Indicators of Diet in Arctic Foxes (Alopex lagopus), Proc. Nutr. Soc. 56, 1067–1081.

    Article  PubMed  CAS  Google Scholar 

  16. Stott, A.W., Davies, E., Tuross, N., and Evershed, R.P. (1997) Monitoring the Routing of Dietary and Biosynthesized Lipids through Compound-Specific Stable Isotope δ13C Measurements at Natural Abundance, Naturwissenschaften 84, 82–86.

    Article  PubMed  CAS  Google Scholar 

  17. Hammer, B.T., Fogel, M.L., and Hoering, T.C. (1998) Stable Carbon Isotope Ratios of Fatty Acids in Seagrass and Redhead Ducks, Chem. Geol. 152, 29–41.

    Article  Google Scholar 

  18. Stott, A.W., Evershed, R.P., Jim, S., Jones, V., Rogers, J.M., Tuross, N., and Ambrose, S.H. (1999) Cholesterol as a New Source of Palaeodietary Information: Experimental Approaches and Archaeological Applications, J. Archaeol. Sci. 26, 705–716.

    Article  Google Scholar 

  19. Jim, S. (2000) The Development of Bone Cholesterol δ13C Values as a New Source of Palaeodietary Information: Models of Its Use in Conjunction with Bone Collagen and Apatite δ13C Values, Ph.D. Thesis, University of Bristol, England, pp. 117–123.

    Google Scholar 

  20. Jim, S., Stott, A.W., Evershed, R.P., Rogers, J.M., and Ambrose, S.H. (2001) Animal Feeding Experiments in the Development of Cholesterol as a Palaeodietary Indicator, in Archaeological Sciences ’97 (Millard, A., ed.), pp. 68–77, BAR International Series 939, Oxford.

  21. Voet, D., and Voet, J.G. (1995) Biochemistry, 2nd edn., pp. 687–688, John Wiley & Sons, New York.

    Google Scholar 

  22. McGarry, J.D. (1997) Lipid Metabolism I: Utilization and Storage of Energy in Lipid Form, in Textbook of Biochemistry with Clinical Correlations (Devlin, T.M., ed.), pp. 361–393, Wiley-Liss, New York.

    Google Scholar 

  23. Krebs, H.A., and Lowenstein, J.M. (1960) The Tricarboxylic Acid Cycle, in Metabolic Pathways (Greenberg, D.M., ed.), Vol. 1, pp. 129–203, Academic Press, New York.

    Google Scholar 

  24. Sabine, J.R. (1977) Cholesterol, p. 81, Marcel Dekker, New York.

    Google Scholar 

  25. Das, S.K., Scott, M.T., and Adhikary, P.K. (1975) Effect of the Nature and Amount of Dietary Energy on Lipid Composition of Rat Bone Marrow, Lipids 10, 584–590.

    PubMed  CAS  Google Scholar 

  26. Pauletto, P., Puato, M., Angeli, M.T., Pessina, A.C., Munhambo, A., Bittolo-Bon, G., and Galli, C. (1996) Blood Pressure, Serum Lipids, and Fatty Acids in Populations on a Lake-Fish Diet or on a Vegetarian Diet in Tanzania, Lipids 31, S309-S312.

    PubMed  CAS  Google Scholar 

  27. Vidgren, H.M., Ågren, J.J., Schwab, U., Rissanen, T., Hänninen, O., and Uusitupa, M.I.J. (1997) Incorporation of n−3 Fatty Acids into Plasma Lipid Fractions, and Erythrocyte Membranes and Platelets During Dietary Supplementation with Fish, Fish Oil, and Docosahexaenoic Acid-Rich Oil Among Healthy Young Men, Lipids 32, 697–705.

    Article  PubMed  CAS  Google Scholar 

  28. Alam, S.Q., Kokkinos, P.P., and Alam, B.S. (1993) Fatty Acid Composition and Arachidonic Acid Concentrations in Alveolar Bone of Rats Fed Diets with Different Lipids, Calcified Tissue Int. 53, 330–332.

    Article  CAS  Google Scholar 

  29. Rambjør, G.S., Wålen, A.I., Winsor, S.L., and Harris, W.S. (1996) Eicosapentaenoic Acid Is Primarily Responsible for Hypotriglyceridemic Effect of Fish Oil in Humans, Lipids 31, S45-S49.

    PubMed  Google Scholar 

  30. Rhee, S.K., Reed, R.G., and Brenna, J.T. (1997) Fatty Acid Carbon Isotope Ratios in Humans on Controlled Diets, Lipids 32, 1257–1263.

    Article  PubMed  CAS  Google Scholar 

  31. Mottram, H.R., and Evershed, R.P. (2001) Elucidation of the Composition of Bovine Milk Fat Triacylglycerols Using High-Performance Liquid Chromatography—Atmospheric Pressure Chemical Ionisation Mass Spectrometry, J. Chromatogr. A 926, 239–253.

    Article  PubMed  CAS  Google Scholar 

  32. DeNiro, M.J., and Epstein, S. (1977) Mechanisms of Carbon Isotope Fractionation Associated with Lipid Synthesis, Science 197, 261–263.

    Article  PubMed  CAS  Google Scholar 

  33. Hayes, J.M. (1993) Factors Controlling 13C Contents of Sedimentary Organic Compounds: Principles and Evidence, Mar. Geol. 113, 111–125.

    Article  CAS  Google Scholar 

  34. Jim, S., Ambrose, S.H., and Evershed, R.P. (in press) Stable Carbon Isotopic Evidence for Differences in the Biosynthetic Origin of Bone Cholesterol, Collagen and Apatite: Implications for Their Use in Palaeodietary Reconstruction, Geochim. Cosmochim. Acta.

Download references

Author information

Authors and Affiliations

  1. Department of Anthropology, University of Illinois, Urbana-Champaign, 61801, Urbana, Illinois

    Stanley H. Ambrose

  2. Organic Geochemistry Unit, Biogeochemistry Research Centre, University of Bristol, School of Chemistry, Cantock’s Close, BS8 1TS, Bristol, UK

    Susan Jim & Richard P. Evershed

Authors
  1. Susan Jim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stanley H. Ambrose
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard P. Evershed
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard P. Evershed.

About this article

Cite this article

Jim, S., Ambrose, S.H. & Evershed, R.P. Natural abundance stable carbon isotope evidence for the routing and de novo synthesis of bone FA and cholesterol. Lipids 38, 179–186 (2003). https://doi.org/10.1007/s11745-003-1049-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-003-1049-1

Keywords

Search

Navigation