Skip to main content
SpringerLink
Log in

Positional specificity of gastric hydrolysis of long-chain n−3 polyunsaturated fatty acids of seal milk triglycerides

  • Article
  • Published:
Lipids

Abstract

Long-chain n−3 polyunsaturated fatty acids (n−3 PUFA) of marine oils are important dietary components for both infants and adults, and are incorporated into milks following maternal dietary intake. However, little is known about the hydrolysis of these PUFA from milk triglycerides (TG) by lipases in suckling young. Seals, like humans, possess gastric lipase; however, the milk lipids of seals and sea lions are almost devoid of the readily hydrolyzable medium-chain fatty acids, and are characterized by a large percentage (10–30%) of n−3 PUFA. Gastric hydrolysis of milk lipids was studiedin vivo in suckling pups of three species (the California sea lion, the harp seal and the hooded seal) in order to elucidate the actions and specificity of gastric lipases on milk TG in relation to fatty acid composition and TG structure. Regardless of milk fat content (31–61% fat) or extent of gastric hydrolysis (10–56%), the same fatty acids were preferentially released in all three species, as determined by their relative enrichment in the free fatty acid (FFA) fraction. In addition to 16∶1 and 18∶0, these were the PUFA of 18 carbons and longer, except for 22∶6n−3. Levels of 20∶5n−3 were most notably enriched in FFA, at up to five times that found in the TG. Although 22∶6n−3 was apparently also released from the TG (reduced in the diglyceride), it was also notably reduced in FFA. Positional analysis of milk TG based on the products of Grignard hydrolysis revealed that these PUFA, including 22∶6n−3, were preferentially esterified at the α-position of the TG, and that the fatty acids not released during gastric hydrolysis were located at thesn-2 position. The extreme reduction of 22∶6n−3 and enrichment of 20∶5n−3 in FFA is discussed. Results from this study are consistent with reports that gastric lipase acts stereo-specifically to release fatty acids at the α-positions (sn−3,sn−1). We conclude that the n−3 PUFA in milk are efficiently hydrolyzed by gastric lipase and that this has important implications for digestion of milks enriched in PUFA by neonates in general.

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

BHT:

butylated hydroxytoluene

DG:

diglyceride

FFA:

free fatty acid

GC:

gas chromatograph

GLC:

gas-liquid chromatography

HPLC:

high-performance liquid chromatography

MCFA:

medium-chain fatty acid

MG:

monoglyceride

MUFA:

monounsaturated fatty acid

PUFA:

polyunsaturated fatty acid

SFA:

saturated fatty acid

TG:

triglyceride

TLC:

thin-layer chromatography

References

  1. Phillipson, B.E., Rothrock, D.W., Connor, W.E., Harris, W.S., and Illingworth, D.R. (1985)N. Engl. J. Med. 312, 1210–1216.

    Article  PubMed  CAS  Google Scholar 

  2. Goodnight, S.H., Harris, W.S., Connor, W.E., and Illingworth, D.R. (1982)Arteriosclerosis 2, 87–113.

    PubMed  CAS  Google Scholar 

  3. Kremer, J.M., Bigauoette, J., Michalek, A.V., Timchalk, M.A., Lininger, L., Rynes, R.I., Huyck, C., Zieminski, J., and Bartholomew, L.E. (1985)Lancet 1, 184–187.

    Article  PubMed  CAS  Google Scholar 

  4. Clandinin, M.R., Chappell, J.E., Heim, T., Swyer, P.R., and Chance, G.W. (1981)Early Human Develop. 5, 355–366.

    Article  CAS  Google Scholar 

  5. Crawford, M.A., Hassam, A.G., and Rivers, J.P.W. (1981)Prog. Lipid Res. 20, 31–40.

    Article  PubMed  CAS  Google Scholar 

  6. Garcia, R.E., and Moodie, D.S. (1989)Pediatrics 84, 751–755.

    PubMed  CAS  Google Scholar 

  7. Jensen, R.G. (1989) inTextbook of Gastroenterology and Nutrition in Infancy, 2nd edn. (Lebenthal, E., ed.) pp. 157–208, Raven Press, Ltd., New York.

    Google Scholar 

  8. Harris, W.S., Connor, W.E., and Lindsey, S. (1984)Am. J. Clin. Nutr. 40, 780–785.

    PubMed  CAS  Google Scholar 

  9. Henderson, R.A., Jensen, R.G., Ferris, A.M., Lammi-Keefe, C.J., and Dardick, K.R. (1992)Lipids 27, 863–869.

    PubMed  CAS  Google Scholar 

  10. Sunshine, P., Herbst, J.J., Koldovsky, O., and Kretchmer, N. (1971)Annals. N.Y. Acad. Sci. 176, 16–29.

    CAS  Google Scholar 

  11. Tavolini, N., and Schaffner, F. (1989)Biol. Neonate 55, 124–135.

    Google Scholar 

  12. Watkins, J.B. (1974)Pediat. Clin. N. Am. 21, 501–512.

    PubMed  CAS  Google Scholar 

  13. Bottino, N.R., Vandenberg, G.A., and Reiser, R. (1967)Lipids 2, 489–493.

    Article  CAS  PubMed  Google Scholar 

  14. Brockerhoff, H. (1970)Biochim. Biophys. Acta 22, 559–565.

    Google Scholar 

  15. Ackman, R.G. (1988)Atherosclerosis 70, 171–173.

    Article  PubMed  CAS  Google Scholar 

  16. Brockerhoff, H., and Hoyle, R.J. (1963)Arch. Biochem. Biophys. 102, 452–457.

    Article  PubMed  CAS  Google Scholar 

  17. Brockerhoff, H., Hoyle, R.J., Hwang, P.C., and Litchfield, C. (1968)Lipids 3, 24–29.

    Article  CAS  PubMed  Google Scholar 

  18. Litchfield, C. (1968)Lipids 3, 417–419.

    Article  CAS  PubMed  Google Scholar 

  19. Brockerhoff, H., Ackman, R.G., and Hoyle, R.J. (1963)Arch. Biochem. Biophys. 100, 9–12.

    Article  PubMed  CAS  Google Scholar 

  20. Brockerhoff, H., Hoyle, R.J., and Hwang, P.C. (1966)Can. J. Biochem. 44, 1519–1525.

    CAS  Google Scholar 

  21. Brockerhoff, H., Hoyle, R.J., and Hwang, P.C. (1967)Biochim. Biophys. Acta 144, 541–548.

    PubMed  CAS  Google Scholar 

  22. Lawson, L.D., and Hughes, B.G. (1988)Biochem. Biophys. Res. Commun. 152, 328–332.

    Article  PubMed  CAS  Google Scholar 

  23. Patton, J.S., Rigler, M.W., Liao, T.H., Hamosh, P., and Hamosh, M. (1982)Biochim. Biophys. Acta 712, 400–407.

    PubMed  CAS  Google Scholar 

  24. Patton, J.S., Vetter, R.D., Hamosh, M., Borgström, B., Lindstrom, M., and Carey, M.C. (1985)Food Microstruct 4, 29–41.

    CAS  Google Scholar 

  25. Bitman, J., Wood, D.L., Hamosh, M., Hamosh, P., and Mehta, N. (1983)Am. J. Clin. Nutr. 38, 300–312.

    PubMed  CAS  Google Scholar 

  26. Jensen, R.G. (1988)The Lipids of Human Milk, CRC Press, Boca Raton.

    Google Scholar 

  27. Smith, S., and Abraham, S. (1975) inLipid Research (Paoletti, R., and Kritchevsky, D., eds.) Vol. 13, pp. 195–239, Academic Press, NY.

    Google Scholar 

  28. Iverson, S.J. (1988) Composition, Intake and Gastric Digestion of Milk Lipids in Pinnipeds, Ph.D. Thesis, University of Maryland, College Park.

    Google Scholar 

  29. Iverson, S.J., and Oftedal, O.T. (1989)Eighth Biennial Conference on the Biology of Marine Mammals, Monterey, CA, Dec. 1989, Abstracts.

  30. Oftedal, O.T., Boness, D.J., and Tedman, R.A. (1987)Curr. Mammal. 1, 175–245.

    Google Scholar 

  31. Oftedal, O.T., Iverson, S.J., and Boness, D.J. (1987)Physiol. Zool. 60, 560–575.

    Google Scholar 

  32. Bowen, W.D., Oftedal, O.T., and Boness, D.J. (1985)Can. J. Zool. 63, 2841–2846.

    Google Scholar 

  33. Bowen, W.D., Boness, D.J., and Oftedal, O.T. (1987)Can. J. Zool. 65, 1–8.

    Google Scholar 

  34. York, C.M., Yao, J., Hamosh, M., Oftedal, O.T., Freed, L.M., and Hamosh, P. (1987)FASEB J. 46, 1084 (Abstract).

    Google Scholar 

  35. Yurkowski, M., and Brockerhoff, H. (1966)Biochim. Biophys. Acta 125, 55–59.

    PubMed  CAS  Google Scholar 

  36. Folch, J., Lees, M., and Sloane-Stanley, G.H. (1957)J. Biol. Chem. 226, 497–509.

    PubMed  CAS  Google Scholar 

  37. Bitman, J., Wood, D.L., and Ruth, J.M. (1981)J. Liq. Chrom. 4, 1007–1021.

    CAS  Google Scholar 

  38. Bitman, J., and Wood, D.L. (1982)J. Liq. Chrom. 5, 1152–1162.

    Article  Google Scholar 

  39. Bitman, J., and Wood, D.L. (1981)J. Liq. Chrom. 4, 1023–1034.

    CAS  Google Scholar 

  40. Brockerhoff, H. (1971)Lipids 6, 942–956.

    Article  PubMed  CAS  Google Scholar 

  41. Christie, W.W. (1982)Lipid Analysis, 2nd edn., Pergamon Press, Oxford.

    Google Scholar 

  42. Thomas III, A.E., Scharoun, J.E., and Ralston, H. (1964)J. Am. Oil Chem. Soc. 42, 789–792.

    Google Scholar 

  43. Sampugna, J., Pallansch, L.A., Enig, M.G., and Keeney, M. (1982)J. Chromatogr. 249, 245–255.

    Article  CAS  Google Scholar 

  44. Ackman, R.G., Ratnayake, W.M.N., and Olsson, B. (1988)J. Am. Oil Chem. Soc. 65, 136–138.

    CAS  Google Scholar 

  45. Oftedal, O.T., Boness, D.J., and Bowen, W.D. (1988)Can. J. Zool. 66, 318–322.

    Article  CAS  Google Scholar 

  46. Iverson, S.J., and Oftedal, O.T. (1992)Lipids 27, 940–943.

    PubMed  CAS  Google Scholar 

  47. Iverson, S.J., Kirk, C.K., Hamosh, M., and Newsome, J. (1991)Biochim. Biophys. Acta 1083, 109–119.

    PubMed  CAS  Google Scholar 

  48. DeNigris, S.J., Hamosh, M., Kasbekar, D.K., Fink, C.S., Lee, T.C., and Hamosh, P. (1985)Biochim. Biophys. Acta 836, 67–72.

    PubMed  CAS  Google Scholar 

  49. Fink, C.S., Hamosh, M., Hamosh, P., DeNigris, S.J., and Kasbekar, D.K. (1985)Am. J. Physiol. 248, G68-G72.

    PubMed  CAS  Google Scholar 

  50. DeNigris, S.J., Hamosh, M., Kasbekar, D.K., Lee, T., and Hamosh, P. (1988)Biochim. Biophys. Acta 959, 38–45.

    PubMed  CAS  Google Scholar 

  51. Moreau, H., Laugier, R., Gargouri, Y., Ferrato, F., and Verger, R. (1988)Gastroenterology 95, 1221–1226.

    PubMed  CAS  Google Scholar 

  52. Kirk, C.L., Iverson, S.J., and Hamosh, M. (1991)Biol. Neonate 59, 78–85.

    Article  PubMed  CAS  Google Scholar 

  53. Hamosh, M., and Hamosh, P. (1989) inHuman Gastrointestinal Development (Lebenthal, E., ed.) pp. 251–276, Raven Press, New York.

    Google Scholar 

  54. Tirrupathi, C., and Balasubramanian, K.A. (1982)Biochim. Biophys. Acta 712, 692–697.

    Google Scholar 

  55. Bernback, S., Hernell, O., and Blackberg, L. (1985)Eur. J. Biochem. 148, 233–238.

    Article  PubMed  CAS  Google Scholar 

  56. Docherty, A.J.P., Bodmer, M.W., Angal, S., Verger, R., Riviere, C., Lowe, P.A., Lyons, A., Emtage, J.S., and Harris, T.J.R. (1985)Nucleic Acids Res. 13, 1891–1903.

    PubMed  CAS  Google Scholar 

  57. Bodmer, M.W., Angal, S., Yarrington, G.T., Harris, T.J.R., Lyons, A., King, D.K., Pieroni, G., Riviere, C., Verger, R., and Lowe, P.A. (1987)Biochim. Biophys. Acta 909, 237–244.

    PubMed  CAS  Google Scholar 

  58. Fernando-Warnakulasuriya, G.J.P., Staggers, J.E., Frost, S.C., and Wells, M.A. (1981)J. Lipids Res. 22, 668–674.

    CAS  Google Scholar 

  59. Staggers, J.E., Warnakulasuriya, G.J.P., and Wells, M.A. (1981)J. Lipid Res. 22, 675–679.

    PubMed  CAS  Google Scholar 

  60. Paltauf, R., Esfandi, F., and Holasek, A. (1974)FEBS Lett. 40, 119–123.

    Article  PubMed  CAS  Google Scholar 

  61. Jensen, R.G., Dejong, F.A., Clark, R.M., Palmgren, L.G., Liao, T.H., and Hamosh, M. (1982)Lipids 17, 570–572.

    PubMed  CAS  Google Scholar 

  62. Davies, D.T., Holt, C., and Christie, W.W. (1983) inBiochemistry of Lactation (Mepham, T.B., ed.), pp. 71–117, Elsevier Science Publishers B.V., Amsterdam.

    Google Scholar 

  63. Parodi, P.W. (1982)Lipids 17, 437–442.

    PubMed  CAS  Google Scholar 

  64. Puppione, D.L., Jandacek, R.J., Kunitake, S.T., and Costa, D.P. (1989) inDietary ω3 and ω6 Fatty Acids (Galli, C., and Simopoulos, A.P., eds.), pp. 361–367, Plenum Press, New York.

    Google Scholar 

  65. Ackman, R.G., Eaton, C.A., and Hooper, S.N. (1968)Can. J. Biochem. 46, 197–203.

    PubMed  CAS  Google Scholar 

  66. Bitman, J., Wood, D.L., Liao, T.H., Fink, C.S., Hamosh, P., and Hamosh, M. (1985)Biochim. Biophys. Acta 834, 58–64.

    PubMed  CAS  Google Scholar 

  67. Schlenk, H., Sand, D.M., and Gellerman, J.L. (1969)Biochim. Biophys. Acta 187, 201–207.

    PubMed  CAS  Google Scholar 

  68. Stoffel, W., Ecker, W., Assad, H., and Sprecher, H. (1970)Zeitschr. Physiol. Chem. 351, 1545–1554.

    CAS  Google Scholar 

  69. von Schacky, C., and Weber, P.C. (1985)J. Clin. Invest. 76, 2446–2450.

    Article  Google Scholar 

  70. Breckenridge, W.C., Marai, L., and Kuksis, A. (1969)Can. J. Biochem. 47, 761–769.

    Article  PubMed  CAS  Google Scholar 

  71. Lin, C.Y., Smith, S., and Abraham, S. (1976)J. Lipid Res. 17, 647–656.

    PubMed  CAS  Google Scholar 

  72. Freudenberg, E. (1953)Die Frauenmilch-Lipase, Karger, Basel.

    Google Scholar 

  73. Hernell, O., and Olivecrona, T. (1974)J. Lipid Res. 15, 367–372.

    PubMed  CAS  Google Scholar 

  74. Freed, L.M., York, C.M., Hamosh, M., Sturman, J.T., Oftedal, O.T., and Hamosh, P. (1986) inHuman Lactation, Maternal-Environmental Factors (Hamosh, M., and Goldman, A.S., eds.) Vol. 2, pp. 595–602, Plenum Press, New York.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. National Zoological Park, Smithsonian Institution, 20008, Washington, D.C.

    Sara J. Iverson & Olav T. Oftedal

  2. Department of Chemistry and Biochemistry, University of Maryland, 20742, College Park, Maryland

    Sara J. Iverson & Joseph Sampugna

Authors
  1. Sara J. Iverson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph Sampugna
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olav T. Oftedal
    View author publications

    You can also search for this author in PubMed Google Scholar

About this article

Cite this article

Iverson, S.J., Sampugna, J. & Oftedal, O.T. Positional specificity of gastric hydrolysis of long-chain n−3 polyunsaturated fatty acids of seal milk triglycerides. Lipids 27, 870–878 (1992). https://doi.org/10.1007/BF02535866

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02535866

Keywords

Search

Navigation