Journal of Comparative Physiology B

, Volume 165, Issue 5, pp 384–395 | Cite as

Lipoprotein lipase activity and its relationship to high milk fat transfer during lactation in grey seals

  • S. J. Iverson
  • M. Hamosh
  • W. D. Bowen
Original Paper


Lipoprotein lipase regulates the hydrolysis of circulating triglyceride and the uptake of fatty acids by most tissues, including the mammary gland and adipose tissue. Thus, lipoprotein lipase is critical for the uptake and secretion of the long-chain fatty acids in milk and for the assimilation of a high-fat milk diet by suckling young. In the lactating female, lipoprotein lipase appears to be regulated such that levels in adipose tissue are almost completely depressed while those in the mammary gland are high. Thus, circulating fatty acids are directed to the mammary gland for milk fat production. Phocid seals serve as excellent models in the study of lipoprotein lipase and fat transfer during lactation because mothers may fast completely while secreting large quantities of high fat milks and pups deposit large amounts of fat as blubber. We measured pup body composition and milk fat intake by isotope (deuterium oxide) dilution and plasma post-heparin lipoprotein lipase activity in six grey seal (Halichoerus grypus) mother-pup pairs at birth and again late in the 16-day laction period. Maternal post-heparin lipoprotein lipase activity increased by an average of four-fold by late lactation (P=0.027), which paralleled an increase in milk fat concentration (from 38 to 56%; P=0.043). Increasing lipoprotein lipase activity was correlated with increasing milk fat output (1.3–2.1 kg fat per day) over lactation (P=0.019). Maternal plasma triglyceride (during fasting) was inversely correlated to lipoprotein lipase activity (P=0.027) and may be associated with the direct incorporation of longchain fatty acids from blubber into milk. In pups, post-heparin lipoprotein lipase activity was already high at birth and increased as total body fat content (P=0.028) and the ratio of body fat: protein incrased (P=0.036) during lactation. Although pup plasma triglyceride increased with increasing daily milk fat intake (P=0.023), pups effectively cleared lipid from the circulation and deposited 70% of milk fat consumed throughout lactation. Lipoprotein lipase may play an important role in the mechanisms involved with the extraordinary rates of fat transfer in phocid seals.

Key words

Lactation Milk fat transfer Fat deposition Lipoprotein lipase Phocid seals 



free fatty acid


hepatic lipase


lipoprotein lipase


post-heparin hepatic lipase


post-heparin lipoprotein lipase


very low density lipoprotein


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen WV (1976) Biochemical aspects of lipid storage and utilization in animals. Am Zool 16: 631–647Google Scholar
  2. Annison EF, Linzell JL, Fazakerley S, Nichols BW (1967) The oxidation and utilization of palmitate, stearate, oleate and acetate by the mammary gland of the fed goat in relation to their overall metabolism and the role of plasma phospholipids and neutral lipids in milk fat synthesis. Biochem J 102: 637–647Google Scholar
  3. Barry JM, Bartley W, Linzell JL, Robinson DS (1963) The uptake from blood of triglyceride fatty acids of chylomicra and low density lipoproteins by mammary gland of the goat. Biochem J 89: 6–11PubMedGoogle Scholar
  4. Bauman DE, Currie WB (1980) Partitioning of nutrients during pregnancy and lactation: a review of mechanisms involving homeostasis and homeorhesis. J Dairy Sci 63: 1514–1529PubMedGoogle Scholar
  5. Bauman DE, Elliot JM (1983) Control of nutrient partitioning in lactating ruminants. In: Mepham TB (ed) Biochemistry of lactation. Elsevier, Amsterdam, pp 437–468Google Scholar
  6. Belfrage P, Vaughan M (1969) Simple liquid-liquid partition systems for isolation of labeled oleic acid from mixtures with glycerides. J Lipid Res 10: 341–343PubMedGoogle Scholar
  7. Bengtsson G, Olivecrona T (1980) Lipoprotein lipase: mechanism of product inhibition. Eur J Biochem 106: 557–562PubMedGoogle Scholar
  8. Bezman A, Felts JM, Havel RJ (1962) Relation between incorporation of triglyceride fatty acids and heparin-released lipoprotein lipase from adipose tissue slices. J Lipid Res 3: 427–431Google Scholar
  9. Blaxter KL (1962) The energy metabolism of ruminants. Hutchinsin, LondonGoogle Scholar
  10. Boness DJ, Bowen WD, Iverson SJ (1995) Does male harassment of females contribute to reproductive synchrony in the grey seal by affecting maternal performance? Behav Ecol Soc Biol 36: 1–10CrossRefGoogle Scholar
  11. Bowen WD (1991) Behavioural ecology of pinniped neonates. In: Renouf D (ed) Behaviour of pinnipeds. Chapman and Hall, London, pp 66–127Google Scholar
  12. Bowen WD, Oftedal OT, Boness DJ (1985) Birth to weaning in 4 days: remarkable growth in the hooded seal, Cystophora cristata. Can J Zool 63: 2841–2846Google Scholar
  13. Bowen WD, Oftedal OT, Boness DJ (1992) Mass and energy transfer during lactation in a small phocid, the harbor seal (Phoca vitulina). Physiol Zool 65: 844–866Google Scholar
  14. Boyd IL (1991) Changes in plasma progesterone and prolactin concentrations during the annual cycle and the role of prolactin in the maintenance of lactation and luteal development in the Antarctic fur seal (Arctocephalus gazella). J Reprod Fert 91: 637–647Google Scholar
  15. Das JB, Joshi ID, Philippart AI (1982) The storage and synthetic pools of heparin-releasable lipoprotein lipase and hepatic triacylglycerol lipase in the growing puppy. Biochem J 206: 663–666PubMedGoogle Scholar
  16. Dhanireddy R, Hamosh M, Sivasubramanian KN, Chowdry P, Scanlon JW, Hamosh P (1981) Postheparin lipolytic activity and intralipid clearance in very low-birth-weight infants. J Pediatr 98: 617–622PubMedGoogle Scholar
  17. Eckel RH (1989) Lipoprotein lipase. A multifunctional enzyme relevant to common metabolic diseases. N Engl J Med 320: 1060–1068PubMedGoogle Scholar
  18. Eckel RH, Goldberg IJ, Steiner L, Yost TJ, Paterniti JR Jr (1988) Plasma lipolytic activity: relationship to postheparin lipolytic activity and evidence for metabolic regulation. Diabetes 37: 610–615PubMedGoogle Scholar
  19. Fedak MA, Anderson SS (1982) The energetics of lactation: accurate measurements from a large wild mammal, the grey seal (Halichoerus grypus). J Zool (London) 198: 473–479Google Scholar
  20. Fedak MA, Boyd IL, Arnbom T, McCann TS (1989) The energetics of lactation in southern elephant seals Mirounga leonina in relation to the mother's size (abstract). Eighth Biennial Conf Biol Mar Mamm. Galveston, TX, p 19Google Scholar
  21. Folch J, Lees M, Sloane-Stanly GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497–509PubMedGoogle Scholar
  22. Gooden JM, Lascelles AK (1973) Effect of feeding protected lipid on the uptake of precursors of milk fat by the bovine mammary gland. Aust J Biol Sci 26: 1201–1210PubMedGoogle Scholar
  23. Hamosh M, Clary TR, Chernick SS, Scow RO (1970) Lipoprotein lipase activity of adipose and mammary tissue and plasma triglyceride in pregnant and lactating rats. Biochim Biophys Acta 210: 473–482PubMedGoogle Scholar
  24. Hamosh M, Hamosh P (1985) Lipoproteins and lipoprotein lipase. In: Fishman AP, Fisher AB (eds) Handbook of physiology — the respiratory system I. The American Physiological Society, Washington D.C., pp 387–418Google Scholar
  25. Hamosh M, Hamosh P (1986) Lipoprotein lipase, hepatic lipase, and their role in lipid clearing during total parenteral nutrition. In: Lebenthal E (ed) Total parenteral nutrition: indications, utilization, complications, and pathophysiological considerations. Raven Press, New York, pp 29–58Google Scholar
  26. Herzberg GR (1991) Dietary regulation of fatty acid and triglyceride metabolism (The 1990 Borden Award Lecture). Can J Physiol Pharmacol 69: 1637–1647PubMedGoogle Scholar
  27. Ikeda Y, Takagi A, Yamamoto A (1989) Purification and characterization of lipoprotein lipase and hepatic triglyceride lipase from human postheparin plasma: production of monospecific antibody to the individual lipase. Biochim Biophys Acta 1003: 254–269PubMedGoogle Scholar
  28. Iverson SJ (1988) Composition, intake and gastric digestion of milk lipids in pinnipeds. Ph.D. Thesis, University of maryland, College ParkGoogle Scholar
  29. Iverson SJ (1993) Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Symp Zool Soc Lond 66: 263–291Google Scholar
  30. Iverson SJ, Bowen WD, Boness DJ, Oftedal OT (1993) The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiol Zool 66: 61–88Google Scholar
  31. Iverson SJ, Kirk CL, Hamosh M, Newsome J (1991) Milk lipid digestion in the neonatal dog: the combined actions of gastric and bile salt stimulated lipases. Biochim Biophys Acta 1083: 109–119PubMedGoogle Scholar
  32. Iverson SJ, Oftedal OT, Bowen WD, Boness DJ, Sampugna J (1995) Prenatal and postnatal transfer of fatty acids from mother to pup in the hooded seal (Cystophora cristata). J Comp Physiol B 165: 1–12PubMedGoogle Scholar
  33. Iverson SJ, Sampugna J, Oftedal OT (1992) Positional specificity of gastric hydrolysis of long-chain n-3 polyunsaturated fatty acids of seal milk triglycerides. Lipids 27: 870–878PubMedGoogle Scholar
  34. Krauss RM, Levy RI, Fredrickson DS (1974) Selective measurement of two lipase activities in post-heparin plasma from normal subjects and patients with hyperlipoproteinemia. J Clin Invest 54: 1107–1124PubMedGoogle Scholar
  35. Krauss RM, Windmueller HG, Levy RI, Fredrickson DS (1983) Selective measurement of two different triglyceride lipase activities in rat postheparin plasma. J Lipid Res 14: 286–295Google Scholar
  36. Kuusi T, Ehnholm C, Nikkila EA (1980) Immunochemical assay of rat postheparin plasma acylglycerol lipases. Atherosclerosis 35: 363–374PubMedGoogle Scholar
  37. McBride OW, Korn ED (1963) The lipoprotein lipase of mammary gland and the correlation of its activity to lactation. J Lipid Res 4: 17–20Google Scholar
  38. McBride OW, Korn ED (1964) Uptake of free fatty acids and chylomicron glycerides by guinea pig mammary gland in pregnancy and lactation. J Lipid Res 5: 453–458PubMedGoogle Scholar
  39. McCance RA, Widdowson EM (1977) Fat. Pediatr Res 11: 1081–1083Google Scholar
  40. Mehta NR, Jones JB, Hamosh M (1982) Lipases in preterm human milk: ontogeny and physiologic significance. J Pediatr Gastroenterol Nutr 1: 317–326PubMedGoogle Scholar
  41. Millar JS (1977) Adaptive features of mammalian reproduction. Evolution 31: 370–386Google Scholar
  42. Moore JH, Christie WW (1979) Lipid metabolism in the mammary gland of ruminant animals. Prog Lipid Res 17: 347–395PubMedGoogle Scholar
  43. Nelson GJ (1992) Dietary fatty acids and lipid metabolism. In: Chow CK (ed) Fatty acids in foods and their health implications. Dekker, New York, p 437–471Google Scholar
  44. Nilsson-Ehle P, Garfinkel AS, Schotz MC (1980) Lipolytic enzymes and plasma lipoprotein metabolism. Annu Rev Biochem 49: 667–693CrossRefPubMedGoogle Scholar
  45. Nilsson-Ehle P, Schotz MC (1976) A stable, radioactive substrate emulsion for assay of lipoprotein lipase. J Lipid Res 17: 536–541PubMedGoogle Scholar
  46. Nordoy A, Vik-Mo H, Mjos OD, Johnsen R (1977) Free fatty acids in plasma and platelets following low and high-dose heparin during alimentary hyperlipidemia. Acta Med Scand 202: 163–171PubMedGoogle Scholar
  47. Nordoy ES, Blix AS (1985) Energy sources in fasting grey seal pups evaluated with computed tomography. Am J Physiol 249: R471-R476PubMedGoogle Scholar
  48. Oftedal OT (1985) Pregnancy and lactation. In: Hudson RJ, White RG (eds) Bioenergetics of wild herbivores. CRC Press, Boca Raton, Florida, pp 215–238Google Scholar
  49. Oftedal OT, Bowen WD, Widdowson EM, Boness DJ (1989) Effects of suckling and the postsuckling fast on weights of the body and internal organs of harp and hooded seal pups. Biol Neonate 56: 283–300PubMedGoogle Scholar
  50. Oftedal OT, Iverson SJ (1987) Hydrogen isotope methodology for measurement of milk intake and energetics of growth in suckling seals. In: Huntley AC et al (eds) Approaches to marine mammal energetics. Allen Press, Lawrence, Kansas, pp 67–96Google Scholar
  51. Oftedal OT, Iverson SJ, Boness DJ (1987) Milk and energy intakes of suckling California sea lion Zalophus californianus pups in relation to sex, growth, and predicted maintenance requirements. Physiol Zool 60: 560–575Google Scholar
  52. Ortiz CL, LeBoeuf BJ, Costa DP (1978) Water and energy flux in elephant seal pups fasting under natural conditions. Physiol Zool 51: 166–178Google Scholar
  53. Patton S, Jensen RG (1976) Biomedical aspects of lactation with special reference to lipid metabolism and membrane functions of the mammary gland. Pergamon Press, OxfordGoogle Scholar
  54. Planche E, Boulange A, De Gasquet P, Tonnu NT (1980) Importance of muscle lipoprotein lipase in rats during suckling. Am J Physiol 238: E511-E517PubMedGoogle Scholar
  55. Ramirez I, Llobera M, Herrera E (1983) Circulating triacylglycerols, lipoproteins, and tissue lipoprotein lipase activities in rat mothers and offspring during the perinatal period: effect of postmaturity. Metabolism 32: 333–341CrossRefPubMedGoogle Scholar
  56. Rapport MM, Alonzo N (1955) Photometric determination of fatty acid ester groups in phospholipids. J Biol Chem 217: 193–198PubMedGoogle Scholar
  57. Reilly JJ (1991) Adaptations to prolonged fasting in free-living weaned gray seal pups. Am J Physiol 260: R267-R272PubMedGoogle Scholar
  58. Robinson DS (1963) Changes in the lipolytic activity of the guinea pig mammary gland at parturition. J Lipid Res 4: 21–23Google Scholar
  59. Robinson DS (1970) The function of the plasma triglycerides in fatty acid transport. In: Florkin M, Stotz EH (eds) Comprehensive biochemistry, vol 18. Elsevier, Amsterdam, pp 51–116Google Scholar
  60. Rudel LL, Star RJ (1990) Species, diet, and gender differences in plasma postheparin lipolytic activities in non-human primates: relationships with plasma lipids and high density lipoproteins. Arteriosclerosis 10: 350–357PubMedGoogle Scholar
  61. Scow RO (1977) Metabolism of chylomicrons in perfused adipose and mammary tissue of the rat. Fed Proc 36: 182–185PubMedGoogle Scholar
  62. Scow RO, Chernick SS (1970) Mobilization, transport and utilization of free fatty acids. In: Florkin M, Stotz EH (eds) Comprehensive biochemistry. Lipid metabolism. Elsevier, North-Holland, pp 19–49Google Scholar
  63. Scow RO, Chernick SS, Fleck TR (1977) Lipoprotein lipase and uptake of tricylglycerol, cholesterol and phosphatidylcholine from chylomicrons by mammary and adipose tissue of lactating rats in vivo. Biochim Biophys Acta 487: 297–306PubMedGoogle Scholar
  64. Scow RO, Hamosh M, Evans AJ, Blanchette-Mackie EJ (1972) Uptake of blood triglyceride by various tissues. Lipids 7: 497–505PubMedGoogle Scholar
  65. Scow RO, Mendelson CR, Zinder O, Hamosh M, Blanchette-Mackie EJ (1973) Role of lipoprotein lipase in the delivery of dietary fatty acids to lactating mammary tissue. In: Galli G et al (eds) Dietary lipids and postnatal development. Raven Press, New York, pp 91–114Google Scholar
  66. Spooner PM, Garrison MM, Scow RO (1977) Regulation of mammary gland and adipose tissue lipoprotein lipase and blood triacylglycerol in rats during late pregnancy. J Clin Invest 60: 702–708PubMedGoogle Scholar
  67. Spray CM, Widdowson EM (1950) The effect of growth and development on the composition of mammals. Br J Nutr 4: 332–353PubMedGoogle Scholar
  68. Tedman RA (1983) Ultrastructural morphology of the mammary gland with observations on the size distribution of fat droplets in milk of the Weddell seal, Leptonychotes weddelli (Pinnipedia). J Zool (London) 200: 131–141Google Scholar
  69. Thompson PD, Kantor MA, Cullinane EM, Sady SP, Saritelli A, Herbert PN (1986) Postheparin plasma lipolytic activities in physically active and sedentary men after varying and repeated doses of intravenous heparin. Metabolism 35: 999–1004CrossRefPubMedGoogle Scholar
  70. Vance JE, Vance DE (1990) Lipoprotein assembly and secretion by hepatocytes. Annu Rev Nutr 10: 337–356CrossRefPubMedGoogle Scholar
  71. Widdowson EM (1950) Chemical composition of newly born mammals. Nature 166: 626–628PubMedGoogle Scholar
  72. Williamson DH (1980) Integration of metabolism in tissues of the lactating rat. FEBS Lett 117: K93-K105CrossRefPubMedGoogle Scholar
  73. Worthy GAJ, Lavigne DM (1983) Changes in energy stores during postnatal development of the harp seal, Phoca groenlandica. J Mammal 64: 89–96Google Scholar
  74. Worthy GAJ, Lavigne DM (1987) Mass loss, metabolic rate, and energy utilization by harp and grey seal pups during the post-weaning fast. Physiol Zool 47: 153–162Google Scholar
  75. Zaidan H, Gutman A, Berkow S, Hamosh P, Hamosh M (1984) Effect of heparin on serum and tissue lipases in the developing rat. Pediatr Res 18: 1321–1324PubMedGoogle Scholar
  76. Zinder O, Hamosh M, Clary Fleck TR, Scow RO (1974) Effect of prolactin on lipoprotein lipase in mammary gland and adipose tissue in rats. Am J Physiol 226: 744–748Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • S. J. Iverson
    • 1
    • 2
  • M. Hamosh
    • 2
  • W. D. Bowen
    • 3
  1. 1.Canadian Institute of Fisheries TechnologyTechnical University of Nova ScotiaHalifaxCanada
  2. 2.Division of Developmental Biology and Nutrition, Department of PediatricsGeorgetown University Medical CenterWashingtonUSA
  3. 3.Marine Fish DivisionBedford Institute of OceanographyDartmouthCanada

Personalised recommendations