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The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1990 Apr;85(4):1221–1226. doi: 10.1172/JCI114556

The complete digestion of human milk triacylglycerol in vitro requires gastric lipase, pancreatic colipase-dependent lipase, and bile salt-stimulated lipase.

S Bernbäck 1, L Bläckberg 1, O Hernell 1
PMCID: PMC296555  PMID: 2318975

Abstract

Gastric lipase, pancreatic colipase-dependent lipase, and bile salt-stimulated lipase all have potential roles in digestion of human milk triacylglycerol. To reveal the function of each lipase, an in vitro study was carried out with purified lipases and cofactors, and with human milk as substrate. Conditions were chosen to resemble those of the physiologic environment in the gastrointestinal tract of breast-fed infants. Gastric lipase was unique in its ability to initiate hydrolysis of milk triacylglycerol. Activated bile salt-stimulated lipase could not on its own hydrolyze native milk fat globule triacylglycerol, whereas a limited hydrolysis by gastric lipase triggered hydrolysis by bile salt-stimulated lipase. Gastric lipase and colipase-dependent lipase, in combination, hydrolyzed about two thirds of total ester bonds, with monoacylglycerol and fatty acids being the end products. Addition of bile salt-stimulated lipase resulted in hydrolysis also of monoacylglycerol. When acting together with colipase-dependent lipase, bile salt-stimulated lipase contributed also to digestion of tri- and diacylglycerol. We conclude that digestion of human milk triacylglycerol depends on three lipases with unique, only partly overlapping, functions. Their concerted action results in complete digestion with free glycerol and fatty acids as final products.

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Selected References

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  1. Atkinson S. A., Bryan M. H., Anderson G. H. Human milk feeding in premature infants: protein, fat, and carbohydrate balances in the first two weeks of life. J Pediatr. 1981 Oct;99(4):617–624. doi: 10.1016/s0022-3476(81)80275-2. [DOI] [PubMed] [Google Scholar]
  2. Bernbäck S., Bläckberg L., Hernell O. Fatty acids generated by gastric lipase promote human milk triacylglycerol digestion by pancreatic colipase-dependent lipase. Biochim Biophys Acta. 1989 Feb 20;1001(3):286–293. doi: 10.1016/0005-2760(89)90113-6. [DOI] [PubMed] [Google Scholar]
  3. Bernbäck S., Hernell O., Bläckberg L. Bovine pregastric lipase: a model for the human enzyme with respect to properties relevant to its site of action. Biochim Biophys Acta. 1987 Nov 21;922(2):206–213. doi: 10.1016/0005-2760(87)90156-1. [DOI] [PubMed] [Google Scholar]
  4. Bläckberg L., Hernell O., Bengtsson G., Olivecrona T. Colipase enhances hydrolysis of dietary triglycerides in the absence of bile salts. J Clin Invest. 1979 Nov;64(5):1303–1308. doi: 10.1172/JCI109586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bläckberg L., Hernell O., Olivecrona T. Hydrolysis of human milk fat globules by pancreatic lipase: role of colipase, phospholipase A2, and bile salts. J Clin Invest. 1981 Jun;67(6):1748–1752. doi: 10.1172/JCI110213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bläckberg L., Hernell O. The bile-salt-stimulated lipase in human milk. Purification and characterization. Eur J Biochem. 1981 May;116(2):221–225. doi: 10.1111/j.1432-1033.1981.tb05322.x. [DOI] [PubMed] [Google Scholar]
  7. Borgström B., Erlanson-Albertsson C. Hydrolysis of milk fat globules by pancreatic lipase. Role of colipase, phospholipase A2, and bile salts. J Clin Invest. 1982 Jul;70(1):30–32. doi: 10.1172/JCI110599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Borgström B. Fat digestion and absorption. Biomembranes. 1974;4B(0):555–620. doi: 10.1007/978-1-4684-3336-4_1. [DOI] [PubMed] [Google Scholar]
  9. Breckenridge W. C., Marai L., Kuksis A. Triglyceride structure of human milk fat. Can J Biochem. 1969 Aug;47(8):761–769. doi: 10.1139/o69-118. [DOI] [PubMed] [Google Scholar]
  10. Brueton M. J., Berger H. M., Brown G. A., Ablitt L., Iyngkaran N., Wharton B. A. Duodenal bile acid conjugation patterns and dietary sulphur amino acids in the newborn. Gut. 1978 Feb;19(2):95–98. doi: 10.1136/gut.19.2.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chappell J. E., Clandinin M. T., Kearney-Volpe C., Reichman B., Swyer P. W. Fatty acid balance studies in premature infants fed human milk or formula: effect of calcium supplementation. J Pediatr. 1986 Mar;108(3):439–447. doi: 10.1016/s0022-3476(86)80893-9. [DOI] [PubMed] [Google Scholar]
  12. Cohen M., Morgan R. G., Hofmann A. F. Lipolytic activity of human gastric and duodenal juice against medium and long chain triglycerides. Gastroenterology. 1971 Jan;60(1):1–15. [PubMed] [Google Scholar]
  13. Fomon S. J., Ziegler E. E., Thomas L. N., Jensen R. L., Filer L. J., Jr Excretion of fat by normal full-term infants fed various milks and formulas. Am J Clin Nutr. 1970 Oct;23(10):1299–1313. doi: 10.1093/ajcn/23.10.1299. [DOI] [PubMed] [Google Scholar]
  14. Fredrikzon B., Hernell O., Bläckberg L., Olivecrona T. Bile salt-stimulated lipase in human milk: evidence of activity in vivo and of a role in the digestion of milk retinol esters. Pediatr Res. 1978 Nov;12(11):1048–1052. doi: 10.1203/00006450-197811000-00004. [DOI] [PubMed] [Google Scholar]
  15. Fredrikzon B., Olivecrona T. Decrease of lipase and esterase activities in intestinal contents of newborn infants during test meals. Pediatr Res. 1978 May;12(5):631–634. doi: 10.1203/00006450-197805000-00004. [DOI] [PubMed] [Google Scholar]
  16. Gargouri Y., Pieroni G., Lowe P. A., Sarda L., Verger R. Human gastric lipase. The effect of amphiphiles. Eur J Biochem. 1986 Apr 15;156(2):305–310. doi: 10.1111/j.1432-1033.1986.tb09583.x. [DOI] [PubMed] [Google Scholar]
  17. Gargouri Y., Pieroni G., Riviere C., Sauniere J. F., Lowe P. A., Sarda L., Verger R. Kinetic assay of human gastric lipase on short- and long-chain triacylglycerol emulsions. Gastroenterology. 1986 Oct;91(4):919–925. doi: 10.1016/0016-5085(86)90695-5. [DOI] [PubMed] [Google Scholar]
  18. Gargouri Y., Pieroni G., Rivière C., Lowe P. A., Saunière J. F., Sarda L., Verger R. Importance of human gastric lipase for intestinal lipolysis: an in vitro study. Biochim Biophys Acta. 1986 Dec 5;879(3):419–423. doi: 10.1016/0005-2760(86)90234-1. [DOI] [PubMed] [Google Scholar]
  19. HOFMANN A. F., BORGSTROEM B. THE INTRALUMINAL PHASE OF FAT DIGESTION IN MAN: THE LIPID CONTENT OF THE MICELLAR AND OIL PHASES OF INTESTINAL CONTENT OBTAINED DURING FAT DIGESTION AND ABSORPTION. J Clin Invest. 1964 Feb;43:247–257. doi: 10.1172/JCI104909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. HOFMANN A. F., BORGSTROM B. Physico-chemical state of lipids in intestinal content during their digestion and absorption. Fed Proc. 1962 Jan-Feb;21:43–50. [PubMed] [Google Scholar]
  21. HOFMANN A. F. THE FUNCTION OF BILE SALTS IN FAT ABSORPTION. THE SOLVENT PROPERTIES OF DILUTE MICELLAR SOLUTIONS OF CONJUGATED BILE SALTS. Biochem J. 1963 Oct;89:57–68. doi: 10.1042/bj0890057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hernell O., Bläckberg L. Digestion of human milk lipids: physiologic significance of sn-2 monoacylglycerol hydrolysis by bile salt-stimulated lipase. Pediatr Res. 1982 Oct;16(10):882–885. doi: 10.1203/00006450-198210000-00016. [DOI] [PubMed] [Google Scholar]
  23. Hernell O. Human milk lipases. III. Physiological implications of the bile salt-stimulated lipase. Eur J Clin Invest. 1975 Jun 12;5(3):267–272. doi: 10.1111/j.1365-2362.1975.tb02294.x. [DOI] [PubMed] [Google Scholar]
  24. Hernell O., Ward H., Bläckberg L., Pereira M. E. Killing of Giardia lamblia by human milk lipases: an effect mediated by lipolysis of milk lipids. J Infect Dis. 1986 Apr;153(4):715–720. doi: 10.1093/infdis/153.4.715. [DOI] [PubMed] [Google Scholar]
  25. Järvenpä A. L. Feeding the low-birth-weight infant. IV. Fat absorption as a function of diet and duodenal bile acids. Pediatrics. 1983 Nov;72(5):684–689. [PubMed] [Google Scholar]
  26. Järvenpä A. L., Rassin D. K., Kuitunen P., Gaull G. E., Räihä N. C. Feeding the low-birth-weight infant. III. Diet influences bile acid metabolism. Pediatrics. 1983 Nov;72(5):677–683. [PubMed] [Google Scholar]
  27. MATTSON F. H., BECK L. W. The specificity of pancreatic lipase for the primary hydroxyl groups of glycerides. J Biol Chem. 1956 Apr;219(2):735–740. [PubMed] [Google Scholar]
  28. Morgan R. G., Borgström B. The mechanism of fat absorption in the bile fistula rat. Q J Exp Physiol Cogn Med Sci. 1969 Apr;54(2):228–243. doi: 10.1113/expphysiol.1969.sp002021. [DOI] [PubMed] [Google Scholar]
  29. Patton J. S., Rigler M. W., Liao T. H., Hamosh P., Hamosh M. Hydrolysis of triacylglycerol emulsions by lingual lipase. A microscopic study. Biochim Biophys Acta. 1982 Aug 18;712(2):400–407. doi: 10.1016/0005-2760(82)90359-9. [DOI] [PubMed] [Google Scholar]
  30. Patton S., Keenan T. W. The milk fat globule membrane. Biochim Biophys Acta. 1975 Oct 31;415(3):273–309. doi: 10.1016/0304-4157(75)90011-8. [DOI] [PubMed] [Google Scholar]
  31. Plucinski T. M., Hamosh M., Hamosh P. Fat digestion in rat: role of lingual lipase. Am J Physiol. 1979 Dec;237(6):E541–E547. doi: 10.1152/ajpendo.1979.237.6.E541. [DOI] [PubMed] [Google Scholar]
  32. Signer E., Murphy G. M., Edkins S., Anderson C. M. Role of bile salts in fat malabsorption of premature infants. Arch Dis Child. 1974 Mar;49(3):174–180. doi: 10.1136/adc.49.3.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sternby B., Borgström B. Purification and characterization of human pancreatic colipase. Biochim Biophys Acta. 1979 Feb 26;572(2):235–243. doi: 10.1016/0005-2760(79)90039-0. [DOI] [PubMed] [Google Scholar]
  34. Tiruppathi C., Balasubramanian K. A. Single-step purification and amino acid and lipid composition of purified acid lipase from human gastric juice. Indian J Biochem Biophys. 1985 Apr;22(2):111–114. [PubMed] [Google Scholar]
  35. Tomarelli R. M., Meyer B. J., Weaber J. R., Bernhart F. W. Effect of positional distribution on the absorption of the fatty acids of human milk and infant formulas. J Nutr. 1968 Aug;95(4):583–590. doi: 10.1093/jn/95.4.583. [DOI] [PubMed] [Google Scholar]
  36. Wang C. S., Hartsuck J. A., Downs D. Kinetics of acylglycerol sequential hydrolysis by human milk bile salt activated lipase and effect of taurocholate as fatty acid acceptor. Biochemistry. 1988 Jun 28;27(13):4834–4840. doi: 10.1021/bi00413a038. [DOI] [PubMed] [Google Scholar]
  37. Wang C. S., Kuksis A., Manganaro F., Myher J. J., Downs D., Bass H. B. Studies on the substrate specificity of purified human milk bile salt-activated lipase. J Biol Chem. 1983 Aug 10;258(15):9197–9202. [PubMed] [Google Scholar]
  38. Watkins J. B. Mechanisms of fat absorption and the development of gastrointestinal function. Pediatr Clin North Am. 1975 Nov;22(4):721–730. doi: 10.1016/s0031-3955(16)33203-5. [DOI] [PubMed] [Google Scholar]
  39. Williamson S., Finucane E., Ellis H., Gamsu H. R. Effect of heat treatment of human milk on absorption of nitrogen, fat, sodium, calcium, and phosphorus by preterm infants. Arch Dis Child. 1978 Jul;53(7):555–563. doi: 10.1136/adc.53.7.555. [DOI] [PMC free article] [PubMed] [Google Scholar]

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