Lipids

, 43:663 | Cite as

Vitamin E Transfer from Lipid Emulsions to Plasma Lipoproteins: Mediation by Multiple Mechanisms

  • M. Hacquebard
  • M. Vandenbranden
  • W. J. Malaisse
  • J. M. Ruysschaert
  • R. J. Deckelbaum
  • Y. A. Carpentier
Original Article

Abstract

The present study determined alpha-tocopherol mass transfer from an alpha-tocopherol-rich emulsion to LDL and HDL, and assessed the potential of different mechanisms to modulate alpha-tocopherol transfers. Emulsion particles rich in alpha-tocopherol were incubated in vitro with physiological concentrations of LDL or HDL. The influence of plasma proteins was assessed by adding human lipoprotein poor plasma (LPP) fraction with intact vs heat inactivated PLTP, or with a specific cholesteryl ester transfer protein (CETP) inhibitor, or by adding purified PLTP or pig LPP which lacks CETP activity. After 4 h incubation in absence of LPP, alpha-tocopherol content was increased by ~80% in LDL and ~160% in HDL. Addition of LPP markedly enhanced alpha-tocopherol transfer leading to 350–400% enrichment in LDL or HDL at 4 h. Higher (~10 fold) enrichment was achieved after 20 h incubation with LPP. Facilitation of alpha-tocopherol transfer was (i) more than 50% higher with human vs pig LPP (despite similar PLTP phospholipid transfer activity), (ii) reduced by specific CETP activity inhibition, (iii) not fully suppressed by heat inactivation, and (iv) not restored by purified PLTP. In conclusion, alpha-tocopherol content in LDL and HDL can be markedly raised by rapid transfer from an alpha-tocopherol-rich emulsion. Our results indicate that alpha-tocopherol mass transfer between emulsion particles and lipoproteins is mediated by more than one single mechanism and that this transfer may be facilitated not only by PLTP but likely also by other plasma proteins such as CETP.

Keywords

Vitamin E Alpha-tocopherol mass transfer Lipid emulsions LDL HDL PLTP CETP 

Abbreviations

CETP

Cholesteryl ester transfer protein

HDL

High density lipoproteins

LDL

Low density lipoproteins

LPP

Lipoprotein poor plasma

PLTP

Phospholipid transfer protein

TC

Total cholesterol

TG

Triglycerides

TGRP

Triglyceride-rich particles

Notes

Acknowledgments

M. Hacquebard is recipient of a fellowship from the Danone Institute, Belgium. Prof. R.J. Deckelbaum receives support from NIH grant #HL40404. The authors gratefully thank Dr. E. Niesor and Dr. C. Maugeais (F. Hoffmann-La Roche, Basel, Switzerland) for kindly providing CETP inhibitor and related information.

References

  1. 1.
    Traber MG, Packer L (1995) Vitamin E: beyond antioxidant function. Am J Clin Nutr 62:1501S–1509SPubMedGoogle Scholar
  2. 2.
    Ricciarelli R, Zingg JM, Azzi A (2002) The 80th anniversary of vitamin E: beyond its antioxidant properties. Biol Chem 383:457–465CrossRefPubMedGoogle Scholar
  3. 3.
    Stampfer MJ, Hennekens CH, Manson JE, Colditz GA, Rosner B, Willett WC (1993) Vitamin E consumption and the risk of coronary disease in women. N Engl J Med 328:1444–1449CrossRefPubMedGoogle Scholar
  4. 4.
    Rimm EB, Stampfer MJ, Ascherio A, Giovannucci E, Colditz GA, Willett WC (1993) Vitamin E consumption and the risk of coronary heart disease in men. N Engl J Med 328:1450–1456CrossRefPubMedGoogle Scholar
  5. 5.
    Stephens NG, Parsons A, Schofield PM, Kelly F, Cheeseman K, Mitchinson MJ (1996) Randomised controlled trial of vitamin E in patients with coronary disease: Cambridge Heart Antioxidant Study (CHAOS). Lancet 347:781–786CrossRefPubMedGoogle Scholar
  6. 6.
    Boaz M, Smetana S, Weinstein T, Matas Z, Gafter U, Iaina A, Knecht A, Weissgarten Y, Brunner D, Fainaru M, Green MS (2000) Secondary prevention with antioxidants of cardiovascular disease in endstage renal disease (SPACE): randomised placebo-controlled trial. Lancet 356:1213–1218CrossRefPubMedGoogle Scholar
  7. 7.
    Yusuf S, Dagenais G, Pogue J, Bosch J, Sleight P (2000) Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N Engl J Med 342:154–160CrossRefPubMedGoogle Scholar
  8. 8.
    (1999) Dietary supplementation with n-3 polyunsaturated fatty acids, vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell’Infarto miocardico. Lancet 354:447–455Google Scholar
  9. 9.
    Miller ER 3rd, Pastor-Barriuso R, Dalal D, Riemersma RA, Appel LJ, Guallar E (2005) Meta-analysis: high-dosage vitamin E supplementation may increase all-cause mortality. Ann Intern Med 142:37–46PubMedGoogle Scholar
  10. 10.
    Behrens WA, Thompson JN, Madere R (1982) Distribution of alpha-tocopherol in human plasma lipoproteins. Am J Clin Nutr 35:691–696PubMedGoogle Scholar
  11. 11.
    Traber MG, Lane JC, Lagmay NR, Kayden HJ (1992) Studies on the transfer of tocopherol between lipoproteins. Lipids 27:657–663CrossRefPubMedGoogle Scholar
  12. 12.
    Kayden HJ, Traber MG (1993) Absorption, lipoprotein transport, and regulation of plasma concentrations of vitamin E in humans. J Lipid Res 34:343–358PubMedGoogle Scholar
  13. 13.
    Kostner GM, Oettl K, Jauhiainen M, Ehnholm C, Esterbauer H, Dieplinger H (1995) Human plasma phospholipid transfer protein accelerates exchange/transfer of alpha-tocopherol between lipoproteins and cells. Biochem J 305(Pt 2):659–667PubMedGoogle Scholar
  14. 14.
    Desrumaux C, Deckert V, Athias A, Masson D, Lizard G, Palleau V, Gambert P, Lagrost L (1999) Plasma phospholipid transfer protein prevents vascular endothelium dysfunction by delivering alpha-tocopherol to endothelial cells. Faseb J 13:883–892PubMedGoogle Scholar
  15. 15.
    Granot E, Tamir I, Deckelbaum RJ (1988) Neutral lipid transfer protein does not regulate alpha-tocopherol transfer between human plasma lipoproteins. Lipids 23:17–21CrossRefPubMedGoogle Scholar
  16. 16.
    Traber MG, Carpentier YA, Kayden HJ, Richelle M, Galeano NF, Deckelbaum RJ (1993) Alterations in plasma alpha- and gamma-tocopherol concentrations in response to intravenous infusion of lipid emulsions in humans. Metabolism 42:701–709CrossRefPubMedGoogle Scholar
  17. 17.
    Steephen AC, Traber MG, Ito Y, Lewis LH, Kayden HJ, Shike M (1991) Vitamin E status of patients receiving long-term parenteral nutrition: is vitamin E supplementation adequate? JPEN J Parenter Enteral Nutr 15:647–652CrossRefPubMedGoogle Scholar
  18. 18.
    Kelly FJ, Sutton GL (1989) Plasma and red blood cell vitamin E status of patients on total parenteral nutrition. JPEN J Parenter Enteral Nutr 13:510–515CrossRefPubMedGoogle Scholar
  19. 19.
    Richelle M, Rubin M, Kulapongse S, Deckelbaum RJ, Elwyn DH, Carpentier YA (1993) Plasma lipoprotein pattern during long-term home parenteral nutrition with two lipid emulsions. JPEN J Parenter Enteral Nutr 17:432–437CrossRefPubMedGoogle Scholar
  20. 20.
    Havel RJ, Eder HA, Bragdon JH (1955) The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest 34:1345–1353CrossRefPubMedGoogle Scholar
  21. 21.
    Albers JJ, Tollefson JH, Chen CH, Steinmetz A (1984) Isolation and characterization of human plasma lipid transfer proteins. Arteriosclerosis 4:49–58PubMedGoogle Scholar
  22. 22.
    Jauhiainen M, Setala NL, Ehnholm C, Metso J, Tervo TM, Eriksson O, Holopainen JM (2005) Phospholipid transfer protein is present in human tear fluid. Biochemistry 44:8111–8116CrossRefPubMedGoogle Scholar
  23. 23.
    Ha YC, Barter PJ (1982) Differences in plasma cholesteryl ester transfer activity in sixteen vertebrate species. Comp Biochem Physiol B 71:265–269CrossRefPubMedGoogle Scholar
  24. 24.
    Speijer H, Groener JE, van Ramshorst E, van Tol A (1991) Different locations of cholesteryl ester transfer protein and phospholipid transfer protein activities in plasma. Atherosclerosis 90:159–168CrossRefPubMedGoogle Scholar
  25. 25.
    Pussinen PJ, Olkkonen VM, Jauhiainen M, Ehnholm C (1997) Molecular cloning and functional expression of cDNA encoding the pig plasma phospholipid transfer protein. J Lipid Res 38:1473–1481PubMedGoogle Scholar
  26. 26.
    Hatam LJ, Kayden HJ (1979) A high-performance liquid chromatographic method for the determination of tocopherol in plasma and cellular elements of the blood. J Lipid Res 20:639–645PubMedGoogle Scholar
  27. 27.
    Traber MG, Olivecrona T, Kayden HJ (1985) Bovine milk lipoprotein lipase transfers tocopherol to human fibroblasts during triglyceride hydrolysis in vitro. J Clin Invest 75:1729–1734CrossRefPubMedGoogle Scholar
  28. 28.
    Traber MG, Kayden HJ (1989) Preferential incorporation of alpha-tocopherol vs gamma-tocopherol in human lipoproteins. Am J Clin Nutr 49:517–526PubMedGoogle Scholar
  29. 29.
    Damen J, Regts J, Scherphof G (1982) Transfer of [14C]phosphatidylcholine between liposomes and human plasma high density lipoprotein. Partial purification of a transfer-stimulating plasma factor using a rapid transfer assay. Biochim Biophys Acta 712:444–452PubMedGoogle Scholar
  30. 30.
    Lagrost L, Athias A, Gambert P, Lallemant C (1994) Comparative study of phospholipid transfer activities mediated by cholesteryl ester transfer protein and phospholipid transfer protein. J Lipid Res 35:825–835PubMedGoogle Scholar
  31. 31.
    Tall AR, Krumholz S, Olivecrona T, Deckelbaum RJ (1985) Plasma phospholipid transfer protein enhances transfer and exchange of phospholipids between very low density lipoproteins and high density lipoproteins during lipolysis. J Lipid Res 26:842–851PubMedGoogle Scholar
  32. 32.
    Nathens AB, Neff MJ, Jurkovich GJ, Klotz P, Farver K, Ruzinski JT, Radella F, Garcia I, Maier RV (2002) Randomized, prospective trial of antioxidant supplementation in critically ill surgical patients. Ann Surg 236:814–822CrossRefPubMedGoogle Scholar
  33. 33.
    Seeger W, Ziegler A, Wolf HR (1987) Serum alpha-tocopherol levels after high-dose enteral vitamin E administration in patients with acute respiratory failure. Intensive Care Med 13:395–400CrossRefPubMedGoogle Scholar
  34. 34.
    Kelly FJ (1994) Vitamin E supplementation in the critically ill patient: too narrow a view? Nutr Clin Pract 9:141–145CrossRefPubMedGoogle Scholar
  35. 35.
    Berger MM, Berger-Gryllaki M, Wiesel PH, Revelly JP, Hurni M, Cayeux C, Tappy L, Chiolero R (2000) Intestinal absorption in patients after cardiac surgery. Crit Care Med 28:2217–2223CrossRefPubMedGoogle Scholar

Copyright information

© AOCS 2008

Authors and Affiliations

  • M. Hacquebard
    • 1
  • M. Vandenbranden
    • 2
  • W. J. Malaisse
    • 1
  • J. M. Ruysschaert
    • 2
  • R. J. Deckelbaum
    • 3
  • Y. A. Carpentier
    • 1
  1. 1.L. Deloyers Laboratory for Experimental SurgeryUniversité Libre de BruxellesBrusselsBelgium
  2. 2.Laboratory of Structure and Function of Biological Membranes-Center of Structural Biology and BioinformaticsUniversité Libre de BruxellesBrusselsBelgium
  3. 3.Institute of Human NutritionColumbia UniversityNew YorkUSA

Personalised recommendations