Selective decrease of bis(monoacylglycero)phosphate content in macrophages by high supplementation with docosahexaenoic acid

Journal of Lipid Research

Volumn 50, Issue 2, 2009, Pages 243-255

  Bouvier, Jérôme ^a   Berry, Karin A Zemski ^b   Hullin Matsuda, Françoise ^a,c   Makino, Asami ^a,c   Michaud, Sabine ^a   Geloën, Alain ^a   Murphy, Robert C ^b   Kobayashi, Toshihide ^c   Lagarde, Michel ^a   Delton Vandenbroucke, Isabelle ^a  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITY OF COLORADO   (United States)

^c RIKEN   (Japan)

Author keywords

BMP synthesis; Cholesterol; Late endosome; Lipid peroxidation; Phosphatidylglycerol

Indexed keywords

ALPHA TOCOPHEROL; BIS(MONOACYLGLYCERO)PHOSPHATE; DIDOCOSAHEXAENOYLPHOSPHATIDYLGLYCEROL; DIOLEOYLPHOSPHATIDYLGLYCEROL; DOCOSAHEXAENOIC ACID; FATTY ACID; OLEIC ACID; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPID; UNCLASSIFIED DRUG; CHOLESTEROL; LIPOSOME; LYSOBISPHOSPHATIDIC ACID; LYSOPHOSPHOLIPID; MONOACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FREE SYSTEM; CHOLESTEROL METABOLISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOSOME; LIPID COMPOSITION; LIPID DEGRADATION; LIPID OXIDATION; LIPID PEROXIDATION; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; DIET SUPPLEMENTATION; METABOLISM; OXIDATION REDUCTION REACTION;

ANIMALS; CELLS, CULTURED; CHOLESTEROL; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; LIPOSOMES; LYSOPHOSPHOLIPIDS; MACROPHAGES; MICE; MONOGLYCERIDES; OXIDATION-REDUCTION; PHOSPHATIDYLGLYCEROLS;

EID: 64749107217     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M800300-JLR200     Document Type: Article

References (68)

1. Kobayashi, T., E. Stang, K. S. Fang, P. de Moerloose, R. G. Parton, and J. Gruenberg. 1998. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature. 392: 193-197.
2. Kobayashi, T., K. Startchev, A. J. Whitney, and J. Gruenber. 2001. Localization of lysobisphosphatidic acid-rich membrane domains in late endosomes. Biol. Chem. 382: 483-485.
3. Kobayashi, T., M. H. Beuchat, J. Chevallier, A. Makino, N. Mayran, J. M. Escola, C. Lebrand, P. Cosson, and J. Gruenberg. 2002. Separation and characterization of late endosomal membrane domains. J. Biol. Chem. 277: 32157-32164.
4. Matsuo, H., J. Chevallier, N. Mayran, I. Le Blanc, C. Ferguson, J. Faure, N. S. Blanc, S. Matile, J. Dubochet, R. Sadoul, et al. 2004. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science. 303: 531-534.
5. Hayakawa, T., A. Makino, M. Murate, I. Sugimoto, Y. Hashimoto, H. Takahashi, K. Ito, T. Fujisawa, H. Matsuo, and T. Kobayashi. 2007. pH-dependent formation of membranous cytoplasmic body-like structure of ganglioside G(M1)/bis(monoacylglycero)phosphate mixed membranes. Biophys. J. 92: L13-L16.
6. Kobayashi, T., M. H. Beuchat, M. Lindsay, S. Frias, R. D. Palmiter, H. Sakuraba, R. G. Parton, and J. Gruenberg. 1999. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol. 1: 113-118.
7. Le Blanc, I., P. P. Luyet, V. Pons, C. Ferguson, N. Emans, A. Petiot, N. Mayran, N. Demaurex, J. Faure, R. Sadoul, et al. 2005. Endosometo-cytosol transport of viral nucleocapsids. Nat. Cell Biol. 7: 653-664.
8. Delton-Vandenbroucke, I., J. Bouvier, A. Makino, N. Besson, J. F. Pageaux, M. Lagarde, and T. Kobayashi. 2007. Anti-bis(monoacylglycero) phosphate antibody accumulates acetylated LDL-derived cholesterol in cultured macrophages. J. Lipid Res. 48: 543-552.
9. Cheruku, S. R., Z. Xu, R. Dutia, P. Lobel, and J. Storch. 2006. Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J. Biol. Chem. 281: 31594-31604.
10. Babalola, J. O., M. Wendeler, B. Breiden, C. Arenz, G. Schwarzmann, S. Locatelli-Hoops, and K. Sandhoff. 2007. Development of an assay for the intermembrane transfer of cholesterol by Niemann-Pick C2 protein. Biol. Chem. 388: 617-626.
11. Kolter, T., and K. Sandhoff. 2005. Principles of lysosomal membrane digestion: stimulation of sphingolipid degradation by sphingolipid activator proteins and anionic lysosomal lipids. Annu. Rev. Cell Dev. Biol. 21: 81-103.
12. Makino, A., K. Ishii, M. Murate, T. Hayakawa, Y. Suzuki, M. Suzuki, K. Ito, T. Fujisawa, H. Matsuo, R. Ishitsuka, et al. 2006. D-threo-I-phenyl-2-decanoylamino-3-morpholino-1-propanol alters cellular cholesterol homeostasis by modulating the endosome lipid domains. Biochemistry. 45: 4530-4541.
13. Galve-de Rochemonteix, B., T. Kobayashi, C. Rosnoblet, M. Lindsay, R. G. Parton, G. Reber, E. de Maistre, D. Wahl, E. K. Kruithof, J. Gruenberg, et al. 2000. Interaction of anti-phospholipid antibodies with late endosomes of human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 20: 563-574.
14. Valesini, G., and C. Alessandri. 2005. New facet of antiphospholipid antibodies. Ann. N. Y. Acad. Sci. 1051: 487-497.
15. Brotherus, J., O. Renkonen, W. Fischer, and J. Herrmann. 1974. Novel stereoconfiguration in lyso-bis-phosphatidic acid of cultured BHK-cells. Chem. Phys. Lipids. 13: 178-182.
16. Joutti, A., J. Brotherus, O. Renkonen, R. Laine, and W. Fischer. 1976. The stereochemical configuration of lysobisphosphatidic acid from rat liver, rabbit lung and pig lung. Biochim. Biophys. Acta. 450: 206-209.
17. Luquain, C., R. Dolmazon, J. M. Enderlin, C. Laugier, M. Lagarde, and J. F. Pageaux. 2000. Bis(monoacylglycerol) phosphate in rat uterine stromal cells: structural characterization and specific esterification of docosahexaenoic acid. Biochem. J. 351: 795-804.
18. Holbrook, P. G., L. K. Pannell, Y. Murata, and J. W. Daly. 1992. Bis(monoacylglycero)phosphate from PC12 cells, a phospholipid that can comigrate with phosphatidic acid: molecular species analysis by fast atom bombardment mass spectrometry. Biochim. Biophys. Acta. 1125: 330-334.
19. Besson, N., F. Hullin-Matsuda, A. Makino, M. Murate, M. Lagarde, J. F. Pageaux, T. Kobayashi, and I. Delton-Vandenbroucke. 2006. Selective incorporation of docosahexaenoic acid into lysobisphosphatidic acid in cultured THP-1 macrophages. Lipids. 41: 189-196.
20. Wherrett, J. R., and S. Huterer. 1973. Bis-(monoacylglyceryl)-phosphate of rat and human liver: fatty acid composition and NMR spectroscopy. Lipids. 8: 531-533.
21. Huterer, S., and J. R. Wherrett. 1986. Incorporation of polyunsaturated fatty acids into bis(monoacylglycero)phosphate and other lipids of macrophages and of fibroblasts from control and Niemann-Pick patients. Biochim. Biophys. Acta. 876: 318-326.
22. Holub, D. J., and B. J. Holub. 2004. Omega-3 fatty acids from fish oils and cardiovascular disease. Mol. Cell. Biochem. 263: 217-225.
23. Stillwell, W., and S. R. Wassall. 2003. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem. Phys. Lipids. 126: 1-27.
24. Stillwell, W., S. R. Shaikh, M. Zerouga, R. Siddiqui, and S. R. Wassall. 2005. Docosahexaenoic acid affects cell signaling by altering lipid rafts. Reprod. Nutr. Dev. 45: 559-579.
25. Poorthuis, B. J., and K. Y. Hostetler. 1978. Conversion of diphosphatidylglycerol to bis(monoacylglyceryl)phosphate by lysosomes. J. Lipid Res. 19: 309-315.
26. Somerharju, P., and O. Renkonen. 1980. Conversion of phosphatidylglycerol lipids to bis(monoacylglycero)phosphate in vivo. Biochim. Biophys. Acta. 618: 407-419.
27. Waite, M., V. Roddick, T. Thornburg, L. King, and F. Cochran. 1987. Conversion of phosphatidylglycerol to lyso(bis)phosphatidic acid by alveolar macrophages. FASEB J. 1: 318-325.
28. Amidon, B., J. D. Schmitt, T. Thuren, L. King, and M. Waite. 1995. Biosynthetic conversion of phosphatidylglycerol to sn-1:sn-1' bis(monoacylglycerol) phosphate in a macrophage-like cell line. Biochemistry. 34: 5554-5560.
29. Hullin-Matsuda, F., K. Kawasaki, I. Delton-Vandenbroucke, Y. Xu, M. Nishijima, M. Lagarde, M. Schlame, and T. Kobayashi. 2007. De novo biosynthesis of the late endosome lipid, bis(monoacylglycero) phosphate. J. Lipid Res. 48: 1997-2008.
30. Hayakawa, T., Y. Hirano, A. Makino, S. Michaud, M. Lagarde, J. F. Pageaux, A. Doutheau, K. Ito, T. Fujisawa, H. Takahashi, et al. 2006. Differential membrane packing of stereoisomers of bis(monoacylglycero) phosphate. Biochemistry. 45: 9198-9209.
31. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
32. Han, X., and R. W. Gross. 2005. Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples. Mass Spectrom. Rev. 24: 367-412.
33. Therasse, J., and F. Lemonnier. 1987. Determination of plasma lipoperoxides by high-performance liquid chromatography. J. Chromatogr. 413: 237-241.
34. Vericel, E., A. Polette, S. Bacot, C. Calzada, and M. Lagarde. 2003. Pro- and antioxidant activities of docosahexaenoic acid on human blood platelets. J. Thromb. Haemost. 1: 566-572.
35. Cosgrove, J. P., D. F. Church, and W. A. Pryor. 1987. The kinetics of the autoxidation of polyunsaturated fatty acids. Lipids. 22: 299-304.
36. Roberts II, L. J., J. P. Fessel, and S. S. Davies. 2005. The biochemistry of the isoprostane, neuroprostane, and isofuran pathways of lipid peroxidation. Brain Pathol. 15: 143-148.
37. Azzi, A., and A. Stocker. 2000. Vitamin E: non-antioxidant roles. Prog. Lipid Res. 39: 231-255.
38. Shinozaki, K., and M. Waite. 1999. A novel phosphatidylglycerol-selective phospholipase A2 from macrophages. Biochemistry. 38: 1669-1675.
39. Gao, R., W. L. Stone, T. Huang, A. M. Papas, and M. Qui. 2002. The uptake of tocopherols by RAW 264.7 macrophages. Nutr. J. 1: 2.
40. Engelmann, B. 2004. Plasmalogens: targets for oxidants and major lipophilic antioxidants. Biochem. Soc. Trans. 32: 147-150.
41. Amidon, B., A. Brown, and M. Waite. 1996. Transacylase and phospholipases in the synthesis of bis(monoacylglycero)phosphate. Biochemistry. 35: 13995-14002.
42. Matsuzawa, Y., B. J. Poorthuis, and K. Y. Hostetler. 1978. Mechanism of phosphatidylinostiol stimulation of lysosomal bis (monoacylglyceryl) phosphate synthesis. J. Biol. Chem. 253: 6650-6653.
43. Huterer, S. J., and J. R. Wherrett. 1989. Formation of bis(monoacylglycero) phosphate by a macrophage transacylase. Biochim. Biophys. Acta. 1001: 68-75.
44. Heravi, J., and M. Waite. 1999. Transacylase formation of bis(monoacylglycerol) phosphate. Biochim. Biophys. Acta. 1437: 277-286.
45. Ohtsuka, T., M. Nishijima, and Y. Akamatsu. 1993. A somatic cell mutant defective in phosphatidylglycerophosphate synthase, with impaired phosphatidylglycerol and cardiolipin biosynthesis. J. Biol. Chem. 268: 22908-22913.
46. Schlame, M., and K. Y. Hostetler. 1997. Cardiolipin synthase from mammalian mitochondria. Biochim. Biophys. Acta. 1348: 207-213.
47. Esko, J. D., and C. R. Raetz. 1980. Mutants of Chinese hamster ovary cells with altered membrane phospholipid composition. Replacement of phosphatidylinositol by phosphatidylglycerol in a myo-inositol auxotroph. J. Biol. Chem. 255: 4474-4480.
48. Thornburg, T., C. Miller, T. Thuren, L. King, and M. Waite. 1991. Glycerol reorientation during the conversion of phosphatidylglycerol to bis(monoacylglycerol)phosphate in macrophage-like RAW 264.7 cells. J. Biol. Chem. 266: 6834-6840.
49. Ito, M., U. Tchoua, M. Okamoto, and H. Tojo. 2002. Purification and properties of a phospholipase A2/lipase preferring phosphatidic acid, bis(monoacylglycerol) phosphate, and monoacylglycerol from rat testis. J. Biol. Chem. 277: 43674-43681.
50. Yu, Z., H. L. Persson, J. W. Eaton, and U. T. Brunk. 2003. Intralysosomal iron: a major determinant of oxidant-induced cell death. Free Radic. Biol. Med. 34: 1243-1252.
51. Austin, C. D., X. Wen, L. Gazzard, C. Nelson, R. H. Scheller, and S. J. Scales. 2005. Oxidizing potential of endosomes and lysosomes limits intracellular cleavage of disulfide-based antibody-drug conjugates. Proc. Natl. Acad. Sci. USA. 102: 17987-17992.
52. Wen, Y., and D. S. Leake. 2007. Low density lipoprotein undergoes oxidation within lysosomes in cells. Circ. Res. 100: 1337-1343.
53. Stinson, A. M., R. D. Wiegand, and R. E. Anderson. 1991. Fatty acid and molecular species compositions of phospholipids and diacylglycerols from rat retinal membranes. Exp. Eye Res. 52: 213-218.
54. Delton-Vandenbroucke, I., M. B. Maude, H. Chen, G. D. Aguirre, G. M. Acland, and R. E. Anderson. 1998. Effect of diet on the fatty acid and molecular species composition of dog retina phospholipids. Lipids. 33: 1187-1193.
55. Bisogno, T., I. Delton-Vandenbroucke, A. Milone, M. Lagarde, and V. Di Marzo. 1999. Biosynthesis and inactivation of N-arachidonoy-lethanolamine (anandamide) and N-docosahexaenoylethanolamine in bovine retina. Arch. Biochem. Biophys. 370: 300-307.
56. Alexander-North, L. S., J. A. North, K. P. Kiminyo, G. R. Buettner, and A. A. Spector. 1994. Polyunsaturated fatty acids increase lipid radical formation induced by oxidant stress in endothelial cells. J. Lipid Res. 35: 1773-1785.
57. Song, J. H., and T. Miyazawa. 2001. Enhanced level of n-3 fatty acid in membrane phospholipids induces lipid peroxidation in rats fed dietary docosahexaenoic acid oil. Atherosclerosis. 155: 9-18.
58. Lyberg, A. M., E. Fasoli, and P. Adlercreutz. 2005. Monitoring the oxidation of docosahexaenoic acid in lipids. Lipids. 40: 969-979.
59. Wiegand, R. D., C. A. Koutz, H. Chen, and R. E. Anderson. 1995. Effect of dietary fat and environmental lighting on the phospholipid molecular species of rat photoreceptor membranes. Exp. Eye Res. 60: 291-306.
60. Wagner, B. A., G. R. Buettner, and C. P. Burns. 1996. Vitamin E slows the rate of free radical-mediated lipid peroxidation in cells. Arch. Biochem. Biophys. 334: 261-267.
61. Singh, U., S. Devaraj, and I. Jialal. 2005. Vitamin E, oxidative stress, and inflammation. Annu. Rev. Nutr. 25: 151-174.
62. Devaraj, S., D. Li, and I. Jialal. 1996. The effects of alpha tocopherol supplementation on monocyte function. Decreased lipid oxidation, interleukin 1 beta secretion, and monocyte adhesion to endothelium. J. Clin. Invest. 98: 756-763.
63. Kelley, E. E., G. R. Buettner, and C. P. Burns. 1995. Relative alphatocopherol deficiency in cultured cells: free radical-mediated lipid peroxidation, lipid oxidizability, and cellular polyunsaturated fatty acid content. Arch. Biochem. Biophys. 319: 102-109.
64. Baoutina, A., R. T. Dean, and W. Jessup. 1998. Alpha-tocopherol supplementation of macrophages does not influence their ability to oxidize LDL. J. Lipid Res. 39: 114-130.
65. Gu, X., M. Sun, B. Gugiu, S. Hazen, J. W. Crabb, and R. G. Salomon. 2003. Oxidatively truncated docosahexaenoate phospholipids: total synthesis, generation, and peptide adduction chemistry. J. Org. Chem. 68: 3749-3761.
66. Gugiu, B. G., C. A. Mesaros, M. Sun, X. Gu, J. W. Crabb, and R. G. Salomon. 2006. Identification of oxidatively truncated ethanolamine phospholipids in retina and their generation from polyunsaturated phosphatidylethanolamines. Chem. Res. Toxicol. 19: 262-271.
67. Harder, A., and H. Debuch. 1982. Effect of chloroquine treatment on the different phospholipid species of rat liver lysosomes. Hoppe Seylers Z. Physiol. Chem. 363: 717-723.
68. Baronas, E. T., J. W. Lee, C. Alden, and F. Y. Hsieh. 2007. Biomarkers to monitor drug-induced phospholipidosis. Toxicol. Appl. Pharmacol. 218: 72-78.