Oxidized LDL-induced endolysosomal phospholipidosis and enzymatically modified LDL-induced foam cell formation determine specific lipid species modulation in human macrophages

Chemistry and Physics of Lipids

Volumn 164, Issue 6, 2011, Pages 479-487

  Orsó, Evelyn ^a   Grandl, Margot ^a   Schmitz, Gerd ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

Bis(monoacylglycero)phosphate; Cardiolipin; Enzymatically modified LDL; Foam cell; Oxidized LDL; Phospholipidosis

Indexed keywords

1 ACYLGLYCEROPHOSPHOCHOLINE ACYLTRANSFERASE; CARDIOLIPIN; CASPASE 3; CD14 ANTIGEN; DIACYLGLYCEROL KINASE; ENZYMATICALLY MODIFIED LOW DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN; LIPOPROTEIN; LYSOBISPHOSPHATIDIC ACID; OXIDIZED LOW DENSITY LIPOPROTEIN; PHOSPHATIDYLGLYCEROL; PROCASPASE 9; PROTEIN MD 2; SECRETORY PHOSPHOLIPASE A2; SPHINGOMYELIN PHOSPHODIESTERASE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN;

APOPTOSIS; CELL MIGRATION; CELL PROLIFERATION; ENZYME ACTIVATION; FOAM CELL; HUMAN; LIPID OXIDATION; LIPID PEROXIDATION; LIPIDOSIS; MACROPHAGE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

ANIMALS; CELL LINE; ENDOSOMES; FOAM CELLS; HUMANS; LIPOPROTEINS, LDL; LYSOSOMAL STORAGE DISEASES; LYSOSOMES; OXIDATION-REDUCTION;

EID: 80051469645     PISSN: 00093084     EISSN: 18732941     Source Type: Journal    
DOI: 10.1016/j.chemphyslip.2011.06.001     Document Type: Review

References (85)

1. M. Abdul-Hammed, B. Breiden, M.A. Adebayo, J.O. Babalola, G. Schwarzmann, and K. Sandhoff Role of endosomal membrane lipids and NPC2 in cholesterol transfer and membrane fusion J. Lipid Res. 51 2010 1747 1760
2. 2 J. Lipid Res. 47 2006 2268 2279 (Pubitemid 44936137)
3. 2 with transacylase activity J. Biol. Chem. 273 1998 8467 8474 (Pubitemid 28168911)
4. A. Abe, and J.A. Shayman The role of negatively charged lipids in lysosomal phospholipase A2 function J. Lipid Res. 50 2009 2027 2035
5. A. Abe, S.R. Wild, W.L. Lee, and J.A. Shayman Agents for the treatment of glycosphingolipid storage disorders Curr. Drug Metab. 2 2001 331 338 (Pubitemid 32782800)
6. J.-M. Alakoskela, P. Vitovič, and P.K.J. Kinnunen Screening for the drug-phospholipid interaction: correlation to phospholipidosis Chem. Med. Chem. 4 2009 1224 1251
7. S. Bhakdi, B. Dorweiler, R. Kirchmann, J. Torzewski, E. Weise, J. Tranum-Jensen, I. Walev, and E. Wieland On the pathogenesis of atherosclerosis: enzymatic transformation of human low density lipoprotein to an atherogenic moiety J. Exp. Med. 182 1995 1959 1971
8. S. Bhakdi, M. Torzewski, K. Paprotka, S. Schmitt, H. Barsoom, P. Suriyaphol, S.R. Han, K.J. Lackner, and M. Husmann Possible protective role for C-reactive protein in atherogenesis: complement activation by modified lipoproteins halts before detrimental terminal sequence Circulation 106 2004 2581 2587
9. S. Bhakdi, K.J. Lackner, S.R. Han, M. torzewski, and M Husmann Beyond cholesterol: the enigma of atherosclerosis revisited Thromb. Haemost. 91 2004 639 645 (Pubitemid 38477443)
10. M. Binder, G. Liebisch, T. Langmann, and G. Schmitz Metabolic profiling of glycerphospholipid synthesis in fibroblasts loaded with free cholesterol and modified low density lipoproteins J. Biol. Chem. 281 2006 21869 21877 (Pubitemid 44181890)
11. V.N. Bochkov, O.V. Oskolkova, K.G. Birukov, A.-L. Levonen, C.J. Binder, and J. Stöckl Generation and biological activities of oxidized phospholipids Antioxid. Redox. Signal 12 2010 1009 1059
12. J. Chevallier, Z. Chamoun, G. Jiang, G. Prestwich, N. Sakai, S. Matile, R.G. Parton, and J. Gruenberg Lysobisphosphatidic acid controls endosomal cholesterol levels J. Biol. Chem. 283 2008 27871 27880
13. M.Y. Chou, L. Fogelstrand, K. Hartvigsen, L.F. Hansen, D. Woelkers, P.X. Shaw, J. Choi, T. Perkmann, F. Bäckhed, Y.I. Miller, S. Hörkkö, M. Corr, J.L. Witztum, and C.J. Binder Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans J. Clin. Invest. 119 2009 1335 1349
14. M. Crimi, and M.D. Esposti Apoptosis-induced changes in mitochondrial lipids Biochim. Biophys. Acta 1813 2011 551 557
15. D.M. Czajkowsky, A. Salanti, S.B. Ditlev, Z. Shao, A. Ghumra, J.A. Rowe, and R.J. Pleass IgM, FcμRs, and malarial immune evasion J. Immunol. 184 2010 4597 4603
16. K. Dersch, H. Ichijo, S. Bhakdi, and M. Husmann Fatty acids liberated from low-density lipoprotein trigger endothelial apoptosis via mitogen-activated protein kinases Cell Death Differ. 12 2005 1107 1114 (Pubitemid 41065427)
17. E.R. Eden, I.J. White, and C.E. Futter Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction Nat. Cell Biol. 12 2010 267 272
18. N. Ermak, B. Lacour, T.B. Drüeke, and S. Vicca Role of reactive oxygen species and Bax in oxidized low density lipoprotein-induced apoptosis of human monocytes Atherosclerosis 200 2008 247 256
19. N. Ermak, B. Lacour, F. Goirand, T.B. Drüeke, and S. Vicca Differential apoptotic pathways activated in response to Cu-induced or HOCl-induced LDL oxidation in U937 monocytic cell line Biochem. Biophys. Res. Commun. 393 2010 783 787
20. Gallala, H.D., Sandhoff, K. Biological function of the cellular lipid BMP-BMP as a key activator for cholesterol sorting and membrane digestion. Neurochem. Res., in press.
21. M. Grandl, S.M. Bared, G. Liebisch, T. Werner, S. Barlage, and G. Schmitz E-LDL and Ox-LDL differentially regulate ceramide and cholesterol raft microdomains in human macrophages Cytometry A 69 2006 189 191
22. M. Grandl, and G. Schmitz Fluorescent high-content imaging allows the discrimination and quantitation of E-LDL-induced lipid droplets and Ox-LDL-generated phospholipidosis in human macrophages Cytometry A 77 2010 231 242
23. J.K. Hakala, R. Oksjoki, P. Laine, H. Du, G.A. Grabowski, P.T. Kovanen, and Pentikäinen MO Lysosomal enzymes are released from cultured human macrophages, hydrolyze LDL in vitro, and are present extracellularly in human atherosclerotic lesions Arterioscler. Thromb. Vasc. Biol. 23 2003 1430 1436 (Pubitemid 37006376)
24. R.T. Hamilton, L. Asatryan, J.T. Nilsen, T.K. Gallaher, T. Sawamura, and Hsiai TK LDL protein nitration: implication for LDL protein unfolding Arch. Biochem. Biophys. 479 2009 1 14
25. C.-Y. Han, and Y.K. Pak Oxidation-dependent effects of oxidized LDL: proliferation or cell death Exp. Mol. Med. 31 1999 165 173 (Pubitemid 30021332)
26. T. Harayama, H. Shindou, R. Ogasawara, A. Suwabe, and T. Shimizu Identification of a novel noninflammatory biosynthetic pathway of platelet-activating factor J. Biol. Chem. 283 2008 11097 11106
27. 2 and phospholipidosis Mol. Cell. Biol. 26 2006 6139 6148
28. M. Hiraoka, A. Abe, and J.A. Shayman Cloning and characterization of a lysosomal phospholipase A2, 1-O-acylceramide synthase J. Biol. Chem. 277 2002 10090 10099 (Pubitemid 34968119)
29. D. Hishikawa, H. Shindou, S. Kobayashi, H. Nakanishi, R. Taguchi, and T. Shimizu Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity Proc. Natl. Acad. Sci. U.S.A. 105 2008 2830 2835 (Pubitemid 351723629)
30. R.H. Houtkooper, M. Turkenburg, B.T. Poll-The, D. Karall, C. Pérez-Cerdá, A. Morrone, S. Malvagia, R.J. Wanders, W. Kulik, and F.M. Vaz The enigmatic role of tafazzin in cardiolipin metabolism Biochim. Biophys. Acta 1788 2009 2003 2014
31. F. Hullin-Matsuda, C. Luquaain-Costaz, and I. Delton-Vandenbroucke Bis(monoacylglycero)phosphate, a peculiar phospholipid to control the fate of cholesterol: implications in pathology Prostaglandins Leukot Essent. Fatty Acids 81 2009 313 324
32. J.H. Hurley, and P,I. Hanson Membrane budding and scission by the ESCRT machinery: it's all in the neck Nat. Rev. Mol. Cell Biol. 11 2010 556 566
33. F. Jiang, M.T. Ryan, M. Schlame, M. Zhao, Z. Gu, M. Klingenberg, N. Pfanner, and M.L. Greenberg Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function J. Biol. Chem. 275 2000 22387 22394 (Pubitemid 30621825)
34. M. Kapinsky, M. Torzewski, Büchler, C.Q. Duong, G. Rothe, and G. Schmitz Enzymatically degraded LDL preferentially binds to CD14(high) CD16(+) monocytes and induced foam cell formation mediated only in part by the class B scavenger-receptor CD36 Arterioscler. Thromb. Vasc. Biol. 21 2001 1004 1010 (Pubitemid 34168660)
35. M. Kazachkov, Q. Chen, L. Wang, and J. Zou Substrate preferences of a lysophosphatidylcholine acyltransferase highlight its role in phospholipid remodeling Lipids 43 2008 895 902
36. T. Kobayashi, M.H. Beuchat, M. Lindsay, S. Frias, R.D. Palmiter, H. Sakuraba, R.G. Parton, and J. Gruenberg Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport Nat. Cell Biol. 1 1999 113 118 (Pubitemid 129501953)
37. T. Kobayashi, E. Stang, K.S. Fang, M.P. de, R.G. Parton, and J. Gruenberg A lipid associated with the antiphospholipid syndrome regulates endosome structure and function Nature 392 1998 193 197 (Pubitemid 28162794)
38. T. Kobayashi, K. Tanaka, K. Inoue, and A. Kakizuka Functional ATPase activity of p97/valosin-containing protein (VCP) is required for the quality control of endoplasmic reticulum in neuronally differentiated mammalian PC12 cells J. Biol. Chem. 277 2002 47358 47365 (Pubitemid 36159250)
39. T. Kolter, and K. Sandhoff Lysosomal degradation of membrane lipids FEBS Lett. 584 2010 1700 1712
40. T. Kolter, F. Winau, U.E. Schaible, M. Leippe, and K. Sandhoff Lipid-binding proteins in membrane digestion, antigen presentation, and antimicrobial defense J. Biol. Chem. 280 2005 41125 41128 (Pubitemid 41832164)
41. HS Kruth Subendothelial accumulation of unesterified cholesterol. An early event in atherosclerotic lesion development Atherosclerosis 57 1985 337 341 (Pubitemid 16235921)
42. G. Lizard, S. Gueldry, O. Sordet, S. Monier, A. Athias, C. Miguet, G. Bessede, S. Lemaire, E. Solary, and P. Gambert Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production FASEB J. 12 1998 1651 1663 (Pubitemid 28553660)
43. G. Lizard, M. Moisant, C. Cordelet, S. Monier, P. Gambert, and L. Lagrost Induction of similar features of apoptosis in human and bovine vascular endothelial cells treated by 7-ketocholesterol J. Pathol. 183 1997 330 338 (Pubitemid 27505220)
44. W. Martinet, M. De Bie, D.M. Schrijvers, G.R.Y. De Meyer, A.G. Herman, and M.M. Kockx 7-ketocholesterol induces protein ubiquitination, myelin figure formation, and light chain 3 processing in vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 24 2004 2296 2301 (Pubitemid 39658032)
45. H. Matsuo, J. Chevallier, N. Mayran, I. Le Blanc, C. Ferguson, J. Faure, N.S. Blanc, S. Matile, J. Dubochet, R. Sadoul, R.G. Parton, F. Vilbois, and J. Gruenberg Role of LBPA and Alix in multivesicular liposome formation and endosome organization Science 303 2004 531 534 (Pubitemid 38120852)
46. P.J. Meikle, S. Duplock, D. Blacklock, P.D. Whitfield, G. MacIntosh, J.J. Hopwood, and M. Fuller Effect of lysosomal storage on bis(monoacylglycero) phosphate Biochem. J. 411 2008 71 78 (Pubitemid 351482348)
47. E.J. Menzel, G. Sobal, and A. Staudinger The role of oxidative stress in the long-term glycation of LDL Biofactors 6 1997 111 124 (Pubitemid 27487815)
48. Y.I. Miller, S.-H. Choi, L. Fang, and R. Harkewicz Toll-like receptor-4 and lipoprotein accumulation in macrophages Trends Cardiovasc. Med. 19 2009 227 232
49. Y.I. Miller, S.-H. Choi, P. Wiesner, L. Fang, R. Harkewicz, K. Hartvigsen, A. Boullier, A. Gonen, C.J. Diehl, X. Que, E. Montano, P.X. Shaw, S. Tsimikas, C.J. Binder, and J.L. Witztum Oxidation-specific epitopes are danger-associated molecular patterns recognized by pattern recognition receptors of innate immunity Circ. Res. 108 2011 235 248
50. J. Montero, M. Mari, A. Colell, A. Morales, G. Basanez, C. Garcia-Ruiz, and J.C. Fernández-Checa Cholesterol and peroxidized cardiolipin in mitochondrial membrane properties, permeabilization and cell death Biochim. Biophys. Acta 1797 2010 1217 1224
51. K. Nakanishi, S. Aono, K. Hirano, Y. Kuroda, M. Ida, Y. Tokita, F. Matsui, and A. Oohira Identification of neurite outgrowth-promoting domains of neuroglycan C, a brain-specific chondroitin sulfate proteoglycan, and involvement of phosphatidylinositol 3-kinase and protein kinase C signaling pathways in neuritogenesis J. Biol. Chem. 281 2006 24970 24978 (Pubitemid 44274267)
52. J. Nie, X. Hao, D. Chen, X. Han, Z. Chang, and Y. Shi A novel function of the human CLS1 in phosphatidylglycerol synthesis and remodeling Biochim. Biophys. Acta 1801 2010 438 445
53. C. Osman, D.R. Voelker, and T. Langer Making heads or tails of phospholipids in mitochondria J. Cell Biol. 192 2011 7 16
54. 2 enzymes contributes to the initiation and progression of atherosclerosis Curr. Opin. Lipidol. 20 2009 421 427
55. S. Parthasarathy, A. Raghavamenon, M.O. Garelnabi, and N. Santanam Oxidized low density lipoprotein Methods Mol. Biol. 610 2010 403 417
56. A. Pfeiffer, A. Böttcher, E. Orsó, M. Kapinsky, P. Nagy, A. Bodnár, I. Spreitzer, G. Liebisch, W. Drobnik, K. Gempel, M. Horn, S. Holmer, T. Hartung, G. Multhoff, G. Schütz, H. Schindler, A.J. Ulmer, H. Heine, F. Stelter, C. Schütt, G. Rothe, J. Szöllôsi, S. Damjanovich, and G. Schmitz Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts Eur. J. Immunol. 31 2001 3153 3164 (Pubitemid 33100507)
57. 2 group V and secretory sphingomyelinase J. Lipid Res. 51 2010 1801 1809
58. N.B. Ray, L. Durairaj, B.B. Chen, B.J. McVerry, A.J. Ryan, M. Donahoe, A.K. Waltenbaugh, C.P. O'Donnell, F.C. Henderson, C.A. Etscheidt, D.M. McCoy, M. Agassandian, E.C. Hayes-Rowan, T.A. Coon, P.L. Butler, L. Gakhar, S.N. Mathur, J.C. Sieren, Y.Y. Tyurina, V.E. Kagan, G. McLennan, and R.K. Mallampalli Dynamic regulation of cardiolipin by the lipid pump Atp8b1 determines the severity of lung injury in experimental pneumonia Nat. Med. 16 2010 1120 1127
59. X. Rousset, B. Vaisman, M. Amar, A.A. Sethi, and A.T. Remaley Lecithin:cholesterol acyltransferase - from biochemistry to role in cardiovascular disease Curr. Opin. Endocrinol. Diab. Obes. 16 2009 163 171
60. J.T. Salonen, S. Ylä-Herttuala, R. Yamamoto, S. Butler, H. Korpela, R. Salonen, K. Nyyssönen, W. Palinski, and J.L. Witztum Autoantibody against oxidised LDL and progression of carotid atherosclerosis Lancet 339 1992 883 887
61. G. Schmitz, and M. Grandl Endolysosomal phospholipidosis and cytosolic lipid droplet storage and release in macrophages Biochim. Biophys. Acta 1791 2009 524 539
62. G. Schmitz, and G. Müller Structure and function of lamellar bodies, lipid-protein complexes involved in storage and secretion of cellular lipids J. Lipid Res. 32 1991 1539 1570
63. M. Schwarz, L. Späth, C.A. Lux, K. Paprotka, M. Torzewski, K. Dersch, C. Koch-Brandt, M. Husmann, and S. Bhakdi Potential protective role of apoprotein J (clusterin) in atherogenesis: Binding to enzymatically modified low-density lipoprotein reduces fatty acid-mediated cytotoxicity Thromb. Haemost. 100 2008 110 118 (Pubitemid 351948752)
64. H. Shima, H. Takatsu, S. Fukuda, M. Ohmae, K. Hase, H. Kubagawa, J.-Y. Wang, and H. Ohno Identification of TOSO/FAIM3 as an Fc receptor for IgM Int. Immunol. 22 2009 149 156
65. H. Shindou, M. Eto, R. Morimoto, and T. Shimizu Identification of membrane O-acyltransferase family motifs Biochim. Biophys. Acta 383 2009 320 325
66. H. Shindou, D. Hishikawa, T. Harayama, K. Yuki, and T. Shimizu Recent progress on acyl CoA: lysophospholipid acyltransferase research J. Lipid Res. 50 2009 S46 S51
67. A. Sigrüner, C. Büchler, S.M. Bared, M. Grandl, C. Aslanidis, P. Ugocsai, M. Gehrmann, and G Schmitz E-LDL upregulates TOSO expression and enhances survival of human macrophages Biochem. Biophys. Res. Commun. 359 2007 723 728 (Pubitemid 46899011)
68. S.K. Singh, M.V. Suresh, D.C. Prayther, J.P. Moorman, A.E. Rusinol, and A. Agrawal C-reactive protein-bound enzymatically modified low-density lipoprotein does not transform macrophages into foam cells J. Immunol. 180 2008 4316 4322
69. F. Sinibaldi, L. Fiorucci, A. Patriarca, R. Lauceri, T. Ferri, M. Coletta, and R. Santucci Insights into cytochrome c-cardiolipin interaction. Role played by ionic strength Biochemistry 47 2008 6928 6935 (Pubitemid 351898947)
70. E. Soupene, H. Fyrst, and F.A. Kuypers Mammalian acyl-CoA: lysophosphatidylcholine acyltransferase enzymes Proc. Natl. Acad. Sci. U.S.A. 105 2008 88 93
71. G.C. Sparagna, and E.J. Lesnefsky Cardiolipin remodelling in the heart J. Cardiovasc. Pharmacol. 53 2009 290 301
72. D. Steinberg The LDL modification hypothesis of atherogenesis: an update J. Lipid Res. 50 2008 S376 S381
73. P. Suriyaphol, D. Fenske, U. Zähringer, S.R. Han, S. Bhakdi, and M. Husmann Enzymatically modified nonoxidized low-density lipoprotein induces interleukin-8 in human endothelial cells: role of free fatty acids Circulation 12 2002 1107 1114
74. I. Tabas Macrophage death and defective inflammation resolution in atherosclerosis Nat. Rev. Immunol. 10 2010 36 46
75. W.A. Taylor, and G.M. Hatch Identification of the human mitochondrial linoleoyl-coenzyme A monolysocardiolipin acyltransferase (MLCL AT-1) J. Biol. Chem. 284 2009 30360 30371
76. E.A. Tengstrand, G.T. Miwa, and F.Y. Hsieh Bis(monoacylglycerol)phosphate as a non-invasive biomarker to monitor the onset and time-course of phospholipidosis with drug-induced toxicities Expert Opin. Drug Metab. Toxicol. 6 2010 555 570
77. M. Torzewski, M. Klouche, J. Hock, M. Meßner, B. Dorweiler, J. Torzewski, H.E. Gabbert, and S. Bhakdi Immunohistochemical demonstration of enzymatically modified human LDL and its colocalization with the terminal complement complex in the early atherosclerotic lesion Arterioscler. Thromb. Vasc. Biol. 18 1998 369 378 (Pubitemid 28125631)
78. F. Ursini, K.J. Davies, M. Maiorino, T. Parasassi, and A. Sevanian Atherosclerosis: another protein misfolding disease? Trends Mol. Med. 8 2002 370 374 (Pubitemid 34826722)
79. A. Vejux, S. Guyot, T. Montange, J.-M. Riedinger, E. Kahn, and G. Lizard Phospholipidosis and down-regulation of the PI3-K/PDK-1/Akt signalling pathway are vitamin E inhibitable events associated with 7-ketocholesterol-induced apoptosis J. Nutr. Biochem. 20 2009 45 61
80. A. Vejux, E. Kahn, F. Ménétrier, T. Montange, J. Lherminier, J.-M. Riedinger, and G. Lizard Cytotoxic oxysterols induce caspase-independent myelin figure formation and caspase-dependent polar lipid accumulation Histochem. Cell Biol. 127 2007 609 624 (Pubitemid 46879054)
81. A. Vejux, L. Malvitte, and G. Lizard Side effects of oxysterols: cytotoxicity, oxidation, inflammation, and phospholipidosis Braz. J. Med. Biol. Res. 41 2008 545 556
82. S. Vicca, C. Hennequin, T. Nguyen-Khoa, Z.A. Massy, B. Descamps-Latscha, T.B. Drüeke, and B. Lacour Caspase-dependent apoptosis in THP-1 cells exposed to oxidized-low density lipoproteins Biochem. Biophys. Res. Commun. 273 2000 948 954 (Pubitemid 30481060)
83. S. Vicca, Z.A. Massy, C. Hennequin, D. Rihane, T.B. Drüeke, and B. Lacour Apoptotic pathways involved in U937 cells exposed to LDL oxidized by hypochlorous acid Free Radic. Biol. Med. 35 2003 603 615 (Pubitemid 37101128)
84. H. Yoshida, and R. Kisugi Mechanisms of LDL oxidation Clin. Chim. Acta 411 2010 1875 1882
85. I.S. Young, C. McFarlane, and McEneny J Oxidative modification of triacylglycerol-rich lipoproteins Biochem. Soc. Trans. 31 2003 1062 1065 (Pubitemid 37305046)