Hydrolysis products generated by lipoprotein lipase and endothelial lipase differentially impact THP-1 macrophage cell signalling pathways

Lipids

Volumn 48, Issue 8, 2013, Pages 769-778

  Essaji, Yasmin ^a   Yang, Yanbo ^a   Albert, Carolyn J ^b   Ford, David A ^b   Brown, Robert J ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antibody array; Atherosclerosis; Cell signalling; Endothelial lipase; Free fatty acid; Lipoprotein lipase; Lipoproteins; Mass spectrometry; Phosphatidylcholine; Triacylglycerol

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; ENDOTHELIAL LIPASE; LIPOPROTEIN LIPASE; MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; PHOSPHATIDYLCHOLINE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; TROPOMYSIN RELATED KINASE A; TROPOMYSIN RELATED KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ARTICLE; ATHEROSCLEROSIS; CELL LYSATE; CONTROLLED STUDY; DISEASE ASSOCIATION; ELECTROSPRAY MASS SPECTROMETRY; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; MACROPHAGE; MASS FRAGMENTOGRAPHY; NUCLEOTIDE SEQUENCE; PROTEIN BLOOD LEVEL; PROTEIN HYDROLYSIS; SIGNAL TRANSDUCTION; THP 1 MACROPHAGE;

CELLS, CULTURED; FATTY ACIDS; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; HUMANS; HYDROLYSIS; LIPASE; LIPOPROTEIN LIPASE; LIPOPROTEINS; MACROPHAGES; PHOSPHATIDYLCHOLINES; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84881130100     PISSN: 00244201     EISSN: 15589307     Source Type: Journal    
DOI: 10.1007/s11745-013-3810-6     Document Type: Article

References (66)

1. Hide WA, Chan L, Li WH (1992) Structure and evolution of the lipase superfamily. J Lipid Res 33:167-178
2. Hirata K, Dichek HL, Cioffi JA, Choi SY, Leeper NJ, Quintana L, Kronmal GS, Cooper AD, Quertermous T (1999) Cloning of a unique lipase from endothelial cells extends the lipase gene family. J Biol Chem 274:14170-14175
3. Jaye M, Lynch KJ, Krawiec J, Marchadier D, Maugeais C, Doan K, South V, Amin D, Perrone M, Rader DJ (1999) A novel endothelial-derived lipase that modulates HDL metabolism. Nat Genet 21:424-428
4. McCoy MG, Sun G-S, Marchadier D, Maugeais C, Glick JM, Rader DJ (2002) Characterization of the lipolytic activity of endothelial lipase. J Lipid Res 43:921-929
5. Cheng CF, Oosta GM, Bensadoun A, Rosenberg RD (1981) Binding of lipoprotein lipase to endothelial cells in culture. J Biol Chem 256:12893-12898
6. Shimada K, Gill PJ, Silbert JE, Douglas WH, Fanburg BL (1981) Involvement of cell surface heparin sulfate in the binding of lipoprotein lipase to cultured bovine endothelial cells. J Clin Invest 68:995-1002
7. Strauss JG, Zimmermann R, Hrzenjak A, Zhou Y, Kratky D, Levak-Frank S, Kostner GM, Zechner R, Frank S (2002) Endothelial cell-derived lipase mediates uptake and binding of high-density lipoprotein (HDL) particles and the selective uptake of HDL-associated cholesterol esters independent of its enzymic activity. Biochem J 368:69-79
8. Brown RJ, Miller GC, Griffon N, Long CJ, Rader DJ (2007) Glycosylation of endothelial lipase at asparagine-116 reduces activity and the hydrolysis of native lipoproteins in vitro and in vivo. J Lipid Res 48:1132-1139
9. Beigneux AP, Davies BS, Gin P, Weinstein MM, Farber E, Qiao X, Peale F, Bunting S, Walzem RL, Wong JS, Blaner WS, Ding ZM, Melford K, Wongsiriroj N, Shu X, de Sauvage F, Ryan RO, Fong LG, Bensadoun A, Young SG (2007) Glycosylphosphatidylinositol-anchored high-density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab 5:279-291
10. Mulder M, Lombardi P, Jansen H, van Berkel TJC, Frants RR, Havekes LM (1992) Heparan sulphate proteoglycans are involved in the lipoprotein lipase-mediated enhancement of the cellular binding of very low density and low density lipoproteins. Biochem Biophys Res Commun 185:582-587
11. Rumsey SC, Obunike JC, Arad Y, Deckelbaum RJ, Goldberg IJ (1992) Lipoprotein lipase-mediated uptake and degradation of low density lipoproteins by fibroblasts and macrophages. J Clin Invest 90:1504-1512
12. Fuki IV, Blanchard N, Jin W, Marchadier DH, Millar JS, Glick JM, Rader DJ (2003) Endogenously produced endothelial lipase enhances binding and cellular processing of plasma lipoproteins via heparan sulfate proteoglycan-mediated pathway. J Biol Chem 278:34331-34338
13. O'Brien KD, Gordon D, Deeb S, Ferguson M, Chait A (1992) Lipoprotein lipase is synthesized by macrophage-derived foam cells in human coronary atherosclerotic plaques. J Clin Invest 89:1544-1550
14. Qiu G (2007) Hill JS (2007) Atorvastatin decreases lipoprotein lipase and endothelial lipase expression in human THP-1 macrophages. J Lipid Res 48:2112-2122
15. Zilversmit DB (1979) Atherogenesis: a postprandial phenomenon. Circulation 60:473-485
16. Ylä-Herttuala S, Lipton BA, Rosenfeld ME, Goldberg IJ, Steinberg D, Witztum JL (1991) Macrophages and smooth muscle cells express lipoprotein lipase in human and rabbit atherosclerotic lesions. Proc Natl Acad Sci USA 88:10143-10147
17. Azumi H, Hirata K, Ishida T, Kojima Y, Rikitake Y, Takeuchi S, Inoue N, Kawashima S, Hayashi Y, Itoh H, Quertermous T, Yokoyama M (2003) Immunohistochemical localization of endothelial cell-derived lipase in atherosclerotic human coronary arteries. Cardiovasc Res 58:647-654
18. Takahashi M, Hiyama Y, Yokoyama M, Yu S, Hu Y, Melford K, Bensadoun A, Goldberg IJ (2008) In vivo arterial lipoprotein lipase expression augments inflammatory responses and impairs vascular dilatation. Arterioscler Thromb Vasc Biol 28:455-462
19. Babaev VR, Fazio S, Gleaves LA, Carter KJ, Semenkovich CF, Linton MF (1999) Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in vivo. J Clin Invest 103:1697-1705
20. Babaev VR, Patel MB, Semenkovich CF, Fazio S, Linton MF (2000) Macrophage lipoprotein lipase promotes foam cell formation and atherosclerosis in low density lipoprotein receptor-deficient mice. J Biol Chem 275:26293-26299
21. Clee SM, Bissada N, Miao F, Miao L, Marais AD, Henderson HE, Steures P, McManus J, McManus B, LeBoeuf RC, Kastelein JJ, Hayden MR (2000) Plasma and vessel wall lipoprotein lipase have different roles in atherosclerosis. J Lipid Res 41:521-531
22. Qiu G, Ho AC, Yu W, Hill JS (2007) Suppression of endothelial or lipoprotein lipase in THP-1 macrophages attenuates proinflammatory cytokine secretion. J Lipid Res 48:385-394
23. Kota RS, Ramana CV, Tenorio FA, Enelow RI, Rutledge JC (2005) Differential effects of lipoprotein lipase on tumor necrosis factor-α and interferon-γ-mediated gene expression in human endothelial cells. J Biol Chem 280:31076-31084
24. Riederer M, Lechleitner M, Hrzenjak A, Koefeler H, Desoye G, Heinemann A, Frank S (2011) Endothelial lipase (EL) and EL-generated lysophosphatidylcholines promote IL-8 expression in endothelial cells. Atherosclerosis 214:338-344
25. Skottova N, Savonen R, Lookene A, Hultin M, Olivecrona G (1995) Lipoprotein lipase enhances removal of chylomicrons and chylomicron remnants by the perfused rat liver. J Lipid Res 36:1334-1344
26. Brundert M, Heeren J, Merkel M, Carambia A, Herkel J, Groitl P, Dobner T, Ramakrishnan R, Moore KJ, Rinninger F (2011) Scavenger receptor CD36 mediates uptake of high density lipoproteins in mice and by cultured cells. J Lipid Res 52:745-758
27. Brown RJ, Gauthier A, Parks RJ, McPherson R, Sparks DL, Schultz JR, Yao Z (2004) Severe hypoalphalipoproteinemia in mice expressing human hepatic lipase deficient in binding to heparan sulfate proteoglycan. J Biol Chem 279:42403-42409
28. Chung BH, Wilkinson T, Geer JC, Segrest JP (1980) Preparative and quantitative isolation of plasma lipoproteins: rapid, single discontinuous density gradient ultracentrifugation in a vertical rotor. J Lipid Res 21:284-291
29. Griffon N, Budreck EC, Long CJ, Broedl UC, Marchadier DHL, Glick JM, Rader DJ (2006) Substrate specificity of lipoprotein lipase and endothelial lipase: studies of lid chimeras. J Lipid Res 47:1803-1811
30. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917
31. Han X, Gross RW (2001) Quantitative analysis and molecular species fingerprinting of triacylglyceride molecular species directly from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry. Anal Biochem 295:88-100
32. Han X, Gross RW (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. Ford DA, Monda JK, Brush RS, Anderson RE, Richards MJ, Fliesler SJ (2008) Lipidomic analysis of the retina in a rat model of Smith-Lemli-Opitz syndrome: alterations in docosahexaenoic acid content of phospholipid molecular species. J Neurochem 105:1032-1047
34. Quehenberger O, Armando A, Dumlao D, Stephens DL, Dennis EA (2008) Lipidomics analysis of essential fatty acids in macrophages. Prostaglandins Leukot Essent Fatty Acids 79:123-129
35. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85
36. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675
37. Gauster M, Rechberger G, Sovic A, Hörl G, Steyrer E, Sattler W, Frank S (2005) Endothelial lipase releases saturated and unsaturated fatty acids of high density lipoprotein phosphatidylcholine. J Lipid Res 46:1517-1525
38. Brown RJ, Rader DJ (2007) Lipases as modulators of atherosclerosis in murine models. Curr Drug Targets 8:1307-1319
39. Bengtsson G, Olivecrona T (1980) Lipoprotein lipase. Mechanism of product inhibition. Eur J Biochem 106:557-562
40. Blanchette-Mackie EJ, Scow RO (1976) Retention of lipolytic products in chylomicrons incubated with lipoprotein lipase: electron microscope study. J Lipid Res 17:57-67
41. Li XA, Hatanaka K, Ishibashi-Ueda H, Yutani C, Yamamoto A (1995) Characterization of serum amyloid P component from human aortic atherosclerotic lesions. Arterioscler Thromb Vasc Biol 15:252-257
42. Schaefer LE, Adlersberg D, Steinberg AG (1958) Serum phospholipids: genetic and environmental influences. Circulation 18:341-347
43. Rider OJ, Holloway CJ, Emmanuel Y, Bloch E, Clarke K, Neubauer S (2012) Increasing plasma free fatty acids in healthy subjects induces aortic distensibility changes seen in obesity. Circ Cardiovasc Imaging 5:367-375
44. Kobayashi J, Hashimoto H, Fukamachi I, Tashiro J, Shirai K, Saito Y, Yoshida S (1993) Lipoprotein lipase mass and activity in severe hypertriglyceridemia. Clin Chim Acta 216:113-123
45. Badellino KO, Wolfe ML, Reilly MP, Rader DJ (2006) Endothelial lipase concentrations are increased in metabolic syndrome and associated with coronary atherosclerosis. PLoS Med 3:e22
46. Krettek A, Östergren-Lundén G, Fager G, Rosmond C, Bondjers G, Lustig F (2001) Expression of PDGF receptors and ligand-induced migration of partially differentiated human monocyte-derived macrophages: influence of IFN-γ and TGF-β. Atherosclerosis 156:267-275
47. Inaba T, Kawamura M, Gotoda T, Harada K, Shimada M, Ohsuga J, Shimano H, Akanuma Y, Yazaki Y, Yamada N (1995) Effects of platelet-derived growth factor on the synthesis of lipoprotein lipase in human monocyte-derived macrophages. Arterioscler Thromb Vasc Biol 15:522-528
48. Stevenson FT, Shearer GC, Atkinson DN (2001) Lipoprotein-stimulated mesangial cell proliferation and gene expression are regulated by lipoprotein lipase. Kidney Int 59:2062-2068
49. Pulford K, Morris SW, Turturro F (2004) Anaplastic lymphoma kinase proteins in growth control and cancer. J Cell Physiol 199:330-358
50. Baruzzi A, Iacobucci I, Soverini S, Lowell CA, Martinelli G, Berton G (2010) c-Abl and Src-family kinases cross-talk in regulation of myeloid cell migration. FEBS Lett 584:15-21
51. Shaposhnik Z, Wang X, Lusis AJ (2010) Arterial colony stimulating factor-1 influences atherosclerotic lesions by regulating monocyte migration and apoptosis. J Lipid Res 51:1962-1970
52. Irvine KM, Andrews MR, Fernandez-Rojo MA, Schroder K, Burns CJ, Su S, Wilks AF, Parton RG, Hume DA, Sweet MJ (2009) Colony-stimulating factor-1 (CSF-1) delivers a proatherogenic signal to human macrophages. J Leukoc Biol 85:278-288
53. Lim W-S, Timmins JM, Seimon TA, Sadler A, Kolodgie FD, Virmani R, Tabas I (2008) Signal transducer and activator of transcription-1 is critical for apoptosis in macrophages subjected to endoplasmic reticulum stress in vitro and in advanced atherosclerotic lesions in vivo. Circulation 117:940-951
54. Shibuya M (2006) Vascular endothelial growth factor receptor-1 (VEGFR-1/Flt-1): a dual regulator for angiogenesis. Angiogenesis 9:225-230
55. Kraemer R, Baker PJ, Kent KC, Ye Y, Han JJ, Tejada R, Silane M, Upmacis R, Deeb R, Chen Y, Levine DM, Hempstead B (2005) Decreased neurotrophin TrkB receptor expression reduces lesion size in the apolipoprotein E-null mutant mouse. Circulation 112:3644-3653
56. Donovan MJ, Miranda RC, Kraemer R, McCaffrey TA, Tessarollo L, Mahadeo D, Sharif S, Kaplan DR, Tsoulfas P, Parada L, Toran-Allerand CD, Hajjar DP, Hempstead BL (1995) Neurotrophin and neurotrophin receptors in vascular smooth muscle cells. Regulation of expression in response to injury. Am J Pathol 147:309-324
57. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296:1655-1657
58. Fernández-Hernando C, József L, Jenkins D, Di Lorenzo A, Sessa WC (2009) Absence of Akt1 reduces vascular smooth muscle cell migration and survival and induces features of plaque vulnerability and cardiac dysfunction during atherosclerosis. Arterioscler Thromb Vasc Biol 29:2033-2040
59. Fernández-Hernando C, Ackah E, Yu J, Suárez Y, Murata T, Iwakiri Y, Prendergast J, Miao RQ, Birnbaum MJ, Sessa WC (2007) Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab 6:446-457
60. Chang JD, Sukhova GK, Libby P, Schvartz E, Lichtenstein AH, Field SJ, Kennedy C, Madhavarapu S, Luo J, Wu D, Cantley LC (2007) Deletion of the phosphoinositide 3-kinase p110γ gene attenuates murine atherosclerosis. Proc Natl Acad Sci USA 104:8077-8082
61. Jin W, Wang X, Millar JS, Quertermous T, Rothblat GH, Glick JM, Rader DJ (2007) Hepatic proprotein convertases modulate HDL metabolism. Cell Metab 6:129-136
62. Singaraja RR, Sivapalaratnam S, Hovingh K, Dubé MP, Castro-Perez J, Collins HL, Adelman SJ, Riwanto M, Manz J, Hubbard B, Tietjen I, Wong K, Mitnaul LJ, van Heek M, Lin L, Roddy TA, McEwen J, Dallinge-Thie G, van Vark-van der Zee L, Verwoert G, Winther M, van Duijn C, Hofman A, Trip MD, Marais AD, Asztalos B, Landmesser U, Sijbrands E, Kastelein JJ, Hayden MR (2013) The impact of partial and complete loss-of-function mutations in endothelial lipase on high-density lipoprotein levels and functionality in humans. Circ Cardiovasc Genet 6:54-62
63. Brown RJ, Lagor WR, Sankaranaravanan S, Yasuda T, Quertermous T, Rothblat GH, Rader DJ (2010) Impact of combined deficiency of hepatic lipase and endothelial lipase on the metabolism of both high-density lipoproteins and apolipoprotein B-containing lipoproteins. Circ Res 107:357-364
64. Escolà-Gil JC, Chen X, Julve J, Quesada H, Santos D, Metso J, Tous M, Jauhiainen M, Blanco-Vaca F (2013) Hepatic lipase- and endothelial lipase-deficiency in mice promotes macrophage-to-feces RCT and HDL antioxidant properties. Biochim Biophys Acta 1831:691-697
65. Ishida T, Choi SY, Kundu RK, Spin J, Yamashita T, Hirata K, Kojima Y, Yokoyama M, Cooper AD, Quertermous T (2004) Endothelial lipase modulates susceptibility to atherosclerosis in apolipoprotein-E-deficient mice. J Biol Chem 279:45085-45092
66. Ko KWS, Paul A, Ma K, Li L, Chan L (2005) Endothelial lipase modulates HDL but has no effect on atherosclerosis development in apoE-/- and LDLR-/- mice. J Lipid Res 46:2586-2594