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Differences between group X and group V secretory phospholipase A2 in lipolytic modification of lipoproteins
Cellular & Molecular Biology Letters volume 17, pages 459–478 (2012)
Abstract
Secretory phospholipases A2 (sPLA2s) are a diverse family of low molecular mass enzymes (13–18 kDa) that hydrolyze the sn-2 fatty acid ester bond of glycerophospholipids to produce free fatty acids and lysophospholipids. We have previously shown that group X sPLA2 (sPLA2-X) had a strong hydrolyzing activity toward phosphatidylcholine in low-density lipoprotein (LDL) linked to the formation of lipid droplets in the cytoplasm of macrophages. Here, we show that group V sPLA2 (sPLA2-V) can also cause the lipolysis of LDL, but its action differs remarkably from that of sPLA2-X in several respects. Although sPLA2-V released almost the same amount of fatty acids from LDL, it released more linoleic acid and less arachidonic acid than sPLA2-X. In addition, the requirement of Ca2+ for the lipolysis of LDL was about 10-fold higher for sPLA2-V than sPLA2-X. In fact, the release of fatty acids from human serum was hardly detectable upon incubation with sPLA2-V in the presence of sodium citrate, which contrasted with the potent response to sPLA2-X. Moreover, sPLA2-X, but not sPLA2-V, was found to specifically interact with LDL among the serum proteins, as assessed by gel-filtration chromatography as well as sandwich enzyme-immunosorbent assay using anti-sPLA2-X and anti-apoB antibodies. Surface plasmon resonance studies have revealed that sPLA2-X can bind to LDL with high-affinity (Kd = 3.1 nM) in the presence of Ca2+. Selective interaction of sPLA2-X with LDL might be involved in the efficient hydrolysis of cell surface or intracellular phospholipids during foam cell formation.
Abbreviations
- Ab:
-
antibody
- apoB:
-
apolipoprotein B
- BSA:
-
bovine serum albumin
- COX:
-
cyclooxygenase
- FCS:
-
fetal calf serum
- HDL:
-
high density lipoprotein
- HPLC:
-
high-performance liquid chromatography
- LDL:
-
low density lipoprotein
- lysoPC:
-
lysophosphatidylcholine
- PBS:
-
phosphate-buffered saline
- PC:
-
phosphatidylcholine
- PLA2 :
-
phospholipase A2
- SDS-PAGE:
-
SDS-polyacrylamide gel electrophoresis
- sPLA2 :
-
secretory PLA2
- sPLA2-IB:
-
group IB sPLA2
- sPLA2-IIA:
-
group IIA sPLA2
- sPLA2-V:
-
group V sPLA2
- sPLA2-X:
-
group X sPLA2
References
Vadas, P. and Pruzanski. W. Role of secretory phospholipases A2 in the pathobiology of disease. Lab. Invest. 55 (1986) 391–404.
Arita, H., Nakano, T. and Hanasaki. K. Thromboxane A2: its generation and role in platelet activation. Prog. Lipid Res. 28 (1989) 273–301.
Balsinde, J., Balboa, M.A., Insel, P.A. and Dennis, E.A. Regulation and inhibition of phospholipase A2. Annu. Rev. Pharmacol. Toxicol. 39 (1999) 175–189.
Six, D.A. and Dennis, E.A. The expanding superfamily of phospholipase A(2) enzymes: classification and characterization. Biochim. Biophys. Acta 1488 (2000) 1–19.
Lambeau, G. and Lazdunski, M. Receptors for a growing family of secreted phospholipases A2. Trends Pharmacol. Sci. 20 (1999) 162–170.
Ishizaki, J., Suzuki, N., Higashino, K., Yokota, Y., Ono, T., Kawamoto, K., Fujii, N., Arita, H. and Hanasaki, K. Cloning and characterization of novel mouse and human secretory phospholipase A(2)s. J. Biol. Chem. 274 (1999) 24973–24979.
Suzuki, N., Ishizaki, J., Yokota, Y., Higashino, K., Ono, T., Ikeda, M., Fujii, N., Kawamoto, K. and Hanasaki, K. Structures, enzymatic properties, and expression of novel human and mouse secretory phospholipase A(2)s. J. Biol. Chem. 275 (2000) 5785–5793.
Gelb, M.H., Valentin, E., Ghomashchi, F., Lazdunski, M. and Lambeau, G. Cloning and recombinant expression of a structurally novel human secreted phospholipase A2. J. Biol. Chem. 275 (2000) 39823–39826.
de Haas, G.H., Postema, N.M., Nieuwenhuizen, W. and van Deenen, L.L. Purification and properties of an anionic zymogen of phospholipase A from porcine pancreas. Biochim. Biophys. Acta 159 (1968) 118–129.
Arita, H., Hanasaki, K., Nakano, T., Oka, S., Teraoka, H. and Matsumoto, K. Novel proliferative effect of phospholipase A2 in Swiss 3T3 cells via specific binding site. J. Biol. Chem. 266 (1991) 19139–19141.
Hanasaki, K. and Arita, H. Characterization of a high affinity binding site for pancreatic-type phospholipase A2 in the rat. Its cellular and tissue distribution. J. Biol. Chem. 267 (1992) 6414–6420.
Ishizaki, J., Hanasaki, K., Higashino, K., Kishino, J., Kikuchi, N., Ohara, O. and Arita, H. Molecular cloning of pancreatic group I phospholipase A2 receptor. J. Biol. Chem. 269 (1994) 5897–5904.
Ohara, O., Ishizaki, J. and Arita, H. Structure and function of phospholipase A2 receptor. Prog. Lipid Res. 34 (1995) 117–138.
Gronroos, J.M. and Nevalainen, T.J. Increased concentrations of synovialtype phospholipase A2 in serum and pulmonary and renal complications in acute pancreatitis. Digestion 52 (1992) 232–236.
Green, J.A., Smith, G.M., Buchta, R., Lee, R., Ho, K.Y., Rajkovic, I.A. and Scott, K.F. Circulating phospholipase A2 activity associated with sepsis and septic shock is indistinguishable from that associated with rheumatoid arthritis. Inflammation 15 (1991) 355–367.
Elinder, L.S., Dumitrescu, A., Larsson, P., Hedin, U., Frostegard, J. and Claesson, H.E. Expression of phospholipase A2 isoforms in human normal and atherosclerotic arterial wall. Arterioscler. Thromb. Vasc. Biol. 17 (1997) 2257–2263.
Romano, M., Romano, E., Bjorkerud, S. and Hurt-Camejo, E. Ultrastructural localization of secretory type II phospholipase A2 in atherosclerotic and nonatherosclerotic regions of human arteries. Arterioscler. Thromb. Vasc. Biol. 18 (1998) 519–525.
Schiering, A., Menschikowski, M., Mueller, E. and Jaross, W. Analysis of secretory group II phospholipase A2 expression in human aortic tissue in dependence on the degree of atherosclerosis. Atherosclerosis 144 (1999) 73–78.
Sartipy, P., Johansen, B., Gasvik, K. and Hurt-Camejo, E. Molecular basis for the association of group IIA phospholipase A(2) and decorin in human atherosclerotic lesions. Circ. Res. 86 (2000) 707–714.
Chen, J., Engle, S.J., Seilhamer, J.J. and Tischfield, J.A. Cloning and characterization of novel rat and mouse low molecular weight Ca(2+)-dependent phospholipase A2s containing 16 cysteines. J. Biol. Chem. 269 (1994) 23018–23024.
Bingham, C.O., 3rd, Fijneman, R.J., Friend, D.S., Goddeau, R.P., Rogers, R.A., Austen, K.F. and Arm, J.P. Low molecular weight group IIA and group V phospholipase A(2) enzymes have different intracellular locations in mouse bone marrow-derived mast cells. J. Biol. Chem. 274 (1999) 31476–31484.
Kim, Y.J., Kim, K.P., Han, S.K., Munoz, N.M., Zhu, X., Sano, H., Leff, A.R. and Cho, W. Group V phospholipase A2 induces leukotriene biosynthesis in human neutrophils through the activation of group IVA phospholipase A2. J. Biol. Chem. 277 (2002) 36479–36488.
Cupillard, L., Koumanov, K., Mattei, M.G., Lazdunski, M. and Lambeau, G. Cloning, chromosomal mapping, and expression of a novel human secretory phospholipase A2. J. Biol. Chem. 272 (1997) 15745–15752.
Saiga, A., Morioka, Y., Ono, T., Nakano, K., Ishimoto, Y., Arita, H. and Hanasaki, K. Group X secretory phospholipase A(2) induces potent productions of various lipid mediators in mouse peritoneal macrophages. Biochim. Biophys. Acta 1530 (2001) 67–76.
Morioka, Y., Saiga, A., Yokota, Y., Suzuki, N., Ikeda, M., Ono, T., Nakano, K., Fujii, N., Ishizaki, J., Arita, H. and Hanasaki, K. Mouse group X secretory phospholipase A2 induces a potent release of arachidonic acid from spleen cells and acts as a ligand for the phospholipase A2 receptor. Arch. Biochem. Biophys. 381 (2000) 31–42.
Morioka, Y., Ikeda, M., Saiga, A., Fujii, N., Ishimoto, Y., Arita, H. and Hanasaki, K. Potential role of group X secretory phospholipase A(2) in cyclooxygenase-2-dependent PGE(2) formation during colon tumorigenesis. FEBS Lett. 487 (2000) 262–266.
Higashino, K., Yokota, Y., Ono, T., Kamitani, S., Arita, H. and Hanasaki, K. Identification of a soluble form phospholipase A2 receptor as a circulating endogenous inhibitor for secretory phospholipase A2. J. Biol. Chem. 277 (2002) 13583–13588.
Hanasaki, K., Ono, T., Saiga, A., Morioka, Y., Ikeda, M., Kawamoto, K., Higashino, K., Nakano, K., Yamada, K., Ishizaki, J. and Arita, H. Purified group X secretory phospholipase A(2) induced prominent release of arachidonic acid from human myeloid leukemia cells. J. Biol. Chem. 274 (1999) 34203–34211.
Bezzine, S., Koduri, R.S., Valentin, E., Murakami, M., Kudo, I., Ghomashchi, F., Sadilek, M., Lambeau, G. and Gelb, M.H. Exogenously added human group X secreted phospholipase A(2) but not the group IB, IIA, and V enzymes efficiently release arachidonic acid from adherent mammalian cells. J. Biol. Chem. 275 (2000) 3179–3191.
Murakami, M., Kambe, T., Shimbara, S., Yamamoto, S., Kuwata, H. and Kudo, I. Functional association of type IIA secretory phospholipase A(2) with the glycosylphosphatidylinositol-anchored heparan sulfate proteoglycan in the cyclooxygenase-2-mediated delayed prostanoidbiosynthetic pathway. J. Biol. Chem. 274 (1999) 29927–29936.
Murakami, M., Koduri, R.S., Enomoto, A., Shimbara, S., Seki, M., Yoshihara, K., Singer, A., Valentin, E., Ghomashchi, F., Lambeau, G., Gelb, M.H. and Kudo, I. Distinct arachidonate-releasing functions of mammalian secreted phospholipase A2s in human embryonic kidney 293 and rat mastocytoma RBL-2H3 cells through heparan sulfate shuttling and external plasma membrane mechanisms. J. Biol. Chem. 276 (2001) 10083–10096.
Munoz, N.M., Kim, Y.J., Meliton, A.Y., Kim, K.P., Han, S.K., Boetticher, E., O’Leary, E., Myou, S., Zhu, X., Bonventre, J.V., Leff, A.R. and Cho, W. Human group V phospholipase A2 induces group IVA phospholipase A2-independent cysteinyl leukotriene synthesis in human eosinophils. J. Biol. Chem. 278 (2003) 38813–38820.
Gesquiere, L., Cho, W. and Subbaiah, P.V. Role of group IIa and group V secretory phospholipases A(2) in the metabolism of lipoproteins. Substrate specificities of the enzymes and the regulation of their activities by sphingomyelin. Biochemistry 41 (2002) 4911–4920.
Hanasaki, K., Yamada, K., Yamamoto, S., Ishimoto, Y., Saiga, A., Ono, T., Ikeda, M., Notoya, M., Kamitani, S. and Arita, H. Potent modification of low density lipoprotein by group X secretory phospholipase A2 is linked to macrophage foam cell formation. J. Biol. Chem. 277 (2002) 29116–29124.
Ishimoto, Y., Yamada, K., Yamamoto, S., Ono, T., Notoya, M. and Hanasaki, K. Group V and X secretory phospholipase A(2)s-induced modification of high-density lipoprotein linked to the reduction of its antiatherogenic functions. Biochim. Biophys. Acta 1642 (2003) 129–138.
Hara, S., Shike, T., Takasu, N. and Mizui, T. Lysophosphatidylcholine promotes cholesterol efflux from mouse macrophage foam cells. Arterioscler. Thromb. Vasc. Biol. 17 (1997) 1258–1266.
Hevonoja, T., Pentikainen, M.O., Hyvonen, M.T., Kovanen, P.T. and Ala-Korpela, M. Structure of low density lipoprotein (LDL) particles: basis for understanding molecular changes in modified LDL. Biochim. Biophys. Acta 1488 (2000) 189–210.
Reynolds, L.J., Hughes, L.L. and Dennis, E.A. Analysis of human synovial fluid phospholipase A2 on short chain phosphatidylcholine-mixed micelles: development of a spectrophotometric assay suitable for a microtiterplate reader. Anal. Biochem. 204 (1992) 190–197.
Tojo, H., Ono, T. and Okamoto, M. Reverse-phase high-performance liquid chromatographic assay of phospholipases: application of spectrophotometric detection to rat phospholipase A2 isozymes. J. Lipid Res. 34 (1993) 837–844.
Dole, V.P. and Meinertz, H. Microdetermination of long-chain fatty acids in plasma and tissues. J. Biol. Chem. 235 (1960) 2595–2599.
Chen, Y. and Dennis, E.A. Expression and characterization of human group V phospholipase A2. Biochim. Biophys. Acta 1394 (1998) 57–64.
Schaloske, R.H. and Dennis, E.A. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 1761 (2006) 1246–1259.
Stremler, K.E., Stafforini, D.M., Prescott, S.M. and McIntyre, T.M. Human plasma platelet-activating factor acetylhydrolase. Oxidatively fragmented phospholipids as substrates. J. Biol. Chem. 266 (1991) 11095–11103.
Davis, B., Koster, G., Douet, L.J., Scigelova, M., Woffendin, G., Ward, J.M., Smith, A., Humphries, J., Burnand, K.G., Macphee, C.H. and Postle, A.D. Electrospray ionization mass spectrometry identifies substrates and products of lipoprotein-associated phospholipase A2 in oxidized human low density lipoprotein. J. Biol. Chem. 283 (2008) 6428–6437.
Han, S.K., Yoon, E.T. and Cho, W. Bacterial expression and characterization of human secretory class V phospholipase A2. Biochem. J. 331(Pt 2) (1998) 353–357.
Murakami, M. and Kudo, I. Secretory phospholipase A2. Biol. Pharm. Bull. 27 (2004) 1158–1164.
Rao, G.N., Baas, A.S., Glasgow, W.C., Eling, T.E., Runge, M.S. and Alexander, R.W. Activation of mitogen-activated protein kinases by arachidonic acid and its metabolites in vascular smooth muscle cells. J. Biol. Chem. 269 (1994) 32586–32591
Tietge, U.J., Maugeais, C., Lund-Katz, S., Grass, D., deBeer, F.C. and Rader, D.J. Human secretory phospholipase A2 mediates decreased plasma levels of HDL cholesterol and apoA-I in response to inflammation in human apoA-I transgenic mice. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 1213–1218.
Lookene, A., Savonen, R. and Olivecrona, G. Interaction of lipoproteins with heparan sulfate proteoglycans and with lipoprotein lipase. Studies by surface plasmon resonance technique. Biochemistry 36 (1997) 5267–5275.
Cseh, K., Karadi, I., Rischak, K., Szollar, L., Janoki, G., Jakab, L. and Romics, L. Binding of fibronectin to human lipoproteins. Clin. Chim. Acta 182 (1989) 75–85.
Carrero, P., Gomez-Coronado, D., Olivecrona, G. and Lasuncion, M.A. Binding of lipoprotein lipase to apolipoprotein B-containing lipoproteins. Biochim. Biophys. Acta 1299 (1996) 198–206.
Fukuchi, Y., Kudo, Y., Kumagai, T., Ebina, K. and Yokota, K. Binding assay of low density lipoprotein to Asp-hemolysin from Aspergillus fumigatus. Biol. Pharm. Bull. 19 (1996) 1380–1381.
Jin, L., Shieh, J.J., Grabbe, E., Adimoolam, S., Durbin, D. and Jonas, A. Surface plasmon resonance biosensor studies of human wild-type and mutant lecithin cholesterol acyltransferase interactions with lipoproteins. Biochemistry 38 (1999) 15659–15665.
Boren, J., Lookene, A., Makoveichuk, E., Xiang, S., Gustafsson, M., Liu, H., Talmud, P. and Olivecrona, G. Binding of low density lipoproteins to lipoprotein lipase is dependent on lipids but not on apolipoprotein B. J. Biol. Chem. 276 (2001) 26916–26922.
Sivaram, P., Choi, S.Y., Curtiss, L.K. and Goldberg, I.J. An amino-terminal fragment of apolipoprotein B binds to lipoprotein lipase and may facilitate its binding to endothelial cells. J. Biol. Chem. 269 (1994) 9409–9412.
Choi, S.Y., Sivaram, P., Walker, D.E., Curtiss, L.K., Gretch, D.G., Sturley, S.L., Attie, A.D., Deckelbaum, R.J. and Goldberg, I.J. Lipoprotein lipase association with lipoproteins involves protein-protein interaction with apolipoprotein B. J. Biol. Chem. 270 (1995) 8081–8086.
Pang, L., Sivaram, P. and Goldberg, I.J. Cell-surface expression of an amino-terminal fragment of apolipoprotein B increases lipoprotein lipase binding to cells. J. Biol. Chem. 271 (1996) 19518–19523.
Choi, S.Y., Pang, L., Kern, P.A., Kayden, H.J., Curtiss, L.K., Vanni-Reyes, T.M. and Goldberg, I.J. Dissociation of LPL and LDL: effects of lipoproteins and anti-apoB antibodies. J. Lipid Res. 38 (1997) 77–85.
Goldberg, I.J., Wagner, W.D., Pang, L., Paka, L., Curtiss, L.K., DeLozier, J.A., Shelness, G.S., Young, C.S. and Pillarisetti, S. The NH2-terminal region of apolipoprotein B is sufficient for lipoprotein association with glycosaminoglycans. J. Biol. Chem. 273 (1998) 35355–35361.
Segrest, J.P., Jones, M.K., De Loof, H. and Dashti, N. Structure of apolipoprotein B-100 in low density lipoproteins. J. Lipid Res. 42 (2001) 1346–1367.
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Kamitani, S., Yamada, K., Yamamoto, S. et al. Differences between group X and group V secretory phospholipase A2 in lipolytic modification of lipoproteins. Cell Mol Biol Lett 17, 459–478 (2012). https://doi.org/10.2478/s11658-012-0019-2
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DOI: https://doi.org/10.2478/s11658-012-0019-2