Group X secreted phospholipase a2 limits the development of atherosclerosis in LDL receptor-null mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 3, 2013, Pages 466-473

  Ait Oufella, Hafid ^a,b   Herbin, Olivier ^a   Lahoute, Charlotte ^a   Coatrieux, Christelle ^c   Loyer, Xavier ^a   Joffre, Jeremie ^a   Laurans, Ludivine ^a   Ramkhelawon, Bhama ^a   Blanc Brude, Olivier ^a   Karabina, Sonia ^d   Girard, Christophe A ^c   Payré, Christine ^c   Yamamoto, Kei ^e   Binder, Christoph J ^e,f   Murakami, Makoto ^g   Tedgui, Alain ^a   Lambeau, Gérard ^c   Mallat, Ziad ^a,g  

^a PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^b HÔPITAL SAINT ANTOINE   (France)

^c INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d INSERM   (France)

^e TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

^g ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

atherosclerosis; immunity; inflammation; lymphocyte; secreted phospholipase A2

Indexed keywords

PHOSPHOLIPASE A2; PLA2G10 ENZYME; UNCLASSIFIED DRUG; VARESPLADIB METHYL;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW CELL; CONTROLLED STUDY; CORONARY ARTERY DISEASE; ENZYME ACTIVITY; ENZYME DEFICIENCY; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SPLEEN CELL; TH1 CELL;

ADAPTIVE IMMUNITY; ANIMALS; AORTA, THORACIC; AORTIC DISEASES; APOPTOSIS; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; GROUP X PHOSPHOLIPASES A2; HUMANS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NECROSIS; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, LDL; TH1 CELLS; TIME FACTORS;

EID: 84874381989     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300309     Document Type: Article

References (50)

1. Lambeau G, Gelb MH. Biochemistry and physiology of mammalian secreted phospholipases A2. Annu Rev Biochem. 2008;77:495-520.
2. Ghesquiere SA, Gijbels MJ, Anthonsen M, van Gorp PJ, van der Made I, Johansen B, Hofker MH, de Winther MP. Macrophage-specific overexpression of group IIa sPLA2 increases atherosclerosis and enhances collagen deposition. J Lipid Res. 2005;46:201-210.
3. Karabina SA, Brochériou I, Le Naour G, Agrapart M, Durand H, Gelb M, Lambeau G, Ninio E. Atherogenic properties of LDL particles modified by human group X secreted phospholipase A2 on human endothelial cell function. FASEB J. 2006;20:2547-2549.
4. Jönsson-Rylander AC, Lundin S, Rosengren B, Pettersson C, Hurt-Camejo E. Role of secretory phospholipases in atherogenesis. Curr Atheroscler Rep. 2008;10:252-259.
5. Boyanovsky B, Zack M, Forrest K, Webb NR. The capacity of group V sPLA2 to increase atherogenicity of ApoE-/-and LDLR-/-mouse LDL in vitro predicts its atherogenic role in vivo. Arterioscler Thromb Vasc Biol. 2009;29:532-538.
6. Sato H, Kato R, Isogai Y, et al. Analyses of group III secreted phospholipase A2 transgenic mice reveal potential participation of this enzyme in plasma lipoprotein modification, macrophage foam cell formation, and atherosclerosis. J Biol Chem. 2008;283:33483-33497.
7. Curfs DM, Ghesquiere SA, Vergouwe MN, van der Made I, Gijbels MJ, Greaves DR, Verbeek JS, Hofker MH, de Winther MP. Macrophage secretory phospholipase A2 group X enhances anti-inflammatory responses, promotes lipid accumulation, and contributes to aberrant lung pathology. J Biol Chem. 2008;283:21640-21648.
8. Mallat Z, Lambeau G, Tedgui A. Lipoprotein-associated and secreted phospholipases A2 in cardiovascular disease: roles as biological effectors and biomarkers. Circulation. 2010;122:2183-2200.
9. Rosenson RS, Hurt-Camejo E. Phospholipase A2 enzymes and the risk of atherosclerosis. Eur Heart J. 2012;33:2899-2909.
10. Mallat Z, Steg PG, Benessiano J, et al. Circulating secretory phospholipase A2 activity predicts recurrent events in patients with severe acute coronary syndromes. J Am Coll Cardiol. 2005;46:1249-1257.
11. Mallat Z, Ait-Oufella H, Tedgui A. Regulatory t cell immunity in atherosclerosis. Trends Cardiovasc Med. 2007;In press
12. Hanasaki K, Yamada K, Yamamoto S, Ishimoto Y, Saiga A, Ono T, Ikeda M, Notoya M, Kamitani S, Arita H. Potent modification of low density lipoprotein by group X secretory phospholipase A2 is linked to macrophage foam cell formation. J Biol Chem. 2002;277:29116-29124.
13. Wooton-Kee CR, Boyanovsky BB, Nasser MS, de Villiers WJ, Webb NR. Group V sPLA2 hydrolysis of low-density lipoprotein results in spontaneous particle aggregation and promotes macrophage foam cell formation. Arterioscler Thromb Vasc Biol. 2004;24:762-767.
14. Hurt-Camejo E, Camejo G. Potential involvement of type II phospholipase A2 in atherosclerosis. Atherosclerosis. 1997;132:1-8.
15. Webb NR, Bostrom MA, Szilvassy SJ, van der Westhuyzen DR, Daugherty A, de Beer FC. Macrophage-expressed group IIA secretory phospholipase A2 increases atherosclerotic lesion formation in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:263-268.
16. Bostrom MA, Boyanovsky BB, Jordan CT, Wadsworth MP, Taatjes DJ, de Beer FC, Webb NR. Group v secretory phospholipase A2 promotes atherosclerosis: evidence from genetically altered mice. Arterioscler Thromb Vasc Biol. 2007;27:600-606.
17. Fraser H, Hislop C, Christie RM, Rick HL, Reidy CA, Chouinard ML, Eacho PI, Gould KE, Trias J. Varespladib (A-002), a secretory phospholipase A2 inhibitor, reduces atherosclerosis and aneurysm formation in ApoE-/-mice. J Cardiovasc Pharmacol. 2009;53:60-65.
18. Shaposhnik Z, Wang X, Trias J, Fraser H, Lusis AJ. The synergistic inhibition of atherogenesis in apoE-/-mice between pravastatin and the sPLA2 inhibitor varespladib (A-002). J Lipid Res. 2009;50:623-629.
19. Rosenson RS. Phospholipase A2 inhibition and atherosclerotic vascular disease: prospects for targeting secretory and lipoprotein-associated phospholipase A2 enzymes. Curr Opin Lipidol. 2010;21:473-480.
20. Nicholls SJ, Cavender MA, Kastelein JJ, Schwartz G, Waters DD, Rosenson RS, Bash D, Hislop C. Inhibition of secretory phospholipase A(2) in patients with acute coronary syndromes: rationale and design of the vascular inflammation suppression to treat acute coronary syndrome for 16 weeks (VISTA-16) trial. Cardiovasc Drugs Ther. 2012;26:71-75.
21. Cupillard L, Koumanov K, Mattéi MG, Lazdunski M, Lambeau G. Cloning, chromosomal mapping, and expression of a novel human secretory phospholipase A2. J Biol Chem. 1997;272:15745-15752.
22. Singer AG, Ghomashchi F, Le Calvez C, Bollinger J, Bezzine S, Rouault M, Sadilek M, Nguyen E, Lazdunski M, Lambeau G, Gelb MH. Interfacial kinetic and binding properties of the complete set of human and mouse groups I, II, V, X, and XII secreted phospholipases A2. J Biol Chem. 2002;277:48535-48549.
23. Henderson WR Jr, Chi EY, Bollinger JG, Tien YT, Ye X, Castelli L, Rubtsov YP, Singer AG, Chiang GK, Nevalainen T, Rudensky AY, Gelb MH. Importance of group X-secreted phospholipase A2 in allergeninduced airway inflammation and remodeling in a mouse asthma model. J Exp Med. 2007;204:865-877.
24. Henderson WR Jr, Oslund RC, Bollinger JG, Ye X, Tien YT, Xue J, Gelb MH. Blockade of human group X secreted phospholipase A2 (GX-sPLA2)-induced airway inflammation and hyperresponsiveness in a mouse asthma model by a selective GX-sPLA2 inhibitor. J Biol Chem. 2011;286:28049-28055.
25. Fujioka D, Saito Y, Kobayashi T, Yano T, Tezuka H, Ishimoto Y, Suzuki N, Yokota Y, Nakamura T, Obata JE, Kanazawa M, Kawabata K, Hanasaki K, Kugiyama K. Reduction in myocardial ischemia/reperfusion injury in group X secretory phospholipase A2-deficient mice. Circulation. 2008;117:2977-2985.
26. Rosenson RS, Hislop C, McConnell D, Elliott M, Stasiv Y, Wang N, Waters DD; PLASMA Investigators. Effects of 1-H-indole-3-glyoxamide (A-002) on concentration of secretory phospholipase A2 (PLASMA study): a phase II double-blind, randomised, placebo-controlled trial. Lancet. 2009;373:649-658.
27. Kimura-Matsumoto M, Ishikawa Y, Komiyama K, Tsuruta T, Murakami M, Masuda S, Akasaka Y, Ito K, Ishiguro S, Morita H, Sato S, Ishii T. Expression of secretory phospholipase A2s in human atherosclerosis development. Atherosclerosis. 2008;196:81-91.
28. Degousee N, Ghomashchi F, Stefanski E, Singer A, Smart BP, Borregaard N, Reithmeier R, Lindsay TF, Lichtenberger C, Reinisch W, Lambeau G, Arm J, Tischfield J, Gelb MH, Rubin BB. Groups IV, V, and X phospholipases A2s in human neutrophils: role in eicosanoid production and gram-negative bacterial phospholipid hydrolysis. J Biol Chem. 2002;277:5061-5073.
29. Shridas P, Bailey WM, Gizard F, Oslund RC, Gelb MH, Bruemmer D, Webb NR. Group X secretory phospholipase A2 negatively regulates ABCA1 and ABCG1 expression and cholesterol efflux in macrophages. Arterioscler Thromb Vasc Biol. 2010;30:2014-2021.
30. Shridas P, Bailey WM, Talbott KR, Oslund RC, Gelb MH, Webb NR. Group X secretory phospholipase A2 enhances TLR4 signaling in macrophages. J Immunol. 2011;187:482-489.
31. Atout R, Karabina SA, Dollet S, Carreras M, Payré C, André P, Lambeau G, Lotteau V, Ninio E, Perrin-Cocon L. Human group X secreted phospholipase A2 induces dendritic cell maturation through lipoprotein-dependent and-independent mechanisms. Atherosclerosis. 2012;222:367-374.
32. Ohtsuki M, Taketomi Y, Arata S, Masuda S, Ishikawa Y, Ishii T, Takanezawa Y, Aoki J, Arai H, Yamamoto K, Kudo I, Murakami M. Transgenic expression of group V, but not group X, secreted phospholipase A2 in mice leads to neonatal lethality because of lung dysfunction. J Biol Chem. 2006;281:36420-36433.
33. Mallat Z, Gojova A, Brun V, Esposito B, Fournier N, Cottrez F, Tedgui A, Groux H. Induction of a regulatory T cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice. Circulation. 2003;108:1232-1237.
34. Eerola LI, Surrel F, Nevalainen TJ, Gelb MH, Lambeau G, Laine VJ. Analysis of expression of secreted phospholipases A2 in mouse tissues at protein and mRNA levels. Biochim Biophys Acta. 2006;1761:745-756.
35. Taleb S, Romain M, Ramkhelawon B, Uyttenhive C, Pasterkamp G, Herbin O, Esposito B, Perez N, Yasukawa H, Van Snick J, Yoshimura A, Tedgui A, Mallat Z. Loss of socs3 expression in t cells reveals a regulatory role for interlukin-17 in atherosclerosis. J Exp Med. 2009;JEM published September 8, 2009, 2010.1084/jem.20090545
36. Friguet B, Chaffotte AF, Djavadi-Ohaniance L, Goldberg ME. Measurements of the true affinity constant in solution of antigenantibody complexes by enzyme-linked immunosorbent assay. J Immunol Methods. 1985;77:305-319.
37. Nevalainen TJ, Eerola LI, Rintala E, Laine VJ, Lambeau G, Gelb MH. Time-resolved fluoroimmunoassays of the complete set of secreted phospholipases A2 in human serum. Biochim Biophys Acta. 2005;1733:210-223.
38. Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/-mice. Arterioscler Thromb Vasc Biol. 2008;28:1421-1428.
39. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R, Offenstadt G, Lesèche G, Cohen PL, Tedgui A, Mallat Z. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:1429-1431.
40. Ait-Oufella H, Kinugawa K, Zoll J, Simon T, Boddaert J, Heeneman S, Blanc-Brude O, Barateau V, Potteaux S, Merval R, Esposito B, Teissier E, Daemen MJ, Leseche G, Boulanger C, Tedgui A, Mallat Z. Lactadherin-defciency induces apoptotic cell accumulation, alters the regulatory immune response, and accelerates atherosclerosis in mice. Circulation. 2007;115:2168-2177
41. Schulte S, Sukhova GK, Libby P. Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis. Am J Pathol. 2008;172:1500-1508.
42. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev. 2006;86:515-581.
43. Buono C, Come CE, Stavrakis G, Maguire GF, Connelly PW, Lichtman AH. Influence of interferon-gamma on the extent and phenotype of diet-induced atherosclerosis in the LDLR-deficient mouse. Arterioscler Thromb Vasc Biol. 2003;23:454-460.
44. Buono C, Binder CJ, Stavrakis G, Witztum JL, Glimcher LH, Lichtman AH. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci USA. 2005;102:1596-1601.
45. Reardon CA, Blachowicz L, Lukens J, Nissenbaum M, Getz GS. Genetic background selectively influences innominate artery atherosclerosis: immune system deficiency as a probe. Arterioscler Thromb Vasc Biol. 2003;23:1449-1454.
46. Zack M, Boyanovsky BB, Shridas P, Bailey W, Forrest K, Howatt DA, Gelb MH, de Beer FC, Daugherty A, Webb NR. Group X secretory phospholipase A(2) augments angiotensin II-induced inflammatory responses and abdominal aortic aneurysm formation in apoE-deficient mice. Atherosclerosis. 2011;214:58-64.
47. Ivandic B, Castellani LW, Wang XP, Qiao JH, Mehrabian M, Navab M, Fogelman AM, Grass DS, Swanson ME, de Beer MC, de Beer F, Lusis AJ. Role of group II secretory phospholipase A2 in atherosclerosis: Increased atherogenesis and altered lipoproteins in transgenic mice expressing group IIa phospholipase A2. Arterioscler Thromb Vasc Biol. 1999;19:1284-1290.
48. Pruzanski W, Lambeau G, Lazdunski M, Cho W, Kopilov J, Kuksis A. Hydrolysis of minor glycerophospholipids of plasma lipoproteins by human group IIA, V and X secretory phospholipases A2. Biochim Biophys Acta. 2007;1771:5-19.
49. Pruzanski W, Lambeau L, Lazdunsky M, Cho W, Kopilov J, Kuksis A. Differential hydrolysis of molecular species of lipoprotein phosphatidylcholine by groups IIA, V and X secretory phospholipases A2. Biochim Biophys Acta. 2005;1736:38-50.
50. Anthera. http://www.Anthera.Com/products-a002.Asp. Accessed March 9, 2012.