Oxidatively modified phosphatidylserines on the surface of apoptotic cells are essential phagocytic 'eat-me' signals: Cleavage and inhibition of phagocytosis by Lp-PLA 2

Cell Death and Differentiation

Volumn 21, Issue 5, 2014, Pages 825-835

  Tyurin, V A ^a   Balasubramanian, K ^a   Winnica, D ^a   Tyurina, Y Y ^a   Vikulina, A S ^a,b   He, R R ^a,c   Kapralov, A A ^a   Macphee, C H ^d   Kagan, V E ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c JINAN UNIVERSITY   (China)

^d GLAXOSMITHKLINE   (United States)

Author keywords

apoptosis; inflammation; lipoprotein associated phospholipase; oxidative stress; oxidized phosphatidylserines; phagocytosis; phosphatidylserines

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; BOVINE SERUM ALBUMIN; CXCL16 CHEMOKINE; FAS ANTIBODY; FATTY ACID; HYDROGEN PEROXIDE; LINOLEIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; STAUROSPORINE;

APOPTOSIS; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; HUMAN; HUMAN CELL; HYDROLYSIS; LIPID ANALYSIS; LIPIDOMICS; LIQUID CHROMATOGRAPHY; MACROPHAGE; NONHUMAN; OXIDATION; PHAGOCYTOSIS; PRIORITY JOURNAL; SPECIES; DRUG EFFECTS; HL 60 CELL LINE; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; APOPTOSIS; HL-60 CELLS; HUMANS; HYDROGEN PEROXIDE; MACROPHAGES; OXIDATION-REDUCTION; PHAGOCYTOSIS; PHOSPHATIDYLSERINES; SIGNAL TRANSDUCTION;

EID: 84898053295     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.1     Document Type: Article

References (59)

1. Green DR. The end and after: how dying cells impact the living organism. Immunity 2011; 35: 441-444.
2. Elliott MR, Ravichandran KS. Clearance of apoptotic cells: implications in health and disease. J Cell Biol 2010; 189: 1059-1070.
3. Rodriguez PL, Harada T, Christian DA, Pantano DA, Tsai RK, Discher DE. Minimal 'Self' peptides that inhibit phagocytic clearance and enhance delivery of nanoparticles. Science 2013; 339: 971-975.
4. Michlewska S, McColl A, Rossi AG, Megson IL, Dransfield I. Clearance of dying cells and autoimmunity. Autoimmunity 2007; 40: 267-273. (Pubitemid 46845519)
5. Tanaka M, Miyake Y. Apoptotic cell clearance and autoimmune disorder. Curr Med Chem 2007; 14: 2892-2897. (Pubitemid 350201655)
6. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 1992; 148: 2207-2216.
7. Shimaoka T, Kume N, Minami M, Hayashida K, Kataoka H, Kita T et al. Molecular cloning of a novel scavenger receptor for oxidized low density lipoprotein, SR-PSOX, on macrophages. J Biol Chem 2000; 275: 40663-40666. (Pubitemid 32054881)
8. Greenberg ME, Sun M, Zhang R, Febbraio M, Silverstein R, Hazen SL. Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med 2006; 203: 2613-2625. (Pubitemid 44833338)
9. Tyurina YY, Kawai K, Tyurin VA, Liu SX, Kagan VE, Fabisiak JP. The plasma membrane is the site of selective phosphatidylserine oxidation during apoptosis: role of cytochrome C. Antioxid Redox Signal 2004; 6: 209-225. (Pubitemid 38332579)
10. Fabisiak JP, Tyurina YY, Tyurin VA, Kagan VE. Quantification of selective phosphati-dylserine oxidation during apoptosis. Methods Mol Biol 2005; 291: 449-456.
11. Arroyo A, Modriansky M, Serinkan FB, Bello RI, Matsura T, Jiang J et al. NADPH oxidase-dependent oxidation and externalization of phosphatidylserine during apoptosis in Me2SO-differentiated HL-60 cells. Role in phagocytic clearance. J Biol Chem 2002; 277: 49965-49975. (Pubitemid 36014447)
12. Frasch SC, Fernandez-Boyanapalli RF, Berry KZ, Leslie CC, Bonventre JV, Murphy RC et al. Signaling via macrophage G2A enhances efferocytosis of dying neutrophils by augmentation of Rac activity. J Biol Chem 2011; 286: 12108-12122.
13. Frasch SC, Bratton DL. Emerging roles for lysophosphatidylserine in resolution of inflammation. Prog Lipid Res 2012; 51: 199-207.
14. Dillon SR, Mancini M, Rosen A, Schlissel MS. Annexin V binds to viable B cells and colocalizes with a marker of lipid rafts upon B cell receptor activation. J Immunol 2000; 164: 1322-1332. (Pubitemid 30067245)
15. Borisenko GG, Matsura T, Liu SX, Tyurin VA, Jianfei J, Serinkan FB et al. Macrophage recognition of externalized phosphatidylserine and phagocytosis of apoptotic Jurkat cells-existence of a threshold. Arch Biochem Biophys 2003; 413: 41-52. (Pubitemid 36434350)
16. Millius A, Weiner OD. Chemotaxis in neutrophil-like HL-60 cells. Methods Mol Biol 2009; 571: 167-177.
17. Mueller HW, O'Flaherty JT, Greene DG, Samuel MP, Wykle RL. 1-O-alkyl-linked glycerophospholipids of human neutrophils: distribution of arachidonate and other acyl residues in the ether-linked and diacyl species. J Lipid Res 1984; 25: 383-388. (Pubitemid 14103956)
18. Tyurin VA, Yanamala N, Tyurina YY, Klein-Seetharaman J, Macphee CH, Kagan VE. Specificity of lipoprotein-associated phospholipase A(2) toward oxidized phosphati-dylserines: liquid chromatography-electrospray ionization mass spectrometry characterization of products and computer modeling of interactions. Biochemistry 2012; 51: 9736-9750.
19. Fox S, Leitch AE, Duffin R, Haslett C, Rossi AG. Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J Innate Immun 2010; 2: 216-227.
20. Sun L, Yau HY, Wong WY, Li RA, Huang Y, Yao X. Role of TRPM2 in H(2)O(2)-induced cell apoptosis in endothelial cells. PLoS ONE 2012; 7: e43186.
21. Blackie JA, Bloomer JC, Brown MJ, Cheng HY, Hammond B, Hickey DM et al. The identification of clinical candidate SB-480848: a potent inhibitor of lipoprotein-associated phospholipase A2. Bioorg Med Chem Lett 2003; 13: 1067-1070. (Pubitemid 36331801)
22. Blackie JA, Bloomer JC, Brown MJ, Cheng HY, Elliott RL, Hammond B et al. The discovery of SB-435495. A potent, orally active inhibitor of lipoprotein-associated phospholipase A(2) for evaluation in man. Bioorg Med Chem Lett 2002; 12: 2603-2606. (Pubitemid 35245291)
23. Kobayashi N, Karisola P, Pena-Cruz V, Dorfman DM, Jinushi M, Umetsu SE et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 2007; 27: 927-940. (Pubitemid 50014866)
24. Nakano T, Ishimoto Y, Kishino J, Umeda M, Inoue K, Nagata K et al. Cell adhesion to phosphatidylserine mediated by a product of growth arrest-specific gene 6. J Biol Chem 1997; 272: 29411-29414.
25. Hanayama R, Tanaka M, Miwa K, Shinohara A, Iwamatsu A, Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 2002; 417: 182-187. (Pubitemid 34506799)
26. Park D, Tosello-Trampont AC, Elliott MR, Lu M, Haney LB, Ma Z et al. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 2007; 450: 430-434. (Pubitemid 350126756)
27. Rollet-Labelle E, Grange MJ, Elbim C, Marquetty C, Gougerot-Pocidalo MA, Pasquier C. Hydroxyl radical as a potential intracellular mediator of polymorphonuclear neutrophil apoptosis. Free Radic Biol Med 1998; 24: 563-572. (Pubitemid 28150474)
28. Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000; 29: 222-230.
29. Hurtado B, Munoz X, Recarte-Pelz P, Garcia N, Luque A, Krupinski J et al. Expression of the vitamin K-dependent proteins GAS6 and protein S and the TAM receptor tyrosine kinases in human atherosclerotic carotid plaques. Thromb Haemost 2011; 105: 873-882.
30. Tjwa M, Moons L, Lutgens E. Pleiotropic role of growth arrest-specific gene 6 in atherosclerosis. Curr Opin Lipidol 2009; 20: 386-392.
31. Driscoll WS, Vaisar T, Tang J, Wilson CL, Raines EW. Macrophage ADAM17 deficiency augments CD36-dependent apoptotic cell uptake and the linked anti-inflammatory phenotype. Circ Res 2013; 113: 52-61.
32. Uza N, Nakase H, Yamamoto S, Yoshino T, Takeda Y, Ueno S et al. SR-PSOX/CXCL16 plays a critical role in the progression of colonic inflammation. Gut 2011; 60: 1494-1505.
33. Nurtanio N, Yang PC. Role of TIM-4 in innate or adaptive immune response. N Am J Med Sci 2011; 3: 217-221.
34. Lemke G, Burstyn-Cohen T. TAM receptors and the clearance of apoptotic cells. Ann N Y Acad Sci 2010; 1209: 23-29.
35. Shao WH, Zhen Y, Eisenberg RA, Cohen PL. The Mer receptor tyrosine kinase is expressed on discrete macrophage subpopulations and mainly uses Gas6 as its ligand for uptake of apoptotic cells. Clin Immunol 2009; 133:138-144.
36. 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.
37. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R et al. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol2008; 28: 1429-1431.
38. Lauber K, Keppeler H, Munoz LE, Koppe U, Schroder K, Yamaguchi H et al. Milk fat globule-EGF factor 8 mediates the enhancement of apoptotic cell clearance by glucocorticoids. Cell Death Differ 2013; 20:1230-1240.
39. Matsuda A, Jacob A, Wu R, Aziz M, Yang WL, Matsutani T et al. Novel therapeutic targets for sepsis: regulation of exaggerated inflammatory responses. J Nippon Med Sch 2012; 79: 4-18.
40. Macphee CH, Nelson JJ, Zalewski A. Lipoprotein-associated phospholipase A2 as a target of therapy. Curr Opin Lipidol 2005; 16: 442-446.
41. Chauffe RJ, Wilensky RL, Mohler ER III. Recent developments with lipoprotein-associated phospholipase A2 inhibitors. Curr Atheroscler Rep 2010; 12: 43-47.
42. Kolodgie FD, Burke AP, Skorija KS, Ladich E, Kutys R, Makuria AT et al. Lipoprotein-associated phospholipase A2 protein expression in the natural progression of human coronary atherosclerosis. Arterioscler Thromb Vasc Biol 2006; 26: 2523-2529. (Pubitemid 44607475)
43. Vangaveti V, Baune BT, Kennedy RL. Hydroxyoctadecadienoic acids: novel regulators of macrophage differentiation and atherogenesis. Ther Adv Endocrinol Metab 2010; 1: 51-60.
44. Domingues MR, Reis A, Domingues P. Mass spectrometry analysis of oxidized phospholipids. Chem Phys Lipids 2008; 156:1-12.
45. O'Donoghue ML, Braunwald E, White HD, Serruys P, Steg PG, Hochman J et al. Study design and rationale for the Stabilization of pLaques usIng Darapladib-Thrombolysis in Myocardial Infarction (SOLID-TIMI 52) trial in patients after an acute coronary syndrome. Am Heart J 2011; 162: 613-619.
46. White H, Held C, Stewart R, Watson D, Harrington R, Budaj A et al. Study design and rationale for the clinical outcomes of the STABILITY Trial (STabilization of Atherosclerotic plaque By Initiation of darapLadIb TherapY) comparing darapladib versus placebo in patients with coronary heart disease. Am Heart J 2010; 160: 655-661.
47. Wilensky RL, Shi Y, Mohler ER III, Hamamdzic D, Burgert ME, Li J et al. Inhibition of lipoprotein-associated phospholipase A2 reduces complex coronary atherosclerotic plaque development. Nat Med 2008; 14:1059-1066.
48. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 2010; 10: 36-46.
49. Wilensky RL, Macphee CH. Lipoprotein-associated phospholipase A(2) and atherosclerosis. Curr Opin Lipidol 2009; 20: 415-420.
50. Bercher M, Hanson B, van SC, Wu K, Ng GY, Lee PH. Agonists of the orphan human G2A receptor identified from inducible G2A expression and beta-lactamase reporter screen. Assay Drug Dev Technol 2009; 7:133-142.
51. Peter C, Waibel M, Radu CG, Yang LV, Witte ON, Schulze-Osthoff K et al. Migration to apoptotic 'find-me' signals is mediated via the phagocyte receptor G2A. J Biol Chem 2008; 283: 5296-5305.
52. Obinata H, Izumi T. G2A as a receptor for oxidized free fatty acids. Prostaglandins Other Lipid Mediat 2009; 89: 66-72.
53. Frasch SC, Fernandez-Boyanapalli RF, Berry KA, Murphy RC, Leslie CC, Nick JA et al. Neutrophils regulate tissue neutrophilia in inflammation via the oxidant-modified lipid lysophosphatidylserine. J Biol Chem 2013; 288: 4583-4593.
54. Tsimikas S, Willeit J, Knoflach M, Mayr M, Egger G, Notdurfter M et al. Lipoprotein-associated phospholipase A2 activity, ferritin levels, metabolic syndrome, and 10-year cardiovascular and non-cardiovascular mortality: results from the Bruneck study. Eur Heart J 2009; 30: 107-115.
55. Thompson A, Gao P, Orfei L, Watson S, Di AE, Kaptoge S et al. Lipoprotein-associated phospholipase A(2) and risk of coronary disease, stroke, and mortality: collaborative analysis of 32 prospective studies. Lancet 2010; 375: 1536-1544.
56. Rosenson RS, Stafforini DM. Modulation of oxidative stress, inflammation, and atherosclerosis by lipoprotein-associated phospholipase A2. J Lipid Res 2012; 53: 1767-1782.
57. Vondracek J, Sheard MA, Krejci P, Minksova K, Hofmanova J, Kozubik A. Modulation of death receptor-mediated apoptosis in differentiating human myeloid leukemia HL-60 cells. J Leukoc Biol 2001; 69: 794-802. (Pubitemid 32466419)
58. Nilsson OS, Dallner G. Transverse asymmetry of phospholipids in subcellular membranes of rat liver. Biochim Biophys Acta 1977; 464: 453-458. (Pubitemid 8008033)
59. Folch J, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226: 497-509.