Extracellular vesicles activate a CD36-dependent signaling pathway to inhibit microvascular endothelial cell migration and tube formation

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 36, Issue 3, 2016, Pages 534-544

  Ramakrishnan, Devi Prasadh ^a,b   Hajj Ali, Rula A ^c   Chen, Yiliang ^b   Silverstein, Roy L ^b,d  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BLOOD RESEARCH INSTITUTE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

angiogenesis; CD36; endothelial cell; extracellular vesicles

Indexed keywords

CD36 ANTIGEN; COMPLEMENTARY DNA; LIPOCORTIN 5; PHOSPHATIDYLSERINE; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ENZYME INHIBITOR;

ANIMAL CELL; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; DNA TRANSFECTION; EXOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UMBILICAL VEIN ENDOTHELIAL CELL; ANGIOGENESIS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL MOTION; DEFICIENCY; DRUG EFFECTS; ENDOTHELIUM CELL; GENETIC TRANSFECTION; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MICROVASCULATURE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; ANNEXIN A5; ANTIGENS, CD36; CELL LINE, TUMOR; CELL MOVEMENT; ENDOTHELIAL CELLS; ENZYME INHIBITORS; EXTRACELLULAR VESICLES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROVESSELS; NADPH OXIDASE; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHATIDYLSERINES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSFECTION;

EID: 84959464380     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.307085     Document Type: Article

References (46)

1. Swerlick RA, Lee KH, Wick TM, Lawley TJ, Human dermal microvascular endothelial but not human umbilical vein endothelial cells express CD36 in vivo and in vitro. J Immunol 1992 148 78 83
2. Albert ML, Pearce SF, Francisco LM, Sauter B, Roy P, Silverstein RL, Bhardwaj N, Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 1998 188 1359 1368
3. Harmon CM, Abumrad NA, Binding of sulfosuccinimidyl fatty acids to adipocyte membrane proteins: isolation and amino-Terminal sequence of an 88-kD protein implicated in transport of long-chain fatty acids. J Membr Biol 1993 133 43 49
4. Silverstein RL, Febbraio M, CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2009 2 re3. doi: 10.1126/scisignal.272re3
5. Sparrow JR, Ryeom SW, Abumrad NA, Ibrahimi A, Silverstein RL, CD36 expression is altered in retinal pigment epithelial cells of the RCS rat. Exp Eye Res 1997 64 45 56
6. Rigotti A, Acton SL, Krieger M, The class B scavenger receptors SR-BI and CD36 are receptors for anionic phospholipids. J Biol Chem 1995 270 16221 16224
7. Baranova IN, Kurlander R, Bocharov AV, Vishnyakova TG, Chen Z, Remaley AT, Csako G, Patterson AP, Eggerman TL, Role of human CD36 in bacterial recognition, phagocytosis, and pathogen-induced JNK-mediated signaling. J Immunol 2008 181 7147 7156
8. Podrez EA, Febbraio M, Sheibani N, Schmitt D, Silverstein RL, Hajjar DP, Cohen PA, Frazier WA, Hoff HF, Hazen SL, Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J Clin Invest 2000 105 1095 1108. doi: 10.1172/JCI8574
9. Ren Y, Silverstein RL, Allen J, Savill J, CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J Exp Med 1995 181 1857 1862
10. Zhu W, Li W, Silverstein RL, Advanced glycation end products induce a prothrombotic phenotype in mice via interaction with platelet CD36. Blood 2012 119 6136 6144. doi: 10.1182/blood-2011-10-387506
11. Sheedy FJ, Grebe A, Rayner KJ, Kalantari P, Ramkhelawon B, Carpenter SB, Becker CE, Ediriweera HN, Mullick AE, Golenbock DT, Stuart LM, Latz E, Fitzgerald KA, Moore KJ, CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat Immunol 2013 14 812 820. doi: 10.1038/ni.2639
12. Wang Y, Fang C, Gao H, Platelet-derived S100 family member myeloid-related protein-14 regulates thrombosis. J Clin Invest 2014 124 2160 2171. doi: 10.1172/JCI70966
13. Jiménez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N, Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med 2000 6 41 48. doi: 10.1038/71517
14. Rege TA, Stewart J Jr, Dranka B, Benveniste EN, Silverstein RL, Gladson CL, Thrombospondin-1-induced apoptosis of brain microvascular endothelial cells can be mediated by TNF-R1. J Cell Physiol 2009 218 94 103. doi: 10.1002/jcp.21570
15. Chu LY, Ramakrishnan DP, Silverstein RL, Thrombospondin-1 modulates VEGF signaling via CD36 by recruiting SHP-1 to VEGFR2 complex in microvascular endothelial cells. Blood 2013 122 1822 1832. doi: 10.1182/blood-2013-01-482315
16. Hale JS, Li M, Sinyuk M, Jahnen-Dechent W, Lathia JD, Silverstein RL, Context dependent role of the CD36-Thrombospondin-histidine-rich glycoprotein axis in tumor angiogenesis and growth. PLoS One 2012 7 e40033. doi: 10.1371/journal.pone.0040033
17. Tait JF, Smith C, Phosphatidylserine receptors: role of CD36 in binding of anionic phospholipid vesicles to monocytic cells. J Biol Chem 1999 274 3048 3054
18. Yamaguchi A, Yamamoto N, Akamatsu N, Saido TC, Kaneda M, Umeda M, Tanoue K, PS-liposome and ox-LDL bind to different sites of the immunodominant domain (#155-183) of CD36: a study with GS95, a new anti-CD36 monoclonal antibody. Thromb Res 2000 97 317 326
19. Ghosh A, Li W, Febbraio M, Espinola RG, McCrae KR, Cockrell E, Silverstein RL, Platelet CD36 mediates interactions with endothelial cell-derived microparticles and contributes to thrombosis in mice. J Clin Invest 2008 118 1934 1943. doi: 10.1172/JCI34904
20. Mostefai HA, Andriantsitohaina R, Martínez MC, Plasma membrane microparticles in angiogenesis: role in ischemic diseases and in cancer. Physiol Res 2008 57 311 320
21. Taraboletti G, D'Ascenzo S, Borsotti P, Giavazzi R, Pavan A, Dolo V, Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-Associated components by endothelial cells. Am J Pathol 2002 160 673 680. doi: 10.1016/S0002-9440(10)64887-0
22. Mezentsev A, Merks RM, O'Riordan E, Chen J, Mendelev N, Goligorsky MS, Brodsky SV, Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol 2005 289 H1106 H1114. doi: 10.1152/ajpheart.00265.2005
23. Yang C, Mwaikambo BR, Zhu T, Gagnon C, Lafleur J, Seshadri S, Lachapelle P, Lavoie JC, Chemtob S, Hardy P, Lymphocytic microparticles inhibit angiogenesis by stimulating oxidative stress and negatively regulating VEGF-induced pathways. Am J Physiol Regul Integr Comp Physiol 2008 294 R467 R476. doi: 10.1152/ajpregu.00432.2007
24. Soleti R, Benameur T, Porro C, Panaro MA, Andriantsitohaina R, Martínez MC, Microparticles harboring Sonic Hedgehog promote angiogenesis through the upregulation of adhesion proteins and proangiogenic factors. Carcinogenesis 2009 30 580 588. doi: 10.1093/carcin/bgp030
25. Morel O, Jesel L, Freyssinet JM, Toti F, Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol 2011 31 15 26. doi: 10.1161/ATVBAHA.109.200956
26. Zwaal RF, Schroit AJ, Pathophysiologic implications of membrane phospholipid asymmetry in blood cells. Blood 1997 89 1121 1132
27. Freyssinet JM, Toti F, Formation of procoagulant microparticles and properties. Thromb Res 2010 125 SUPPL 1 S46 S48. doi: 10.1016/j.thromres.2010.01.036
28. Park YM, Febbraio M, Silverstein RL, CD36 modulates migration of mouse and human macrophages in response to oxidized LDL and may contribute to macrophage trapping in the arterial intima. J Clin Invest 2009 119 136 145. doi: 10.1172/JCI35535
29. Li W, Febbraio M, Reddy SP, Yu DY, Yamamoto M, Silverstein RL, CD36 participates in a signaling pathway that regulates ROS formation in murine VSMCs. J Clin Invest 2010 120 3996 4006. doi: 10.1172/JCI42823
30. Cheng R, Li C, Li C, Wei L, Li L, Zhang Y, Yao Y, Gu X, Cai W, Yang Z, Ma J, Yang X, Gao G, The artemisinin derivative artesunate inhibits corneal neovascularization by inducing ROS-dependent apoptosis in vascular endothelial cells. Invest Ophthalmol Vis Sci 2013 54 3400 3409. doi: 10.1167/iovs.12-11068
31. Lu CC, Chen HP, Chiang JH, Jin YA, Kuo SC, Wu TS, Hour MJ, Yang JS, Chiu YJ, Quinazoline analog HMJ-30 inhibits angiogenesis: involvement of endothelial cell apoptosis through ROS-JNK-mediated death receptor 5 signaling. Oncol Rep 2014 32 597 606. doi: 10.3892/or.2014.3250
32. Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, Bouck NP, A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci U S A 1990 87 6624 6628
33. Mwaikambo BR, Sennlaub F, Ong H, Chemtob S, Hardy P, Activation of CD36 inhibits and induces regression of inflammatory corneal neovascularization. Invest Ophthalmol Vis Sci 2006 47 4356 4364. doi: 10.1167/iovs.05-1656
34. Srikanthan S, Li W, Silverstein RL, McIntyre TM, Exosome poly-ubiquitin inhibits platelet activation, downregulates CD36 and inhibits pro-Atherothombotic cellular functions. J Thromb Haemost 2014 12 1906 1917. doi: 10.1111/jth.12712
35. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Köppel T, Jahantigh MN, Lutgens E, Wang S, Olson EN, Schober A, Weber C, Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009 2 ra81. doi: 10.1126/scisignal.2000610
36. Martínez MC, Larbret F, Zobairi F, Coulombe J, Debili N, Vainchenker W, Ruat M, Freyssinet JM, Transfer of differentiation signal by membrane microvesicles harboring hedgehog morphogens. Blood 2006 108 3012 3020. doi: 10.1182/blood-2006-04-019109
37. Martinez MC, Andriantsitohaina R, Microparticles in angiogenesis: therapeutic potential. Circ Res 2011 109 110 119. doi: 10.1161/CIRCRESAHA.110.233049
38. Hajj-Ali R, Silverstein, Roy, Hoffman, Gary, Zhang, Li, Imrey, Peter, Langford, Carol A, The correlation between circulating microparticles and platelet aggregation and disease activity in Wegener Granulomatosis. Arthritis Rheumatism 2010 62 (SUPPL 10):2047
39. Hong Y, Eleftheriou D, Hussain AA, Price-Kuehne FE, Savage CO, Jayne D, Little MA, Salama AD, Klein NJ, Brogan PA, Anti-neutrophil cytoplasmic antibodies stimulate release of neutrophil microparticles. J Am Soc Nephrol 2012 23 49 62. doi: 10.1681/ASN.2011030298
40. Erdbruegger U, Grossheim M, Hertel B, Wyss K, Kirsch T, Woywodt A, Haller H, Haubitz M, Diagnostic role of endothelial microparticles in vasculitis. Rheumatology (Oxford) 2008 47 1820 1825. doi: 10.1093/rheumatology/ken373
41. Fadok VA, Warner ML, Bratton DL, Henson PM, CD36 is required for phagocytosis of apoptotic cells by human macrophages that use either a phosphatidylserine receptor or the vitronectin receptor (alpha v beta 3). J Immunol 1998 161 6250 6257
42. Fadok VA, Bratton DL, Frasch SC, Warner ML, Henson PM, The role of phosphatidylserine in recognition of apoptotic cells by phagocytes. Cell Death Differ 1998 5 551 562. doi: 10.1038/sj.cdd.4400404
43. Savill J, Fadok V, Henson P, Haslett C, Phagocyte recognition of cells undergoing apoptosis. Immunol Today 1993 14 131 136. doi: 10.1016/0167-5699(93)90215-7
44. Ryeom SW, Silverstein RL, Scotto A, Sparrow JR, Binding of anionic phospholipids to retinal pigment epithelium may be mediated by the scavenger receptor CD36. J Biol Chem 1996 271 20536 20539
45. Brodsky SV, Zhang F, Nasjletti A, Goligorsky MS, Endothelium-derived microparticles impair endothelial function in vitro. Am J Physiol Heart Circ Physiol 2004 286 H1910 H1915. doi: 10.1152/ajpheart.01172.2003
46. Camus SM, Gausserès B, Bonnin P, Loufrani L, Grimaud L, Charue D, De Moraes JA, Renard JM, Tedgui A, Boulanger CM, Tharaux PL, Blanc-Brude OP, Erythrocyte microparticles can induce kidney vaso-occlusions in a murine model of sickle cell disease. Blood 2012 120 5050 5058. doi: 10.1182/blood-2012-02-413138