Platelet-derived exosomes induce endothelial cell apoptosis through peroxynitrite generation: Experimental evidence for a novel mechanism of septic vascular dysfunction

Critical Care

Volumn 11, Issue 5, 2007, Pages

  Gambim, Marcela Helena ^a   de Oliveira do Carmo, Alipio ^b   Marti, Luciana ^b   Veríssimo Filho, Sidney ^a   Lopes, Lucia Rossetti ^a   Janiszewski, Mariano ^a,b  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; ISOMERASE; ISOPROTEIN; LIPOPOLYSACCHARIDE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE; PHOSPHATIDYLSERINE; TETRASPANIN; THROMBIN; TUMOR NECROSIS FACTOR ALPHA; PEROXYNITROUS ACID;

ANIMAL CELL; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; DISEASE EXACERBATION; DISEASE SEVERITY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXOSOME; FLOW CYTOMETRY; HOMEOSTASIS; HUMAN; HUMAN CELL; ISCHEMIA; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REPERFUSION; SEPSIS; THROMBOCYTE; VASCULAR DISEASE; WESTERN BLOTTING; ADULT; ANIMAL; BLOOD; CELL CULTURE; COMPARATIVE STUDY; CYTOPLASM VESICLE; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; PHYSIOLOGY; RABBIT; REFERENCE VALUE; VASCULAR ENDOTHELIUM;

ADULT; ANIMALS; APOPTOSIS; CASPASE 3; CELLS, CULTURED; CYTOPLASMIC VESICLES; ENDOTHELIUM, VASCULAR; HUMANS; LIPOPOLYSACCHARIDES; MIDDLE AGED; NITRIC OXIDE; PEROXYNITROUS ACID; RABBITS; REFERENCE VALUES; SEPSIS; VASCULAR DISEASES;

EID: 37549003988     PISSN: 13648535     EISSN: 1466609X     Source Type: Journal    
DOI: 10.1186/cc6133     Document Type: Article

References (47)

1. Ahn J Johnstone RM Origin of a soluble truncated transferrin receptor Blood 1993, 81:2442-2451 8481524
2. Gassart A Géminard C Hoekstra D Vidal M Exosome secretion: The art of reutilizing nonrecycled proteins? Traffic 2004, 5:896-903 10.1111/ j.1600-0854.2004.00223.x 15479454
3. Thery C Regnault A Garin J Wolfers J Zitvogel L Ricciardi-Castagnoli P Raposo G Amigorena S Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73 J Cell Biol 1999, 147:599-610 10.1083/jcb.147.3.599 10545503
4. Escola JM Kleijmeer MJ Stoorvogel WJ Griffin M Yoshie O Geuze HJ Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B lymphocytes J Biol Chem 1998, 273:20121-20127 10.1074/jbc.273.32.20121 9685355
5. Mallegol J Van Niel G Heyman M Phenotypic and functional characterization of intestinal epithelial exosomes Blood Cells Mol Dis 2005, 35:11-16 10.1016/j.bcmd.2005.04.001 15893486
6. Shen TRF Knepper MA Identification and proteomic profiling of exosomes in human urine Proc Natl Acad Sci USA 2004, 101:13368-13373 516573 15326289 10.1073/pnas.0403453101
7. Heijnen HF Schiel AE Fijnheer R Geuze HJ Sixma JJ Activated platelets release two types of membrane vesicles: Microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha granules Blood 1999, 94:3791-3799 10572093
8. Raposo G Février B Exosomes: Endosomal-derived vesicles shipping extracellular messages Curr Opin Cell Biol 2004, 16:415-421 10.1016/ j.ceb.2004.06.003 15261674
9. Couzin J The ins and outs of exosomes Science 2005, 308:1862-1863 10.1126/science.308.5730.1862 15976285
10. Cai H Harrison DG Endothelial dysfunction in cardiovascular diseases Circ Res 2000, 87:840-844 11073878
11. Li JM Shah AM Endothelial cell superoxide generation: Regulation and relevance for cardiovascular pathophysiology Am J Physiol Regul Integr Comp Physiol 2004, 287:R1014-R1030 15475499
12. Zhang DX Gutterman DD Mitochondrial reactive oxygen species-mediated signaling in endothelial cells Am J Physiol Heart Circ Physiol 2007, 292:H2023-H2031 10.1152/ajpheart.01283.2006 17237240
13. Ray R Shah AM NADPH oxidase and endothelial cell function Clin Sci 2005, 109:217-226 10.1042/CS20050067 16104842
14. Goligorsky MS Noiri E Sukahara HT Budzikowski AS Li H A pivotal role of nitric oxide in endothelial cell dysfunction Acta Physiol Scand 2000, 168:33-40 10.1046/j.1365-201x.2000.00636.x 10691777
15. Davidson SM Duchen MR Endothelial mitochondria: Contributing to vascular function and disease Circ Res 2007, 100:1128-1141 10.1161/ 01.RES.0000261970.18328.1d 17463328
16. Begonja AJ Teichmann L Geiger J Gambaryan S Walter U Platelet regulation by NO/cGMP signaling and NAD(P)H oxidase-generated ROS Blood Cells Mol Dis 2006, 36:166-170 10.1016/j.bcmd.2005.12.028 16469512
17. Chlopicki S Olszanecki R Janiszewski M Laurindo FR Panz T Miedzobrodzki J Functional role of NADPH oxidase in activation of platelets Antioxid Redox Signal 2004, 6:691-698 10.1089/1523086041361640 15242549
18. Janiszewski M Carmo AO Pedro MA Silva E Knobel E Laurindo FRM Platelet-derived exosomes of septic individuals possess proapoptotic NAD(P)H oxidase activity: A novel vascular redox pathway Crit Care Med 2004, 32:818-825 10.1097/01.CCM.0000114829.17746.19 15090968
19. Venter JC Buonassisi V Hormone and neurotransmitter receptors in an established vascular endothelial cell line Proc Natl Acad Sci USA 1976, 73:1612-1616 430349 179091 10.1073/pnas.73.6.2013
20. American College of Chest Physicians - Society of Critical Care Medicine Consensus Conference Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis: The ACCP/SCCM Consensus Conference Committee - American College of Chest Physicians/ Society of Critical Care Medicine Consensus Conference Committee Chest 1992, 101:1644-1655 10.1378/chest.101.6.1644 1303622
21. Triantafilou M Triantafilou K Lipopolysaccharide recognition: CD14, TLRs and the LPS-activation cluster Trends Immunol 2002, 23:301-304 10.1016/ S1471-4906(02)02233-0 12072369
22. Hehlgans T Pfeffer K The intriguing biology of the tumour necrosis factor/tumour necrosis factor receptor superfamily: Players, rules and the games Immunology 2005, 115:1-20 1782125 15819693 10.1111/ j.1365-2567.2005.02143.x
23. Bateman RM Sharpe MD Ellis CG Bench-to-bedside review: Microvascular dysfunction in sepsis - hemodynamics, oxygen transport, and nitric oxide Crit Care 2003, 7:359-373 270719 12974969 10.1186/cc2353
24. Thery C Boussac M Veron P Ricciardi-Castagnoli P Raposo G Garin J Amigorena S Proteomic analysis of dendritic cell-derived exosomes: A secreted subcellular compartment distinct from apoptotic vesicles J Immunol 2001, 166:7309-7318 11390481
25. Myhre O Andersen JM Aarnes H Fonnum F Evaluation of the probes 2,7-dichlorofluorescin diacetate, luminol, and lucigenin as indicators of reactive species formation Biochem Pharmacol 2003, 65:1575-1582 10.1016/S0006-2952(03)00083-2 12754093
26. Jourd'heuil D Increased nitric oxide-dependent nitrosylation of 4,5-diaminofluorescein by oxidants: Implications for the measurement of intracellular nitric oxide Free Radic Biol Med 2002, 33:676-684 10.1016/ S0891-5849(02)00955-3 12208354
27. 2 - and systolic blood pressure in mice Circ Res 2001, 8:408-414 10.1161/ hh1701.096037
28. Dhanabal M Ramchandran R Waterman MJF Lu H Knebelmann B Segal M Sukhatme VP Endostatin induces endothelial cell apoptosis J Biol Chem 1999, 274:11721-11726 10.1074/jbc.274.17.11721 10206987
29. Meij JTA Haselton CL Hillman KL Murlikrishnan D Ebadi M Yu L Differential mechanisms of nitric oxide- and peroxynitrite-induced cell death Molec Pharmacol 2004, 66:1043-1052 10.1124/mol.104.001354
30. Zhu C Wang X Qiu L Peeters-Scholte C Hagberg H Blomgren K Nitrosylation precedes caspase-3 activation and translocation of apoptosis-inducing factor in neonatal rat cerebral hypoxia-ischaemia J Neurochem 2004, 90:462-471 10.1111/j.1471-4159.2004.02500.x 15228602
31. Rössig L Fichtlscherer B Breitschopf K Haendeler J Zeiher A Mülsch A Dimmeler S Nitric oxide inhibits caspase-3 by S-nitrosation in vivo J Biol Chem 1999, 274:6823-6826 10.1074/ jbc.274.11.6823 10066732
32. Baj-Krzyworzeka M Majka M Pratico D Ratajczak J Vilaire G Kijowski J Reca R Janowska-Wieczorek A Ratajczak MZ Platelet-derived microparticles stimulate proliferation, survival, adhesion and chemotaxis of hematopoietic cells Exp Hematol 2002, 30:450-459 10.1016/ S0301-472X(02)00791-9 12031651
33. Gassart A Géminard C Février B Raposo G Vidal M Lipid raft-associated protein sorting in exosomes Blood 2003, 102:4336-4344 10.1182/blood-2003-03-0871 12881314
34. Lancaster GI Febbraio MA Exosome-dependent trafficking of HSP70 - a novel secretory pathway for cellular stress proteins J Biol Chem 2005, 280:23349-23355 10.1074/jbc.M502017200 15826944
35. Janiszewski M Lopes LR Carmo AO Pedro MA Brandes RP Santos CX Laurindo FR Regulation of NAD(P)H oxidase by associated protein disulfide isomerase in vascular smooth muscle cells J Biol Chem 2005, 280:40813-40819 10.1074/jbc.M509255200 16150729
36. Denzer K Kleijmeer MJ Heijnen HFG Stoorvogel W Geuze HJ Exosome: From internal vesicle of the multivesicular body to intercellular signaling device J Cell Sci 2000, 113:3365-3374 10984428
37. Luo B Regier DS Topham MK Prescott SM Diacylglycerol kinases Cell Signal 2004, 16:983-989 15212759
38. Los AP van Baal J de Widt J Divecha N van Blitterswijk WJ Structure-activity relationship of diacylglycerol kinase θ Biochim Biophys Acta 2004, 1636:169-174 15164764
39. Johnstone RM Exosomes biological significance: A concise review Blood Cells Mol Dis 2006, 36:315-321 10.1016/j.bcmd.2005.12.001 16487731
40. Barry OP Pratico D Lawson JA FitzGerald GA Transcellular activation of platelets and endothelial cells by bioactive lipids in platelet microparticles J Clin Invest 1997, 99:2118-2127 508042 9151784
41. Miyamoto S Kowalska MA Marcinkiewicz C Marcinkiewicz MM Mosser D Edmunds LH Jr Niewiarowski S Interaction of leukocytes with platelet microparticles derived from outdated platelet concentrates Thromb Haemost 1998, 80:982-988 9869171
42. Brunetti M Martelli N Manarini S Mascetra N Musiani P Cerletti C Aiello FB Evangelista V Polymorphonuclear leukocyte apoptosis is inhibited by platelet-released mediators, role of TGFβ-1 Thromb Haemost 2000, 84:478-483 11019975
43. Janowska-Wieczorek A Wysoczynski M Kijowski J Marquez-Curtis L Machalinski B Ratajczak J Ratajczak MZ Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer Int J Cancer 2005, 113:752-760 10.1002/ijc.20657 15499615
44. Boulanger CM Scoazec A Ebrahimian T Henry P Mathieu E Tedgui A Mallat Z Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction Circulation 2001, 104:2649-2652 10.1161/ hc4701.100516 11723013
45. Albina JE Cui S Mateo RB Reichner JS Nitric oxide-mediated apoptosis in murine peritoneal macrophages J Immunol 1993, 150:5080-5085 7684418
46. Mannick JB Asano K Izumi K Kieff E Stammler JS Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation Cell 1994, 79:1137-1146 10.1016/0092-8674(94)90005-1 7528106
47. Dimmeler S Zeiher AM Nitric oxide and apoptosis: Another paradigm for the double-edged role of nitric oxide Nitric Oxide 1997, 1:275-281 10.1006/niox.1997.0133 9441899