Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation

Blood

Volumn 122, Issue 20, 2013, Pages 3405-3414

  Hottz, Eugenio D ^a,b   Lopes, Juliana F ^a   Freitas, Carla ^a   Valls De Souza, Rogério ^b   Oliveira, Marcus F ^c   Bozza, Marcelo T ^c   Da Poian, Andrea T ^c   Weyrich, Andrew S ^d   Zimmerman, Guy A ^a,d   Bozza, Fernando A ^b   Bozza, Patricia T ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Funda??o Oswaldo Cruz   (Brazil)

^c FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALBUMIN; ASPARTATE AMINOTRANSFERASE; CRYOPYRIN; IMMUNOGLOBULIN M; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE; PROSTAGLANDIN E1; RANTES; REACTIVE OXYGEN METABOLITE; CARRIER PROTEIN; IMIDAZOLE DERIVATIVE; INDOLE DERIVATIVE; INFLAMMASOME; MITOTEMPO; NECROSTATIN-1; NLRP3 PROTEIN, HUMAN; ORGANOPHOSPHORUS COMPOUND; PIPERIDINE DERIVATIVE; TOSYLPHENYLALANYL CHLOROMETHYL KETONE; TYROSYL-VALYL-ALANYL-ASPARTIC ACID FLUOROMETHYL KETONE;

ADULT; ARTICLE; BINDING AFFINITY; BLOOD VESSEL PERMEABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DENGUE; DENGUE VIRUS; ENDOTHELIUM; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; MALE; MEMBRANE PERMEABILITY; PLATELET MICROPARTICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; THROMBOCYTE; THROMBOCYTE ACTIVATION; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; BLOOD; CAPILLARY PERMEABILITY; DRUG EFFECTS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; MEMBRANE MICROPARTICLE; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; PHYSIOLOGY; SECRETION (PROCESS); ULTRASTRUCTURE; UPREGULATION; VASCULAR ENDOTHELIUM;

ADULT; BLOOD PLATELETS; CAPILLARY PERMEABILITY; CARRIER PROTEINS; CASPASE 1; CELL-DERIVED MICROPARTICLES; DENGUE; ENDOTHELIUM, VASCULAR; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; IMIDAZOLES; INDOLES; INFLAMMASOMES; INTERLEUKIN-1BETA; MALE; MITOCHONDRIA; ORGANOPHOSPHORUS COMPOUNDS; PIPERIDINES; PLATELET ACTIVATION; REACTIVE OXYGEN SPECIES; TOSYLPHENYLALANYL CHLOROMETHYL KETONE; UP-REGULATION;

EID: 84888222496     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-05-504449     Document Type: Article

References (50)

1. Schmidt AC. Response to dengue fever-the good, the bad, and the ugly? N Engl J Med. 2010; 363(5):484-487.
2. World Health Organization. Dengue: guidelines for diagnosis, treatment, prevention and control. WHO Press. 2009.
3. Bhatt S, Gething PW, Brady OJ, et al. The global distribution and burden of dengue. Nature. 2013; 496(7446):504-507.
4. Vaughn DW, Green S, Kalayanarooj S, et al. Dengue in the early febrile phase: viremia and antibody responses. J Infect Dis. 1997;176(2): 322-330.
5. Bozza FA, Cruz OG, Zagne SM, et al. Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis. 2008;8:86.
6. Schexneider KI, Reedy EA. Thrombocytopenia in dengue fever. Curr Hematol Rep. 2005;4(2):145-148.
7. Semple JW, Italiano JE Jr, Freedman J. Platelets and the immune continuum. Nat Rev Immunol. 2011;11(4):264-274.
8. Vieira-de-Abreu A, Campbell RA, Weyrich AS, Zimmerman GA. Platelets: versatile effector cells in hemostasis, inflammation, and the immune continuum. Semin Immunopathol. 2012;34(1):5-30.
9. Suharti C, van Gorp EC, Setiati TE, et al. The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome. Thromb Haemost. 2002;87(1):42-46.
10. Jaiyen Y, Masrinoul P, Kalayanarooj S, Pulmanausahakul R, Ubol S. Characteristics of dengue virus-infected peripheral blood mononuclear cell death that correlates with the severity of illness. Microbiol Immunol. 2009;53(8): 442-450.
11. Houghton-Triviño N, Martín K, Giaya K, Rodríguez JA, Bosch I, Castellanos JE. [Comparison of the transcriptional profiles of patients with dengue fever and dengue hemorrhagic fever reveals differences in the immune response and clues in immunopathogenesis]. Biomedica. 2010; 30(4):587-597.
12. Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011;29:707-735.
13. Lamkanfi M, Dixit VM. Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol. 2011;187(2):597-602.
14. Martinon F, Pétrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006; 440(7081):237-241.
15. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature. 2011;469(7329):221-225.
16. Wu MF, Chen ST, Yang AH, et al. CLEC5A is critical for dengue virus-induced inflammasome activation in human macrophages. Blood. 2013; 121(1):95-106.
17. Denis MM, Tolley ND, Bunting M, et al. Escaping the nuclear confines: signal-dependent premRNA splicing in anucleate platelets. Cell. 2005; 122(3):379-391.
18. Shashkin PN, Brown GT, Ghosh A, Marathe GK, McIntyre TM. Lipopolysaccharide is a direct agonist for platelet RNA splicing. J Immunol. 2008;181(5):3495-3502.
19. Aggrey AA, Srivastava K, Ture S, Field DJ, Morrell CN. Platelet induction of the acute-phase response is protective in murine experimental cerebral malaria. J Immunol. 2013;190(9): 4685-4691.
20. Brown GT, McIntyre TM. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles. J Immunol. 2011;186(9): 5489-5496.
21. Burnier L, Fontana P, Kwak BR, Angelillo-Scherrer A. Cell-derived microparticles in haemostasis and vascular medicine. Thromb Haemost. 2009;101(3):439-451.
22. Hottz ED, Oliveira MF, Nunes PC, et al. Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases. J Thromb Haemost. 2013;11(5):951-962.
23. Falconar AK, de Plata E, Romero-Vivas CM. Altered enzyme-linked immunosorbent assay immunoglobulin M (IgM)/IgG optical density ratios can correctly classify all primary or secondary dengue virus infections 1 day after the onset of symptoms, when all of the viruses can be isolated. Clin Vaccine Immunol. 2006;13(9):1044-1051.
24. Kuno G, Gómez I, Gubler DJ. An ELISA procedure for the diagnosis of dengue infections. J Virol Methods. 1991;33(1-2):101-113.
25. Shu PY, Chen LK, Chang SF, et al. Comparison of capture immunoglobulin M (IgM) and IgG enzyme-linked immunosorbent assay (ELISA) and nonstructural protein NS1 serotype-specific IgG ELISA for differentiation of primary and secondary dengue virus infections. Clin Diagn Lab Immunol. 2003;10(4):622-630.
26. Hamburger SA, McEver RP. GMP-140 mediates adhesion of stimulated platelets to neutrophils. Blood. 1990;75(3):550-554.
27. Weyrich AS, Lindemann S, Zimmerman GA. The evolving role of platelets in inflammation. J Thromb Haemost. 2003;1(9):1897-1905.
28. MacKenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity. 2001;15(5):825-835.
29. Vince JE, Wong WW, Gentle I, et al. Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation. Immunity. 2012;36(2): 215-227.
30. Pang T, Cardosa MJ, Guzman MG. Of cascades and perfect storms: the immunopathogenesis of dengue haemorrhagic fever-dengue shock syndrome (DHF/DSS). Immunol Cell Biol. 2007; 85(1):43-45.
31. Mitrakul C, Poshyachinda M, Futrakul P, Sangkawibha N, Ahandrik S. Hemostatic and platelet kinetic studies in dengue hemorrhagic fever. Am J Trop Med Hyg. 1977;26(5 Pt 1):975-984.
32. Schwertz H, Tolley ND, Foulks JM, et al. Signaldependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J Exp Med. 2006;203(11):2433-2440.
33. Cho YS, Challa S, Moquin D, Genga R, Ray TD, Guildford M, Chan FK. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell. 2009;137(6):1112-1123.
34. Vanlangenakker N, Vanden Berghe T, Bogaert P, et al. cIAP1 and TAK1 protect cells from TNFinduced necrosis by preventing RIP1/RIP3-dependent reactive oxygen species production. Cell Death Differ. 2011;18(4):656-665.
35. Nasirudeen AM, Liu DX. Gene expression profiling by microarray analysis reveals an important role for caspase-1 in dengue virusinduced p53-mediated apoptosis. J Med Virol. 2009;81(6):1069-1081.
36. Yu CY, Chiang RL, Chang TH, Liao CL, Lin YL. The interferon stimulator mitochondrial antiviral signaling protein facilitates cell death by disrupting the mitochondrial membrane potential and by activating caspases. J Virol. 2010;84(5):2421-2431.
37. Burdette D, Haskett A, Presser L, McRae S, Iqbal J, Waris G. Hepatitis C virus activates interleukin-1β via caspase-1-inflammasome complex. J Gen Virol. 2012;93(Pt 2):235-246.
38. Kaushik DK, Gupta M, Kumawat KL, Basu A. NLRP3 inflammasome: key mediator of neuroinflammation in murine Japanese encephalitis. PLoS ONE. 2012;7(2):e32270.
39. Dachary-Prigent J, Freyssinet JM, Pasquet JM, Carron JC, Nurden AT. Annexin V as a probe of aminophospholipid exposure and platelet membrane vesiculation: a flow cytometry study showing a role for free sulfhydryl groups. Blood. 1993;81(10):2554-2565.
40. Shcherbina A, Bretscher A, Kenney DM, Remold-O'Donnell E. Moesin, the major ERM protein of lymphocytes and platelets, differs from ezrin in its insensitivity to calpain. FEBS Lett. 1999; 443(1):31-36.
41. Shcherbina A, Kenney DM, Bretscher A, Remold-O-Donnell E. Dynamic association of moesin with the membrane skeleton of thrombin-activated platelets. Blood. 1999;93(6):2128-2129.
42. Shcherbina A, Remold-O'Donnell E. Role of caspase in a subset of human platelet activation responses. Blood. 1999;93(12):4222-4231.
43. Wang JG, Williams JC, Davis BK, Jacobson K, Doerschuk CM, Ting JP, Mackman N. Monocytic microparticles activate endothelial cells in an IL-1β-dependent manner. Blood. 2011;118(8): 2366-2374.
44. Kaplanski G, Porat R, Aiura K, Erban JK, Gelfand JA, Dinarello CA. Activated platelets induce endothelial secretion of interleukin-8 in vitro via an interleukin-1-mediated event. Blood. 1993;81(10): 2492-2495.
45. Mause SF, von Hundelshausen P, Zernecke A, Koenen RR, Weber C. Platelet microparticles: a transcellular delivery system for RANTES promoting monocyte recruitment on endothelium. Arterioscler Thromb Vasc Biol. 2005;25(7): 1512-1518.
46. Noisakran S, Chokephaibulkit K, Songprakhon P, et al. A re-evaluation of the mechanisms leading to dengue hemorrhagic fever. Ann N Y Acad Sci. 2009;1171(Suppl 1):E24-E35.
47. Noisakran S, Gibbons RV, Songprakhon P, et al. Detection of dengue virus in platelets isolated from dengue patients. Southeast Asian J Trop Med Public Health. 2009;40(2):253-262.
48. Hottz E, Toley N, Zimmerman G, Weyrich A, Bozza F. Platelets in dengue infection. Drug Discov Today Dis Mech. 2011;8(1-2):e33-e38.
49. Wang S, He R, Patarapotikul J, Innis BL, Anderson R. Antibody-enhanced binding of dengue-2 virus to human platelets. Virology. 1995;213(1):254-257.
50. van de Weg CA, Koraka P, van Gorp EC, et al. Lipopolysaccharide levels are elevated in dengue virus infected patients and correlate with disease severity. J Clin Virol. 2012;53(1):38-42.