Inflammasome in platelets: Allying coagulation and inflammation in infectious and sterile diseases?

Mediators of Inflammation

Volumn 2015, Issue , 2015, Pages

  Hottz, Eugenio D ^a   Monteiro, Ana Paula T ^a   Bozza, Fernando A ^b,c   Bozza, Patrícia T ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b Funda??o Oswaldo Cruz   (Brazil)

^c D OR INSTITUTE FOR RESEARCH AND EDUCATION IDOR   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

INFLAMMASOME; INTERLEUKIN 1BETA; RNA;

BLOOD CLOTTING; INFECTION; INFLAMMATION; INFLAMMATORY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOSIS; COMMUNICABLE DISEASE; HUMAN; IMMUNOLOGY; PHYSIOLOGY; SECRETION (PROCESS);

BLOOD COAGULATION; BLOOD PLATELETS; COMMUNICABLE DISEASES; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; SIGNAL TRANSDUCTION; THROMBOSIS;

EID: 84924559749     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2015/435783     Document Type: Review

References (116)

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2. A. Vieira-de-Abreu, R. A. Campbell, A. S. Weyrich, and G. A. Zimmerman, "Platelets: versatile effector cells in hemosta-sis, inflammation, and the immune continuum," Seminars in Immunopathology, Vol. 34, no. 1, pp. 5-30, 2012.
3. M. M. Denis, N. D. Tolley, M. Bunting et al., "Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets," Cell, Vol. 122, no. 3, pp. 379-391, 2005.
4. E. D. Hottz, J. F. Lopes, C. Freitas et al., "Platelets mediate increased endothelium permeability in dengue through NLRP3-in ammasome activation," Blood, Vol. 122, no. 20, pp. 3405-3414, 2013.
5. S. Lindemann, N. D. Tolley, D. A. Dixon et al., "Activated platelets mediate inflammatory signaling by regulated inter-leukin 1beta synthesis," The Journal of Cell Biology, Vol. 154, no. 3, pp. 485-490, 2001.
6. G. T. Brown and T. M. McIntyre, "Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles," Journal of Immunology, Vol. 186, no. 9, pp. 5489-5496, 2011.
7. F. A. Bozza, O. G. Cruz, S. M. O. Zagne et al., "Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity," BMC Infectious Diseases, Vol. 8, article 86, 2008.
8. C. Suharti, E. C. M. van Gorp, T. E. Setiati et al., "The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome," Thrombosis and Haemostasis, Vol. 87, no. 1, pp. 42-46, 2002.
9. D. P. Abulafia, J. P. de Rivero Vaccari, J. D. Lozano, G. Lotocki, R. W. Keane, and W. D. Dietrich, "Inhibition of the in ammasome complex reduces the inflammatory response after thromboembolic stroke in mice," Journal of Cerebral Blood Flow and Metabolism, Vol. 29, no. 3, pp. 534-544, 2009.
10. H. Yang, H.-J. Ko, J.-Y. Yang et al., "Interleukin-1 promotes coagulation, which is necessary for protective immunity in the lung against streptococcus pneumoniae infection," Journal of Infectious Diseases, Vol. 207, no. 1, pp. 50-60, 2013.
11. C. A. Dinarello, "Immunological and inflammatory functions of the interleukin-1 family," Annual Review of Immunology, Vol. 27, pp. 519-550, 2009.
12. H. Loppnow, R. Bil, S. Hirt et al., "Platelet-derived interleukin-1 induces cytokine production, but not proliferation of human vascular smooth muscle cells," Blood, Vol. 91, no. 1, pp. 134-141, 1998.
13. G. Kaplanski, R. Porat, K. Aiura, J. K. Erban, J. A. Gelfand, and C. A. Dinarello, "Activated platelets induce endothelial secretion of interleukin-8 in vitro via an interleukin-1-mediated event," Blood, Vol. 81, no. 10, pp. 2492-2495, 1993.
14. C. M. Hawrylowicz, G. L. Howells, and M. Feldmann, "Platelet-derived interleukin 1 induces human endothelial adhesion molecule expression and cytokine production," Journal of Experimental Medicine, Vol. 174, no. 4, pp. 785-790, 1991.
15. C. M. Hawrylowicz, S. A. Santoro, F. M. Platt, and E. R. Unanue, "Activated platelets express IL-1 activity," Journal of Immunology, Vol. 143, no. 12, pp. 4015-4018, 1989.
16. G. T. Brown, P. Narayanan, W. Li, R. L. Silverstein, and T. M. McIntyre, "Lipopolysaccharide stimulates platelets through an IL-1beta autocrine loop," Journal of Immunology, Vol. 191, no. 10, pp. 5196-5203, 2013.
17. B. K. Davis, H. Wen, and J. P.-Y. Ting, "The In ammasome NLRs in immunity, inflammation, and associated diseases," Annual Review of Immunology, Vol. 29, pp. 707-735, 2011.
18. M. Lamkanfi and V. M. Dixit, "Modulation of in ammasome pathways by bacterial and viral pathogens," The Journal of Immunology, Vol. 187, no. 2, pp. 597-602, 2011.
19. R. Zhou, A. S. Yazdi, P. Menu, and J. Tschopp, "A role for mitochondria in NLRP3 in ammasome activation," Nature, Vol. 469, no. 7329, pp. 221-226, 2011.
20. J. W. Rowley, A. J. Oler, N. D. Tolley et al., "Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes," Blood, Vol. 118, no. 14, pp. e101-e111, 2011.
21. H. Schwertz, N. D. Tolley, J. M. Foulks et al., "Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombo-genecity of human platelets," Journal of Experimental Medicine, Vol. 203, no. 11, pp. 2433-2440, 2006.
22. P. N. Shashkin, G. T. Brown, A. Ghosh, G. K. Marathe, and T. M. McIntyre, "Lipopolysaccharide is a direct agonist for platelet RNA splicing," Journal of Immunology, Vol. 181, no. 5, pp. 3495-3502, 2008.
23. A.-L. Ståhl, M. Svensson, M. Mörgelin et al., "Lipopolysaccha-ride from enterohemorrhagic Escherichia coli binds to platelets through TLR4 and CD62 and is detected on circulating platelets in patients with hemolytic uremic syndrome," Blood, Vol. 108, no. 1, pp. 167-176, 2006.
24. L. Rivadeneyra, A. Carestia, J. Etulain et al., "Regulation of platelet responses triggered by Toll-like receptor 2 and 4 ligands is another non-genomic role of nuclear factor-kappaB," Thrombosis Research, Vol. 133, no. 2, pp. 235-243, 2014.
25. Z. Zhou, F. C. Gushiken, D. Bolgiano et al., "Signal transducer and activator of transcription 3 (STAT3) regulates collagen-induced Platelet aggregation independently of its transcription factor activity," Circulation, Vol. 127, no. 4, pp. 476-485, 2013.
26. S. Boukour, J.-M. Massé, L. Bénit, A. Dubart-Kupperschmitt, and E. M. Cramer, "Lentivirus degradation and DC-SIGN expression by human platelets and megakaryocytes," Journal of Thrombosis and Haemostasis, Vol. 4, no. 2, pp. 426-435, 2006.
27. C. Flaujac, S. Boukour, and E. Cramer-Bordé, "Platelets and viruses: an ambivalent relationship," Cellular and Molecular Life Sciences, Vol. 67, no. 4, pp. 545-556, 2010.
28. E. Pokidysheva, Y. Zhang, A. J. Battisti et al., "Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN," Cell, Vol. 124, no. 3, pp. 485-493, 2006.
29. B. Tassaneetrithep, T. H. Burgess, A. Granelli-Piperno et al., "DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells," Journal of Experimental Medicine, Vol. 197, no. 7, pp. 823-829, 2003.
30. E. D. Hottz, M. F. Oliveira, P. C. G. Nunes et al., "Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases," Journal of Thrombosis and Haemostasis, Vol. 11, no. 5, pp. 951-962, 2013.
31. J. E. Vince, W. W.-L. Wong, I. Gentle et al., "Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation," Immunity, Vol. 36, no. 2, pp. 215-227, 2012.
32. P. P. Lemons, D. Chen, A. M. Bernstein, M. K. Bennett, and S. W. Whiteheart, "Regulated secretion in platelets: identification of elements of the platelet exocytosis machinery," Blood, Vol. 90, no. 4, pp. 1490-1500, 1997.
33. F. Rendu and B. Brohard-Bohn, "The platelet release reaction: granules' constituents, secretion and functions," Platelets, Vol. 12, no. 5, pp. 261-273, 2001.
34. F. Martinon, V. Pétrilli, A. Mayor, A. Tardivel, and J. Tschopp, "Gout-associated uric acid crystals activate the NALP3 inflam-masome," Nature, Vol. 440, no. 7081, pp. 237-241, 2006.
35. L. M. Beaulieu, E. Lin, E. Mick et al., "Interleukin 1 receptor 1 and interleukin 1β regulate megakaryocyte maturation, platelet activation, and transcript profile during inflammation in mice and humans," Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 34, no. 3, pp. 552-564, 2014.
36. D. Varga-Szabo, I. Pleines, and B. Nieswandt, "Cell adhesion mechanisms in platelets," Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 28, no. 3, pp. 403-412, 2008.
37. J. E. Freedman, "Molecular regulation of platelet-dependent thrombosis," Circulation, Vol. 112, no. 17, pp. 2725-2734, 2005.
38. S. Nishimura, I. Manabe, M. Nagasaki et al., "In vivo imaging visualizes discoid platelet aggregations without endothe-lium disruption and implicates contribution of inflammatory cytokine and integrin signaling," Blood, Vol. 119, no. 8, pp. e45-e56, 2012.
39. S. J. Shattil, C. Kim, and M. H. Ginsberg, "The final steps of integrin activation: the end game," Nature Reviews Molecular Cell Biology, Vol. 11, no. 4, pp. 288-300, 2010.
40. M. Gawaz, F.-J. Neumann, T. Dickfeld et al., "Activated platelets induce monocyte chemotactic protein-1 secretion and surface expression of intercellular adhesion molecule-1 on endothelial cells," Circulation, Vol. 98, no. 12, pp. 1164-1171, 1998.
41. P. Thornton, B. W. McColl, A. Greenhalgh, A. Denes, S. M. Allan, and N. J. Rothwell, "Platelet interleukin-1alpha drives cerebrovascular inflammation," Blood, Vol. 115, no. 17, pp. 3632-3639, 2010.
42. E. Boilard, P. A. Nigrovic, K. Larabee et al., "Platelets amplify inflammation in arthritis via collagen-dependent microparticle production," Science, Vol. 327, no. 5965, pp. 580-583, 2010.
43. E. D. Hottz, I. M. Medeiros-de-Moraes, A. Vieira-de-Abreu et al., "Platelet activation and apoptosis modulate monocyte inflammatory responses in dengue," The Journal of Immunology, Vol. 193, no. 4, pp. 1864-1872, 2014.
44. M. T. Rondina, H. Schwertz, E. S. Harris et al., "The septic milieu triggers expression of spliced tissue factor mRNA in human platelets," Journal of Thrombosis and Haemostasis, Vol. 9, no. 4, pp. 748-758, 2011.
45. E. Mayne, N. T. Funderburg, S. F. Sieg et al., "Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression," Journal of Acquired Immune Deficiency Syndromes, Vol. 59, no. 4, pp. 340-346, 2012.
46. F. M. Campos, B. S. Franklin, A. Teixeira-Carvalho et al., "Augmented plasma microparticles during acute Plasmodium vivax infection," Malaria Journal, Vol. 9, no. 1, article 327, 2010.
47. A. A. Aggrey, K. Srivastava, S. Ture, D. J. Field, and C. N. Morrell, "Platelet induction of the acute-phase response is protective in murine experimental cerebral malaria," Journal of Immunology, Vol. 190, no. 9, pp. 4685-4691, 2013.
48. G. Andonegui, S. M. Kerfoot, K. McNagny, K. V. J. Ebbert, K. D. Patel, and P. Kubes, "Platelets express functional Toll-like receptor-4," Blood, Vol. 106, no. 7, pp. 2417-2423, 2005.
49. C. A. Moxon, S. C. Wassmer, D. A. Milner Jr. et al., "Loss of endothelial protein C receptors links coagulation and inflam-mation to parasite sequestration in cerebral malaria in African children," Blood, Vol. 122, no. 5, pp. 842-851, 2013.
50. D. Faille, F. El-Assaad, M.-C. Alessi, T. Fusai, V. Combes, and G. E. R. Grau, "Platelet-endothelial cell interactions in cerebral malaria: the end of a cordial understanding," Thrombosis and Haemostasis, Vol. 102, no. 6, pp. 1093-1102, 2009.
51. H. C. C. Coelho, S. C. P. Lopes, J. P. D. Pimentel et al., "Thrombocytopenia in Plasmodium vivax malaria is related to platelets phagocytosis," PLoS ONE, Vol. 8, no. 5, Article ID e63410, 2013.
52. K. Srivastava, I. A. Cockburn, A. Swaim et al., "Platelet factor 4 mediates inflammation in experimental cerebral malaria," Cell Host and Microbe, Vol. 4, no. 2, pp. 179-187, 2008.
53. S. Bhatt, P. W. Gething, O. J. Brady et al., "The global distribution and burden of dengue," Nature, Vol. 496, no. 7446, pp. 504-507, 2013.
54. WHO, Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control, 2009.
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60. A. Vieira-de-Abreu, R. A. Campbell, A. S. Weyrich, and G. A. Zimmerman, "Platelets: versatile effector cells in hemosta-sis, inflammation, and the immune continuum," Seminars in Immunopathology, Vol. 34, no. 1, pp. 5-30, 2012.
61. M. M. Denis, N. D. Tolley, M. Bunting et al., "Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets," Cell, Vol. 122, no. 3, pp. 379-391, 2005.
62. E. D. Hottz, J. F. Lopes, C. Freitas et al., "Platelets mediate increased endothelium permeability in dengue through NLRP3-in ammasome activation," Blood, Vol. 122, no. 20, pp. 3405-3414, 2013.
63. S. Lindemann, N. D. Tolley, D. A. Dixon et al., "Activated platelets mediate inflammatory signaling by regulated inter-leukin 1beta synthesis," The Journal of Cell Biology, Vol. 154, no. 3, pp. 485-490, 2001.
64. G. T. Brown and T. M. McIntyre, "Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles," Journal of Immunology, Vol. 186, no. 9, pp. 5489-5496, 2011.
65. F. A. Bozza, O. G. Cruz, S. M. O. Zagne et al., "Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity," BMC Infectious Diseases, Vol. 8, article 86, 2008.
66. C. Suharti, E. C. M. van Gorp, T. E. Setiati et al., "The role of cytokines in activation of coagulation and fibrinolysis in dengue shock syndrome," Thrombosis and Haemostasis, Vol. 87, no. 1, pp. 42-46, 2002.
67. D. P. Abulafia, J. P. de Rivero Vaccari, J. D. Lozano, G. Lotocki, R. W. Keane, and W. D. Dietrich, "Inhibition of the in ammasome complex reduces the inflammatory response after thromboembolic stroke in mice," Journal of Cerebral Blood Flow and Metabolism, Vol. 29, no. 3, pp. 534-544, 2009.
68. H. Yang, H.-J. Ko, J.-Y. Yang et al., "Interleukin-1 promotes coagulation, which is necessary for protective immunity in the lung against streptococcus pneumoniae infection," Journal of Infectious Diseases, Vol. 207, no. 1, pp. 50-60, 2013.
69. C. A. Dinarello, "Immunological and inflammatory functions of the interleukin-1 family," Annual Review of Immunology, Vol. 27, pp. 519-550, 2009.
70. H. Loppnow, R. Bil, S. Hirt et al., "Platelet-derived interleukin-1 induces cytokine production, but not proliferation of human vascular smooth muscle cells," Blood, Vol. 91, no. 1, pp. 134-141, 1998.
71. G. Kaplanski, R. Porat, K. Aiura, J. K. Erban, J. A. Gelfand, and C. A. Dinarello, "Activated platelets induce endothelial secretion of interleukin-8 in vitro via an interleukin-1-mediated event," Blood, Vol. 81, no. 10, pp. 2492-2495, 1993.
72. C. M. Hawrylowicz, G. L. Howells, and M. Feldmann, "Platelet-derived interleukin 1 induces human endothelial adhesion molecule expression and cytokine production," Journal of Experimental Medicine, Vol. 174, no. 4, pp. 785-790, 1991.
73. C. M. Hawrylowicz, S. A. Santoro, F. M. Platt, and E. R. Unanue, "Activated platelets express IL-1 activity," Journal of Immunology, Vol. 143, no. 12, pp. 4015-4018, 1989.
74. G. T. Brown, P. Narayanan, W. Li, R. L. Silverstein, and T. M. McIntyre, "Lipopolysaccharide stimulates platelets through an IL-1beta autocrine loop," Journal of Immunology, Vol. 191, no. 10, pp. 5196-5203, 2013.
75. B. K. Davis, H. Wen, and J. P.-Y. Ting, "The In ammasome NLRs in immunity, inflammation, and associated diseases," Annual Review of Immunology, Vol. 29, pp. 707-735, 2011.
76. M. Lamkanfi and V. M. Dixit, "Modulation of in ammasome pathways by bacterial and viral pathogens," The Journal of Immunology, Vol. 187, no. 2, pp. 597-602, 2011.
77. R. Zhou, A. S. Yazdi, P. Menu, and J. Tschopp, "A role for mitochondria in NLRP3 in ammasome activation," Nature, Vol. 469, no. 7329, pp. 221-226, 2011.
78. J. W. Rowley, A. J. Oler, N. D. Tolley et al., "Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes," Blood, Vol. 118, no. 14, pp. e101-e111, 2011.
79. H. Schwertz, N. D. Tolley, J. M. Foulks et al., "Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombo-genecity of human platelets," Journal of Experimental Medicine, Vol. 203, no. 11, pp. 2433-2440, 2006.
80. P. N. Shashkin, G. T. Brown, A. Ghosh, G. K. Marathe, and T. M. McIntyre, "Lipopolysaccharide is a direct agonist for platelet RNA splicing," Journal of Immunology, Vol. 181, no. 5, pp. 3495-3502, 2008.
81. A.-L. Ståhl, M. Svensson, M. Mörgelin et al., "Lipopolysaccha-ride from enterohemorrhagic Escherichia coli binds to platelets through TLR4 and CD62 and is detected on circulating platelets in patients with hemolytic uremic syndrome," Blood, Vol. 108, no. 1, pp. 167-176, 2006.
82. L. Rivadeneyra, A. Carestia, J. Etulain et al., "Regulation of platelet responses triggered by Toll-like receptor 2 and 4 ligands is another non-genomic role of nuclear factor-kappaB," Thrombosis Research, Vol. 133, no. 2, pp. 235-243, 2014.
83. Z. Zhou, F. C. Gushiken, D. Bolgiano et al., "Signal transducer and activator of transcription 3 (STAT3) regulates collagen-induced Platelet aggregation independently of its transcription factor activity," Circulation, Vol. 127, no. 4, pp. 476-485, 2013.
84. S. Boukour, J.-M. Massé, L. Bénit, A. Dubart-Kupperschmitt, and E. M. Cramer, "Lentivirus degradation and DC-SIGN expression by human platelets and megakaryocytes," Journal of Thrombosis and Haemostasis, Vol. 4, no. 2, pp. 426-435, 2006.
85. C. Flaujac, S. Boukour, and E. Cramer-Bordé, "Platelets and viruses: an ambivalent relationship," Cellular and Molecular Life Sciences, Vol. 67, no. 4, pp. 545-556, 2010.
86. E. Pokidysheva, Y. Zhang, A. J. Battisti et al., "Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN," Cell, Vol. 124, no. 3, pp. 485-493, 2006.
87. B. Tassaneetrithep, T. H. Burgess, A. Granelli-Piperno et al., "DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells," Journal of Experimental Medicine, Vol. 197, no. 7, pp. 823-829, 2003.
88. E. D. Hottz, M. F. Oliveira, P. C. G. Nunes et al., "Dengue induces platelet activation, mitochondrial dysfunction and cell death through mechanisms that involve DC-SIGN and caspases," Journal of Thrombosis and Haemostasis, Vol. 11, no. 5, pp. 951-962, 2013.
89. J. E. Vince, W. W.-L. Wong, I. Gentle et al., "Inhibitor of apoptosis proteins limit RIP3 kinase-dependent interleukin-1 activation," Immunity, Vol. 36, no. 2, pp. 215-227, 2012.
90. P. P. Lemons, D. Chen, A. M. Bernstein, M. K. Bennett, and S. W. Whiteheart, "Regulated secretion in platelets: identification of elements of the platelet exocytosis machinery," Blood, Vol. 90, no. 4, pp. 1490-1500, 1997.
91. F. Rendu and B. Brohard-Bohn, "The platelet release reaction: granules' constituents, secretion and functions," Platelets, Vol. 12, no. 5, pp. 261-273, 2001.
92. F. Martinon, V. Pétrilli, A. Mayor, A. Tardivel, and J. Tschopp, "Gout-associated uric acid crystals activate the NALP3 inflam-masome," Nature, Vol. 440, no. 7081, pp. 237-241, 2006.
93. L. M. Beaulieu, E. Lin, E. Mick et al., "Interleukin 1 receptor 1 and interleukin 1β regulate megakaryocyte maturation, platelet activation, and transcript profile during inflammation in mice and humans," Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 34, no. 3, pp. 552-564, 2014.
94. D. Varga-Szabo, I. Pleines, and B. Nieswandt, "Cell adhesion mechanisms in platelets," Arteriosclerosis, Thrombosis, and Vascular Biology, Vol. 28, no. 3, pp. 403-412, 2008.
95. J. E. Freedman, "Molecular regulation of platelet-dependent thrombosis," Circulation, Vol. 112, no. 17, pp. 2725-2734, 2005.
96. S. Nishimura, I. Manabe, M. Nagasaki et al., "In vivo imaging visualizes discoid platelet aggregations without endothe-lium disruption and implicates contribution of inflammatory cytokine and integrin signaling," Blood, Vol. 119, no. 8, pp. e45-e56, 2012.
97. S. J. Shattil, C. Kim, and M. H. Ginsberg, "The final steps of integrin activation: the end game," Nature Reviews Molecular Cell Biology, Vol. 11, no. 4, pp. 288-300, 2010.
98. M. Gawaz, F.-J. Neumann, T. Dickfeld et al., "Activated platelets induce monocyte chemotactic protein-1 secretion and surface expression of intercellular adhesion molecule-1 on endothelial cells," Circulation, Vol. 98, no. 12, pp. 1164-1171, 1998.
99. P. Thornton, B. W. McColl, A. Greenhalgh, A. Denes, S. M. Allan, and N. J. Rothwell, "Platelet interleukin-1alpha drives cerebrovascular inflammation," Blood, Vol. 115, no. 17, pp. 3632-3639, 2010.
100. E. Boilard, P. A. Nigrovic, K. Larabee et al., "Platelets amplify inflammation in arthritis via collagen-dependent microparticle production," Science, Vol. 327, no. 5965, pp. 580-583, 2010.
101. E. D. Hottz, I. M. Medeiros-de-Moraes, A. Vieira-de-Abreu et al., "Platelet activation and apoptosis modulate monocyte inflammatory responses in dengue," The Journal of Immunology, Vol. 193, no. 4, pp. 1864-1872, 2014.
102. M. T. Rondina, H. Schwertz, E. S. Harris et al., "The septic milieu triggers expression of spliced tissue factor mRNA in human platelets," Journal of Thrombosis and Haemostasis, Vol. 9, no. 4, pp. 748-758, 2011.
103. E. Mayne, N. T. Funderburg, S. F. Sieg et al., "Increased platelet and microparticle activation in HIV infection: upregulation of P-selectin and tissue factor expression," Journal of Acquired Immune Deficiency Syndromes, Vol. 59, no. 4, pp. 340-346, 2012.
104. F. M. Campos, B. S. Franklin, A. Teixeira-Carvalho et al., "Augmented plasma microparticles during acute Plasmodium vivax infection," Malaria Journal, Vol. 9, no. 1, article 327, 2010.
105. A. A. Aggrey, K. Srivastava, S. Ture, D. J. Field, and C. N. Morrell, "Platelet induction of the acute-phase response is protective in murine experimental cerebral malaria," Journal of Immunology, Vol. 190, no. 9, pp. 4685-4691, 2013.
106. G. Andonegui, S. M. Kerfoot, K. McNagny, K. V. J. Ebbert, K. D. Patel, and P. Kubes, "Platelets express functional Toll-like receptor-4," Blood, Vol. 106, no. 7, pp. 2417-2423, 2005.
107. C. A. Moxon, S. C. Wassmer, D. A. Milner Jr. et al., "Loss of endothelial protein C receptors links coagulation and inflam-mation to parasite sequestration in cerebral malaria in African children," Blood, Vol. 122, no. 5, pp. 842-851, 2013.
108. D. Faille, F. El-Assaad, M.-C. Alessi, T. Fusai, V. Combes, and G. E. R. Grau, "Platelet-endothelial cell interactions in cerebral malaria: the end of a cordial understanding," Thrombosis and Haemostasis, Vol. 102, no. 6, pp. 1093-1102, 2009.
109. H. C. C. Coelho, S. C. P. Lopes, J. P. D. Pimentel et al., "Thrombocytopenia in Plasmodium vivax malaria is related to platelets phagocytosis," PLoS ONE, Vol. 8, no. 5, Article ID e63410, 2013.
110. K. Srivastava, I. A. Cockburn, A. Swaim et al., "Platelet factor 4 mediates inflammation in experimental cerebral malaria," Cell Host and Microbe, Vol. 4, no. 2, pp. 179-187, 2008.
111. S. Bhatt, P. W. Gething, O. J. Brady et al., "The global distribution and burden of dengue," Nature, Vol. 496, no. 7446, pp. 504-507, 2013.
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