Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015 (2015), Article ID 435783, 7 pages
http://dx.doi.org/10.1155/2015/435783
Review Article

Inflammasome in Platelets: Allying Coagulation and Inflammation in Infectious and Sterile Diseases?

1Laboratório de Imunofarmacologia, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, 21040-900 Rio de Janeiro, RJ, Brazil
2Laboratório de Medicina Intensiva, Instituto Nacional de Infectologia Evandro Chagas, Fundação Oswaldo Cruz, 21040-900 Rio de Janeiro, RJ, Brazil
3Instituto D’Or de Pesquisa e Ensino, 22281-100 Rio de Janeiro, RJ, Brazil

Received 19 September 2014; Revised 24 January 2015; Accepted 26 January 2015

Academic Editor: Bernardo S. Franklin

Copyright © 2015 Eugenio D. Hottz et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. W. Semple, J. E. Italiano Jr., and J. Freedman, “Platelets and the immune continuum,” Nature Reviews Immunology, vol. 11, no. 4, pp. 264–274, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Vieira-de-Abreu, R. A. Campbell, A. S. Weyrich, and G. A. Zimmerman, “Platelets: versatile effector cells in hemostasis, inflammation, and the immune continuum,” Seminars in Immunopathology, vol. 34, no. 1, pp. 5–30, 2012. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  4. E. D. Hottz, J. F. Lopes, C. Freitas et al., “Platelets mediate increased endothelium permeability in dengue through NLRP3-inflammasome activation,” Blood, vol. 122, no. 20, pp. 3405–3414, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Lindemann, N. D. Tolley, D. A. Dixon et al., “Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis,” The Journal of Cell Biology, vol. 154, no. 3, pp. 485–490, 2001. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  9. D. P. Abulafia, J. P. de Rivero Vaccari, J. D. Lozano, G. Lotocki, R. W. Keane, and W. D. Dietrich, “Inhibition of the inflammasome 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  11. C. A. Dinarello, “Immunological and inflammatory functions of the interleukin-1 family,” Annual Review of Immunology, vol. 27, pp. 519–550, 2009. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  17. B. K. Davis, H. Wen, and J. P.-Y. Ting, “The Inflammasome NLRs in immunity, inflammation, and associated diseases,” Annual Review of Immunology, vol. 29, pp. 707–735, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. M. Lamkanfi and V. M. Dixit, “Modulation of inflammasome pathways by bacterial and viral pathogens,” The Journal of Immunology, vol. 187, no. 2, pp. 597–602, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. R. Zhou, A. S. Yazdi, P. Menu, and J. Tschopp, “A role for mitochondria in NLRP3 inflammasome activation,” Nature, vol. 469, no. 7329, pp. 221–226, 2011. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Schwertz, N. D. Tolley, J. M. Foulks et al., “Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenecity of human platelets,” Journal of Experimental Medicine, vol. 203, no. 11, pp. 2433–2440, 2006. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  23. A.-L. Ståhl, M. Svensson, M. Mörgelin et al., “Lipopolysaccharide 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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Martinon, V. Pétrilli, A. Mayor, A. Tardivel, and J. Tschopp, “Gout-associated uric acid crystals activate the NALP3 inflammasome,” Nature, vol. 440, no. 7081, pp. 237–241, 2006. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  37. J. E. Freedman, “Molecular regulation of platelet-dependent thrombosis,” Circulation, vol. 112, no. 17, pp. 2725–2734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Nishimura, I. Manabe, M. Nagasaki et al., “In vivo imaging visualizes discoid platelet aggregations without endothelium disruption and implicates contribution of inflammatory cytokine and integrin signaling,” Blood, vol. 119, no. 8, pp. e45–e56, 2012. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  49. C. A. Moxon, S. C. Wassmer, D. A. Milner Jr. et al., “Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children,” Blood, vol. 122, no. 5, pp. 842–851, 2013. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  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. View at Publisher · View at Google Scholar · View at Scopus
  54. WHO, Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control, 2009.
  55. K. I. Schexneider and E. A. Reedy, “Thrombocytopenia in dengue fever,” Current hematology reports., vol. 4, no. 2, pp. 145–148, 2005. View at Publisher · View at Google Scholar · View at Scopus
  56. M. P. G. Mourão, M. V. G. Lacerda, V. O. Macedo, and J. B. Santos, “Thrombocytopenia in patients with dengue virus infection in the Brazilian Amazon,” Platelets, vol. 18, no. 8, pp. 605–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. E. Hottz, N. D. Tolley, G. A. Zimmerman, A. S. Weyrich, and F. A. Bozza, “Platelets in dengue infection,” Drug Discovery Today: Disease Mechanisms, vol. 8, no. 1-2, pp. e33–e38, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. Y. Jaiyen, P. Masrinoul, S. Kalayanarooj, R. Pulmanausahakul, and S. Ubol, “Characteristics of dengue virus-infected peripheral blood mononuclear cell death that correlates with the severity of illness,” Microbiology and Immunology, vol. 53, no. 8, pp. 442–450, 2009. View at Publisher · View at Google Scholar · View at Scopus