Lipopolysaccharide stimulates platelets through an IL-1β autocrine loop

Journal of Immunology

Volumn 191, Issue 10, 2013, Pages 5196-5203

  Thomas Brown, G ^a   Narayanan, Padmini ^a   Li, Wei ^a   Silverstein, Roy L ^a,b   McIntyre, Thomas M ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MESSENGER RNA; TOLL LIKE RECEPTOR 4; TLR4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME ACTIVATION; ENZYME INHIBITION; FLOW CYTOMETRY; GENE REPRESSION; HUMAN; HUMAN CELL; IMMUNITY; MOUSE; NONHUMAN; PLATELET MICROPARTICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RNA SPLICING; SIGNAL TRANSDUCTION; THROMBOCYTE ACTIVATION; THROMBOSIS; TRANSLATION INITIATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL CULTURE; IMMUNOLOGY; INFLAMMATION; METABOLISM; THROMBOCYTE;

ANIMALS; BLOOD PLATELETS; CASPASE 1; CELLS, CULTURED; HUMANS; INFLAMMATION; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MICE; PLATELET ACTIVATION; RECEPTORS, INTERLEUKIN-1 TYPE I; RNA SPLICING; RNA, MESSENGER; SIGNAL TRANSDUCTION; THROMBOSIS; TOLL-LIKE RECEPTOR 4;

EID: 84887480564     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300354     Document Type: Article

References (46)

1. Dinarello, C. A. 2009. Immunological and inflammatory functions of the interleukin-1 family. Annu. Rev. Immunol. 27:519-550.
2. Dinarello, C. A. 2009. Interleukin-1β and the autoinflammatory diseases. N. Engl. J. Med. 360:2467-2470.
3. Qu, Y., L. Franchi, G. Nunez, and G. R. Dubyak. 2007. Nonclassical IL-1β secretion stimulated by P2X7 receptors is dependent on inflammasome activation and correlated with exosome release in murine macrophages. J. Immunol. 179:1913-1925.
4. Andrei, C., C. Dazzi, L. Lotti, M. R. Torrisi, G. Chimini, and A. Rubartelli. 1999. The secretory route of the leaderless protein interleukin 1b involves exocytosis of endolysosome-related vesicles. Mol. Biol. Cell 10:1463-1475.
5. MacKenzie, A., H. L. Wilson, E. Kiss-Toth, S. K. Dower, R. A. North, and A. Surprenant. 2001. Rapid secretion of interleukin-1β by microvesicle shedding. Immunity 15:825-835.
6. Wang, J. G., J. C. Williams, B. K. Davis, K. Jacobson, C. M. Doerschuk, J. P. Ting, and N. Mackman. 2011. Monocytic microparticles activate endothelial cells in an IL-1β-dependent manner. Blood 118:2366-2374.
7. Dinarello, C. A., T. Ikejima, S. J. Warner, S. F. Orencole, G. Lonnemann, J. G. Cannon, and P. Libby. 1987. Interleukin 1 induces interleukin 1. I. Induction of circulating interleukin 1 in rabbits in vivo and in human mononuclear cells in vitro. J. Immunol. 139:1902-1910.
8. Warner, S. J., K. R. Auger, and P. Libby. 1987. Interleukin 1 induces interleukin 1. II. Recombinant human interleukin 1 induces interleukin 1 production by adult human vascular endothelial cells. J. Immunol. 139:1911-1917.
9. Oda, K., and H. Kitano. 2006. A comprehensive map of the Toll-like receptor signaling network. Mol. Syst. Biol. 2:2006.0015.
10. Pålsson-McDermott, E. M., and L. A. O'Neill. 2004. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 113:153-162.
11. Andonegui, G., S. M. Kerfoot, K. McNagny, K. V. Ebbert, K. D. Patel, and P. Kubes. 2005. Platelets express functional Toll-like receptor-4. Blood 106:2417-2423.
12. Cognasse, F., H. Hamzeh, P. Chavarin, S. Acquart, C. Genin, and O. Garraud. 2005. Evidence of Toll-like receptor molecules on human platelets. Immunol. Cell Biol. 83:196-198.
13. Aslam, R., E. R. Speck, M. Kim, A. R. Crow, K. W. Bang, F. P. Nestel, H. Ni, A. H. Lazarus, J. Freedman, and J. W. Semple. 2006. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-α production in vivo. Blood 107:637-641.
14. Ståhl, A. L., M. Svensson, M. Mörgelin, C. Svanborg, P. I. Tarr, J. C. Mooney, S. L. Watkins, R. Johnson, and D. Karpman. 2006. 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 108:167-176.
15. Rumbaut, R. E., R. V. Bellera, J. K. Randhawa, C. N. Shrimpton, S. K. Dasgupta, J. F. Dong, and A. R. Burns. 2006. Endotoxin enhances microvascular thrombosis in mouse cremaster venules via a TLR4-dependent, neutrophil- independent mechanism. Am. J. Physiol. Heart Circ. Physiol. 290:H1671-H1679.
16. Clark, S. R., A. C. Ma, S. A. Tavener, B. McDonald, Z. Goodarzi, M. M. Kelly, K. D. Patel, S. Chakrabarti, E. McAvoy, G. D. Sinclair, et al. 2007. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13:463-469.
17. Stark, R. J., N. Aghakasiri, and R. E. Rumbaut. 2012. Platelet-derived Toll-like receptor 4 (Tlr-4) is sufficient to promote microvascular thrombosis in endotoxemia. PLoS ONE 7:e41254.
18. Ward, J. R., L. Bingle, H. M. Judge, S. B. Brown, R. F. Storey, M. K. Whyte, S. K. Dower, D. J. Buttle, and I. Sabroe. 2005. Agonists of Toll-like receptor (TLR) 2 and TLR4 are unable to modulate platelet activation by adenosine diphosphate and platelet activating factor. Thromb. Haemost. 94:831-838.
19. Brown, G. T., and T. M. McIntyre. 2011. Lipopolysaccharide signaling without a nucleus: kinase cascades stimulate platelet shedding of proinflammatory IL-1b-rich microparticles. J. Immunol. 186:5489-5496.
20. Zhang, G., J. Han, E. J. Welch, R. D. Ye, T. A. Voyno-Yasenetskaya, A. B. Malik, X. Du, and Z. Li. 2009. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J. Immunol. 182:7997-8004.
21. Weyrich, A. S., H. Schwertz, L. W. Kraiss, and G. A. Zimmerman. 2009. Protein synthesis by platelets: historical and new perspectives. J. Thromb. Haemost. 7:241-246.
22. Brogren, H., L. Karlsson, M. Andersson, L. Wang, D. Erlinge, and S. Jern. 2004. Platelets synthesize large amounts of active plasminogen activator inhibitor 1. Blood 104:3943-3948.
23. Weyrich, A. S., M. M. Denis, H. Schwertz, N. D. Tolley, J. Foulks, E. Spencer, L. W. Kraiss, K. H. Albertine, T. M. McIntyre, and G. A. Zimmerman. 2007. mTOR-dependent synthesis of Bcl-3 controls the retraction of fibrin clots by activated human platelets. Blood 109:1975-1983.
24. Denis, M. M., N. D. Tolley, M. Bunting, H. Schwertz, H. Jiang, S. Lindemann, C. C. Yost, F. J. Rubner, K. H. Albertine, K. J. Swoboda, et al. 2005. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 122:379-391.
25. Lindemann, S., N. D. Tolley, D. A. Dixon, T. M. McIntyre, S. M. Prescott, G. A. Zimmerman, and A. S. Weyrich. 2001. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J. Cell Biol. 154:485-490.
26. Schwertz, H., N. D. Tolley, J. M. Foulks, M. M. Denis, B. W. Risenmay, M. Buerke, R. E. Tilley, M. T. Rondina, E. M. Harris, L. W. Kraiss, et al. 2006. Signal-dependent splicing of tissue factor pre-mRNA modulates the thrombogenicity of human platelets. J. Exp. Med. 203:2433-2440.
27. Shashkin, P. N., G. T. Brown, A. Ghosh, G. K. Marathe, and T. M. McIntyre. 2008. Lipopolysaccharide is a direct agonist for platelet RNA splicing. J. Immunol. 181:3495-3502.
28. Rondina, M. T., B. Brewster, C. K. Grissom, G. A. Zimmerman, D. H. Kastendieck, E. S. Harris, and A. S. Weyrich. 2012. In vivo platelet activation in critically ill patients with primary 2009 influenza A (H1N1). Chest 141:1490-1495.
29. Lockyer, S., and J. Kambayashi. 1999. Demonstration of flow and platelet dependency in a ferric chloride-induced model of thrombosis. J. Cardiovasc. Pharmacol. 33:718-725.
30. Weyrich, A. S., M. R. Elstad, R. P. McEver, T. M. McIntyre, K. L. Moore, J. H. Morrissey, S. M. Prescott, and G. A. Zimmerman. 1996. Activated platelets signal chemokine synthesis by human monocytes. J. Clin. Invest. 97:1525-1534.
31. Chen, K., W. Li, J. Major, S. O. Rahaman, M. Febbraio, and R. L. Silverstein. 2011. Vav guanine nucleotide exchange factors link hyperlipidemia and a prothrombotic state. Blood 117:5744-5750.
32. Li, W., T. M. McIntyre, and R. L. Silverstein. 2013. Ferric chloride-induced murine carotid arterial injury: a model of redoxpathology. Redox Biol. 1:50-55.
33. Schwartz, H. S., J. E. Sodergren, and R. Y. Ambaye. 1968. Actinomycin D: drug concentrations and actions in mouse tissues and tumors. Cancer Res. 28:192-197.
34. Lee, R. D., D. A. Barcel, J. C. Williams, J. G. Wang, J. C. Boles, D. A. Manly, N. S. Key, and N. Mackman. 2012. Pre-analytical and analytical variables affecting the measurement of plasma-derived microparticle tissue factor activity. Thromb. Res. 129:80-85.
35. Kappelmayer, J., I. Beke Debreceni, A. Vida, P. Antal-Szalmás, K. J. Clemetson, and B. Nagy, Jr. 2013. Distinct effects of Re- and S-forms of LPS on modulating platelet activation. J. Thromb. Haemost. 11:775-778.
36. Van De Veerdonk, F. L., M. G. Netea, C. A. Dinarello, and L. A. Joosten. 2011. Inflammasome activation and IL-1β and IL-18 processing during infection. Trends Immunol. 32:110-116.
37. Arend, W. P. 2002. The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev. 13:323-340.
38. Alexander, M. R., C. W. Moehle, J. L. Johnson, Z. Yang, J. K. Lee, C. L. Jackson, and G. K. Owens. 2012. Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J. Clin. Invest. 122:70-79.
39. Mileno, M. D., N. H. Margolis, B. D. Clark, C. A. Dinarello, J. F. Burke, and J. A. Gelfand. 1995. Coagulation of whole blood stimulates interleukin-1β gene expression. J. Infect. Dis. 172:308-311.
40. Schindler, R., B. D. Clark, and C. A. Dinarello. 1990. Dissociation between interleukin-1β mRNA and protein synthesis in human peripheral blood mononuclear cells. J. Biol. Chem. 265:10232-10237.
41. Rowley, J. W., A. J. Oler, N. D. Tolley, B. N. Hunter, E. N. Low, D. A. Nix, C. C. Yost, G. A. Zimmerman, and A. S. Weyrich. 2011. Genome-wide RNA-seq analysis of human and mouse platelet transcriptomes. Blood 118:e101-e111.
42. Flaumenhaft, R. 2006. Formation and fate of platelet microparticles. Blood Cells Mol. Dis. 36:182-187.
43. Reimers, J., L. D. Wogensen, B. Welinder, K. R. Hejnaes, S. S. Poulsen, P. Nilsson, and J. Nerup. 1991. The pharmacokinetics, distribution and degradation of human recombinant interleukin 1β in normal rats. Scand. J. Immunol. 34:597-610.
44. Arend, W. P., and C. J. Guthridge. 2000. Biological role of interleukin 1 receptor antagonist isoforms. Ann. Rheum. Dis. 59 (Suppl 1):i60-i64.
45. Park, J. S., F. Gamboni-Robertson, Q. He, D. Svetkauskaite, J. Y. Kim, D. Strassheim, J. W. Sohn, S. Yamada, I. Maruyama, A. Banerjee, et al. 2006. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am. J. Physiol. Cell Physiol. 290:C917-C924.
46. Vogl, T., K. Tenbrock, S. Ludwig, N. Leukert, C. Ehrhardt, M. A. Van Zoelen, W. Nacken, D. Foell, T. Van Der Poll, C. Sorg, and J. Roth. 2007. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 13:1042-1049.