Lipopolysaccharide signaling without a nucleus: Kinase cascades stimulate platelet shedding of proinflammatory IL-1β-rich microparticles

Journal of Immunology

Volumn 186, Issue 9, 2011, Pages 5489-5496

  Brown, G Thomas ^a,b   McIntyre, Thomas M ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN KINASE B; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PLATELET MICROPARTICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; THROMBOCYTE RELEASE REACTION;

ANIMALS; BLOOD PLATELETS; CELL NUCLEUS; CELL SEPARATION; CELL-DERIVED MICROPARTICLES; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; PLATELET ACTIVATION; PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA SPLICING; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; VASCULAR CELL ADHESION MOLECULE-1;

EID: 79955534720     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001623     Document Type: Article

References (51)

1. Heffner, J. E., S. A. Sahn, and J. E. Repine. 1987. The role of platelets in the adult respiratory distress syndrome. Culprits or bystanders? Am. Rev. Respir. Dis. 135: 482-492.
2. Davis, R. B., W. R. Meeker, and D. G. McQuarrie. 1960. Immediate effects of intravenous endotoxin on serotonin concentrations and blood platelets. Circ. Res. 8: 234-239.
3. Shibazaki, M., Y. Kawabata, T. Yokochi, A. Nishida, H. Takada, and Y. Endo. 1999. Complement-dependent accumulation and degradation of platelets in the lung and liver induced by injection of lipopolysaccharides. Infect. Immun. 67: 5186-5191.
4. Vincent, J. L., A. Yagushi, and O. Pradier. 2002. Platelet function in sepsis. Crit. Care Med. 30(5, Suppl): S313-S317.
5. 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.
6. 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. (Pubitemid 41510815)
7. Abdelnoor, A. M., H. Kassem, A. B. Bikhazi, and A. Nowotny. 1980. Effect of gram-negative bacterial lipopolysaccharide-derived polysaccharides, glycolipids, and lipopolysaccharides on rabbit and human platelets in vitro. Immunobiology 157: 145-153. (Pubitemid 10082173)
8. 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.
9. McMorran, B. J., V. M. Marshall, C. de Graaf, K. E. Drysdale, M. Shabbar, G. K. Smyth, J. E. Corbin, W. S. Alexander, and S. J. Foote. 2009. Platelets kill intraerythrocytic malarial parasites and mediate survival to infection. Science 323: 797-800.
10. 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.
11. 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.
12. 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-alpha production in vivo. Blood 107: 637-641.
13. 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.
14. Lødrup Carlsen, K. C., and B. Granum. 2007. Soluble CD14: role in atopic disease and recurrent infections, including otitis media. Curr. Allergy Asthma Rep. 7: 436-443.
15. Liu, F., S. Morris, J. Epps, and R. Carroll. 2002. Demonstration of an activation regulated NF-kappaB/I-kappaBalpha complex in human platelets. Thromb. Res. 106: 199-203.
16. Malaver, E., M. A. Romaniuk, L. P. D'Atri, R. G. Pozner, S. Negrotto, R. Benzadón, and M. Schattner. 2009. NF-kappaB inhibitors impair platelet activation responses. J. Thromb. Haemost. 7: 1333-1343.
17. Kauskot, A., F. Adam, A. Mazharian, N. Ajzenberg, E. Berrou, A. Bonnefoy, J. P. Rosa, M. F. Hoylaerts, and M. Bryckaert. 2007. Involvement of the mitogen-activated protein kinase c-Jun NH2-terminal kinase 1 in thrombus formation. J. Biol. Chem. 282: 31990-31999.
18. Chen, K., M. Febbraio, W. Li, and R. L. Silverstein. 2008. A specific CD36-dependent signaling pathway is required for platelet activation by oxidized low-density lipoprotein. Circ. Res. 102: 1512-1519.
19. Barry, F. A., and J. M. Gibbins. 2002. Protein kinase B is regulated in platelets by the collagen receptor glycoprotein VI. J. Biol. Chem. 277: 12874-12878.
20. Kim, S., P. Mangin, C. Dangelmaier, R. Lillian, S. P. Jackson, J. L. Daniel, and S. P. Kunapuli. 2009. Role of phosphoinositide 3-kinase beta in glycoprotein VI-mediated Akt activation in platelets. J. Biol. Chem. 284: 33763-33772.
21. Zhang, B., G. Ramesh, S. Uematsu, S. Akira, and W. B. Reeves. 2008. TLR4 signaling mediates inflammation and tissue injury in nephrotoxicity. J. Am. Soc. Nephrol. 19: 923-932.
22. Kirschenbaum, L. A., D. McKevitt, M. Rullan, B. Reisbeck, T. Fujii, and M. E. Astiz. 2004. Importance of platelets and fibrinogen in neutrophil-endothelial cell interactions in septic shock. Crit. Care Med. 32: 1904-1909.
23. Muraki, M., B. Ohkawara, T. Hosoya, H. Onogi, J. Koizumi, T. Koizumi, K. Sumi, J. Yomoda, M. V. Murray, H. Kimura, et al. 2004. Manipulation of alternative splicing by a newly developed inhibitor of Clks. J. Biol. Chem. 279: 24246-24254.
24. Uto, T., X. Wang, K. Sato, M. Haraguchi, T. Akagi, M. Akashi, and M. Baba. 2007. Targeting of antigen to dendritic cells with poly(gamma-glutamic acid) nanoparticles induces antigen-specific humoral and cellular immunity. J. Immunol. 178: 2979-2986. (Pubitemid 46333177)
25. Horng, T., G. M. Barton, and R. Medzhitov. 2001. TIRAP: an adapter molecule in the Toll signaling pathway. Nat. Immunol. 2: 835-841.
26. McWhirter, S. M., S. S. Pullen, J. M. Holton, J. J. Crute, M. R. Kehry, and T. Alber. 1999. Crystallographic analysis of CD40 recognition and signaling by human TRAF2. Proc. Natl. Acad. Sci. USA 96: 8408-8413.
27. Bharti, A. C., Y. Takada, S. Shishodia, and B. B. Aggarwal. 2004. Evidence that receptor activator of nuclear factor (NF)-kappaB ligand can suppress cell proliferation and induce apoptosis through activation of a NF-kappaB-independent and TRAF6-dependent mechanism. J. Biol. Chem. 279: 6065-6076.
28. Comalada, M., J. Xaus, A. F. Valledor, C. López-López, D. J. Pennington, and A. Celada. 2003. PKC epsilon is involved in JNK activation that mediates LPS-induced TNF-alpha, which induces apoptosis in macrophages. Am. J. Physiol. Cell Physiol. 285: C1235-C1245.
29. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptormediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6: 777-784.
30. Pawlinski, R., J. G.Wang, A. P. Owens, III, J. Williams, S. Antoniak, M. Tencati, T. Luther, J. W. Rowley, E. N. Low, A. S. Weyrich, and N. Mackman. 2010. Hematopoietic and nonhematopoietic cell tissue factor activates the coagulation cascade in endotoxemic mice. Blood 116: 806-814.
31. Cosemans, J. M., I. C. Munnix, R. Wetzker, R. Heller, S. P. Jackson, and J. W. Heemskerk. 2006. Continuous signaling via PI3K isoforms beta and gamma is required for platelet ADP receptor function in dynamic thrombus stabilization. Blood 108: 3045-3052.
32. Trumel, C., B. Payrastre, M. Plantavid, B. Hechler, C. Viala, P. Presek, E. A. Martinson, J. P. Cazenave, H. Chap, and C. Gachet. 1999. A key role of adenosine diphosphate in the irreversible platelet aggregation induced by the PAR1-activating peptide through the late activation of phosphoinositide 3-kinase. Blood 94: 4156-4165.
33. Jackson, S. P., S. M. Schoenwaelder, I. Goncalves, W. S. Nesbitt, C. L. Yap, C. E. Wright, V. Kenche, K. E. Anderson, S. M. Dopheide, Y. Yuan, et al. 2005. PI 3-kinase p110beta: a newtarget for antithrombotic therapy. Nat. Med. 11: 507-514.
34. Yin, H., A. Stojanovic, N. Hay, and X. Du. 2008. The role of Akt in the signaling pathway of the glycoprotein Ib-IXinduced platelet activation. Blood 111: 658-665.
35. Kroner, C., K. Eybrechts, and J. W. Akkerman. 2000. Dual regulation of platelet protein kinase B. J. Biol. Chem. 275: 27790-27798.
36. Woulfe, D., H. Jiang, A. Morgans, R. Monks, M. Birnbaum, and L. F. Brass. 2004. Defects in secretion, aggregation, and thrombus formation in platelets from mice lacking Akt2. J. Clin. Invest. 113: 441-450.
37. Chen, J., S. De, D. S. Damron, W. S. Chen, N. Hay, and T. V. Byzova. 2004. Impaired platelet responses to thrombin and collagen in AKT-1-deficient mice. Blood 104: 1703-1710.
38. Jang, S. W., X. Liu, H. Fu, H. Rees, M. Yepes, A. Levey, and K. Ye. 2009. Interaction of Akt-phosphorylated SRPK2 with 14-3-3 mediates cell cycle and cell death in neurons. J. Biol. Chem. 284: 24512-24525.
39. Cheng, C., Y. Qin, X. Shao, H. Wang, Y. Gao, M. Cheng, and A. Shen. 2007. Induction of TNF-alpha by LPS in Schwann cell is regulated by MAPK activation signals. Cell. Mol. Neurobiol. 27: 909-921.
40. Rodriguez, N., R. Lang, N. Wantia, C. Cirl, T. Ertl, S. Dürr, H. Wagner, and T. Miethke. 2008. Induction of iNOS by Chlamydophila pneumoniae requires MyD88-dependent activation of JNK. J. Leukoc. Biol. 84: 1585-1593.
41. Flevaris, P., Z. Li, G. Zhang, Y. Zheng, J. Liu, and X. Du. 2009. Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signaling pathway. Blood 113: 893-901.
42. Jackson, E. C., and A. McNicol. 2010. Cyclic nucleotides inhibit MAP kinase activity in low-dose collagen-stimulated platelets. Thromb. Res. 125: 147-151.
43. Charruyer, A., S. Grazide, C. Bezombes, S. Müller, G. Laurent, and J. P. Jaffrézou. 2005. UV-C light induces raft-associated acid sphingomyelinase and JNK activation and translocation independently on a nuclear signal. J. Biol. Chem. 280: 19196-19204.
44. Bowman, T. V., A. J. McCooey, A. A. Merchant, C. A. Ramos, P. Fonseca, A. Poindexter, S. B. Bradfute, D. M. Oliveira, R. Green, Y. Zheng, et al. 2006. Differential mRNA processing in hematopoietic stem cells. Stem Cells 24: 662-670. (Pubitemid 44464770)
45. Behre, G., I. Schedel, B. Nentwig, B. Wörmann, M. Essink, and W. Hiddemann. 1992. Endotoxin concentration in neutropenic patients with suspected gram-negative sepsis: correlation with clinical outcome and determination of anti-endotoxin core antibodies during therapy with polyclonal immunoglobulin M-enriched immunoglobulins. Antimicrob. Agents Chemother. 36: 2139-2146.
46. Opal, S. M., P. J. Scannon, J. L. Vincent, M. White, S. F. Carroll, J. E. Palardy, N. A. Parejo, J. P. Pribble, and J. H. Lemke. 1999. Relationship between plasma levels of lipopolysaccharide (LPS) and LPS-binding protein in patients with severe sepsis and septic shock. J. Infect. Dis. 180: 1584-1589.
47. Ilkka, L., and J. Takala. 1996. Plasma endotoxin levels in the early phase of septic shock. Intensive Care Med. 22(Suppl. 1): S9.
48. Guidet, B., V. Barakett, T. Vassal, J. C. Petit, and G. Offenstadt. 1994. Endotoxemia and bacteremia in patients with sepsis syndrome in the intensive care unit. Chest 106: 1194-1201. (Pubitemid 24309562)
49. 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 in- flammatory signaling by regulated interleukin 1beta synthesis. J. Cell Biol. 154: 485-490.
50. 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.
51. 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.