Platelet Toll-like receptor expression and activation induced by lipopolysaccharide and sepsis

Platelets

Volumn 30, Issue 3, 2019, Pages 296-304

  Claushuis, Theodora A M ^a   Van Der Veen, Annelou I P ^a   Horn, Janneke ^a   Schultz, Marcus J ^a   Houtkooper, Riekelt H ^a,b   Van ’T Veer, Cornelis ^a   Van Der Poll, Tom ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Metabolism; platelet activation; platelets; sepsis; Toll like receptors

Indexed keywords

CD63 ANTIGEN; LIPOPOLYSACCHARIDE; PADGEM PROTEIN; PHOSPHATIDYLSERINE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 9;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; LEUKOCYTE; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEPSIS; SIGNAL TRANSDUCTION; THROMBOCYTE; THROMBOCYTE ACTIVATION; ANIMAL; BLOOD; METABOLISM; PHYSIOLOGY;

ANIMALS; BLOOD PLATELETS; FEMALE; HUMANS; LIPOPOLYSACCHARIDES; MICE; PLATELET ACTIVATION; SEPSIS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 85043510049     PISSN: 09537104     EISSN: 13691635     Source Type: Journal    
DOI: 10.1080/09537104.2018.1445841     Document Type: Article

References (37)

1. 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.
2. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, Patel KD, Chakrabarti S, McAvoy E. Sinclair GD and others. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. 2007;13(4):463–469.
3. Claushuis TAM, Van Vught LA, Scicluna BP, Wiewel MA, Klein Klouwenberg PM, Hoogendijk AJ, Ong DS, Cremer OL, Horn J. Franitza M and others. Thrombocytopenia is associated with a dysregulated host response in critically ill sepsis patients. Blood. 2016;127(24):3062–3072.
4. Van Der Poll T, Van De Veerdonk FL, Scicluna BP, Netea MG. The immunopathology of sepsis and potential therapeutic targets. Nat Rev Immunol. 2017;17(7):407–420.
5. Cognasse F, Hamzeh H, Chavarin P, Acquart S, Genin C, Garraud O. Evidence of toll-like receptor molecules on human platelets. Immunol Cell Biol. 2005;83(2):196–198.
6. Zhang G, Han J, Welch EJ, Ye RD, Voyno-Yasenetskaya TA, Malik AB, Du X, Li Z. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J Immunol. 2009;182(12):7997–8004.
7. Cognasse F, Hamzeh-Cognasse H, Lafarge S, Delezay O, Pozzetto B, McNicol A, Garraud O. Toll-like receptor 4 ligand can differentially modulate the release of cytokines by human platelets. Br J Haematol. 2008;141(1):84–91.
8. Ward JR, Bingle L,HMJ, Brown SB, Storey RF,MKBW, Dower SK, Buttle DJ, Sabroe I. Agonists of toll-like receptor (TLR)2 and TLR4 are unable to modulate platelet activation by adenosine diphosphate and platelet activating factor. Thromb Haemost. 2005;94:831–838.
9. Montrucchio G, Bosco O, Del Sorbo L, Fascio Pecetto P, Lupia E, Goffi A, Omede P, Emanuelli G, Camussi G. Mechanisms of the priming effect of low doses of lipopoly-saccharides on leukocyte-dependent platelet aggregation in whole blood. Thromb Haemost. 2003;90(5):872–881.
10. Sheu JR, Hung WC, Kan YC, Lee YM, Yen MH. Mechanisms involved in the antiplatelet activity of Escherichia coli lipopolysaccharide in human platelets. Br J Haematol. 1998;103:29–38.
11. Aslam R, Speck ER, Kim M, Crow AR, Bang KWA, Nestel FP, Ni H, Lazarus AH, Freedman J, Semple JW. Platelet toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-α production in vivo. Blood. 2006;107:637–641.
12. De Stoppelaar SF, Claushuis TA, Schaap MC, Hou B, Van Der Poll T, Nieuwland R, Van ‘T Veer C. toll-Like receptor signalling is not involved in platelet response to streptococcus pneumoniae in vitro or in vivo. PLoS One. 2016;11(6):e0156977.
13. De Stoppelaar SF, Claushuis TA, Jansen MP, Hou B, Roelofs JJ, Van ‘T Veer C, Van Der Poll T. The role of platelet MyD88 in host response during gram-negative sepsis. J Thromb Haemost. 2015;13(9):1709–1720.
14. Russwurm S, Vickers J, Meier-Hellmann A, Spangenberg P, Bredle D, Reinhart K, Losche W. Platelet and leukocyte activation correlate with the severity of septic organ dysfunction. Shock. 2002;17(4):263–268.
15. Gawaz M, Dickfeld T, Bogner C, Fateh-Moghadam S, Neumann FJ. Platelet function in septic multiple organ dysfunction syndrome. Intensive Care Med. 1997;23:379–385.
16. Tsai JC, Lin YW, Huang CY, Lin CY, Tsai YT, Shih CM, Lee CY, Chen YH, Li CY. Chang NC and others. The role of calpain-myosin 9-rab7b pathway in mediating the expression of toll-like receptor 4 in platelets: a novel mechanism involved in alpha-granules trafficking. PLoS One. 2014;9(1):e85833.
17. Thon JN, Peters CG, Machlus KR, Aslam R, Rowley J, Macleod H, Devine MT, Fuchs TA, Weyrich AS. Semple JW and others. T granules in human platelets function in TLR9 organization and signaling. J Cell Biol. 2012;198(4):561–574.
18. Beaulieu LM, Lin E, Morin KM, Tanriverdi K, Freedman JE. Regulatory effects of TLR2 on megakaryocytic cell function. Blood. 2011;117(22):5963–5974.
19. Boshuizen M, Leopold JH, Zakharkina T, Knobel HH, Weda H, Nijsen TM, Vink TJ, Sterk PJ, Schultz MJ. Bos LD and others. Levels of cytokines in broncho-alveolar lavage fluid, but not in plasma, are associated with levels of markers of lipid peroxidation in breath of ventilated ICU patients. J Breath Res. 2015;9(3):036010.
20. Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RMH, Sibbald WJ. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Chest. 1992;101(6):1644–1655.
21. Weehuizen TA, Hommes TJ, Lankelma JM, De Jong HK, Roelofs JJ, De Vos AF, Colonna M, Van Der Poll T, Wiersinga WJ. Triggering Receptor Expressed on Myeloid Cells (TREM)-2 impairs host defense in experimental melioidosis. PLoS Negl Trop Dis. 2016;10(6):e0004747.
22. Lankelma JM, Birnie E, Weehuizen TAF, Scicluna BP, Belzer C, Houtkooper RH, Roelofs J, De Vos AF, Van Der Poll T. Budding AE and others. The gut microbiota as a modulator of innate immunity during melioidosis. PLoS Negl Trop Dis. 2017;11(4):e0005548.
23. De Stoppelaar SF, Van ’T Veer C, Claushuis TAM, Albersen BJA, Roelofs JJTH, Van Der Poll T. Thrombocytopenia impairs host defense in gram-negative pneumonia–derived sepsis in mice. Blood. 2014;124(25):3781–3790.
24. Palsson-McDermott EM, O’Neill LA. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology. 2004;113(2):153–162.
25. Koupenova M, Mick E, Mikhalev E, Benjamin EJ, Tanriverdi K, Freedman JE. Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 2015;35(4):1030–1037.
26. Nocella C, Carnevale R, Bartimoccia S, Novo M, Cangemi R, Pastori D, Calvieri C, Pignatelli P, Violi F. Lipopolysaccharide as trigger of platelet aggregation via eicosanoid over-production. Thromb Haemost. 2017;117(8):1558–1570.
27. Kramer PA, Ravi S, Chacko B, Johnson MS, Darley-Usmar VM. A review of the mitochondrial and glycolytic metabolism in human platelets and leukocytes: implications for their use as bioenergetic biomarkers. Redox Biol. 2014;2:206–210.
28. Middleton EA, Weyrich AS, Zimmerman GA. Platelets in pulmonary immune responses and inflammatory lung diseases. Physiol Rev. 2016;96(4):1211–1259.
29. Berthet J, Damien P, Hamzeh-Cognasse H, Arthaud CA, Eyraud MA, Zeni F, Pozzetto B, McNicol A, Garraud O, Cognasse F. Human platelets can discriminate between various bacterial LPS isoforms via TLR4 signaling and differential cytokine secretion. Clin Immunol. 2012;145(3):189–200.
30. Zhao L, Ohtaki Y, Yamaguchi K, Matsushita M, Fujita T, Yokochi T, Takada H, Endo Y. LPS-induced platelet response and rapid shock in mice: contribution of O-antigen region of LPS and involvement of the lectin pathway of the complement system. Blood. 2002;100(9):3233–3239.
31. Damien P, Cognasse F, Eyraud MA, Arthaud CA, Pozzetto B, Garraud O, Hamzeh-Cognasse H. LPS stimulation of purified human platelets is partly dependent on plasma soluble CD14 to secrete their main secreted product, soluble-CD40-Ligand. BMC Immunol. 2015;16:3.
32. Flaumenhaft R, Dilks JR, Rozenvayn N, Monahan-Earley RA, Feng D, Dvorak M. The actin cytoskeleton differentially regulates platelet a-granule and dense-granule secretion. Blood Coagul Fibrinolysis. 2005;105:3879–3887.
33. Italiano JE, Jr., Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood. 2008;111(3):1227–1233.
34. Kamykowski J, Carlton P, Sehgal S, Storrie B. Quantitative immunofluorescence mapping reveals little functional coclustering of proteins within platelet alpha-granules. Blood. 2011;118(5):1370–1373.
35. Jonnalagadda D, Izu LT, Whiteheart SW. Platelet secretion is kinetically heterogeneous in an agonist-responsive manner. Blood. 2012;120(26):5209–5216.
36. Zharikov S, Shiva S. Platelet mitochondrial function: from regulation of thrombosis to biomarker of disease. Biochem Soc Trans. 2013;41(1):118–123.
37. Gurses KM, Kocyigit D, Yalcin MU, Canpinar H, Oto MA, Ozer N, Tokgozoglu L, Guc D, Aytemir K. Enhanced platelet toll-like receptor 2 and 4 expression in acute coronary syndrome and stable angina pectoris. Am J Cardiol. 2015;116(11):1666–1671.