Thrombosis Research
Volume 125, Issue 3 , Pages 205-209 , March 2010

The role of inflammation in regulating platelet production and function: Toll-like receptors in platelets and megakaryocytes

Received 27 October 2009 ,Revised 27 October 2009 ,Accepted 2 November 2009.

References 

  1. Medzhitov R, Janeway CA. Decoding the patterns of self and nonself by the innate immune system. Science. Apr 12 2002;296(5566):298–300
  2. Medzhitov R, Janeway CA. Innate immunity: impact on the adaptive immune response. Curr Opin Immunol. Feb 1997;9(1):4–9
  3. Medzhitov R, Preston-Hurlburt P, Janeway CA. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature. Jul 24 1997;388(6640):394–397
  4. Wetzler LM. The role of Toll-like receptor 2 in microbial disease and immunity. Vaccine. Jun 1 2003;21(Suppl 2):S55–S60
  5. Beachey EH, Chiang TM, Ofek I, Kang AH. Interaction of lipoteichoic acid of group A streptococci with human platelets. Infect Immun. May 1977;16(2):649–654
  6. Berg M, Offermanns S, Seifert R, Schultz G. Synthetic lipopeptide Pam3CysSer(Lys)4 is an effective activator of human platelets. Am J Physiol. Jun 1994;266(6 Pt 1):C1684–C1691
  7. Travlos GS. Normal structure, function, and histology of the bone marrow. Toxicol Pathol. 2006;34(5):548–565
  8. Stohlawetz P, Folman CC, von dem Borne AE, Pernerstorfer T, Eichler HG, Panzer S, et al. Effects of endotoxemia on thrombopoiesis in men. Thromb Haemost. Apr 1999;81(4):613–617
  9. Pick M, Perry C, Lapidot T, Guimaraes-Sternberg C, Naparstek E, Deutsch V, et al. Stress-induced cholinergic signaling promotes inflammation-associated thrombopoiesis. Blood. Apr 15 2006;107(8):3397–3406
  10. Shiraki R, Inoue N, Kawasaki S, Takei A, Kadotani M, Ohnishi Y, et al. Expression of Toll-like receptors on human platelets. Thromb Res. 2004;113(6):379–385
  11. Ward JR, Bingle L, Judge HM, Brown SB, Storey RF, Whyte MK, et al. Agonists of toll-like receptor (TLR)2 and TLR4 are unable to modulate platelet activation by adenosine diphosphate and platelet activating factor. Thromb Haemost. Oct 2005;94(4):831–838
  12. Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional Toll-like receptor-4. Blood. Oct 1 2005;106(7):2417–2423
  13. Maratheftis CI, Andreakos E, Moutsopoulos HM, Voulgarelis M. Toll-like receptor-4 is up-regulated in hematopoietic progenitor cells and contributes to increased apoptosis in myelodysplastic syndromes. Clin Cancer Res. Feb 15 2007;13(4):1154–1160
  14. Jayachandran M, Brunn GJ, Karnicki K, Miller RS, Owen WG, Miller VM. In vivo effects of lipopolysaccharide and TLR4 on platelet production and activity: implications for thrombotic risk. J Appl Physiol. Jan 2007;102(1):429–433
  15. Alves-Filho JC. Toll-like receptors on platelets: the key for disseminated intravascular coagulation in sepsis?. Thromb Res. 2005;115(6):537–538
  16. Funayama H, Huang L, Sato T, Ohtaki Y, Asada Y, Yokochi T, et al. Pharmacological characterization of anaphylaxis-like shock responses induced in mice by mannan and lipopolysaccharide. Int Immunopharmacol. 2009;9(13–14):1518–1524
  17. 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. Oct 1998;103(1):29–38
  18. Davis RB, Meeker WR, Mc QD. Immediate effects of intravenous endotoxin on serotonin concentrations and blood platelets. Circ Res. Jan 1960;8:234–239
  19. Tang YQ, Yeaman MR, Selsted ME. Antimicrobial peptides from human platelets. Infect Immun. Dec 2002;70(12):6524–6533
  20. Klinger MH, Jelkmann W. Role of blood platelets in infection and inflammation. J Interferon Cytokine Res. Sep 2002;22(9):913–922
  21. Liu CZ, Huang HY, Tsai PJ, Shih MH. Blockade of glycoprotein IIb/IIIa by crotavirin, a member of disintegrins, prevents platelet from activation and aggregation by Staphylococcus aureus bacteria. Thromb Res. 2005;116(2):145–155
  22. Sjobring U, Ringdahl U, Ruggeri ZM. Induction of platelet thrombi by bacteria and antibodies. Blood. Dec 15 2002;100(13):4470–4477
  23. Loughman A, Fitzgerald JR, Brennan MP, Higgins J, Downer R, Cox D, et al. Roles for fibrinogen, immunoglobulin and complement in platelet activation promoted by Staphylococcus aureus clumping factor A. Mol Microbiol. Aug 2005;57(3):804–818
  24. Byrne MF, Kerrigan SW, Corcoran PA, Atherton JC, Murray FE, Fitzgerald DJ, et al. Helicobacter pylori binds von Willebrand factor and interacts with GPIb to induce platelet aggregation. Gastroenterology. Jun 2003;124(7):1846–1854
  25. Kerrigan SW, Douglas I, Wray A, Heath J, Byrne MF, Fitzgerald D, et al. A role for glycoprotein Ib in Streptococcus sanguis-induced platelet aggregation. Blood. Jul 15 2002;100(2):509–516
  26. Chia JS, Lin YL, Lien HT, Chen JY. Platelet aggregation induced by serotype polysaccharides from Streptococcus mutans. Infect Immun. May 2004;72(5):2605–2617
  27. Zeller JA, Lenz A, Eschenfelder CC, Zunker P, Deuschl G. Platelet-leukocyte interaction and platelet activation in acute stroke with and without preceding infection. Arterioscler Thromb Vasc Biol. Jul 2005;25(7):1519–1523
  28. Matera C, Falzarano C, Berrino L, Rossi F. Effects of tetanus toxin, Salmonella typhimurium porin, and bacterial lipopolysaccharide on platelet aggregation. J Med. 1992;23(5):327–338
  29. Kalvegren H, Majeed M, Bengtsson T. Chlamydia pneumoniae binds to platelets and triggers P-selectin expression and aggregation: a causal role in cardiovascular disease?. Arterioscler Thromb Vasc Biol. Sep 1 2003;23(9):1677–1683
  30. Kalvegren H, Andersson J, Grenegard M, Bengtsson T. Platelet activation triggered by Chlamydia pneumoniae is antagonized by 12-lipoxygenase inhibitors but not cyclooxygenase inhibitors. Eur J Pharmacol. Jul 2 2007;566(1–3):20–27
  31. Sharma A, Novak EK, Sojar HT, Swank RT, Kuramitsu HK, Genco RJ. Porphyromonas gingivalis platelet aggregation activity: outer membrane vesicles are potent activators of murine platelets. Oral Microbiol Immunol. Dec 2000;15(6):393–396
  32. Pham K, Feik D, Hammond BF, Rams TE, Whitaker EJ. Aggregation of human platelets by gingipain-R from Porphyromonas gingivalis cells and membrane vesicles. Platelets. Feb 2002;13(1):21–30
  33. Lourbakos A, Yuan YP, Jenkins AL, Travis J, Andrade-Gordon P, Santulli R, et al. Activation of protease-activated receptors by gingipains from Porphyromonas gingivalis leads to platelet aggregation: a new trait in microbial pathogenicity. Blood. Jun 15 2001;97(12):3790–3797
  34. Curtis MA, Macey M, Slaney JM, Howells GL. Platelet activation by Protease I of Porphyromonas gingivalis W83. FEMS Microbiol Lett. Jun 15 1993;110(2):167–173
  35. Naito M, Sakai E, Shi Y, Ideguchi H, Shoji M, Ohara N, et al. Porphyromonas gingivalis-induced platelet aggregation in plasma depends on Hgp44 adhesin but not Rgp proteinase. Mol Microbiol. Jan 2006;59(1):152–167
  36. Montrucchio G, Bosco O, Del Sorbo L, Fascio Pecetto P, Lupia E, Goffi A, et al. Mechanisms of the priming effect of low doses of lipopoly-saccharides on leukocyte-dependent platelet aggregation in whole blood. Thromb Haemost. Nov 2003;90(5):872–881
  37. Cognasse F, Hamzeh H, Chavarin P, Acquart S, Genin C, Garraud O. Evidence of Toll-like receptor molecules on human platelets. Immunol Cell Biol. Apr 2005;83(2):196–198
  38. Aslam R, Speck ER, Kim M, Crow AR, Bang KW, Nestel FP, et al. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo. Blood. Jan 15 2006;107(2):637–641
  39. Shibazaki M, Nakamura M, Endo Y. Biphasic, organ-specific, and strain-specific accumulation of platelets induced in mice by a lipopolysaccharide from Escherichia coli and its possible involvement in shock. Infect Immun. Dec 1996;64(12):5290–5294
  40. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med. Apr 2007;13(4):463–469
  41. Scott T, Owens MD. Thrombocytes respond to lipopolysaccharide through Toll-like receptor-4, and MAP kinase and NF-kappaB pathways leading to expression of interleukin-6 and cyclooxygenase-2 with production of prostaglandin E2. Mol Immunol. Feb 2008;45(4):1001–1008
  42. Cognasse F, Lafarge S, Chavarin P, Acquart S, Garraud O. Lipopolysaccharide induces sCD40L release through human platelets TLR4, but not TLR2 and TLR9. Intensive Care Med. Feb 2007;33(2):382–384
  43. Cognasse F, Hamzeh-Cognasse H, Lafarge S, Delezay O, Pozzetto B, McNicol A, et al. Toll-like receptor 4 ligand can differentially modulate the release of cytokines by human platelets. Br J Haematol. Apr 2008;141(1):84–91
  44. Stahl AL, Svensson M, Morgelin M, Svanborg C, Tarr PI, Mooney JC, 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. Jul 1 2006;108(1):167–176
  45. Rumbaut RE, Bellera RV, Randhawa JK, Shrimpton CN, Dasgupta SK, Dong JF, et al. Endotoxin enhances microvascular thrombosis in mouse cremaster venules via a TLR4-dependent, neutrophil-independent mechanism. Am J Physiol Heart Circ Physiol. Apr 2006;290(4):H1671–H1679
  46. Zhang G, Han J, Welch EJ, Ye RD, Voyno-Yasenetskaya TA, Malik AB, et al. Lipopolysaccharide stimulates platelet secretion and potentiates platelet aggregation via TLR4/MyD88 and the cGMP-dependent protein kinase pathway. J Immunol. Jun 15 2009;182(12):7997–8004
  47. Patrignani P, Di Febbo C, Tacconelli S, Moretta V, Baccante G, Sciulli MG, et al. Reduced thromboxane biosynthesis in carriers of toll-like receptor 4 polymorphisms in vivo. Blood. May 1 2006;107(9):3572–3574
  48. Damas JK, Jensenius M, Ueland T, Otterdal K, Yndestad A, Froland SS, et al. Increased levels of soluble CD40L in African tick bite fever: possible involvement of TLRs in the pathogenic interaction between Rickettsia africae, endothelial cells, and platelets. J Immunol. Aug 15 2006;177(4):2699–2706
  49. Blair P, Rex S, Vitseva O, Beaulieu L, Tanriverdi K, Chakrabarti S, et al. Stimulation of Toll-like receptor 2 in human platelets induces a thromboinflammatory response through activation of phosphoinositide 3-kinase. Circ Res. Feb 13 2009;104(3):346–354
  50. Rex S, Beaulieu LM, Perlman DH, Vitseva O, Blair PS, McComb ME, et al. Immune versus thrombotic stimulation of platelets differentially regulates signalling pathways, intracellular protein-protein interactions, and alpha-granule release. Thromb Haemost. Jul 2009;102(1):97–110

PII: S0049-3848(09)00504-0

doi: 10.1016/j.thromres.2009.11.004

Thrombosis Research
Volume 125, Issue 3 , Pages 205-209 , March 2010