Platelets Promote Macrophage Polarization toward Pro-inflammatory Phenotype and Increase Survival of Septic Mice

Cell Reports

Volumn 28, Issue 4, 2019, Pages 896-908.e5

  Carestia, Agostina ^a,d   Mena, Hebe A ^a   Olexen, Cinthia M ^a   Ortiz Wilczyñski, Juan M ^a   Negrotto, Soledad ^a   Errasti, Andrea E ^b   Gómez, Ricardo M ^c   Jenne, Craig N ^d   Carrera Silva, Eugenio A ^a   Schattner, Mirta ^a  

^a ACADEMIA NACIONAL DE MEDICINA   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSIDAD NACIONAL DE LA PLATA   (Argentina)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD163 ANTIGEN; CD206 ANTIGEN; CD64 ANTIGEN; GLYCOPROTEIN IB; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; LYMPHOCYTE ANTIGEN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ADHESION RECEPTOR; ANTIINFLAMMATORY AGENT; AUTACOID; CYTOKINE; THROMBIN RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL CLEARANCE; BLOOD SAMPLING; CELL CONTACT; CELL CULTURE; CELL FUNCTION; CELL ISOLATION; CELL MIGRATION; CLINICAL OUTCOME; CONTROLLED STUDY; EXPERIMENTAL SEPSIS; FEMALE; FLOW CYTOMETRY; FLUORESCENCE IMAGING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MEMBRANE DEPOLARIZATION; MIDDLE AGED; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN SECRETION; SEPSIS; STAINING; SURVIVAL RATE; THROMBOCYTE TRANSFUSION; ANIMAL; BLOOD; C57BL MOUSE; CELL COMMUNICATION; CELL POLARITY; DRUG EFFECT; INFLAMMATION; METABOLISM; MONOCYTE; PATHOLOGY; SEPTIC SHOCK; SURVIVAL ANALYSIS; THROMBOCYTE;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BLOOD PLATELETS; CD11B ANTIGEN; CELL COMMUNICATION; CELL POLARITY; CYTOKINES; INFLAMMATION; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE, INBRED C57BL; MONOCYTES; NITRIC OXIDE SYNTHASE TYPE II; PHENOTYPE; PLATELET GLYCOPROTEIN GPIB-IX COMPLEX; PLATELET TRANSFUSION; SEPSIS; SHOCK, SEPTIC; SURVIVAL ANALYSIS;

EID: 85068962356     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2019.06.062     Document Type: Article

References (54)

1. Abdelgawwad, M.S., Cao, W., Zheng, L., Kocher, N.K., Williams, L.A., Zheng, X.L., Transfusion of Platelets Loaded With Recombinant ADAMTS13 (A Disintegrin and Metalloprotease With Thrombospondin Type 1 Repeats-13) Is Efficacious for Inhibiting Arterial Thrombosis Associated With Thrombotic Thrombocytopenic Purpura. Arterioscler. Thromb. Vasc. Biol. 38 (2018), 2731–2743.
2. Ali, R.A., Wuescher, L.M., Dona, K.R., Worth, R.G., Platelets Mediate Host Defense against Staphylococcus aureus through Direct Bactericidal Activity and by Enhancing Macrophage Activities. J. Immunol. 198 (2017), 344–351.
3. Banerjee, M., Whiteheart, S.W., The ins and outs of endocytic trafficking in platelet functions. Curr. Opin. Hematol. 24 (2017), 467–474.
4. Bang, K.W., Speck, E.R., Blanchette, V.S., Freedman, J., Semple, J.W., Unique processing pathways within recipient antigen-presenting cells determine IgG immunity against donor platelet MHC antigens. Blood 95 (2000), 1735–1742.
5. Bevers, E.M., Comfurius, P., Zwaal, R.F., Changes in membrane phospholipid distribution during platelet activation. Biochim. Biophys. Acta 736 (1983), 57–66.
6. Bosurgi, L., Cao, Y.G., Cabeza-Cabrerizo, M., Tucci, A., Hughes, L.D., Kong, Y., Weinstein, J.S., Licona-Limon, P., Schmid, E.T., Pelorosso, F., et al. Macrophage function in tissue repair and remodeling requires IL-4 or IL-13 with apoptotic cells. Science 356 (2017), 1072–1076.
7. Carestia, A., Kaufman, T., Rivadeneyra, L., Landoni, V.I., Pozner, R.G., Negrotto, S., D'Atri, L.P., Gómez, R.M., Schattner, M., Mediators and molecular pathways involved in the regulation of neutrophil extracellular trap formation mediated by activated platelets. J. Leukoc. Biol. 99 (2016), 153–162.
8. Carrera Silva, E.A., Chan, P.Y., Joannas, L., Errasti, A.E., Gagliani, N., Bosurgi, L., Jabbour, M., Perry, A., Smith-Chakmakova, F., Mucida, D., et al. T cell-derived protein S engages TAM receptor signaling in dendritic cells to control the magnitude of the immune response. Immunity 39 (2013), 160–170.
9. Claushuis, T.A.M., van Vught, L.A., Scicluna, B.P., Wiewel, M.A., Klein Klouwenberg, P.M.C., Hoogendijk, A.J., Ong, D.S.Y., Cremer, O.L., Horn, J., Franitza, M., et al., Molecular Diagnosis and Risk Stratification of Sepsis Consortium. Thrombocytopenia is associated with a dysregulated host response in critically ill sepsis patients. Blood 127 (2016), 3062–3072.
10. Cloutier, N., Allaeys, I., Marcoux, G., Machlus, K.R., Mailhot, B., Zufferey, A., Levesque, T., Becker, Y., Tessandier, N., Melki, I., et al. Platelets release pathogenic serotonin and return to circulation after immune complex-mediated sequestration. Proc. Natl. Acad. Sci. USA 115 (2018), E1550–E1559.
11. de Stoppelaar, S.F., van ’t Veer, C., Claushuis, T.A.M., Albersen, B.J.A., Roelofs, J.J.T.H., van der Poll, T., Thrombocytopenia impairs host defense in gram-negative pneumonia-derived sepsis in mice. Blood 124 (2014), 3781–3790.
12. Deppermann, C., Kubes, P., Platelets and infection. Semin. Immunol. 28 (2016), 536–545.
13. Dewitte, A., Lepreux, S., Villeneuve, J., Rigothier, C., Combe, C., Ouattara, A., Ripoche, J., Blood platelets and sepsis pathophysiology: A new therapeutic prospect in critical ill patients?. Ann. Intensive Care, 7, 2017, 115.
14. Giangola, M.D., Yang, W.-L., Rajayer, S.R., Nicastro, J., Coppa, G.F., Wang, P., Growth arrest-specific protein 6 attenuates neutrophil migration and acute lung injury in sepsis. Shock 40 (2013), 485–491.
15. Gleissner, C.A., Macrophage Phenotype Modulation by CXCL4 in Atherosclerosis. Front. Physiol. 3 (2012), 1–7.
16. Gudbrandsdottir, S., Hasselbalch, H.C., Nielsen, C.H., Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes. J. Immunol. 191 (2013), 4059–4067.
17. Halvorsen, B., Smedbakken, L.M., Michelsen, A.E., Skjelland, M., Bjerkeli, V., Sagen, E.L., Taskén, K., Bendz, B., Gullestad, L., Holm, S., et al. Activated platelets promote increased monocyte expression of CXCR5 through prostaglandin E2-related mechanisms and enhance the anti-inflammatory effects of CXCL13. Atherosclerosis 234 (2014), 352–359.
18. Hamzeh-Cognasse, H., Damien, P., Chabert, A., Pozzetto, B., Cognasse, F., Garraud, O., Platelets and infections - complex interactions with bacteria. Front. Immunol., 6, 2015, 82.
19. Kapur, R., Semple, J.W., Platelets as immune-sensing cells. Blood Adv. 1 (2016), 10–14.
20. Kapur, R., Zufferey, A., Boilard, E., Semple, J.W., Nouvelle cuisine: platelets served with inflammation. J. Immunol. 194 (2015), 5579–5587.
21. Klement, G.L., Yip, T.-T., Cassiola, F., Kikuchi, L., Cervi, D., Podust, V., Italiano, J.E., Wheatley, E., Abou-Slaybi, A., Bender, E., et al. Platelets actively sequester angiogenesis regulators. Blood 113 (2009), 2835–2842.
22. Koupenova, M., Clancy, L., Corkrey, H.A., Freedman, J.E., Circulating Platelets as Mediators of Immunity, Inflammation, and Thrombosis. Circ. Res. 122 (2018), 337–351.
23. Kraemer, B.F., Campbell, R.A., Schwertz, H., Cody, M.J., Franks, Z., Tolley, N.D., Kahr, W.H.A., Lindemann, S., Seizer, P., Yost, C.C., et al. Novel anti-bacterial activities of β-defensin 1 in human platelets: suppression of pathogen growth and signaling of neutrophil extracellular trap formation. PLoS Pathog., 7, 2011, e1002355.
24. Kral, J.B., Schrottmaier, W.C., Salzmann, M., Assinger, A., Platelet Interaction with Innate Immune Cells. Transfus. Med. Hemother. 43 (2016), 78–88.
25. Li, J.L., Zarbock, A., Hidalgo, A., Platelets as autonomous drones for hemostatic and immune surveillance. J. Exp. Med. 214 (2017), 2193–2204.
26. 2 and Cytokines. Mediators Inflamm., 2017, 2017, 1463216.
27. Martinez, F.O., Gordon, S., The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep., 6, 2014, 13.
28. Mena, H.A., Lokajczyk, A., Dizier, B., Strier, S.E., Voto, L.S., Boisson-Vidal, C., Schattner, M., Negrotto, S., Acidic preconditioning improves the proangiogenic responses of endothelial colony forming cells. Angiogenesis 17 (2014), 867–879.
29. Murray, P.J., Macrophage Polarization. Annu. Rev. Physiol. 79 (2017), 541–566.
30. Murray, P.J., Allen, J.E., Biswas, S.K., Fisher, E.A., Gilroy, D.W., Goerdt, S., Gordon, S., Hamilton, J.A., Ivashkiv, L.B., Lawrence, T., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41 (2014), 14–20.
31. Pierre, S., Linke, B., Suo, J., Tarighi, N., Del Turco, D., Thomas, D., Ferreiros, N., Stegner, D., Frölich, S., Sisignano, M., et al. GPVI and Thromboxane Receptor on Platelets Promote Proinflammatory Macrophage Phenotypes during Cutaneous Inflammation. J. Invest. Dermatol. 137 (2017), 686–695.
32. Rittirsch, D., Huber-Lang, M.S., Flierl, M.A., Ward, P.A., Immunodesign of experimental sepsis by cecal ligation and puncture. Nat. Protoc. 4 (2009), 31–36.
33. Rivadeneyra, L., Carestia, A., Etulain, J., Pozner, R.G., Fondevila, C., Negrotto, S., Schattner, M., Regulation of platelet responses triggered by Toll-like receptor 2 and 4 ligands is another non-genomic role of nuclear factor-kappaB. Thromb. Res. 133 (2014), 235–243.
34. Rivadeneyra, L., Pozner, R.G., Meiss, R., Fondevila, C., Gómez, R.M., Schattner, M., Poly (I:C) downregulates platelet production and function through type I interferon. Thromb. Haemost. 114 (2015), 982–993.
35. Rondina, M.T., Carlisle, M., Fraughton, T., Brown, S.M., Miller, R.R. 3rd, Harris, E.S., Weyrich, A.S., Zimmerman, G.A., Supiano, M.A., Grissom, C.K., Platelet-monocyte aggregate formation and mortality risk in older patients with severe sepsis and septic shock. J. Gerontol. A Biol. Sci. Med. Sci. 70 (2015), 225–231.
36. Rothlin, C.V., Carrera-Silva, E.A., Bosurgi, L., Ghosh, S., TAM receptor signaling in immune homeostasis. Annu. Rev. Immunol. 33 (2015), 355–391.
37. Sayeh, E., Sterling, K., Speck, E., Freedman, J., Semple, J.W., IgG antiplatelet immunity is dependent on an early innate natural killer cell-derived interferon-gamma response that is regulated by CD8+ T cells. Blood 103 (2004), 2705–2709.
38. Scheuerer, B., Ernst, M., Dürrbaum-Landmann, I., Fleischer, J., Grage-Griebenow, E., Brandt, E., Flad, H.D., Petersen, F., The CXC-chemokine platelet factor 4 promotes monocyte survival and induces monocyte differentiation into macrophages. Blood 95 (2000), 1158–1166.
39. Schwarz, H.P., Heeb, M.J., Wencel-Drake, J.D., Griffin, J.H., Identification and quantitation of protein S in human platelets. Blood 66 (1985), 1452–1455.
40. Scull, C.M., Hays, W.D., Fischer, T.H., Macrophage pro-inflammatory cytokine secretion is enhanced following interaction with autologous platelets. J. Inflamm. (Lond.), 7, 2010, 53.
41. Semple, J.W., Speck, E.R., Milev, Y.P., Blanchette, V., Freedman, J., Indirect allorecognition of platelets by T helper cells during platelet transfusions correlates with anti-major histocompatibility complex antibody and cytotoxic T lymphocyte formation. Blood 86 (1995), 805–812.
42. Semple, J.W., Italiano, J.E. Jr., Freedman, J., Platelets and the immune continuum. Nat. Rev. Immunol. 11 (2011), 264–274.
43. Shi, C., Zhang, X., Chen, Z., Sulaiman, K., Feinberg, M.W., Ballantyne, C.M., Jain, M.K., Simon, D.I., Integrin engagement regulates monocyte differentiation through the forkhead transcription factor Foxp1. J. Clin. Invest. 114 (2004), 408–418.
44. Shi, C., Sakuma, M., Mooroka, T., Liscoe, A., Gao, H., Croce, K.J., Sharma, A., Kaplan, D., Greaves, D.R., Wang, Y., Simon, D.I., Down-regulation of the forkhead transcription factor Foxp1 is required for monocyte differentiation and macrophage function. Blood 112 (2008), 4699–4711.
45. Simon, D.I., Chen, Z., Xu, H., Li, C.Q., Dong, Jf., McIntire, L.V., Ballantyne, C.M., Zhang, L., Furman, M.I., Berndt, M.C., López, J.A., Platelet glycoprotein ibalpha is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J. Exp. Med. 192 (2000), 193–204.
46. Tiemessen, M.M., Jagger, A.L., Evans, H.G., van Herwijnen, M.J.C., John, S., Taams, L.S., CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc. Natl. Acad. Sci. USA 104 (2007), 19446–19451.
47. Vallance, T.M., Zeuner, M.-T., Williams, H.F., Widera, D., Vaiyapuri, S., Toll-Like Receptor 4 Signalling and Its Impact on Platelet Function, Thrombosis, and Haemostasis. Mediators Inflamm., 2017, 2017, 9605894.
48. Vogel, S., Rath, D., Borst, O., Mack, A., Loughran, P., Lotze, M.T., Neal, M.D., Billiar, T.R., Gawaz, M., Platelet-derived high-mobility group box 1 promotes recruitment and suppresses apoptosis of monocytes. Biochem. Biophys. Res. Commun. 478 (2016), 143–148.
49. Wang, Y., Gao, H., Shi, C., Erhardt, P.W., Pavlovsky, A., A Soloviev, D., Bledzka, K., Ustinov, V., Zhu, L., Qin, J., et al. Leukocyte integrin Mac-1 regulates thrombosis via interaction with platelet GPIbα. Nat. Commun., 8, 2017, 15559.
50. Weyrich, A.S., Elstad, M.R., McEver, R.P., McIntyre, T.M., Moore, K.L., Morrissey, J.H., Prescott, S.M., Zimmerman, G.A., Activated platelets signal chemokine synthesis by human monocytes. J. Clin. Invest. 97 (1996), 1525–1534.
51. Wong, C.H.Y., Jenne, C.N., Petri, B., Chrobok, N.L., Kubes, P., Nucleation of platelets with blood-borne pathogens on Kupffer cells precedes other innate immunity and contributes to bacterial clearance. Nat. Immunol. 14 (2013), 785–792.
52. Wuescher, L.M., Takashima, A., Worth, R.G., A novel conditional platelet depletion mouse model reveals the importance of platelets in protection against Staphylococcus aureus bacteremia. J. Thromb. Haemost. 13 (2015), 303–313.
53. Xiang, B., Zhang, G., Guo, L., Li, X.-A., Morris, A.J., Daugherty, A., Whiteheart, S.W., Smyth, S.S., Li, Z., Platelets protect from septic shock by inhibiting macrophage-dependent inflammation via the cyclooxygenase 1 signalling pathway. Nat. Commun., 4, 2013, 2657.
54. Zagórska, A., Través, P.G., Lew, E.D., Dransfield, I., Lemke, G., Diversification of TAM receptor tyrosine kinase function. Nat. Immunol. 15 (2014), 920–928.