Brucella abortus-infected platelets modulate the activation of neutrophils.

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    • Source:
      Publisher: Wiley Country of Publication: United States NLM ID: 8706300 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1440-1711 (Electronic) Linking ISSN: 08189641 NLM ISO Abbreviation: Immunol Cell Biol Subsets: MEDLINE
    • Publication Information:
      Publication: 2018- : [Hoboken, NJ] : Wiley
      Original Publication: [Adelaide, South Australia] : University of Adelaide, [c1987-
    • Subject Terms:
    • Abstract:
      Brucellosis is a contagious disease caused by bacteria of the genus Brucella. Platelets (PLTs) have been widely involved in the modulation of the immune response. We have previously reported the modulation of Brucella abortus-mediated infection of monocytes. As a result, PLTs cooperate with monocytes and increase their inflammatory capacity, promoting the resolution of the infection. Extending these results, in this study we demonstrate that patients with brucellosis present slightly elevated levels of complexes between PLTs and both monocytes and neutrophils. We then assessed whether PLTs were capable of modulating functional aspects of neutrophils. The presence of PLTs throughout neutrophil infection increased the production of interleukin-8, CD11b surface expression and reactive oxygen species formation, whereas it decreased the expression of CD62L, indicating an activated status of these cells. We next analyzed whether this modulation was mediated by released factors. To discriminate between these options, neutrophils were treated with supernatants collected from B. abortus-infected PLTs. Our results show that CD11b expression was induced by soluble factors of PLTs but direct contact between cell populations was needed to enhance the respiratory burst. Additionally, B. abortus-infected PLTs recruit polymorphonuclear (PMN) cells to the site of infection. Finally, the presence of PLTs did not modify the initial invasion of PMN cells by B. abortus but improved the control of the infection at extended times. Altogether, our results demonstrate that PLTs interact with neutrophils and promote a proinflammatory phenotype which could also contribute to the resolution of the infection.
      (© 2020 Australian and New Zealand Society for Immunology Inc.)
    • References:
      Young EJ. Human brucellosis. Rev Infect Dis 1983; 5: 821-842.
      Moral M. Enfermedades infecciosas: Brucelosis. Vol. 12, Guía para el equipo de salud. Buenos Aires, Argentina: Ministerio de Salud de la Nación Argentina; 2013.
      Baldi PC, Giambartolomei GH. Immunopathology of Brucella infection. Recent Pat Antiinfect Drug Discov 2013; 8: 18-26.
      Sevinc A, Buyukberber N, Camci C, Buyukberber S, Karsligil T. Thrombocytopenia in brucellosis: case report and literature review. J Natl Med Assoc 2005; 97: 290-293.
      Ariza J, Corredoira J, Pallares R, et al. Characteristics of and risk factors for relapse of brucellosis in humans. Clin Infect Dis 1995; 20: 1241-1249.
      Franco MP, Mulder M, Gilman RH, Smits HL. Human brucellosis. Lancet Infect Dis 2007; 7: 775-786.
      Sari I, Altuntas F, Hacioglu S, et al. A multicenter retrospective study defining the clinical and hematological manifestations of brucellosis and pancytopenia in a large series: hematological malignancies, the unusual cause of pancytopenia in patients with brucellosis. Am J Hematol 2008; 83: 334-339.
      Xie S, Zhou Y, Zheng R, et al. Brucella-induced thrombocytopenia: a retrospective study of 16 patients. J Int Med Res 2019; 47: 3008-3013.
      Clemetson KJ. Platelets and primary haemostasis. Thromb Res 2012; 129: 220-224.
      Kahn F, Hurley S, Shannon O. Platelets promote bacterial dissemination in a mouse model of streptococcal sepsis. Microbes Infect 2013; 15: 669-676.
      Gudbrandsdottir S, Hasselbalch HC, Nielsen CH. Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes. J Immunol 2013; 191: 4059-4067.
      Wuescher LM, Takashima A, Worth RG. A novel conditional platelet depletion mouse model reveals the importance of platelets in protection against Staphylococcus aureus bacteremia. J Thromb Haemost 2015; 13: 303-313.
      Aslam R, Speck ER, Kim M, et al. Platelet Toll-like receptor expression modulates lipopolysaccharide-induced thrombocytopenia and tumor necrosis factor-alpha production in vivo. Blood 2006; 107: 637-641.
      Speth C, Loffler J, Krappmann S, Lass-Florl C, Rambach G. Platelets as immune cells in infectious diseases. Futur Microbiol 2013; 8: 1431-1451.
      Semple JW, Italiano JE Jr, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011; 11: 264-274.
      Cognasse F, Hamzeh H, Chavarin P, et al. Evidence of Toll-like receptor molecules on human platelets. Immunol Cell Biol 2005; 83: 196-198.
      Fitzgerald JR, Foster TJ, Cox D. The interaction of bacterial pathogens with platelets. Nat Rev Microbiol 2006; 4: 445-457.
      Ghasemzadeh M, Hosseini E. Platelet-leukocyte crosstalk: linking proinflammatory responses to procoagulant state. Thromb Res 2013; 131: 191-197.
      Li C, Li J, Li Y, et al. Crosstalk between platelets and the immune system: old systems with new discoveries. Adv Hematol 2012; 2012: 384685.
      von Bruhl ML, Stark K, Steinhart A, et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J Exp Med 2012; 209: 819-835.
      Trotta A, Velasquez LN, Milillo MA, et al. Platelets promote Brucella abortus monocyte invasion by establishing complexes with monocytes. Front Immunol 2018; 9: 1000.
      McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 2012; 12: 324-333.
      Barquero-Calvo E, Chaves-Olarte E, Weiss DS, et al. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS One 2007; 2: e631.
      Conde-Álvarez R, Arce-Gorvel V, Iriarte M, et al. The lipopolysaccharide core of Brucella abortus acts as a shield against innate immunity recognition. PLoS Pathog 2012; 8: e1002675.
      Barquero-Calvo E, Martirosyan A, Ordoñez-Rueda D, et al. Neutrophil exert a supressive effect on TH1 responses to intracellular pathogen Brucella abortus. PLoS One 2013; 9: e1003167.
      Gutiérrez-Jiménez C, Mora-Cartín R, Altamirano-Silva P, et al. Neutrophils as trojan horse vehicles for Brucella abortus macrophage infection. Front Immunol 2019; 10: 1012.
      Laskay T, Van Zandbergen G, Solbach W. Neutrophil granulocytes-Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol 2003; 11: 210-214.
      Kreutzer DL, Dreyfus LA, Robertson DC. Interaction of polymorphonuclear leukocytes with smooth and rough strains of Brucella abortus. Infect Immun 1979; 23: 737-742.
      Canning PC, Roth JA, Tabatabai LB, Deyoe BL. Isolation of components of Brucella abortus responsible for inhibition of function in bovine neutrophils. J Infect Dis 1985; 152: 913-921.
      Braude AI. Studies in the pathology and pathogenesis of experimental brucellosis. J Infect Dis 1951; 89: 87-94.
      Ackermann MR, Cheville NF, Deyoe BL. Bovine ileal dome lymphoepithelial cells: endocytosis and transport of Brucella abortus strain 19. Vet Pathol 1988; 25: 28-35.
      Martinez de Tejada G, Pizarro-Cerda J, Moreno E, Moriyón I. The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides. Infect Immun 1995; 63: 3054-3061.
      Zwerdling A, Delpino MV, Pasquevich KA, et al. Brucella abortus activates human neutrophils. Microbes Infect 2009; 11: 689-697.
      Trotta A, Velásquez LN, Milillo MA, et al. Platelets promote Brucella abortus monocyte invasion by establishing complexes with monocytes. Front Immunol 2018; 9: 1000.
      Kim SJ, Jenne CN. Role of platelets in neutrophil extracellular trap (NET) production and tissue injury. Semin Immunol 2016; 28: 546-554.
      Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R. Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 2009; 31: 761-771.
      Silva MT. When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J Leukoc Biol 2010; 87: 93-106.
      Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 2011; 11: 519-531.
      Spörri R, Joller N, Hilbi H, Oxenius A. A novel role for neutrophils as critical activators of NK cells. J Immunol 2008; 181: 7121-7130.
      Yang C-W, Strong BSI, Miller MJ, Unanue ER. Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 2010; 185: 2927-2934.
      Metcalf Pate KA, Lyons CE, Dorsey JL, et al. Platelet activation and platelet-monocyte aggregate formation contribute to decreased platelet count during acute simian immunodeficiency virus infection in pig-tailed macaques. J Infect Dis 2013; 874-883.
      Stevens MG, Pugh GW, Tabatabai LB. Effects of gamma interferon and indomethacin in preventing Brucella abortus infections in mice. Infect Immun 1992; 60: 4407-4409.
      Schmielau J, Finn OJ. Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res 2001; 61: 4756-4760.
      Moore KL, Varki A, McEver RG. GMP-140 binds to a glycoprotein receptor on human neutrophils: evidence for a lectin-like interaction. J Cell Biol 1991; 112: 491-499.
      Larsen E, Palabrica T, Sajer S, et al. PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15). Cell 1990; 63: 467-474.
      Hamburger SA, McEver RP. GMP-140 mediates adhesion of stimulated platelets to neutrophils. Blood 1990; 75: 550-554.
      Moore KL, Patel KD, Bruehl RE, et al. P-selectin glycoprotein ligand-1 mediates rolling of human neutrophils on P-selectin. J Cell Biol 1995; 128: 661-671.
      Page C, Pitchford S. Neutrophil and platelet complexes and their relevance to neutrophil recruitment and activation. Int Immunopharmacol 2013; 17: 1176-1184.
      Blomgran R, Desvignes L, Briken V, Ernst JD. Mycobacterium tuberculosis inhibits neutrophil apoptosis, leading to delayed activation of naive CD4 T cells. Cell Host Microbe 2012; 11: 81-90.
      Cassatella MA. The production of cytokines by polymorphonuclear neutrophils. Immunol Today 1995; 16: 21-26.
      Fernandes DM, Jiang X, Jung JH, Baldwin CL. Comparison of T cell cytokines in resistant and susceptible mice infected with virulent Brucella abortus strain 2308. FEMS Immunol Med Microbiol 1996; 16: 193-203.
      Li N, Hu H, Lindqvist M, et al. Platelet-leukocyte cross talk in whole blood. Arter Thromb Vasc Biol. 2000; 20: 2702-2708.
      Zhu X, Tan Z, Chen J, Zhu M, Xu Y. Effects of ropivacaine on adhesion molecule CD11b expression and function in human neutrophils. Int Immunopharmacol 2010; 10: 662-667.
      Read RA, Moore EE, Moore FA, et al. Platelet-activating factor-induced polymorphonuclear neutrophil priming independent of CD11(B) adhesion. Surgery 1993; 114: 308-313.
      Lishko VK, Yakubenko VP, Ugarova TP, Podolnikova NP. Leukocyte integrin Mac-1 (CD11b/CD18, αMβ2, CR3) acts as a functional receptor for platelet factor 4. J Biol Chem 2018; 293: 6869-6882.
      Tateda K, Moore TA, Deng JC, et al. Early recruitment of neutrophils determines subsequent T1/T2 host responses in a murine model of Legionella pneumophila pneumonia. J Immunol 2001; 166: 3355-3361.
      Fortin CF, Lesur O, Fulop T. Effects of TREM-1 activation in human neutrophils: activation of signaling pathways, recruitment into lipid rafts and association with TLR4. Int Immunol 2007; 19: 41-50.
      Radsak MP, Salih HR, Rammensee H-G, Schild H. Triggering receptor expressed on myeloid cells-1 in neutrophil inflammatory responses: differential regulation of activation and survival. J Immunol 2004; 172: 4956-4963.
      Haselmayer P, Grosse-Hovest L, Von Landenberg P, Schild H, Radsak MP. TREM-1 ligand expression on platelets enhances neutrophil activation. Blood 2007; 110: 1029-1035.
      Kornerup KN, Salmon GP, Pitchford SC, Liu WL, Page CP. Circulating platelet-neutrophil complexes are important for subsequent neutrophil activation and migration. J Appl Physiol 2010; 109: 758-767.
      De Sanctis GT, Wolyniec WW, Green FHY, et al. Reduction of allergic airway responses in P-selectin-deficient mice. J Appl Physiol 1997; 83: 681-687.
      Bengtsson T, Frydén A, Zalavary S, et al. Platelets enhance neutrophil locomotion: evidence for a role of P-selectin. Scand J Clin Lab Invest 1999; 59: 439-449.
      Brandt E, Petersen F, Ludwig A, et al. The β-thromboglobulins and platelet factor 4: blood platelet-derived CXC chemokines with divergent roles in early neutrophil regulation. J Leukoc Biol 2000; 67: 471-478.
      Walz A, Dewald B, von Tscharner V, Baggiolini M. Effects of the neutrophil-activating peptide NAP-2, platelet basic protein, connective tissue-activating peptide III and platelet factor 4 on human neutrophils. J Exp Med 1989; 170: 1745-1750.
      Grommes J, Alard J-E, Drechsler M, et al. Disruption of platelet-derived chemokine heteromers prevents neutrophil extravasation in acute lung injury. Am J Respir Crit Care Med 2012; 185: 628-636.
      Palmantier R, Borgeat P. Thrombin-activated platelets promote leukotriene B4 synthesis in polymorphonuclear leucocytes stimulated by physiological agonists. Br J Pharmacol 1991; 103: 1909-1916.
      Pabuccuoglu O, Ecemis T, El S, et al. Evaluation of serological tests for diagnosis of brucellosis. Jpn J Infect Dis 2011; 64: 272-276.
      Young EJ. Clinical manifestations of human brucellosis. In: Young EJ, Corbel MJ, eds. Brucellosis Clinical and Laboratory Aspects. Boca Raton, FL: CRC Press; 1989:97-126.
      Böyum A. Separation of leukocytes from blood and bone marrow. Introduction. Scand J Clin Lab Investig Suppl 1968; 97: 7.
      Leech M, Hutchinson P, Holdsworth SR, Morand EF. Endogenous glucocorticoids modulate neutrophil migration and synovial P-selectin but not neutrophil phagocytic or oxidative function in experimental arthritis. Clin Exp Immunol 1998; 112: 383-388.
    • Contributed Indexing:
      Keywords: Brucella abortus; brucellosis; early infection; immune complexes; platelets; polymorphonuclear cells
    • Publication Date:
      Date Created: 20200706 Date Completed: 20210824 Latest Revision: 20210824
    • Publication Date:
      20240829
    • Accession Number:
      10.1111/imcb.12373
    • Accession Number:
      32623755