Ectosomes from neutrophil-like cells down-regulate nickel-induced dendritic cell maturation and promote Th2 polarization

Journal of Leukocyte Biology

Volumn 97, Issue 4, 2015, Pages 737-749

  Turbica, Isabelle ^a,c   Gallais, Yann ^a,c   Gueguen, Claire ^d   Tharinger, Hugo ^b   Sabbagh, Chantal Al ^c,e   Gorges, Roseline ^a,c   Gary Gouy, Hélène ^b   Kerdine Römer, Saadia ^a,c   Pallardy, Marc ^a,c   Mascarell, Laurent ^d   Gleizes, Aude ^a,c   Chollet Martin, Sylvie ^a,c,f  

^a INSERM   (France)

^b IPSIT   (France)

^c PRES UniverSud Paris   (France)

^d Stallergenes SA   (France)

^e UNIV PARIS SUD   (France)

^f BICHAT HOSPITAL   (France)

Author keywords

Chemical sensitizer; Contact dermatitis; Inflammation regulation; Microparticles

Indexed keywords

ALLERGEN; B7 ANTIGEN; BIOLOGICAL MARKER; CD4 ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; HLA DR ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12P40; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; NICKEL; PROGRAMMED DEATH 1 LIGAND 1; PROTEIN NMES1; TRANSCRIPTION FACTOR EMX1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CD274 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; LIPOSOME; LYMPHOKINE; NICKEL SULFATE; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 4;

ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL ORGANELLE; CELL POLARITY; COCULTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; ECTOSOME; EFFECTOR CELL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INTERNALIZATION; LYSOSOME; MARKER GENE; NEUTROPHIL; PRIORITY JOURNAL; TH2 CELL; ACUTE MYELOBLASTIC LEUKEMIA; AGONISTS; BIOSYNTHESIS; BONE MARROW CELL; CYTOLOGY; DERMATITIS, ALLERGIC CONTACT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MEMBRANE MICROPARTICLE; MONOCYTE; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

NISO;

ALLERGENS; ANTIGENS, CD; ANTIGENS, CD274; CELL DIFFERENTIATION; CELL-DERIVED MICROPARTICLES; COCULTURE TECHNIQUES; DENDRITIC CELLS; DERMATITIS, ALLERGIC CONTACT; GENE EXPRESSION REGULATION; HLA-DR ANTIGENS; HUMANS; LEUKEMIA, MYELOID, ACUTE; LIPOSOMES; LYMPHOKINES; MONOCYTES; MYELOID CELLS; NEUTROPHILS; NICKEL; TH2 CELLS; TOLL-LIKE RECEPTOR 4;

EID: 84929192523     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0314-132RR     Document Type: Article

References (73)

1. Kaplan, D. H., Igyártó, B. Z., Gaspari, A. A. (2012) Early immune events in the induction of allergic contact dermatitis. Nat. Rev. Immunol. 12, 114–124.
2. Martin, S. F. (2012) Allergic contact dermatitis: xenoinflammation of the skin. Curr. Opin. Immunol. 24, 720–729.
3. Raghavan, B., Martin, S. F., Esser, P. R., Goebeler, M., Schmidt, M. (2012) Metal allergens nickel and cobalt facilitate TLR4 homodimerization independently of MD 2. EMBO Rep. 13, 1109–1115.
4. Schmidt, M., Raghavan, B., Müller, V., Vogl, T., Fejer, G., Tchaptchet, S., Keck, S., Kalis, C., Nielsen, P. J., Galanos, C., Roth, J., Skerra, A., Martin, S. F., Freudenberg, M. A., Goebeler, M. (2010) Crucial role for human Toll-like receptor 4 in the development of contact allergy to nickel. Nat. Immunol. 11, 814–819.
5. Antonios, D., Ade, N., Kerdine-Römer, S., Assaf-Vandecasteele, H., Larangé, A., Azouri, H., Pallardy, M. (2009) Metallic haptens induce differential phenotype of human dendritic cells through activation of mitogen-activated protein kinase and NF-kappaB pathways. Toxicol. In Vitro 23, 227–234.
6. Antonios, D., Rousseau, P., Larangé, A., Kerdine-Römer, S., Pallardy, M. (2010) Mechanisms of IL-12 synthesis by human dendritic cells treated with the chemical sensitizer NiSO 4. J. Immunol. 185, 89–98.
7. Engeman, T., Gorbachev, A. V., Kish, D. D., Fairchild, R. L. (2004) The intensity of neutrophil infiltration controls the number of antigen-primed CD8 T cells recruited into cutaneous antigen challenge sites. J. Leukoc. Biol. 76, 941–949.
8. Vocanson, M., Hennino, A., Roziéres, A., Poyet, G., Nicolas, J. F. (2009) Effector and regulatory mechanisms in allergic contact dermatitis. Allergy 64, 1699–1714.
9. Martin, S. F. (2012) Contact dermatitis: from pathomechanisms to immunotoxicology. Exp. Dermatol. 21, 382–389.
10. Martin, S. F., Esser, P. R., Weber, F. C., Jakob, T., Freudenberg, M. A., Schmidt, M., Goebeler, M. (2011) Mechanisms of chemical-induced innate immunity in allergic contact dermatitis. Allergy 66, 1152–1163.
11. Nauseef, W. M., Borregaard, N. (2014) Neutrophils at work. Nat. Immunol. 15, 602–611.
12. Jönsson, F., Mancardi, D. A., Albanesi, M., Bruhns, P. (2013) Neutrophils in local and systemic antibody-dependent inflammatory and anaphylactic reactions. J. Leukoc. Biol. 94, 643–656.
13. Kolaczkowska, E., Kubes, P. (2013) Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175.
14. Schuster, S., Hurrell, B., Tacchini-Cottier, F. (2013) Crosstalk between neutrophils and dendritic cells: a context-dependent process. J. Leukoc. Biol. 94, 671–675.
15. Mantovani, A., Cassatella, M. A., Costantini, C., Jaillon, S. (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519–531.
16. Van Gisbergen, K. P., Geijtenbeek, T. B., van Kooyk, Y. (2005) Close encounters of neutrophils and DCs. Trends Immunol. 26, 626–631.
17. Yang, D., de la Rosa, G., Tewary, P., Oppenheim, J. J. (2009) Alarmins link neutrophils and dendritic cells. Trends Immunol. 30, 531–537.
18. Barrientos, L., Bignon, A., Gueguen, C., de Chaisemartin, L., Gorges, R., Sandré, C., Mascarell, L., Balabanian, K., Kerdine-Römer, S., Pallardy, M., Marin-Esteban, V., Chollet-Martin, S. (2014) Neutrophil extracellular traps downregulate lipopolysaccharide-induced activation of monocytederived dendritic cells. J. Immunol. 193, 5689–5698.
19. Eken, C., Gasser, O., Zenhaeusern, G., Oehri, I., Hess, C., Schifferli, J. A. (2008) Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J. Immunol. 180, 817–824.
20. Cocucci, E., Racchetti, G., Meldolesi, J. (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol. 19, 43–51.
21. Mause, S. F., Weber, C. (2010) Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 107, 1047–1057.
22. Théry, C., Ostrowski, M., Segura, E. (2009) Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581–593.
23. Van der Pol, E., Böing, A. N., Harrison, P., Sturk, A., Nieuwland, R. (2012) Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol. Rev. 64, 676–705.
24. Angelillo-Scherrer, A. (2012) Leukocyte-derived microparticles in vascular homeostasis. Circ. Res. 110, 356–369.
25. Burger, D., Schock, S., Thompson, C. S., Montezano, A. C., Hakim, A. M., Touyz, R. M. (2013) Microparticles: biomarkers and beyond. Clin. Sci. 124, 423–441.
26. Morel, O., Morel, N., Jesel, L., Freyssinet, J. M., Toti, F. (2011) Microparticles: a critical component in the nexus between inflammation, immunity, and thrombosis. Semin. Immunopathol. 33, 469–486.
27. Montoro-García, S., Shantsila, E., Marín, F., Blann, A., Lip, G. Y. (2011) Circulating microparticles: new insights into the biochemical basis of microparticle release and activity. Basic Res. Cardiol. 106, 911–923.
28. Beyer, C., Pisetsky, D. S. (2010) The role of microparticles in the pathogenesis of rheumatic diseases. Nat. Rev. Rheumatol. 6, 21–29.
29. György, B., Szabó, T. G., Turiák, L., Wright, M., Herczeg, P., Lédeczi, Z., Kittel, A., Polgár, A., Tóth, K., Dérfalvi, B., Zelenák, G., Böröcz, I., Carr, B., Nagy, G., Vékey, K., Gay, S., Falus, A., Buzás, E. I. (2012) Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases. PLoS ONE 7, e49726.
30. Huisse, M. G., Pease, S., Hurtado-Nedelec, M., Arnaud, B., Malaquin, C., Wolff, M., Gougerot-Pocidalo, M. A., Kermarrec, N., Bezeaud, A., Guillin, M. C., Paoletti, X., Chollet-Martin, S. (2008) Leukocyte activation: the link between inflammation and coagulation during heatstroke. A study of patients during the 2003 heat wave in Paris. Crit. Care Med. 36, 2288–2295.
31. Muralidharan-Chari, V., Clancy, J. W., Sedgwick, A., D’Souza-Schorey, C. (2010) Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123, 1603–1611.
32. Pisetsky, D. S., Gauley, J., Ullal, A. J. (2011) Microparticles as a source of extracellular DNA. Immunol. Res. 49, 227–234.
33. Ardoin, S. P., Shanahan, J. C., Pisetsky, D. S. (2007) The role of microparticles in inflammation and thrombosis. Scand. J. Immunol. 66, 159–165.
34. Kornek, M., Lynch, M., Mehta, S. H., Lai, M., Exley, M., Afdhal, N. H., Schuppan, D. (2012) Circulating microparticles as disease-specific biomarkers of severity of inflammation in patients with hepatitis C or nonalcoholic steatohepatitis. Gastroenterology 143, 448–458.
35. Reid, V. L., Webster, N. R. (2012) Role of microparticles in sepsis. Br. J. Anaesth. 109, 503–513.
36. Timár, C. I., Lorincz, A. M., Csépányi-Kömi, R., Vályi-Nagy, A., Nagy, G., Buzás, E. I., Iványi, Z., Kittel, A., Powell, D. W., McLeish, K. R., Ligeti, E. (2013) Antibacterial effect of microvesicles released from human neutrophilic granulocytes. Blood 121, 510–518.
37. Sadallah, S., Eken, C., Schifferli, J. A. (2011) Ectosomes as immunomodulators. Semin. Immunopathol. 33, 487–495.
38. Sadallah, S., Eken, C., Schifferli, J. A. (2011) Ectosomes as modulators of inflammation and immunity. Clin. Exp. Immunol. 163, 26–32.
39. Pliyev, B. K., Kalintseva, M. V., Abdulaeva, S. V., Yarygin, K. N., Savchenko, V. G. (2014) Neutrophil microparticles modulate cytokine production by natural killer cells. Cytokine 65, 126–129.
40. Dalli, J., Norling, L. V., Renshaw, D., Cooper, D., Leung, K. Y., Perretti, M. (2008) Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 112, 2512–2519.
41. Eken, C., Martin, P. J., Sadallah, S., Treves, S., Schaller, M., Schifferli, J. A. (2010) Ectosomes released by polymorphonuclear neutrophils induce a MerTK-dependent anti-inflammatory pathway in macrophages. J. Biol. Chem. 285, 39914–39921.
42. Eken, C., Sadallah, S., Martin, P. J., Treves, S., Schifferli, J. A. (2013) Ectosomes of polymorphonuclear neutrophils activate multiple signaling pathways in macrophages. Immunobiology 218, 382–392.
43. Duarte, T. A., Noronha-Dutra, A. A., Nery, J. S., Ribeiro, S. B., Pitanga, T. N., Lapa E Silva, J. R., Arruda, S., Boéchat, N. (2012) Mycobacterium tuberculosis-induced neutrophil ectosomes decrease macrophage activation. Tuberculosis (Edinb.) 92, 218–225.
44. Sémiramoth, N., Gleizes, A., Turbica, I., Sandré, C., Gorges, R., Kansau, I., Servin, A., Chollet-Martin, S. (2009) Escherichia coli type 1 pili trigger late IL-8 production by neutrophil-like differentiated PLB-985 cells through a Src family kinase- and MAPK-dependent mechanism. J. Leukoc. Biol. 85, 310–321.
45. Bangham, A. D., Standish, M. M., Watkins, J. C. (1965) Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 13, 238–252.
46. Frey, B., Gaipl, U. S. (2011) The immune functions of phosphatidylserine in membranes of dying cells and microvesicles. Semin. Immunopathol. 33, 497–516.
47. Lygre, H., Moe, G., Skålevik, R., Holmsen, H. (2003) Interaction of triclosan with eukaryotic membrane lipids. Eur. J. Oral Sci. 111, 216–222.
48. Zimmer, A., Bouley, J., Le Mignon, M., Pliquet, E., Horiot, S., Turfkruyer, M., Baron-Bodo, V., Horak, F., Nony, E., Louise, A., Moussu, H., Mascarell, L., Moingeon, P. (2012) A regulatory dendritic cell signature correlates with the clinical efficacy of allergen-specific sublingual immunotherapy. J. Allergy Clin. Immunol. 129, 1020–1030.
49. Larangé, A., Antonios, D., Pallardy, M., Kerdine-Römer, S. (2009) TLR7 and TLR8 agonists trigger different signaling pathways for human dendritic cell maturation. J. Leukoc. Biol. 85, 673–683.
50. Van der Pol, E., Hoekstra, A. G., Sturk, A., Otto, C., van Leeuwen, T. G., Nieuwland, R. (2010) Optical and non-optical methods for detection and characterization of microparticles and exosomes. J. Thromb. Haemost. 8, 2596–2607.
51. Van Ierssel, S. H., Van Craenenbroeck, E. M., Conraads, V. M., Van Tendeloo, V. F., Vrints, C. J., Jorens, P. G., Hoymans, V. Y. (2010) Flow cytometric detection of endothelial microparticles (EMP): effects of centrifugation and storage alter with the phenotype studied. Thromb. Res. 125, 332–339.
52. Ayers, L., Kohler, M., Harrison, P., Sargent, I., Dragovic, R., Schaap, M., Nieuwland, R., Brooks, S. A., Ferry, B. (2011) Measurement of circulating cell-derived microparticles by flow cytometry: sources of variability within the assay. Thromb. Res. 127, 370–377.
53. Thery, C., Amigorena, S., Raposo, G., Clayton, A. (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3, Unit 3 22.
54. Heijnen, H. F., Schiel, A. E., Fijnheer, R., Geuze, H. J., Sixma, J. J. (1999) Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94, 3791–3799.
55. Jy, W., Minagar, A., Jimenez, J. J., Sheremata, W. A., Mauro, L. M., Horstman, L. L., Bidot, C., Ahn, Y. S. (2004) Endothelial microparticles (EMP) bind and activate monocytes: elevated EMP-monocyte conjugates in multiple sclerosis. Front. Biosci. 9, 3137–3144.
56. Van der Pol, E., van Gemert, M. J., Sturk, A., Nieuwland, R., van Leeuwen, T. G. (2012) Single vs. swarm detection of microparticles and exosomes by flow cytometry. J. Thromb. Haemost. 10, 919–930.
57. Gasser, O., Hess, C., Miot, S., Deon, C., Sanchez, J. C., Schifferli, J. A. (2003) Characterisation and properties of ectosomes released by human polymorphonuclear neutrophils. Exp. Cell Res. 285, 243–257.
58. Shet, A. S. (2008) Characterizing blood microparticles: technical aspects and challenges. Vasc. Health Risk Manag. 4, 769–774.
59. Larson, M. C., Woodliff, J. E., Hillery, C. A., Kearl, T. J., Zhao, M. (2012) Phosphatidylethanolamine is externalized at the surface of microparticles. Biochim. Biophys. Acta 1821, 1501–1507.
60. Yuana, Y., Oosterkamp, T. H., Bahatyrova, S., Ashcroft, B., Garcia Rodriguez, P., Bertina, R. M., Osanto, S. (2010) Atomic force microscopy: a novel approach to the detection of nanosized blood microparticles. J. Thromb. Haemost. 8, 315–323.
61. Lacroix, R., Robert, S., Poncelet, P., Kasthuri, R. S., Key, N. S., Dignat- George, F.; ISTH SSC Workshop. (2010) Standardization of plateletderived microparticle enumeration by flow cytometry with calibrated beads: results of the International Society on Thrombosis and Haemostasis SSC Collaborative workshop. J. Thromb. Haemost. 8, 2571–2574.
62. Gasser, O., Schifferli, J. A. (2004) Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 104, 2543–2548.
63. Faille, D., El-Assaad, F., Mitchell, A. J., Alessi, M. C., Chimini, G., Fusai, T., Grau, G. E., Combes, V. (2012) Endocytosis and intracellular processing of platelet microparticles by brain endothelial cells. J. Cell. Mol. Med. 16, 1731–1738.
64. Aiba, S., Manome, H., Nakagawa, S., Mollah, Z. U., Mizuashi, M., Ohtani, T., Yoshino, Y., Tagami, H. (2003) P38 Mitogen-activated protein kinase and extracellular signal-regulated kinases play distinct roles in the activation of dendritic cells by two representative haptens, NiCl2 and 2,4- dinitrochlorobenzene. J. Invest. Dermatol. 120, 390–399.
65. Ade, N., Antonios, D., Kerdine-Romer, S., Boisleve, F., Rousset, F., Pallardy, M. (2007) NF-kappaB plays a major role in the maturation of human dendritic cells induced by NiSO(4) but not by DNCB. Toxicol. Sci. 99, 488–501.
66. Sadallah, S., Eken, C., Martin, P. J., Schifferli, J. A. (2011) Microparticles (ectosomes) shed by stored human platelets downregulate macrophages and modify the development of dendritic cells. J. Immunol. 186, 6543–6552.
67. Hitzler, M., Majdic, O., Heine, G., Worm, M., Ebert, G., Luch, A., Peiser, M. (2012) Human Langerhans cells control Th cells via programmed death-ligand 1 in response to bacterial stimuli and nickel-induced contact allergy. PLoS ONE 7, e46776.
68. Williams, E. H., Williams, C. A., McLeod, J. D. (2010) Identification of PDL-1 as a novel biomarker of sensitizer exposure in dendritic-like cells. Toxicol. In Vitro 24, 1727–1735.
69. Chen, X., Doffek, K., Sugg, S. L., Shilyansky, J. (2004) Phosphatidylserine regulates the maturation of human dendritic cells. J. Immunol. 173, 2985–2994.
70. Doffek, K., Chen, X., Sugg, S. L., Shilyansky, J. (2011) Phosphatidylserine inhibits NFkB and p38 MAPK activation in human monocyte derived dendritic cells. Mol. Immunol. 48, 1771–1777.
71. Moed, H., Boorsma, D. M., Stoof, T. J., von Blomberg, B. M., Bruynzeel, D. P., Scheper, R. J., Gibbs, S., Rustemeyer, T. (2004) Nickel-responding T cells are CD4+ CLA+ CD45RO+ and express chemokine receptors CXCR3, CCR4 and CCR 10. Br. J. Dermatol. 151, 32–41.
72. Jakobson, E., Masjedi, K., Ahlborg, N., Lundeberg, L., Karlberg, A. T., Scheynius, A. (2002) Cytokine production in nickel-sensitized individuals analysed with enzyme-linked immunospot assay: possible implication for diagnosis. Br. J. Dermatol. 147, 442–449.
73. Minang, J. T., Troye-Blomberg, M., Lundeberg, L., Ahlborg, N. (2005) Nickel elicits concomitant and correlated in vitro production of Th1-, Th2-type and regulatory cytokines in subjects with contact allergy to nickel. Scand. J. Immunol. 62, 289–296.