extracellular vesicles; inflammation; neutrophils; therapy; Anti-Inflammatory Agents; Nucleic Acids; Lipids; Humans; Neutrophils/metabolism; Inflammation/metabolism; Anti-Inflammatory Agents/metabolism; Extracellular Vesicles/metabolism; Nucleic Acids/metabolism; Biochemistry, Genetics and Molecular Biology (all); General Medicine
Résumé :
[en] Extracellular vesicles (EVs) are released in the extracellular environment during cell activation or apoptosis. Working as signal transducers, EVs are important mediators of intercellular communication through the convoying of proteins, nucleic acids, lipids, and metabolites. Neutrophil extracellular vesicles (nEVs) contain molecules acting as key modulators of inflammation and immune responses. Due to their potential as therapeutic tools, studies about nEVs have been increasing in recent years. However, our knowledge about nEVs is still in its infancy. In this review, we summarize the current understanding of the role of nEVs in the framework of neutrophil inflammation functions and disease development. The therapeutic potential of nEVs as clinical treatment strategies is deeply discussed. Moreover, the promising research landscape of nEVs in the near future is also examined.
Disciplines :
Biochimie, biophysique & biologie moléculaire
Auteur, co-auteur :
ZHOU, Yang ; University of Luxembourg > Faculty of Science, Technology and Medicine > Department of Life Sciences and Medicine > Team Jean-Luc BUEB
BRECHARD, Sabrina ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Life Sciences and Medicine (DLSM)
Co-auteurs externes :
no
Langue du document :
Anglais
Titre :
Neutrophil Extracellular Vesicles: A Delicate Balance between Pro-Inflammatory Responses and Anti-Inflammatory Therapies.
This work was supported by the University of Luxembourg and the Fonds National de la Recherche through the PRIDE/11012546/NEXTIMMUNE FNR-PRIDE Doctoral Training Unit program NEXTIMMUNE (PRIDE/11012546/NEXTIMMUNE).
Chargaff E. West R. The Biological Significance of the Thromboplastic Protein of Blood J. Biol. Chem. 1946 166 189 197 10.1016/S0021-9258(17)34997-9
Aaronson S. Behrens U. Orner R. Haines T.H. Ultrastructure of Intracellular and Extracellular Vesicles, Membranes, and Myelin Figures Produced by Ochromonas Danica J. Ultrastruct. Res. 1971 35 418 430 10.1016/S0022-5320(71)80003-5
Wolf P. The Nature and Significance of Platelet Products in Human Plasma Br. J. Haematol. 1967 13 269 288 10.1111/j.1365-2141.1967.tb08741.x
Pitt J.M. Kroemer G. Zitvogel L. Extracellular Vesicles: Masters of Intercellular Communication and Potential Clinical Interventions J. Clin. Investig. 2016 126 1139 1143 10.1172/JCI87316
Berumen Sánchez G. Bunn K.E. Pua H.H. Rafat M. Extracellular Vesicles: Mediators of Intercellular Communication in Tissue Injury and Disease Cell Commun. Signal. 2021 19 104 10.1186/s12964-021-00787-y
Avalos P.N. Forsthoefel D.J. An Emerging Frontier in Intercellular Communication: Extracellular Vesicles in Regeneration Front. Cell Dev. Biol. 2022 10 849905 10.3389/fcell.2022.849905
van der Pol E. Böing A.N. Harrison P. Sturk A. Nieuwland R. Classification, Functions, and Clinical Relevance of Extracellular Vesicles Pharmacol. Rev. 2012 64 676 705 10.1124/pr.112.005983
Cocozza F. Grisard E. Martin-Jaular L. Mathieu M. Théry C. SnapShot: Extracellular Vesicles Cell 2020 182 262.e1 10.1016/j.cell.2020.04.054
Simpson R.J. Lim J.W. Moritz R.L. Mathivanan S. Exosomes: Proteomic Insights and Diagnostic Potential Expert Rev. Proteom. 2009 6 267 283 10.1586/epr.09.17
Loyer X. Vion A.-C. Tedgui A. Boulanger C.M. Microvesicles as Cell–Cell Messengers in Cardiovascular Diseases Circ. Res. 2014 114 345 353 10.1161/CIRCRESAHA.113.300858
Valadi H. Ekström K. Bossios A. Sjöstrand M. Lee J.J. Lötvall J.O. Exosome-Mediated Transfer of MRNAs and MicroRNAs Is a Novel Mechanism of Genetic Exchange between Cells Nat. Cell Biol. 2007 9 654 659 10.1038/ncb1596
Barros F.M. Carneiro F. Machado J.C. Melo S.A. Exosomes and Immune Response in Cancer: Friends or Foes? Front. Immunol. 2018 9 730 10.3389/fimmu.2018.00730
Srinivasan A. Sundar I.K. Recent Updates on the Role of Extracellular Vesicles in the Pathogenesis of Allergic Asthma Extracell. Vesicles Circ. Nucleic Acids 2021 2 127 10.20517/evcna.2021.03
Bobrie A. Colombo M. Raposo G. Théry C. Exosome Secretion: Molecular Mechanisms and Roles in Immune Responses Traffic 2011 12 1659 1668 10.1111/j.1600-0854.2011.01225.x
György B. Szabó T.G. Pásztói M. Pál Z. Misják P. Aradi B. László V. Pállinger É. Pap E. Kittel Á. et al. Membrane Vesicles, Current State-of-the-Art: Emerging Role of Extracellular Vesicles Cell. Mol. Life Sci. 2011 68 2667 2688 10.1007/s00018-011-0689-3
Colombo M. Raposo G. Théry C. Biogenesis, Secretion, and Intercellular Interactions of Exosomes and Other Extracellular Vesicles Annu. Rev. Cell Dev. Biol. 2014 30 255 289 10.1146/annurev-cellbio-101512-122326
Akers J.C. Gonda D. Kim R. Carter B.S. Chen C.C. Biogenesis of Extracellular Vesicles (EV): Exosomes, Microvesicles, Retrovirus-like Vesicles, and Apoptotic Bodies J. Neurooncol. 2013 113 1 11 10.1007/s11060-013-1084-8
Kakarla R. Hur J. Kim Y.J. Kim J. Chwae Y.-J. Apoptotic Cell-Derived Exosomes: Messages from Dying Cells Exp. Mol. Med. 2020 52 1 6 10.1038/s12276-019-0362-8
Bazzan E. Tinè M. Casara A. Biondini D. Semenzato U. Cocconcelli E. Balestro E. Damin M. Radu C.M. Turato G. et al. Critical Review of the Evolution of Extracellular Vesicles’ Knowledge: From 1946 to Today Int. J. Mol. Sci. 2021 22 6417 10.3390/ijms22126417
Théry C. Witwer K.W. Aikawa E. Alcaraz M.J. Anderson J.D. Andriantsitohaina R. Antoniou A. Arab T. Archer F. Atkin-Smith G.K. et al. Minimal Information for Studies of Extracellular Vesicles 2018 (MISEV2018): A Position Statement of the International Society for Extracellular Vesicles and Update of the MISEV2014 Guidelines J. Extracell. Vesicles 2018 7 1535750 10.1080/20013078.2018.1535750
Kowal J. Arras G. Colombo M. Jouve M. Morath J.P. Primdal-Bengtson B. Dingli F. Loew D. Tkach M. Théry C. Proteomic Comparison Defines Novel Markers to Characterize Heterogeneous Populations of Extracellular Vesicle Subtypes Proc. Natl. Acad. Sci. USA 2016 113 E968 E977 10.1073/pnas.1521230113
Zhang H. Freitas D. Kim H.S. Fabijanic K. Li Z. Chen H. Mark M.T. Molina H. Martin A.B. Bojmar L. et al. Identification of Distinct Nanoparticles and Subsets of Extracellular Vesicles by Asymmetric Flow Field-Flow Fractionation Nat. Cell Biol. 2018 20 332 343 10.1038/s41556-018-0040-4
Zhang Q. Higginbotham J.N. Jeppesen D.K. Yang Y.-P. Li W. McKinley E.T. Graves-Deal R. Ping J. Britain C.M. Dorsett K.A. et al. Transfer of Functional Cargo in Exomeres Cell Rep. 2019 27 940 954.e6 10.1016/j.celrep.2019.01.009
Anand S. Samuel M. Mathivanan S. Exomeres: A New Member of Extracellular Vesicles Family Subcell. Biochem. 2021 97 89 97 10.1007/978-3-030-67171-6_5
Busser B. Sancey L. Brambilla E. Coll J.-L. Hurbin A. The Multiple Roles of Amphiregulin in Human Cancer Biochim. Biophys. Acta-Rev. Cancer 2011 1816 119 131 10.1016/j.bbcan.2011.05.003
Lu J. Gu J. Significance of β-Galactoside A2,6 Sialyltranferase 1 in Cancers Molecules 2015 20 7509 7527 10.3390/molecules20057509
Jiang J. Zhao W. Tang Q. Wang B. Li X. Feng Z. Over Expression of Amphiregulin Promoted Malignant Progression in Gastric Cancer Pathol. Res. Pract. 2019 215 152576 10.1016/j.prp.2019.152576
Garnham R. Scott E. Livermore K. Munkley J. ST6GAL1: A Key Player in Cancer (Review) Oncol. Lett. 2019 18 983 989 10.3892/ol.2019.10458
Zhang Q. Jeppesen D.K. Higginbotham J.N. Graves-Deal R. Trinh V.Q. Ramirez M.A. Sohn Y. Neininger A.C. Taneja N. McKinley E.T. et al. Supermeres Are Functional Extracellular Nanoparticles Replete with Disease Biomarkers and Therapeutic Targets Nat. Cell Biol. 2021 23 1240 1254 10.1038/s41556-021-00805-8
Zhang W.C. Chin T.M. Yang H. Nga M.E. Lunny D.P. Lim E.K.H. Sun L.L. Pang Y.H. Leow Y.N. Malusay S.R.Y. et al. Tumour-Initiating Cell-Specific MiR-1246 and MiR-1290 Expression Converge to Promote Non-Small Cell Lung Cancer Progression Nat. Commun. 2016 7 11702 10.1038/ncomms11702
Kanlikilicer P. Bayraktar R. Denizli M. Rashed M.H. Ivan C. Aslan B. Mitra R. Karagoz K. Bayraktar E. Zhang X. et al. Exosomal MiRNA Confers Chemo Resistance via Targeting Cav1/p-Gp/M2-Type Macrophage Axis in Ovarian Cancer EBioMedicine 2018 38 100 112 10.1016/j.ebiom.2018.11.004 30487062
Du P. Lai Y. Yao D. Chen J. Ding N. Downregulation of MicroRNA-1246 Inhibits Tumor Growth and Promotes Apoptosis of Cervical Cancer Cells by Targeting Thrombospondin-2 Oncol. Lett. 2019 18 2491 2499 10.3892/ol.2019.10571
Torii C. Maishi N. Kawamoto T. Morimoto M. Akiyama K. Yoshioka Y. Minami T. Tsumita T. Alam M.T. Ochiya T. et al. MiRNA-1246 in Extracellular Vesicles Secreted from Metastatic Tumor Induces Drug Resistance in Tumor Endothelial Cells Sci. Rep. 2021 11 13502 10.1038/s41598-021-92879-5 34226586
Borregaard N. Development of Neutrophil Granule Diversity Ann. N. Y. Acad Sci. 1997 832 62 68 10.1111/j.1749-6632.1997.tb46237.x 9704037
Faurschou M. Borregaard N. Neutrophil Granules and Secretory Vesicles in Inflammation Microbes Infect. 2003 5 1317 1327 10.1016/j.micinf.2003.09.008
Häger M. Cowland J.B. Borregaard N. Neutrophil Granules in Health and Disease J. Intern. Med. 2010 268 25 34 10.1111/j.1365-2796.2010.02237.x
Cassatella M.A. Östberg N.K. Tamassia N. Soehnlein O. Biological Roles of Neutrophil-Derived Granule Proteins and Cytokines Trends Immunol. 2019 40 648 664 10.1016/j.it.2019.05.003
Reeves E.P. Lu H. Jacobs H.L. Messina C.G.M. Bolsover S. Gabella G. Potma E.O. Warley A. Roes J. Segal A.W. Killing Activity of Neutrophils Is Mediated through Activation of Proteases by K+Flux Nature 2002 416 291 297 10.1038/416291a
Winterbourn C.C. Kettle A.J. Hampton M.B. Reactive Oxygen Species and Neutrophil Function Annu. Rev. Biochem. 2016 85 765 792 10.1146/annurev-biochem-060815-014442
Nauseef W.M. The Phagocyte NOX2 NADPH Oxidase in Microbial Killing and Cell Signaling Curr. Opin. Immunol. 2019 60 130 140 10.1016/j.coi.2019.05.006
Schenten V. Plançon S. Jung N. Hann J. Bueb J.-L. Bréchard S. Tschirhart E.J. Tolle F. Secretion of the Phosphorylated Form of S100A9 from Neutrophils Is Essential for the Proinflammatory Functions of Extracellular S100A8/A9 Front Immunol. 2018 9 447 10.3389/fimmu.2018.00447 29593718
Brinkmann V. Reichard U. Goosmann C. Fauler B. Uhlemann Y. Weiss D.S. Weinrauch Y. Zychlinsky A. Neutrophil Extracellular Traps Kill Bacteria Science 2004 303 1532 1535 10.1126/science.1092385 15001782
Papayannopoulos V. Zychlinsky A. NETs: A New Strategy for Using Old Weapons Trends Immunol. 2009 30 513 521 10.1016/j.it.2009.07.011
Jorch S.K. Kubes P. An Emerging Role for Neutrophil Extracellular Traps in Noninfectious Disease Nat. Med. 2017 23 279 287 10.1038/nm.4294 28267716
Tecchio C. Micheletti A. Cassatella M.A. Neutrophil-Derived Cytokines: Facts Beyond Expression Front Immunol. 2014 5 508 10.3389/fimmu.2014.00508
Tamassia N. Bianchetto-Aguilera F. Arruda-Silva F. Gardiman E. Gasperini S. Calzetti F. Cassatella M.A. Cytokine Production by Human Neutrophils: Revisiting the “Dark Side of the Moon” Eur. J. Clin. Investig. 2018 48 e12952 10.1111/eci.12952
Eken C. Martin P.J. Sadallah S. Treves S. Schaller M. Schifferli J.A. Ectosomes Released by Polymorphonuclear Neutrophils Induce a MerTK-Dependent Anti-Inflammatory Pathway in Macrophages J. Biol. Chem. 2010 285 39914 39921 10.1074/jbc.M110.126748 20959443
Sadallah S. Eken C. Schifferli J.A. Ectosomes as Modulators of Inflammation and Immunity Clin. Exp. Immunol. 2010 163 26 32 10.1111/j.1365-2249.2010.04271.x
Johnson B.L. III Kuethe J.W. Caldwell C.C. Neutrophil Derived Microvesicles: Emerging Role of a Key Mediator to the Immune Response Endocr. Metab. Immune Disord. Drug Targets 2014 14 210 217 10.2174/1871530314666140722083717
Nauseef W.M. Borregaard N. Neutrophils at Work Nat. Immunol. 2014 15 602 611 10.1038/ni.2921
Kolonics F. Kajdácsi E. Farkas V.J. Veres D.S. Khamari D. Kittel Á. Merchant M.L. McLeish K.R. Lőrincz Á.M. Ligeti E. Neutrophils Produce Proinflammatory or Anti-inflammatory Extracellular Vesicles Depending on the Environmental Conditions J. Leukoc. Biol. 2021 109 793 806 10.1002/JLB.3A0320-210R 32946637
Stein J.M. Luzio J.P. Ectocytosis Caused by Sublytic Autologous Complement Attack on Human Neutrophils. The Sorting of Endogenous Plasma-Membrane Proteins and Lipids into Shed Vesicles Biochem. J. 1991 274 381 386 10.1042/bj2740381 1848755
Gasser O. Hess C. Miot S. Deon C. Sanchez J.-C. Schifferli J.A. Characterisation and Properties of Ectosomes Released by Human Polymorphonuclear Neutrophils Exp. Cell Res. 2003 285 243 257 10.1016/S0014-4827(03)00055-7
Timár C.I. Lőrincz Á.M. Csépányi-Kömi R. Vályi-Nagy A. Nagy G. Buzás E.I. Iványi Z. Kittel Á. Powell D.W. McLeish K.R. et al. Antibacterial Effect of Microvesicles Released from Human Neutrophilic Granulocytes Blood 2013 121 510 518 10.1182/blood-2012-05-431114
Dalli J. Serhan C.N. Specific Lipid Mediator Signatures of Human Phagocytes: Microparticles Stimulate Macrophage Efferocytosis and pro-Resolving Mediators Blood 2012 120 e60 e72 10.1182/blood-2012-04-423525 22904297
Lorincz A.M. Schutte M. Timar C.I. Veres D.S. Kittel A. McLeish K.R. Merchant M.L. Ligeti E. Functionally and Morphologically Distinct Populations of Extracellular Vesicles Produced by Human Neutrophilic Granulocytes J. Leukoc. Biol. 2015 98 583 589 10.1189/jlb.3VMA1014-514R
Kolonics F. Szeifert V. Timár C.I. Ligeti E. Lőrincz Á.M. The Functional Heterogeneity of Neutrophil-Derived Extracellular Vesicles Reflects the Status of the Parent Cell Cells 2020 9 2718 10.3390/cells9122718
Eken C. Gasser O. Zenhaeusern G. Oehri I. Hess C. Schifferli J.A. Polymorphonuclear Neutrophil-Derived Ectosomes Interfere with the Maturation of Monocyte-Derived Dendritic Cells J. Immunol. 2008 180 817 824 10.4049/jimmunol.180.2.817
Gasser O. Schifferli J.A. Activated Polymorphonuclear Neutrophils Disseminate Anti-Inflammatory Microparticles by Ectocytosis Blood 2004 104 2543 2548 10.1182/blood-2004-01-0361
Eken C. Sadallah S. Martin P.J. Treves S. Schifferli J.A. Ectosomes of Polymorphonuclear Neutrophils Activate Multiple Signaling Pathways in Macrophages Immunobiology 2013 218 382 392 10.1016/j.imbio.2012.05.021
Hong Y. Eleftheriou D. Hussain A.A.K. Price-Kuehne F.E. Savage C.O. Jayne D. Little M.A. Salama A.D. Klein N.J. Brogan P.A. Anti-Neutrophil Cytoplasmic Antibodies Stimulate Release of Neutrophil Microparticles J. Am. Soc. Nephrol. 2012 23 49 62 10.1681/ASN.2011030298 22052057
Hess C. Sadallah S. Hefti A. Landmann R. Schifferli J.A. Ectosomes Released by Human Neutrophils Are Specialized Functional Units J. Immunol. 1999 163 4564 4573 10.1016/S0161-5890(98)90627-7
Hong C.-W. Extracellular Vesicles of Neutrophils Immune Netw. 2018 18 e43 10.4110/in.2018.18.e43
Youn Y.-J. Shrestha S. Lee Y.-B. Kim J.-K. Lee J.H. Hur K. Mali N.M. Nam S.-W. Kim S.-H. Lee S. et al. Neutrophil-Derived Trail Is a Proinflammatory Subtype of Neutrophil-Derived Extracellular Vesicles Theranostics 2021 11 2770 2787 10.7150/thno.51756 33456572
Hyun Y.-M. Sumagin R. Sarangi P.P. Lomakina E. Overstreet M.G. Baker C.M. Fowell D.J. Waugh R.E. Sarelius I.H. Kim M. Uropod Elongation Is a Common Final Step in Leukocyte Extravasation through Inflamed Vessels J. Exp. Med. 2012 209 1349 1362 10.1084/jem.20111426 22711877
Hind L.E. Vincent W.J.B. Huttenlocher A. Leading from the Back: The Role of the Uropod in Neutrophil Polarization and Migration Dev. Cell 2016 38 161 169 10.1016/j.devcel.2016.06.031 27459068
Rhys H.I. Dell’Accio F. Pitzalis C. Moore A. Norling L.v. Perretti M. Neutrophil Microvesicles from Healthy Control and Rheumatoid Arthritis Patients Prevent the Inflammatory Activation of Macrophages EBioMedicine 2018 29 60 69 10.1016/j.ebiom.2018.02.003
Zhang J. Ji C. Zhang H. Shi H. Mao F. Qian H. Xu W. Wang D. Pan J. Fang X. et al. Engineered Neutrophil-Derived Exosome-like Vesicles for Targeted Cancer Therapy Sci. Adv. 2022 8 eabj8207 10.1126/sciadv.abj8207 35020437
Rossaint J. Kühne K. Skupski J. van Aken H. Looney M.R. Hidalgo A. Zarbock A. Directed Transport of Neutrophil-Derived Extracellular Vesicles Enables Platelet-Mediated Innate Immune Response Nat. Commun. 2016 7 13464 10.1038/ncomms13464 27845343
Vargas A. Roux-Dalvai F. Droit A. Lavoie J.-P. Neutrophil-Derived Exosomes: A New Mechanism Contributing to Airway Smooth Muscle Remodeling Am. J. Respir. Cell Mol. Biol. 2016 55 450 461 10.1165/rcmb.2016-0033OC
Genschmer K.R. Russell D.W. Lal C. Szul T. Bratcher P.E. Noerager B.D. Abdul Roda M. Xu X. Rezonzew G. Viera L. et al. Activated PMN Exosomes: Pathogenic Entities Causing Matrix Destruction and Disease in the Lung Cell 2019 176 113 126.e15 10.1016/j.cell.2018.12.002 30633902
Greene C.M. McElvaney N.G. Proteases and Antiproteases in Chronic Neutrophilic Lung Disease—Relevance to Drug Discovery Br. J. Pharmacol. 2009 158 1048 1058 10.1111/j.1476-5381.2009.00448.x 19845686
Margaroli C. Madison M.C. Viera L. Russell D.W. Gaggar A. Genschmer K.R. Blalock J.E. An in Vivo Model for Extracellular Vesicle–Induced Emphysema JCI Insight 2022 7 e153560 10.1172/jci.insight.153560 35077395
Slater T.W. Finkielsztein A. Mascarenhas L.A. Mehl L.C. Butin-Israeli V. Sumagin R. Neutrophil Microparticles Deliver Active Myeloperoxidase to Injured Mucosa to Inhibit Epithelial Wound Healing J. Immunol. 2017 198 2886 2897 10.4049/jimmunol.1601810
Butin-Israeli V. Houser M.C. Feng M. Thorp E.B. Nusrat A. Parkos C.A. Sumagin R. Deposition of Microparticles by Neutrophils onto Inflamed Epithelium: A New Mechanism to Disrupt Epithelial Intercellular Adhesions and Promote Transepithelial Migration FASEB J. 2016 30 4007 4020 10.1096/fj.201600734R
Kamekura R. Nava P. Feng M. Quiros M. Nishio H. Weber D.A. Parkos C.A. Nusrat A. Inflammation-Induced Desmoglein-2 Ectodomain Shedding Compromises the Mucosal Barrier Mol. Biol. Cell 2015 26 3165 3177 10.1091/mbc.e15-03-0147
Soni S. Garner J.L. O’Dea K.P. Koh M. Finney L. Tirlapur N. Srikanthan K. Tenda E.D. Aboelhassan A.M. Singh S. et al. Intra-Alveolar Neutrophil-Derived Microvesicles Are Associated with Disease Severity in COPD Am. J. Physiol. Lung Cell. Mol. Physiol. 2021 320 L73 L83 10.1152/ajplung.00099.2020 33146567
Forrest O.A. Dobosh B. Ingersoll S.A. Rao S. Rojas A. Laval J. Alvarez J.A. Brown M.R. Tangpricha V. Tirouvanziam R. Neutrophil-derived Extracellular Vesicles Promote Feed-forward Inflammasome Signaling in Cystic Fibrosis Airways J. Leukoc. Biol. 2022 112 707 716 10.1002/JLB.3AB0321-149R
Amjadi M.F. Avner B.S. Greenlee-Wacker M.C. Horswill A.R. Nauseef W.M. Neutrophil-derived Extracellular Vesicles Modulate the Phenotype of Naïve Human Neutrophils J. Leukoc. Biol. 2021 110 917 925 10.1002/JLB.3AB0520-339RR
Mercado N. Thimmulappa R. Thomas C.M.R. Fenwick P.S. Chana K.K. Donnelly L.E. Biswal S. Ito K. Barnes P.J. Decreased Histone Deacetylase 2 Impairs Nrf2 Activation by Oxidative Stress Biochem. Biophys. Res. Commun. 2011 406 292 298 10.1016/j.bbrc.2011.02.035
Kersul A.L. Iglesias A. Ríos Á. Noguera A. Forteza A. Serra E. Agustí A. Cosío B.G. Mecanismos Moleculares de Inflamación Durante Las Agudizaciones de La Enfermedad Pulmonar Obstructiva Crónica Arch Bronconeumol. 2011 47 176 183 10.1016/j.arbres.2010.12.003 21454005
Goyette J. Geczy C.L. Inflammation-Associated S100 Proteins: New Mechanisms That Regulate Function Amino Acids 2011 41 821 842 10.1007/s00726-010-0528-0 20213444
Ehlermann P. Eggers K. Bierhaus A. Most P. Weichenhan D. Greten J. Nawroth P.P. Katus H.A. Remppis A. Increased Proinflammatory Endothelial Response to S100A8/A9 after Preactivation through Advanced Glycation End Products Cardiovasc. Diabetol. 2006 5 6 10.1186/1475-2840-5-6 16573830
Vogl T. Tenbrock K. Ludwig S. Leukert N. Ehrhardt C. van Zoelen M.A.D. Nacken W. Foell D. van der Poll T. Sorg C. et al. Mrp8 and Mrp14 Are Endogenous Activators of Toll-like Receptor 4, Promoting Lethal, Endotoxin-Induced Shock Nat. Med. 2007 13 1042 1049 10.1038/nm1638 17767165
Loser K. Vogl T. Voskort M. Lueken A. Kupas V. Nacken W. Klenner L. Kuhn A. Foell D. Sorokin L. et al. The Toll-like Receptor 4 Ligands Mrp8 and Mrp14 Are Crucial in the Development of Autoreactive CD8+ T Cells Nat. Med. 2010 16 713 717 10.1038/nm.2150
Ryckman C. Vandal K. Rouleau P. Talbot M. Tessier P.A. Proinflammatory Activities of S100: Proteins S100A8, S100A9, and S100A8/A9 Induce Neutrophil Chemotaxis and Adhesion J. Immunol. 2003 170 3233 3242 10.4049/jimmunol.170.6.3233 12626582
Viemann D. Strey A. Janning A. Jurk K. Klimmek K. Vogl T. Hirono K. Ichida F. Foell D. Kehrel B. et al. Myeloid-Related Proteins 8 and 14 Induce a Specific Inflammatory Response in Human Microvascular Endothelial Cells Blood 2005 105 2955 2962 10.1182/blood-2004-07-2520
Pruenster M. Kurz A.R.M. Chung K.-J. Cao-Ehlker X. Bieber S. Nussbaum C.F. Bierschenk S. Eggersmann T.K. Rohwedder I. Heinig K. et al. Extracellular MRP8/14 Is a Regulator of Β2 Integrin-Dependent Neutrophil Slow Rolling and Adhesion Nat. Commun. 2015 6 6915 10.1038/ncomms7915
Donato R. Cannon B.R. Sorci G. Riuzzi F. Hsu K. Weber D.J. Geczy C.L. Functions of S100 Proteins Curr. Mol. Med. 2013 13 24 57 10.2174/156652413804486214 22834835
Simard J.-C. Noël C. Tessier P.A. Girard D. Human S100A9 Potentiates IL-8 Production in Response to GM-CSF or FMLP via Activation of a Different Set of Transcription Factors in Neutrophils FEBS Lett. 2014 588 2141 2146 10.1016/j.febslet.2014.04.027
Holzinger D. Nippe N. Vogl T. Marketon K. Mysore V. Weinhage T. Dalbeth N. Pool B. Merriman T. Baeten D. et al. Myeloid-Related Proteins 8 and 14 Contribute to Monosodium Urate Monohydrate Crystal-Induced Inflammation in Gout Arthritis Rheumatol. 2014 66 1327 1339 10.1002/art.38369
Chiu C.-W. Chen H.-M. Wu T.-T. Shih Y.-C. Huang K.-K. Tsai Y.-F. Hsu Y.-L. Chen S.-F. Differential Proteomics of Monosodium Urate Crystals-Induced Inflammatory Response in Dissected Murine Air Pouch Membranes by ITRAQ Technology Proteomics 2015 15 3338 3348 10.1002/pmic.201400626 26205848
Gao H. Hou J. Meng H. Zhang X. Zheng Y. Peng L. Proinflammatory Effects and Mechanisms of Calprotectin on Human Gingival Fibroblasts J. Periodontal Res. 2017 52 975 983 10.1111/jre.12465
Austermann J. Spiekermann C. Roth J. S100 Proteins in Rheumatic Diseases Nat. Rev. Rheumatol. 2018 14 528 541 10.1038/s41584-018-0058-9 30076385
Foell D. Roth J. Proinflammatory S100 Proteins in Arthritis and Autoimmune Disease Arthritis Rheum. 2004 50 3762 3771 10.1002/art.20631
Vogl T. Eisenblätter M. Völler T. Zenker S. Hermann S. van Lent P. Faust A. Geyer C. Petersen B. Roebrock K. et al. Alarmin S100A8/S100A9 as a Biomarker for Molecular Imaging of Local Inflammatory Activity Nat. Commun. 2014 5 4593 10.1038/ncomms5593 25098555
Scott N.R. Swanson R.v. Al-Hammadi N. Domingo-Gonzalez R. Rangel-Moreno J. Kriel B.A. Bucsan A.N. Das S. Ahmed M. Mehra S. et al. S100A8/A9 Regulates CD11b Expression and Neutrophil Recruitment during Chronic Tuberculosis J. Clin. Investig. 2020 130 3098 3112 10.1172/JCI130546 32134742
Kim R.Y. Sunkara K.P. Bracke K.R. Jarnicki A.G. Donovan C. Hsu A.C. Ieni A. Beckett E.L. Galvão I. Wijnant S. et al. A MicroRNA-21–Mediated SATB1/S100A9/NF-ΚB Axis Promotes Chronic Obstructive Pulmonary Disease Pathogenesis Sci. Transl. Med. 2021 13 eaav7223 10.1126/scitranslmed.aav7223
Sunahori K. Yamamura M. Yamana J. Takasugi K. Kawashima M. Yamamoto H. Chazin W.J. Nakatani Y. Yui S. Makino H. The S100A8/A9 Heterodimer Amplifies Proinflammatory Cytokine Production by Macrophages via Activation of Nuclear Factor Kappa B and P38 Mitogen-Activated Protein Kinase in Rheumatoid Arthritis Arthritis Res. Ther. 2006 8 R69 10.1186/ar1939 16613612
Grevers L.C. de Vries T.J. Vogl T. Abdollahi-Roodsaz S. Sloetjes A.W. Leenen P.J.M. Roth J. Everts V. van den Berg W.B. van Lent P.L.E.M. S100A8 Enhances Osteoclastic Bone Resorption in Vitro through Activation of Toll-like Receptor 4: Implications for Bone Destruction in Murine Antigen-Induced Arthritis Arthritis Rheum. 2011 63 1365 1375 10.1002/art.30290 21337316
Bianchi M. Niemiec M.J. Siler U. Urban C.F. Reichenbach J. Restoration of Anti-Aspergillus Defense by Neutrophil Extracellular Traps in Human Chronic Granulomatous Disease after Gene Therapy Is Calprotectin-Dependent J. Allergy Clin. Immunol. 2011 127 1243 1252.e7 10.1016/j.jaci.2011.01.021 21376380
Sprenkeler E.G.G. Zandstra J. van Kleef N.D. Goetschalckx I. Verstegen B. Aarts C.E.M. Janssen H. Tool A.T.J. van Mierlo G. van Bruggen R. et al. S100A8/A9 Is a Marker for the Release of Neutrophil Extracellular Traps and Induces Neutrophil Activation Cells 2022 11 236 10.3390/cells11020236 35053354
Rammes A. Roth J. Goebeler M. Klempt M. Hartmann M. Sorg C. Myeloid-Related Protein (MRP) 8 and MRP14, Calcium-Binding Proteins of the S100 Family, Are Secreted by Activated Monocytes via a Novel, Tubulin-Dependent Pathway J. Biol. Chem. 1997 272 9496 9502 10.1074/jbc.272.14.9496 9083090
Li L. Zuo X. Xiao Y. Liu D. Luo H. Zhu H. Neutrophil-Derived Exosome from Systemic Sclerosis Inhibits the Proliferation and Migration of Endothelial Cells Biochem. Biophys. Res. Commun. 2020 526 334 340 10.1016/j.bbrc.2020.03.088 32220494
Kambas K. Chrysanthopoulou A. Vassilopoulos D. Apostolidou E. Skendros P. Girod A. Arelaki S. Froudarakis M. Nakopoulou L. Giatromanolaki A. et al. Tissue Factor Expression in Neutrophil Extracellular Traps and Neutrophil Derived Microparticles in Antineutrophil Cytoplasmic Antibody Associated Vasculitis May Promote Thromboinflammation and the Thrombophilic State Associated with the Disease Ann. Rheum. Dis. 2014 73 1854 1863 10.1136/annrheumdis-2013-203430
Flint J. Morgan M.D. Savage C.O.S. Pathogenesis of ANCA-Associated Vasculitis Rheum. Dis. Clin. N. Am. 2010 36 463 477 10.1016/j.rdc.2010.05.006
Millet A. Pederzoli-Ribeil M. Guillevin L. Witko-Sarsat V. Mouthon L. Antineutrophil Cytoplasmic Antibody-Associated Vasculitides: Is It Time to Split up the Group? Ann. Rheum. Dis. 2013 72 1273 1279 10.1136/annrheumdis-2013-203255
Ramacciotti E. Hawley A.E. Wrobleski S.K. Myers D.D. Strahler J.R. Andrews P.C. Guire K.E. Henke P.K. Wakefield T.W. Proteomics of Microparticles after Deep Venous Thrombosis Thromb. Res. 2010 125 e269 e274 10.1016/j.thromres.2010.01.019
Rapaport S.I. Rao L.V. The Tissue Factor Pathway: How It Has Become a “Prima Ballerina” Thromb. Haemost. 1995 74 7 17 10.1055/s-0038-1642646
Butenas S. Orfeo T. Mann K.G. Tissue Factor in Coagulation Arter. Thromb. Vasc. Biol. 2009 29 1989 1996 10.1161/ATVBAHA.108.177402
Li L. Zhu D. Huang L. Zhang J. Bian Z. Chen X. Liu Y. Zhang C.-Y. Zen K. Argonaute 2 Complexes Selectively Protect the Circulating MicroRNAs in Cell-Secreted Microvesicles PLoS ONE 2012 7 e46957 10.1371/journal.pone.0046957 23077538
Lv Z. Wei Y. Wang D. Zhang C.-Y. Zen K. Li L. Argonaute 2 in Cell-Secreted Microvesicles Guides the Function of Secreted MiRNAs in Recipient Cells PLoS ONE 2014 9 e103599 10.1371/journal.pone.0103599 25072345
Zhao C. Sun X. Li L. Biogenesis and Function of Extracellular MiRNAs ExRNA 2019 1 38 10.1186/s41544-019-0039-4
Ryo A. Suizu F. Yoshida Y. Perrem K. Liou Y.-C. Wulf G. Rottapel R. Yamaoka S. Lu K.P. Regulation of NF-ΚB Signaling by Pin1-Dependent Prolyl Isomerization and Ubiquitin-Mediated Proteolysis of P65/RelA Mol. Cell 2003 12 1413 1426 10.1016/S1097-2765(03)00490-8
Yeung F. Hoberg J.E. Ramsey C.S. Keller M.D. Jones D.R. Frye R.A. Mayo M.W. Modulation of NF-ΚB-Dependent Transcription and Cell Survival by the SIRT1 Deacetylase EMBO J. 2004 23 2369 2380 10.1038/sj.emboj.7600244
Jiao Y. Zhang T. Zhang C. Ji H. Tong X. Xia R. Wang W. Ma Z. Shi X. Exosomal MiR-30d-5p of Neutrophils Induces M1 Macrophage Polarization and Primes Macrophage Pyroptosis in Sepsis-Related Acute Lung Injury Crit. Care 2021 25 356 10.1186/s13054-021-03775-3
Gomez I. Ward B. Souilhol C. Recarti C. Ariaans M. Johnston J. Burnett A. Mahmoud M. Luong L.A. West L. et al. Neutrophil Microvesicles Drive Atherosclerosis by Delivering MiR-155 to Atheroprone Endothelium Nat. Commun. 2020 11 214 10.1038/s41467-019-14043-y
Glémain A. Néel M. Néel A. André-Grégoire G. Gavard J. Martinet B. le Bloas R. Riquin K. Hamidou M. Fakhouri F. et al. Neutrophil-Derived Extracellular Vesicles Induce Endothelial Inflammation and Damage through the Transfer of MiRNAs J. Autoimmun. 2022 129 102826 10.1016/j.jaut.2022.102826
Mercer T.R. Dinger M.E. Mattick J.S. Long Non-Coding RNAs: Insights into Functions Nat. Rev. Genet. 2009 10 155 159 10.1038/nrg2521
Chen L.-L. Carmichael G.G. Decoding the Function of Nuclear Long Non-Coding RNAs Curr. Opin. Cell Biol. 2010 22 357 364 10.1016/j.ceb.2010.03.003 20356723
Derrien T. Johnson R. Bussotti G. Tanzer A. Djebali S. Tilgner H. Guernec G. Martin D. Merkel A. Knowles D.G. et al. The GENCODE v7 Catalog of Human Long Noncoding RNAs: Analysis of Their Gene Structure, Evolution, and Expression Genome Res. 2012 22 1775 1789 10.1101/gr.132159.111 22955988
Gao Y. Li S. Zhang Z. Yu X. Zheng J. The Role of Long Non-Coding RNAs in the Pathogenesis of RA, SLE, and SS Front. Med. 2018 5 193 10.3389/fmed.2018.00193
Zhang X.-Y. Chen Z.-C. Li N. Wang Z.-H. Guo Y.-L. Tian C.-J. Cheng D.-J. Tang X.-Y. Zhang L.-X. Exosomal Transfer of Activated Neutrophil-Derived LncRNA CRNDE Promotes Proliferation and Migration of Airway Smooth Muscle Cells in Asthma Hum. Mol. Genet. 2021 31 638 650 10.1093/hmg/ddab283 34590683
Krishnamoorthy N. Douda D.N. Brüggemann T.R. Ricklefs I. Duvall M.G. Abdulnour R.-E.E. Martinod K. Tavares L. Wang X. Cernadas M. et al. Neutrophil Cytoplasts Induce T H 17 Differentiation and Skew Inflammation toward Neutrophilia in Severe Asthma Sci. Immunol. 2018 3 eaao474 10.1126/sciimmunol.aao4747 30076281
Tsoi K.M. MacParland S.A. Ma X.-Z. Spetzler V.N. Echeverri J. Ouyang B. Fadel S.M. Sykes E.A. Goldaracena N. Kaths J.M. et al. Mechanism of Hard-Nanomaterial Clearance by the Liver Nat. Mater. 2016 15 1212 1221 10.1038/nmat4718
Liang Y. Duan L. Lu J. Xia J. Engineering Exosomes for Targeted Drug Delivery Theranostics 2021 11 3183 3195 10.7150/thno.52570
Choi H. Choi Y. Yim H.Y. Mirzaaghasi A. Yoo J.-K. Choi C. Biodistribution of Exosomes and Engineering Strategies for Targeted Delivery of Therapeutic Exosomes Tissue Eng. Regen. Med. 2021 18 499 511 10.1007/s13770-021-00361-0
Qi H. Liu C. Long L. Ren Y. Zhang S. Chang X. Qian X. Jia H. Zhao J. Sun J. et al. Blood Exosomes Endowed with Magnetic and Targeting Properties for Cancer Therapy ACS Nano 2016 10 3323 3333 10.1021/acsnano.5b06939
Kim M.S. Haney M.J. Zhao Y. Yuan D. Deygen I. Klyachko N.L. Kabanov A.v. Batrakova E.v. Engineering Macrophage-Derived Exosomes for Targeted Paclitaxel Delivery to Pulmonary Metastases: In Vitro and in Vivo Evaluations Nanomedicine 2018 14 195 204 10.1016/j.nano.2017.09.011 28982587
Susa F. Limongi T. Dumontel B. Vighetto V. Cauda V. Engineered Extracellular Vesicles as a Reliable Tool in Cancer Nanomedicine Cancers 2019 11 1979 10.3390/cancers11121979 31835327
Longatti A. Schindler C. Collinson A. Jenkinson L. Matthews C. Fitzpatrick L. Blundy M. Minter R. Vaughan T. Shaw M. et al. High Affinity Single-Chain Variable Fragments Are Specific and Versatile Targeting Motifs for Extracellular Vesicles Nanoscale 2018 10 14230 14244 10.1039/C8NR03970D 30010165
Krishnamoorthy S. Recchiuti A. Chiang N. Yacoubian S. Lee C.-H. Yang R. Petasis N.A. Serhan C.N. Resolvin D1 Binds Human Phagocytes with Evidence for Proresolving Receptors Proc. Nat. Acad. Sci. USA 2010 107 1660 1665 10.1073/pnas.0907342107
Norling L.v. Dalli J. Flower R.J. Serhan C.N. Perretti M. Resolvin D1 Limits Polymorphonuclear Leukocyte Recruitment to Inflammatory Loci Arter. Thromb. Vasc. Biol. 2012 32 1970 1978 10.1161/ATVBAHA.112.249508
Flesher R.P. Herbert C. Kumar R.K. Resolvin E1 Promotes Resolution of Inflammation in a Mouse Model of an Acute Exacerbation of Allergic Asthma Clin. Sci. 2014 126 805 818 10.1042/CS20130623
Gao J. Wang S. Dong X. Leanse L.G. Dai T. Wang Z. Co-Delivery of Resolvin D1 and Antibiotics with Nanovesicles to Lungs Resolves Inflammation and Clears Bacteria in Mice Commun. Biol. 2020 3 680 10.1038/s42003-020-01410-5
Gao J. Dong X. Su Y. Wang Z. Human Neutrophil Membrane-Derived Nanovesicles as a Drug Delivery Platform for Improved Therapy of Infectious Diseases Acta Biomater. 2021 123 354 363 10.1016/j.actbio.2021.01.020
Dong X. Gao J. Zhang C.Y. Hayworth C. Frank M. Wang Z. Neutrophil Membrane-Derived Nanovesicles Alleviate Inflammation To Protect Mouse Brain Injury from Ischemic Stroke ACS Nano 2019 13 1272 1283 10.1021/acsnano.8b06572
Headland S.E. Jones H.R. Norling L.v. Kim A. Souza P.R. Corsiero E. Gil C.D. Nerviani A. Dell’Accio F. Pitzalis C. et al. Neutrophil-Derived Microvesicles Enter Cartilage and Protect the Joint in Inflammatory Arthritis Sci. Transl. Med. 2015 7 315ra190 10.1126/scitranslmed.aac5608
Zhang Q. Dehaini D. Zhang Y. Zhou J. Chen X. Zhang L. Fang R.H. Gao W. Zhang L. Neutrophil Membrane-Coated Nanoparticles Inhibit Synovial Inflammation and Alleviate Joint Damage in Inflammatory Arthritis Nat. Nanotechnol. 2018 13 1182 1190 10.1038/s41565-018-0254-4 30177807
Zhang L. Qin Z. Sun H. Chen X. Dong J. Shen S. Zheng L. Gu N. Jiang Q. Nanoenzyme Engineered Neutrophil-Derived Exosomes Attenuate Joint Injury in Advanced Rheumatoid Arthritis via Regulating Inflammatory Environment Bioact. Mater. 2022 18 1 14 10.1016/j.bioactmat.2022.02.017
Liao T.-L. Chen Y.-M. Tang K.-T. Chen P.-K. Liu H.-J. Chen D.-Y. MicroRNA-223 Inhibits Neutrophil Extracellular Traps Formation through Regulating Calcium Influx and Small Extracellular Vesicles Transmission Sci. Rep. 2021 11 15676 10.1038/s41598-021-95028-0 34344968
McCormick M.M. Rahimi F. Bobryshev Y.v. Gaus K. Zreiqat H. Cai H. Lord R.S.A. Geczy C.L. S100A8 and S100A9 in Human Arterial Wall J. Biol. Chem. 2005 280 41521 41529 10.1074/jbc.M509442200
Ikemoto M. Murayama H. Itoh H. Totani M. Fujita M. Intrinsic Function of S100A8/A9 Complex as an Anti-Inflammatory Protein in Liver Injury Induced by Lipopolysaccharide in Rats Clin. Chim. Acta 2007 376 197 204 10.1016/j.cca.2006.08.018 17011539
Otsuka K. Terasaki F. Ikemoto M. Fujita S. Tsukada B. Katashima T. Kanzaki Y. Sohmiya K. Kono T. Toko H. et al. Suppression of Inflammation in Rat Autoimmune Myocarditis by S100A8/A9 through Modulation of the Proinflammatory Cytokine Network Eur. J. Heart Fail. 2009 11 229 237 10.1093/eurjhf/hfn049 19151078
Wang S. Song R. Wang Z. Jing Z. Wang S. Ma J. S100A8/A9 in Inflammation Front. Immunol. 2018 9 1298 10.3389/fimmu.2018.01298
