Biological Roles of Neutrophil-Derived Granule Proteins and Cytokines

Trends in Immunology - Tập 40 - Trang 648-664 - 2019
Marco Antonio Cassatella1, Nataliya K. Östberg2,3, Nicola Tamassia1, Oliver Soehnlein2,3,4,5
1Department of Medicine, Section of General Pathology, University of Verona, Verona, Italy
2Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden
3Department of Medicine, Karolinska Institutet, Stockholm, Sweden
4Institute for Cardiovascular Prevention (IPEK), Klinikum der LMU, München, Germany
5German Centre for Cardiovascular Research (DZHK), Partner site, Munich, Germany

Tài liệu tham khảo

Meuret, 1973, Neutrophil kinetics in man. Studies using autotransfusion of 3 H-DFP labeled blood cells and autoradiography, Blut, 26, 97, 10.1007/BF01635759 Mantovani, 2011, Neutrophils in the activation and regulation of innate and adaptive immunity, Nat. Rev. Immunol., 11, 519, 10.1038/nri3024 Soehnlein, 2017, Neutrophils as protagonists and targets in chronic inflammation, Nat. Rev. Immunol., 17, 248, 10.1038/nri.2017.10 Ortega-Gomez, 2016, Cathepsin G controls arterial but not venular myeloid cell recruitment, Circulation, 134, 1176, 10.1161/CIRCULATIONAHA.116.024790 Coffelt, 2016, Neutrophils in cancer: neutral no more, Nat. Rev. Cancer, 16, 431, 10.1038/nrc.2016.52 Talukdar, 2012, Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase, Nat. Med., 18, 1407, 10.1038/nm.2885 Zenaro, 2015, Neutrophils promote Alzheimer’s disease-like pathology and cognitive decline via LFA-1 integrin, Nat. Med., 21, 880, 10.1038/nm.3913 Soehnlein, 2011, Neutrophil-derived cathelicidin protects from neointimal hyperplasia, Sci. Transl. Med., 3, 10.1126/scitranslmed.3002531 Jones, 2016, The role of neutrophils in inflammation resolution, Semin. Immunol., 28, 137, 10.1016/j.smim.2016.03.007 Ferraro, 2019, Annexin A1 induces a pro-angiogenic macro-phage phenotype to promote myocardial repair, J. Am. Coll. Cardiol., 10.1016/j.jacc.2019.03.503 Butin-Israeli, 2019, Neutrophil-induced genomic instability impedes resolution of inflammation and wound healing, J. Clin. Invest., 129, 712, 10.1172/JCI122085 Scapini, 2014, Social networking of human neutrophils within the immune system, Blood, 124, 710, 10.1182/blood-2014-03-453217 McLeish, 2013, Technical note: proteomic approaches to fundamental questions about neutrophil biology, J. Leukoc. Biol., 94, 683, 10.1189/jlb.1112591 Luerman, 2010, Application of proteomics to neutrophil biology, J. Proteome, 73, 552, 10.1016/j.jprot.2009.06.013 Uriarte, 2008, Comparison of proteins expressed on secretory vesicle membranes and plasma membranes of human neutrophils, J. Immunol., 180, 5575, 10.4049/jimmunol.180.8.5575 Nebl, 2002, Proteomic analysis of a detergent-resistant membrane skeleton from neutrophil plasma membranes, J. Biol. Chem., 277, 43399, 10.1074/jbc.M205386200 Xu, 2009, Subproteome analysis of the neutrophil cytoskeleton, Proteomics, 9, 2037, 10.1002/pmic.200800674 Rørvig, 2013, Proteome profiling of human neutrophil granule subsets, secretory vesicles, and cell membrane: correlation with transcriptome profiling of neutrophil precursors, J. Leukoc. Biol., 94, 711, 10.1189/jlb.1212619 Lominadze, 2005, Proteomic analysis of human neutrophil granules, Mol. Cell. Proteomics, 4, 1503, 10.1074/mcp.M500143-MCP200 Galkina, 2015, Inhibition of the GTPase dynamin or actin depolymerisation initiates outward plasma membrane tubulation/vesiculation (cytoneme formation) in neutrophils, Biol. Cell., 107, 144, 10.1111/boc.201400063 Galkina, 2012, Proteome analysis identified human neutrophil membrane tubulovesicular extensions (cytonemes, membrane tethers) as bactericide trafficking, Biochim. Biophys. Acta, 1820, 1705, 10.1016/j.bbagen.2012.06.016 Aslam, 2013, Activation of neutrophils by the two-component Leukotoxin LukE/D from Staphylococcus aureus: proteomic analysis of the secretions, J. Proteome Res., 12, 3667, 10.1021/pr400199x Lim, 2018, Thrombin and plasmin alter the proteome of neutrophil extracellular traps, Front. Immunol., 9, 1554, 10.3389/fimmu.2018.01554 O’Donoghue, 2013, Global substrate profiling of proteases in human neutrophil extracellular traps reveals consensus motif predominantly contributed by elastase, PLoS One, 8, 10.1371/journal.pone.0075141 Urban, 2009, Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans, PLoS Pathog., 5, 10.1371/journal.ppat.1000639 Dalli, 2013, Heterogeneity in neutrophil microparticles reveals distinct proteome and functional properties, Mol. Cell. Proteomics, 12, 2205, 10.1074/mcp.M113.028589 Jethwaney, 2007, Proteomic analysis of plasma membrane and secretory vesicles from human neutrophils, Proteome Sci., 5, 12, 10.1186/1477-5956-5-12 Silvestre-Roig, 2019, Externalized histone H4 orchestrates chronic inflammation by inducing lytic cell death, Nature, 569, 236, 10.1038/s41586-019-1167-6 Lee, 2017, Neutrophil extracellular traps (NETs) in autoimmune diseases: a comprehensive review, Autoimmun. Rev., 16, 1160, 10.1016/j.autrev.2017.09.012 Albrengues, 2018, Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice, Science, 361, 10.1126/science.aao4227 Park, 2016, Cancer cells induce metastasis-supporting neutrophil extracellular DNA traps, Sci. Transl. Med., 8, 10.1126/scitranslmed.aag1711 Wang, 2018, A label-free quantitative proteomic analysis of mouse neutrophil extracellular trap formation induced by Streptococcus suis or phorbol myristate acetate (PMA), Front. Immunol., 9, 2615, 10.3389/fimmu.2018.02615 Lominadze, 2006, Proteomic analysis of human neutrophils, Methods Mol. Biol., 332, 343 de Souza Castro, 2006, Proteome analysis of resting human neutrophils, Protein Pept. Lett., 13, 481, 10.2174/092986606776819529 Trusch, 2012, Displacement chromatography as first separating step in online two-dimensional liquid chromatography coupled to mass spectrometry analysis of a complex protein sample--the proteome of neutrophils, J. Chromatogr. A, 1232, 288, 10.1016/j.chroma.2012.02.029 Tomazella, 2010, Analysis of detergent-insoluble and whole cell lysate fractions of resting neutrophils using high-resolution mass spectrometry, J. Proteome Res., 9, 2030, 10.1021/pr1000253 Tomazella, 2009, Proteomic analysis of total cellular proteins of human neutrophils, Proteome Sci., 7, 32, 10.1186/1477-5956-7-32 Kennedy, 2011, Benefits of heat treatment to the protease packed neutrophil for proteome analysis: halting protein degradation, Proteomics, 11, 2560, 10.1002/pmic.201000625 Rieckmann, 2017, Social network architecture of human immune cells unveiled by quantitative proteomics, Nat. Immunol., 18, 583, 10.1038/ni.3693 Muschter, 2015, Mass spectrometric phosphoproteome analysis of small-sized samples of human neutrophils, Clin. Chim. Acta, 451, 199, 10.1016/j.cca.2015.09.030 Luerman, 2011, Identification of phosphoproteins associated with human neutrophil granules following chemotactic peptide stimulation, Mol. Cell. Proteomics, 10, 10.1074/mcp.M110.001552 Chacko, 2016, Pleiotropic effects of 4-hydroxynonenal on oxidative burst and phagocytosis in neutrophils, Redox Biol., 9, 57, 10.1016/j.redox.2016.06.003 Zhu, 2014, Quantitative proteomics reveals differential biological processes in healthy neonatal cord neutrophils and adult neutrophils, Proteomics, 14, 1688, 10.1002/pmic.201400009 Jassinskaja, 2017, Comprehensive proteomic characterization of ontogenic changes in hematopoietic stem and progenitor cells, Cell Rep., 21, 3285, 10.1016/j.celrep.2017.11.070 Tak, 2017, Human CD62Ldim neutrophils identified as a separate subset by proteome profiling and in vivo pulse-chase labeling, Blood, 129, 3476, 10.1182/blood-2016-07-727669 Capuozzo, 2017, A proteomic approach to study the effect of thiotaurine on human neutrophil activation, Adv. Exp. Med. Biol., 975, 563, 10.1007/978-94-024-1079-2_44 Aquino, 2016, Proteomic analysis of neutrophil priming by PAF, Protein Pept. Lett., 23, 142, 10.2174/0929866523666151202210604 Shahriary, 2015, Comparative proteome analysis of peripheral neutrophils from sulfur mustard-exposed and COPD patients, J. Immunotoxicol., 12, 132, 10.3109/1547691X.2014.914110 Grabowski, 2019, Proteome analysis of human neutrophil granulocytes from patients with monogenic disease using data-independent acquisition, Mol. Cell. Proteomics, 18, 760, 10.1074/mcp.RA118.001141 Serwas, 2018, CEBPE-mutant specific granule deficiency correlates with aberrant granule organization and substantial proteome alterations in neutrophils, Front. Immunol., 9, 588, 10.3389/fimmu.2018.00588 Sørensen, 2014, Papillon-Lefèvre syndrome patient reveals species-dependent requirements for neutrophil defenses, J. Clin. Invest., 124, 4539, 10.1172/JCI76009 Kazama, 2014, Peroxiredoxin 2 expression is increased in neutrophils of patients with refractory cytopenia with multilineage dysplasia, Br. J. Haematol., 166, 720, 10.1111/bjh.12954 Yu, 2017, Comprehensive metaproteomic analyses of urine in the presence and absence of neutrophil-associated inflammation in the urinary tract, Theranostics, 7, 238, 10.7150/thno.16086 Loi, 2017, Proteomic profiling of peripheral blood neutrophils identifies two inflammatory phenotypes in stable COPD patients, Respir. Res., 18, 100, 10.1186/s12931-017-0586-x Abdel Malik, 2017, AMP-activated protein kinase α2 in neutrophils regulates vascular repair via hypoxia-inducible factor-1α and a network of proteins affecting metabolism and apoptosis, Circ. Res., 120, 99, 10.1161/CIRCRESAHA.116.309937 UniProt Consortium, 2019, UniProt: a worldwide hub of protein knowledge, Nucleic Acids Res., 47, D506, 10.1093/nar/gky1049 Borregaard, 1997, Granules of the human neutrophilic polymorphonuclear leukocyte, Blood, 89, 3503, 10.1182/blood.V89.10.3503 Mollinedo, 2019, Neutrophil degranulation, plasticity, and cancer metastasis, Trends Immunol., 40, 228, 10.1016/j.it.2019.01.006 Sheshachalam, 2014, Granule protein processing and regulated secretion in neutrophils, Front. Immunol., 5, 448, 10.3389/fimmu.2014.00448 Fiedler, 2012, The role of transcription factors in the guidance of granulopoiesis, Am. J. Blood Res., 2, 57 Roberts, 2005, G-CSF: a key regulator of neutrophil production, but that’s not all!, Growth Factors, 23, 33, 10.1080/08977190500055836 Grassi, 2018, Dynamics of transcription regulation in human bone marrow myeloid differentiation to mature blood neutrophils, Cell Rep., 24, 2784, 10.1016/j.celrep.2018.08.018 Avellino, 2017, Expression and regulation of C/EBPα in normal myelopoiesis and in malignant transformation, Blood, 129, 2083, 10.1182/blood-2016-09-687822 Vassen, 2007, Gfi1b:green fluorescent protein knock-in mice reveal a dynamic expression pattern of Gfi1b during hematopoiesis that is largely complementary to Gfi1, Blood, 109, 2356, 10.1182/blood-2006-06-030031 Hock, 2003, Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation, Immunity, 18, 109, 10.1016/S1074-7613(02)00501-0 Karsunky, 2002, Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1, Nat. Genet., 30, 295, 10.1038/ng831 Tamura, 2017, Regulation of mononuclear phagocyte development by IRF8, Rinsho Ketsueki, 58, 798 Friedman, 2007, C/EBPα induces PU.1 and interacts with AP-1 and NF-κB to regulate myeloid development, Blood Cells Mol. Dis., 39, 340, 10.1016/j.bcmd.2007.06.010 Liu, 2012, Gfi-1 inhibits the expression of eosinophil major basic protein (MBP) during G-CSF-induced neutrophilic differentiation, Int. J. Hematol., 95, 640, 10.1007/s12185-012-1078-x Skokowa, 2006, LEF-1 is crucial for neutrophil granulocytopoiesis and its expression is severely reduced in congenital neutropenia, Nat. Med., 12, 1191, 10.1038/nm1474 Bjerregaard, 2003, The in vivo profile of transcription factors during neutrophil differentiation in human bone marrow, Blood, 101, 4322, 10.1182/blood-2002-03-0835 Jin, 2016, c-Myb acts in parallel and cooperatively with Cebp1 to regulate neutrophil maturation in zebrafish, Blood, 128, 415, 10.1182/blood-2015-12-686147 Behre, 1999, c-Jun is a JNK-independent coactivator of the PU.1 transcription factor, J. Biol. Chem., 274, 4939, 10.1074/jbc.274.8.4939 Malu, 2016, Cooperative activity of GABP with PU.1 or C/EBPε regulates lamin B receptor gene expression, implicating their roles in granulocyte nuclear maturation, J. Immunol., 197, 910, 10.4049/jimmunol.1402285 Segel, 2011, The paradox of the neutrophil’s role in tissue injury, J. Leukoc. Biol., 89, 359, 10.1189/jlb.0910538 Almkvist, 2001, Lipopolysaccharide-induced gelatinase granule mobilization primes neutrophils for activation by galectin-3 and formylmethionyl-Leu-Phe, Infect. Immun., 69, 832, 10.1128/IAI.69.2.832-837.2001 Simard, 2010, Induction of neutrophil degranulation by S100A9 via a MAPK-dependent mechanism, J. Leukoc. Biol., 87, 905, 10.1189/jlb.1009676 Niessen, 1991, Release of azurophilic granule contents in fMLP-stimulated neutrophils requires two activation signals, one of which is a rise in cytosolic free Ca2+, Cell. Signal., 3, 625, 10.1016/0898-6568(91)90039-W Lacy, 2006, Mechanisms of degranulation in neutrophils, Allergy, Asthma Clin. Immunol., 2, 98, 10.1186/1710-1492-2-3-98 Martín-Martín, 2000, Involvement of SNAP-23 and syntaxin 6 in human neutrophil exocytosis, Blood, 96, 2574, 10.1182/blood.V96.7.2574 Mollinedo, 2006, Combinatorial SNARE complexes modulate the secretion of cytoplasmic granules in human neutrophils, J. Immunol., 177, 2831, 10.4049/jimmunol.177.5.2831 Pivot-Pajot, 2008, Munc13-4 regulates granule secretion in human neutrophils, J. Immunol., 180, 6786, 10.4049/jimmunol.180.10.6786 Herrero-Turrión, 2008, Rab27a regulates exocytosis of tertiary and specific granules in human neutrophils, J. Immunol., 181, 3793, 10.4049/jimmunol.181.6.3793 Mollinedo, 2003, J. Immunol., 170, 1034, 10.4049/jimmunol.170.2.1034 Jiménez-Alcázar, 2017, Host DNases prevent vascular occlusion by neutrophil extracellular traps, Science, 358, 1202, 10.1126/science.aam8897 Cassatella, 1999, Neutrophil-derived proteins: selling cytokines by the pound, Adv. Immunol., 73, 369, 10.1016/S0065-2776(08)60791-9 Ley, 2018, Neutrophils: new insights and open questions, Sci. Immunol., 3, 10.1126/sciimmunol.aat4579 Tamassia, 2018, Cytokine production by human neutrophils: revisiting the “dark side of the moon.”, Eur. J. Clin. Investig., 48, 10.1111/eci.12952 Németh, 2016, Neutrophil-specific deletion of the CARD9 gene expression regulator suppresses autoantibody-induced inflammation in vivo, Nat. Commun., 7, 10.1038/ncomms11004 Roth, 2015, Secondary necrotic neutrophils release interleukin-16C and macrophage migration inhibitory factor from stores in the cytosol, Cell Death Discov., 1, 10.1038/cddiscovery.2015.56 Arruda-Silva, 2017, Human neutrophils produce CCL23 in response to various TLR-agonists and TNFα, Front. Cell. Infect. Microbiol., 7, 176, 10.3389/fcimb.2017.00176 Tamassia, 2019, Human neutrophils activated via TLR8 promote Th17 polarization through IL-23, J. Leukoc. Biol., 10.1002/JLB.MA0818-308R Xu, 2017, IL33-mediated ILC2 activation and neutrophil IL5 production in the lung response after severe trauma: a reverse translation study from a human cohort to a mouse trauma model, PLoS Med., 14, 10.1371/journal.pmed.1002365 Sun, 2018, Characterization and allergic role of IL-33-induced neutrophil polarization, Cell. Mol. Immunol., 15, 782, 10.1038/cmi.2017.163 Cheung, 2018, Cysteinyl leukotriene receptor 1 expression identifies a subset of neutrophils during the antiviral response that contributes to postviral atopic airway disease, J. Allergy Clin. Immunol., 142, 1206, 10.1016/j.jaci.2017.11.026 Wang, 2016, Nonredundant roles of keratinocyte-derived IL-34 and neutrophil-derived CSF1 in Langerhans cell renewal in the steady state and during inflammation, Eur. J. Immunol., 46, 552, 10.1002/eji.201545917 Bozoyan, 2015, Interleukin-36γ is expressed by neutrophils and can activate microglia, but has no role in experimental autoimmune encephalomyelitis, J. Neuroinflammation, 12, 173, 10.1186/s12974-015-0392-7 Scapini, 1999, On the detection of neutrophil-derived vascular endothelial growth factor (VEGF), J. Immunol. Methods, 232, 121, 10.1016/S0022-1759(99)00170-2 Manfroi, 2017, CXCL-8/IL8 produced by diffuse large B-cell lymphomas recruits neutrophils expressing a proliferation-inducing ligand APRIL, Cancer Res., 77, 1097, 10.1158/0008-5472.CAN-16-0786 Kobayashi, 2010, Rapid neutrophil destruction following phagocytosis of Staphylococcus aureus, J. Innate Immun., 2, 560, 10.1159/000317134 Fradin, 2007, The early transcriptional response of human granulocytes to infection with Candida albicans is not essential for killing but reflects cellular communications, Infect. Immun., 75, 1493, 10.1128/IAI.01651-06 Muntaka, 2019, Gamma interferon and interleukin-17A differentially influence the response of human macrophages and neutrophils to Pseudomonas aeruginosa infection, Infect. Immun., 87, 10.1128/IAI.00814-18 Charmoy, 2010, Neutrophil-derived CCL3 is essential for the rapid recruitment of dendritic cells to the site of Leishmania major inoculation in resistant mice, PLoS Pathog., 6, 10.1371/journal.ppat.1000755 Puga, 2011, B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen, Nat. Immunol., 13, 170, 10.1038/ni.2194 Lim, 2015, Neutrophil trails guide influenza-specific CD8+ T cells in the airways, Science, 349, 10.1126/science.aaa4352 Giambelluca, 2014, TNF-α expression in neutrophils and its regulation by glycogen synthase kinase-3: a potentiating role for lithium, FASEB J., 28, 3679, 10.1096/fj.14-251900 Huang, 2017, MicroRNA-142-3p and let-7g negatively regulates augmented IL-6 production in neonatal polymorphonuclear leukocytes, Int. J. Biol. Sci., 13, 690, 10.7150/ijbs.17030 Scapini, 2005, Proinflammatory mediators elicit secretion of the intracellular B-lymphocyte stimulator pool (BLyS) that is stored in activated neutrophils: implications for inflammatory diseases, Blood, 105, 830, 10.1182/blood-2004-02-0564 Cassatella, 2006, Interferon-activated neutrophils store a TNF-related apoptosis-inducing ligand (TRAIL/Apo-2 ligand) intracellular pool that is readily mobilizable following exposure to proinflammatory mediators, J. Leukoc. Biol., 79, 123, 10.1189/jlb.0805431 Ostuni, 2016, Epigenetic regulation of neutrophil development and function, Semin. Immunol., 28, 83, 10.1016/j.smim.2016.04.002 Scapini, 2001, Neutrophils produce biologically active macrophage inflammatory protein-3alpha (MIP-3alpha)/CCL20 and MIP-3beta/CCL19, Eur. J. Immunol., 31, 1981, 10.1002/1521-4141(200107)31:7<1981::AID-IMMU1981>3.0.CO;2-X Tamassia, 2008, Activation of an immunoregulatory and antiviral gene expression program in poly(I:C)-transfected human neutrophils, J. Immunol., 181, 6563, 10.4049/jimmunol.181.9.6563 Davidson, 2013, Gene expression profile of endotoxin-stimulated leukocytes of the term new born: control of cytokine gene expression by interleukin-10, PLoS One, 8, 10.1371/journal.pone.0053641 Tamassia, 2007, The MyD88-independent pathway is not mobilized in human neutrophils stimulated via TLR4, J. Immunol., 178, 7344, 10.4049/jimmunol.178.11.7344 Tamassia, 2013, Cutting edge: an inactive chromatin configuration at the IL-10 locus in human neutrophils, J. Immunol., 190, 1921, 10.4049/jimmunol.1203022 Zimmermann, 2015, Chromatin remodelling and autocrine TNFα are required for optimal interleukin-6 expression in activated human neutrophils, Nat. Commun., 6, 6061, 10.1038/ncomms7061 Monticelli, 2017, Transcriptional determination and functional specificity of myeloid cells: making sense of diversity, Nat. Rev. Immunol., 17, 595, 10.1038/nri.2017.51 Heinz, 2015, The selection and function of cell type-specific enhancers, Nat. Rev. Mol. Cell Biol., 16, 144, 10.1038/nrm3949 Lyons, 2007, Microarray analysis of human leucocyte subsets: the advantages of positive selection and rapid purification, BMC Genomics, 8, 64, 10.1186/1471-2164-8-64 Hahn, 2019, Aggregated neutrophil extracellular traps resolve inflammation by proteolysis of cytokines and chemokines and protection from antiproteases, FASEB J., 33, 1401, 10.1096/fj.201800752R Clancy, 2018, Extracellular neutrophil proteases are efficient regulators of IL-1, IL-33, and IL-36 cytokine activity but poor effectors of microbial killing, Cell Rep., 22, 2937, 10.1016/j.celrep.2018.02.062 Haneke, 1979, The Papillon-Lefèvre syndrome: keratosis palmoplantaris with periodontopathy. Report of a case and review of the cases in the literature, Hum. Genet., 51, 1, 10.1007/BF00278288 McLoed, 2016, Neutrophil-derived IL-1β impairs the efficacy of NF-κB inhibitors against lung cancer, Cell Rep., 16, 120, 10.1016/j.celrep.2016.05.085 Soehnlein, 2008, Neutrophil secretion products pave the way for inflammatory monocytes, Blood, 112, 1461, 10.1182/blood-2008-02-139634 Wantha, 2013, Neutrophil-derived cathelicidin promotes adhesion of classical monocytes, Circ. Res., 112, 792, 10.1161/CIRCRESAHA.112.300666 Döring, 2012, Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice, Circ. Res., 110, 1052, 10.1161/CIRCRESAHA.112.265868 Winter, 2018, Chrono-pharmacological targeting of the CCL2-CCR2 axis ameliorates atherosclerosis, Cell Metab., 28, 175, 10.1016/j.cmet.2018.05.002 von Hundelshausen, 2017, Chemokine interactome mapping enables tailored intervention in acute and chronic inflammation, Sci. Transl. Med., 9, 10.1126/scitranslmed.aah6650 Alard, 2015, Recruitment of classical monocytes can be inhibited by disturbing heteromers of neutrophil HNP1 and platelet CCL5, Sci. Transl. Med., 7, 10.1126/scitranslmed.aad5330 Grégoire, 2015, Neutrophils trigger a NF-κB dependent polarization of tumor-supportive stromal cells in germinal center B-cell lymphomas, Oncotarget, 6, 16471, 10.18632/oncotarget.4106 Di Mitri, 2014, Tumour-infiltrating Gr-1+ myeloid cells antagonize senescence in cancer, Nature, 515, 134, 10.1038/nature13638 Calcinotto, 2018, IL-23 secreted by myeloid cells drives castration-resistant prostate cancer, Nature, 559, 363, 10.1038/s41586-018-0266-0 Houghton, 2010, Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth, Nat. Med., 16, 219, 10.1038/nm.2084 Casanova-Acebes, 2018, Neutrophils instruct homeostatic and pathological states in naive tissues, J. Exp. Med., 215, 2778, 10.1084/jem.20181468 Adrover, 2019, A neutrophil timer coordinates immune defense and vascular protection, Immunity, 50, 390, 10.1016/j.immuni.2019.01.002 Horckmans, 2017, Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype, Eur. Heart J., 38, 187 Tahir, 2018, Analysis of the effect of intestinal ischemia and reperfusion on the rat neutrophils proteome, Front. Mol. Biosci., 5, 89, 10.3389/fmolb.2018.00089 Arshid, 2017, Neutrophil proteomic analysis reveals the participation of antioxidant enzymes, motility and ribosomal proteins in the prevention of ischemic effects by preconditioning, J. Proteome, 151, 162, 10.1016/j.jprot.2016.05.016 Arshid, 2017, High performance mass spectrometry based proteomics reveals enzyme and signaling pathway regulation in neutrophils during the early stage of surgical trauma, Proteomics Clin. Appl., 11 Singh, 2014, Proteome dynamics in neutrophils of adult zebrafish upon chemically-induced inflammation, Fish Shellfish Immunol., 40, 217, 10.1016/j.fsi.2014.06.035 Calzetti, 2017, The importance of being "pure" neutrophils, J. Allergy Clin. Immunol., 139, 352, 10.1016/j.jaci.2016.06.025 Tamassia, 2014, Fast and accurate quantitative analysis of cytokine gene expression in human neutrophils, Methods Mol. Biol., 1124, 451, 10.1007/978-1-62703-845-4_27 Tamassia, 2018, A reappraisal on the potential ability of human neutrophils to express and produce IL-17 family members in vitro: failure to reproducibly detect it, Front. Immunol., 9, 795, 10.3389/fimmu.2018.00795