Neutrophil migration in infection and wound repair: going forward in reverse (original) (raw)

• Kolaczkowska, E. & Kubes, P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175 (2013).
  Article CAS PubMed Google Scholar
• Nathan, C. Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173–182 (2006).
  CAS PubMed Google Scholar
• Borregaard, N. Neutrophils, from marrow to microbes. Immunity 33, 657–670 (2010).
  CAS PubMed Google Scholar
• Caielli, S., Banchereau, J. & Pascual, V. Neutrophils come of age in chronic inflammation. Curr. Opin. Immunol. 24, 671–677 (2012).
  CAS PubMed PubMed Central Google Scholar
• Ley, K. Integration of inflammatory signals by rolling neutrophils. Immunol. Rev. 186, 8–18 (2002).
  CAS PubMed Google Scholar
• Gambardella, L. & Vermeren, S. Molecular players in neutrophil chemotaxis—focus on PI3K and small GTPases. J. Leukoc. Biol. 94, 603–612 (2013).
  CAS PubMed Google Scholar
• Ng, L. G. et al. Visualizing the neutrophil response to sterile tissue injury in mouse dermis reveals a three-phase cascade of events. J. Investigative Dermatol. 131, 2058–2068 (2011).
  CAS Google Scholar
• Lämmermann, T. In the eye of the neutrophil swarm-navigation signals that bring neutrophils together in inflamed and infected tissues. J. Leukoc. Biol. pii: jlb.1MR0915-403 (2015).
• Nourshargh, S. & Alon, R. Leukocyte migration into inflamed tissues. Immunity 41, 694–707 (2014).
  CAS PubMed Google Scholar
• Weninger, W., Biro, M. & Jain, R. Leukocyte migration in the interstitial space of non-lymphoid organs. Nat. Rev. Immunol. 14, 232–246 (2014).
  CAS PubMed Google Scholar
• Futosi, K., Fodor, S. & Mócsai, A. Neutrophil cell surface receptors and their intracellular signal transduction pathways. Int. Immunopharmacol. 17, 638–650 (2013).
  CAS PubMed PubMed Central Google Scholar
• Sun, L. & Ye, R. D. Role of G protein-coupled receptors in inflammation. Acta Pharmacol. Sin. 33, 342–350 (2012).
  CAS PubMed PubMed Central Google Scholar
• Viola, A. & Luster, A. D. Chemokines and their receptors: drug targets in immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 48, 171–197 (2008).
  CAS PubMed Google Scholar
• Pittman, K. & Kubes, P. Damage-associated molecular patterns control neutrophil recruitment. J. Innate Immun. 5, 315–323 (2013).
  CAS PubMed Google Scholar
• Broggi, A. & Granucci, F. Microbe- and danger-induced inflammation. Mol. Immunol. 63, 127–133 (2015).
  CAS PubMed Google Scholar
• Vénéreau, E., Ceriotti, C. & Bianchi, M. E. DAMPs from Cell Death to New Life. Frontiers Immunol. 6, 422 (2015).
  Google Scholar
• Cordeiro, J. V. V. & Jacinto, A. The role of transcription-independent damage signals in the initiation of epithelial wound healing. Nat. Rev. Mol. Cell Biol. 14, 249–262 (2013).
  CAS PubMed Google Scholar
• Niethammer, P., Grabher, C., Look, A. T. & Mitchison, T. J. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996–999 (2009). This is the first paper to visualize H 2 O 2 tissue gradients in wound-induced inflammatory responses using zebrafish.
  CAS PubMed PubMed Central Google Scholar
• Moreira, S., Stramer, B., Evans, I., Wood, W. & Martin, P. Prioritization of competing damage and developmental signals by migrating macrophages in the Drosophila embryo. Curr. Biol. 20, 464–470 (2010).
  CAS PubMed Google Scholar
• Yoo, S. K., Starnes, T. W., Deng, Q. & Huttenlocher, A. Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature 480, 109–112 (2011).
  CAS PubMed PubMed Central Google Scholar
• Klyubin, I. V., Kirpichnikova, K. M. & Gamaley, I. A. Hydrogen peroxide-induced chemotaxis of mouse peritoneal neutrophils. Eur. J. Cell Biol. 70, 347–351 (1996).
  CAS PubMed Google Scholar
• Kovács, M. et al. The Src family kinases Hck, Fgr, and Lyn are critical for the generation of the in vivo inflammatory environment without a direct role in leukocyte recruitment. J. Exp. Med. 211, 1993–2011 (2014).
  PubMed PubMed Central Google Scholar
• Baroja-Mazo, A., Barberà- Cremades, M. & Pelegrín, P. The participation of plasma membrane hemichannels to purinergic signaling. Biochim. Biophys. Acta 1828, 79–93 (2013).
  CAS PubMed Google Scholar
• de Oliveira, S. et al. ATP modulates acute inflammation in vivo through dual oxidase 1-derived H2O2 production and NF-κB activation. J. Immunol. 192, 5710–5719 (2014).
  CAS PubMed Google Scholar
• Elliott, M. R. et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461, 282–286 (2009).
  CAS PubMed PubMed Central Google Scholar
• Chen, Y. et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 314, 1792–1795 (2006).
  CAS PubMed Google Scholar
• Bao, Y. et al. mTOR and differential activation of mitochondria orchestrate neutrophil chemotaxis. J. Cell Biol. 210, 1153–1164 (2015).
  CAS PubMed PubMed Central Google Scholar
• Kukulski, F. et al. Extracellular ATP and P2 receptors are required for IL-8 to induce neutrophil migration. Cytokine 46, 166–170 (2009).
  CAS PubMed PubMed Central Google Scholar
• Lecut, C. et al. P2X1 ion channels promote neutrophil chemotaxis through Rho kinase activation. J. Immunol. 183, 2801–2809 (2009).
  CAS PubMed Google Scholar
• Zhang, Q. et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464, 104–107 (2010).
  CAS PubMed PubMed Central Google Scholar
• Raoof, M., Zhang, Q., Itagaki, K. & Hauser, C. J. Mitochondrial peptides are potent immune activators that activate human neutrophils via FPR-1. J. Trauma 68, 1328 (2010).
  CAS PubMed Google Scholar
• Li, L. et al. New development in studies of formyl-peptide receptors: critical roles in host defense. J. Leukoc. Biol. 99, 425–435 (2015).
  PubMed PubMed Central Google Scholar
• McDonald, B. et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330, 362–366 (2010).
  CAS PubMed Google Scholar
• Pase, L. et al. Neutrophil-delivered myeloperoxidase dampens the hydrogen peroxide burst after tissue wounding in zebrafish. Curr. Biol. 22, 1818–1824 (2012).
  CAS PubMed Google Scholar
• Russo, R. C., Garcia, C. C., Teixeira, M. M. & Amaral, F. A. The CXCL8/IL-8 chemokine family and its receptors in inflammatory diseases. Expert Rev. Clin. Immunol. 10, 593–619 (2014).
  CAS PubMed Google Scholar
• Kobayashi, Y. The role of chemokines in neutrophil biology. Frontiers Biosci. 13, 2400–2407 (2008).
  CAS Google Scholar
• Sai, J., Raman, D., Liu, Y., Wikswo, J. & Richmond, A. Parallel phosphatidylinositol 3-kinase (PI3K)-dependent and Src-dependent pathways lead to CXCL8-mediated Rac2 activation and chemotaxis. J. Biol. Chem. 283, 26538–26547 (2008).
  CAS PubMed PubMed Central Google Scholar
• Neel, N. F. et al. VASP is a CXCR2-interacting protein that regulates CXCR2-mediated polarization and chemotaxis. J. Cell Sci. 122, 1882–1894 (2009).
  CAS PubMed PubMed Central Google Scholar
• Lindley, I. et al. Synthesis and expression in Escherichia coli of the gene encoding monocyte-derived neutrophil-activating factor: biological equivalence between natural and recombinant neutrophil-activating factor. Proc. Natl Acad. Sci. USA 85, 9199–9203 (1988).
  CAS PubMed Google Scholar
• de Oliveira, S. et al. Cxcl8 (IL-8) mediates neutrophil recruitment and behavior in the zebrafish inflammatory response. J. Immunol. 190, 4349–4359 (2013).
  CAS PubMed PubMed Central Google Scholar
• Deng, Q. et al. Localized bacterial infection induces systemic activation of neutrophils through Cxcr2 signaling in zebrafish. J. Leukoc. Biol. 93, 761–769 (2013).
  CAS PubMed PubMed Central Google Scholar
• Sarris, M. et al. Inflammatory chemokines direct and restrict leukocyte migration within live tissues as glycan-bound gradients. Curr. Biol. 22, 2375–2382 (2012). This work identified glycan-bound CXCL8 gradients in vivo that mediate neutrophil directed migration to inflamed tissue in zebrafish.
  CAS PubMed Google Scholar
• Cacalano, G. et al. Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265, 682–684 (1994).
  CAS PubMed Google Scholar
• Devalaraja, R. M. et al. Delayed wound healing in CXCR2 knockout mice. J. Invest. Dermatol. 115, 234–244 (2000).
  CAS PubMed PubMed Central Google Scholar
• Monneau, Y., Arenzana-Seisdedos, F. & Lortat-Jacob, H. The sweet spot: how GAGs help chemokines guide migrating cells. J. Leukoc. Biol. pii: jlb.3MR0915-440R (2015).
• Middleton, J. et al. Transcytosis and surface presentation of IL-8 by venular endothelial cells. Cell 91, 385–395 (1997).
  CAS PubMed Google Scholar
• Powell, W. S., Gravel, S., MacLeod, R. J., Mills, E. & Hashefi, M. Stimulation of human neutrophils by 5-oxo-6,8,11,14-eicosatetraenoic acid by a mechanism independent of the leukotriene B4 receptor. J. Biol. Chem. 268, 9280–9286 (1993).
  CAS PubMed Google Scholar
• Øynebråten, I. et al. Characterization of a novel chemokine-containing storage granule in endothelial cells: evidence for preferential exocytosis mediated by protein kinase A and diacylglycerol. J. Immunol. 175, 5358–5369 (2005).
  PubMed Google Scholar
• Hol, J., Wilhelmsen, L. & Haraldsen, G. The murine IL-8 homologues KC, MIP-2, and LIX are found in endothelial cytoplasmic granules but not in Weibel-Palade bodies. J. Leukoc. Biol. 87, 501–508 (2010).
  CAS PubMed Google Scholar
• Iyer, S. S. et al. Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc. Natl Acad. Sci. USA 106, 20388–20393 (2009).
  CAS PubMed Google Scholar
• Enyedi, B., Kala, S., Nikolich-Zugich, T. & Niethammer, P. Tissue damage detection by osmotic surveillance. Nat. Cell Biol. 15, 1123–1130 (2013).
  CAS PubMed PubMed Central Google Scholar
• Sadik, C. D. & Luster, A. D. Lipid-cytokine-chemokine cascades orchestrate leukocyte recruitment in inflammation. J. Leukoc. Biol. 91, 207–215 (2012).
  CAS PubMed PubMed Central Google Scholar
• Afonso, P. V. et al. LTB4 is a signal-relay molecule during neutrophil chemotaxis. Dev. Cell 22, 1079–1091 (2012). This study describes the role of autocrine LTB 4 gradients at the leading edge that guide neutrophil recruitment to sites of inflammation.
  CAS PubMed PubMed Central Google Scholar
• Lämmermann, T. et al. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498, 371–375 (2013). This work reports an initial molecular map of different factors that modulate neutrophil swarming behaviour in response to tissue damage in mice.
  PubMed Google Scholar
• Wipke, B. T. & Allen, P. M. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J. Immunol. 167, 1601–1608 (2001).
  CAS PubMed Google Scholar
• Chen, M. et al. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis. J. Exp. Med. 203, 837–842 (2006).
  CAS PubMed PubMed Central Google Scholar
• Hazeldine, J., Hampson, P., Opoku, F. A., Foster, M. & Lord, J. M. N-Formyl peptides drive mitochondrial damage associated molecular pattern induced neutrophil activation through ERK1/2 and P38 MAP kinase signalling pathways. Injury 46, 975–984 (2015).
  PubMed Google Scholar
• Chou, R. C. et al. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 33, 266–278 (2010).
  CAS PubMed PubMed Central Google Scholar
• Van den Steen, P. E., Proost, P., Wuyts, A., Van Damme, J. & Opdenakker, G. Neutrophil gelatinase B potentiates interleukin-8 tenfold by amino-terminal processing, whereas it degrades CTAP-III, PF-4, and GRO-α and leaves RANTES and MCP-2 intact. Blood 96, 2673–2681 (2000).
  CAS PubMed Google Scholar
• Tester, A. M. et al. LPS responsiveness and neutrophil chemotaxis in vivo require PMN MMP-8 activity. PLoS ONE 2, e312. (2007).
  PubMed PubMed Central Google Scholar
• Afonso, P. V., McCann, C. P., Kapnick, S. M. & Parent, C. A. Discoidin domain receptor 2 regulates neutrophil chemotaxis in 3D collagen matrices. Blood 121, 1644–1650 (2013).
  CAS PubMed PubMed Central Google Scholar
• Soehnlein, O. & Lindbom, L. Phagocyte partnership during the onset and resolution of inflammation. Nat. Rev. Immunol. 10, 427–439 (2010).
  CAS PubMed Google Scholar
• Peters, N. C. et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321, 970–974 (2008).
  CAS PubMed PubMed Central Google Scholar
• Kreisel, D. et al. In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc. Natl Acad. Sci. USA 107, 18073–18078 (2010).
  CAS PubMed Google Scholar
• Chtanova, T. et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29, 487–496 (2008).
  CAS PubMed PubMed Central Google Scholar
• Silva, M. T. Bacteria-induced phagocyte secondary necrosis as a pathogenicity mechanism. J. Leukoc. Biol. 88, 885–896 (2010).
  CAS PubMed Google Scholar
• Gonzalez, C. D., Ledo, C., Giai, C., Garófalo, A. & Gómez, M. I. The Sbi protein contributes to Staphylococcus aureus inflammatory response during systemic infection. PLoS ONE 10, e0131879 (2015).
  PubMed PubMed Central Google Scholar
• Abtin, A. et al. Perivascular macrophages mediate neutrophil recruitment during bacterial skin infection. Nat. Immunol. 15, 45–53 (2014).
  CAS PubMed Google Scholar
• Spinner, J. L., Hasenkrug, A. M., Shannon, J. G., Kobayashi, S. D. & Hinnebusch, B. J. Role of the Yersinia YopJ protein in suppressing interleukin-8 secretion by human polymorphonuclear leukocytes. Microbes Infect. 18, 21–29 (2016).
  CAS PubMed Google Scholar
• Palm, N. W. & Medzhitov, R. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 227, 221–233 (2009).
  CAS PubMed Google Scholar
• Schiwon, M. et al. Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium. Cell 156, 456–468 (2014).
  CAS PubMed PubMed Central Google Scholar
• Sacramento, L. et al. TLR9 signaling on dendritic cells regulates neutrophil recruitment to inflammatory foci following Leishmania infantum infection. Infect. Immun. 83, 4604–4616 (2015).
  CAS PubMed PubMed Central Google Scholar
• Abraham, S. N. & John, A. L. Mast cell-orchestrated immunity to pathogens. Nat. Rev. Immunol. 10, 440–452 (2010).
  CAS PubMed PubMed Central Google Scholar
• Krishna, S. & Miller, L. S. Innate and adaptive immune responses against Staphylococcus aureus skin infections. Semin. Immunopathol. 34, 261–280 (2012).
  CAS PubMed Google Scholar
• Malaviya, R., Ikeda, T., Ross, E. & Abraham, S. N. Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-α. Nature 381, 77–80 (1996).
  CAS PubMed Google Scholar
• Huang, C. et al. Induction of a selective and persistent extravasation of neutrophils into the peritoneal cavity by tryptase mouse mast cell protease 6. J. Immunol. 160, 1910–1919 (1998).
  CAS PubMed Google Scholar
• Malaviya, R. & Abraham, S. N. Role of mast cell leukotrienes in neutrophil recruitment and bacterial clearance in infectious peritonitis. J. Leukoc. Biol. 67, 841–846 (2000).
  CAS PubMed Google Scholar
• Miller, L. S. et al. Inflammasome-mediated production of IL-1β is required for neutrophil recruitment against Staphylococcus aureus in vivo. J. Immunol. 179, 6933–6942 (2007).
  CAS PubMed Google Scholar
• Shimada, T. et al. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1β secretion. Cell Host Microbe 7, 38–49 (2010).
  CAS PubMed PubMed Central Google Scholar
• Miller, L. S. et al. MyD88 mediates neutrophil recruitment initiated by IL-1R but not TLR2 activation in immunity against Staphylococcus aureus. Immunity 24, 79–91 (2006).
  CAS PubMed Google Scholar
• Sun, K., Salmon, S. L., Lotz, S. A. & Metzger, D. W. Interleukin-12 promotes γ interferon-dependent neutrophil recruitment in the lung and improves protection against respiratory Streptococcus pneumoniae infection. Infect. Immun. 75, 1196–1202 (2007).
  CAS PubMed PubMed Central Google Scholar
• Kabir, S. The role of interleukin-17 in the Helicobacter pylori induced infection and immunity. Helicobacter 16, 1–8 (2011).
  CAS PubMed Google Scholar
• Scapini, P. & Cassatella, M. A. Social networking of human neutrophils within the immune system. Blood 124, 710–719 (2014).
  CAS PubMed Google Scholar
• Isailovic, N., Daigo, K., Mantovani, A. & Selmi, C. Interleukin-17 and innate immunity in infections and chronic inflammation. J. Autoimmun 60, 1–11 (2015).
  CAS PubMed Google Scholar
• Rendon, J. L. & Choudhry, M. A. Th17 cells: critical mediators of host responses to burn injury and sepsis. J. Leukoc. Biol. 92, 529–538 (2012).
  CAS PubMed PubMed Central Google Scholar
• Mölne, L., Verdrengh, M. & Tarkowski, A. Role of neutrophil leukocytes in cutaneous infection caused by Staphylococcus aureus. Infect. Immun. 68, 6162–6167 (2000).
  PubMed PubMed Central Google Scholar
• Ley, K., Smith, E. & Stark, M. A. IL-17A-producing neutrophil-regulatory Tn lymphocytes. Immunol. Res. 34, 229–242 (2006).
  CAS PubMed Google Scholar
• Xu, S. & Cao, X. Interleukin-17 and its expanding biological functions. Cell. Mol. Immunol. 7, 164–174 (2010).
  CAS PubMed PubMed Central Google Scholar
• Cho, J. S. et al. IL-17 is essential for host defense against cutaneous Staphylococcus aureus infection in mice. J. Clin. Invest. 120, 1762–1773 (2010).
  PubMed PubMed Central Google Scholar
• Liese, J., Rooijakkers, S. H., van Strijp, J. A., Novick, R. P. & Dustin, M. L. Intravital two-photon microscopy of host-pathogen interactions in a mouse model of Staphylococcus aureus skin abscess formation. Cell. Microbiol. 15, 891–909 (2013).
  CAS PubMed Google Scholar
• Tan, R. S., Ho, B., Leung, B. P. & Ding, J. L. TLR cross-talk confers specificity to innate immunity. Int. Rev. Immunol. 33, 443–453 (2014).
  CAS PubMed PubMed Central Google Scholar
• Deng, Q., Harvie, E. A. & Huttenlocher, A. Distinct signalling mechanisms mediate neutrophil attraction to bacterial infection and tissue injury. Cell. Microbiol. 14, 517–528 (2012).
  CAS PubMed PubMed Central Google Scholar
• Yan, B. et al. IL-1β and reactive oxygen species differentially regulate neutrophil directional migration and Basal random motility in a zebrafish injury-induced inflammation model. J. Immunol. 192, 5998–6008 (2014).
  CAS PubMed Google Scholar
• Hamza, B. & Irimia, D. Whole blood human neutrophil trafficking in a microfluidic model of infection and inflammation. Lab. Chip 15, 2625–2633 (2015). This work shows that zymosan particles can 'trap' neutrophils and inhibit neutrophil fugetaxis in vitro.
  CAS PubMed PubMed Central Google Scholar
• Liu, Y., Chen, G.-Y. Y. & Zheng, P. CD24-Siglec G/10 discriminates danger- from pathogen-associated molecular patterns. Trends Immunol. 30, 557–561 (2009).
  CAS PubMed PubMed Central Google Scholar
• Chen, G.-Y. Y., Brown, N. K., Zheng, P. & Liu, Y. Siglec-G/10 in self-nonself discrimination of innate and adaptive immunity. Glycobiology 24, 800–806 (2014).
  CAS PubMed PubMed Central Google Scholar
• Chen, G.-Y. Y., Tang, J., Zheng, P. & Liu, Y. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 323, 1722–1725 (2009).
  CAS PubMed PubMed Central Google Scholar
• Kruger, P. et al. Neutrophils: Between host defence, immune modulation, and tissue injury. PLoS Pathog. 11, e1004651 (2015).
  PubMed PubMed Central Google Scholar
• Buckley, C. D., Gilroy, D. W., Serhan, C. N., Stockinger, B. & Tak, P. P. The resolution of inflammation. Nat. Rev. Immunol. 13, 59–66 (2013).
  CAS PubMed Google Scholar
• Hughes, J. et al. Neutrophil fate in experimental glomerular capillary injury in the rat. Emigration exceeds in situ clearance by apoptosis. Am. J. Pathol. 150, 223–234 (1997).
  CAS PubMed PubMed Central Google Scholar
• Mathias, J. R. et al. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 80, 1281–1288 (2006). This paper is the first time that neutrophil reverse migration was visualized in vivo using zebrafish.
  CAS PubMed Google Scholar
• Yoo, S. K. & Huttenlocher, A. Spatiotemporal photolabeling of neutrophil trafficking during inflammation in live zebrafish. J. Leukoc. Biol. 89, 661–667 (2011).
  CAS PubMed PubMed Central Google Scholar
• Hall, C. et al. Transgenic zebrafish reporter lines reveal conserved Toll-like receptor signaling potential in embryonic myeloid leukocytes and adult immune cell lineages. J. Leukoc. Biol. 85, 751–765 (2009).
  CAS PubMed Google Scholar
• Buckley, C. D. et al. Identification of a phenotypically and functionally distinct population of long-lived neutrophils in a model of reverse endothelial migration. J. Leukoc. Biol. 79, 303–311 (2006). This study identifies a subpopulation of human neutrophils that undergo rTEM in vitro . In addition, the authors identify this subpopulation in the human circulation in inflammatory conditions.
  CAS PubMed Google Scholar
• Elks, P. M. et al. Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood 118, 712–722 (2011).
  CAS PubMed Google Scholar
• Ellett, F., Elks, P. M., Robertson, A. L., Ogryzko, N. V. & Renshaw, S. A. Defining the phenotype of neutrophils following reverse migration in zebrafish. J. Leukoc. Biol. 98, 975–981 (2015).
  CAS PubMed PubMed Central Google Scholar
• Robertson, A. L. et al. A zebrafish compound screen reveals modulation of neutrophil reverse migration as an anti-inflammatory mechanism. Sci. Transl Med. 6, 225ra29 (2014). This work shows how zebrafish can be used for high-throughput drug screens to identify small molecules that modulate neutrophil reverse migration.
  PubMed PubMed Central Google Scholar
• Tauzin, S., Starnes, T. W., Becker, F. B., Lam, P.-Y. Y. & Huttenlocher, A. Redox and Src family kinase signaling control leukocyte wound attraction and neutrophil reverse migration. J. Cell Biol. 207, 589–598 (2014). This paper characterizes a macrophage ROS–SFK signalling pathway that mediates neutrophil reverse migration.
  CAS PubMed PubMed Central Google Scholar
• Duffy, D. et al. Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8+ T cells. Immunity 37, 917–929 (2012). This study shows that neutrophils can transport virus from the dermis to the bone marrow, providing a source of antigen that triggers proliferation of virus-specific memory CD8+ T cells.
  CAS PubMed Google Scholar
• Woodfin, A. et al. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12, 761–769 (2011). This is the first report of rTEM in vivo in an ischaemia–reperfusion mouse model.
  CAS PubMed PubMed Central Google Scholar
• Hamza, B. et al. Retrotaxis of human neutrophils during mechanical confinement inside microfluidic channels. Integr. Biol. 6, 175–183 (2014). This study reports that more than 90% of human neutrophils can move persistently against chemoattractant gradients over long distances (retrotaxis) using microfluidic channels.
  CAS Google Scholar
• Vianello, F., Olszak, I. T. & Poznansky, M. C. Fugetaxis: active movement of leukocytes away from a chemokinetic agent. J. Mol. Med. 83, 752–763 (2005).
  PubMed Google Scholar
• Starnes, T. W. & Huttenlocher, A. Neutrophil reverse migration becomes transparent with zebrafish. Adv. Hematol. 2012, 398640 (2012).
  PubMed PubMed Central Google Scholar
• Tharp, W. G. et al. Neutrophil chemorepulsion in defined interleukin-8 gradients in vitro and in vivo. J. Leukoc. Biol. 79, 539–554 (2006).
  CAS PubMed Google Scholar
• Kuijpers, T. & Lutter, R. Inflammation and repeated infections in CGD: two sides of a coin. Cell. Mol. Life Sci. 69, 7–15 (2012).
  CAS PubMed Google Scholar
• Serhan, C. N., Chiang, N., Dalli, J. & Levy, B. D. Lipid mediators in the resolution of inflammation. Cold Spring Harb. Perspect. Biol. 7, a016311 (2015).
  PubMed Central Google Scholar
• Buckley, C. D., Gilroy, D. W. & Serhan, C. N. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 40, 315–327 (2014).
  CAS PubMed PubMed Central Google Scholar
• Serhan, C. N. & Chiang, N. Resolution phase lipid mediators of inflammation: agonists of resolution. Curr. Opin. Pharm. 13, 632–640 (2013).
  CAS Google Scholar
• Colom, B. et al. Leukotriene B4-neutrophil elastase axis drives neutrophil reverse transendothelial cell migration in vivo. Immunity 42, 1075–1086 (2015). This paper identifies a LTB 4 –neutrophil elastase pathway that cleaves endothelial JAMC, leading to neutrophil rTEM and systemic inflammation.
  CAS PubMed PubMed Central Google Scholar
• Beyrau, M., Bodkin, J. V. & Nourshargh, S. Neutrophil heterogeneity in health and disease: a revitalized avenue in inflammation and immunity. Open Biol. 2, 120134 (2012).
  PubMed PubMed Central Google Scholar
• Holmes, G. R. et al. Drift-diffusion analysis of neutrophil migration during inflammation resolution in a zebrafish model. Adv. Hematol. 2012, 792163 (2012).
  PubMed PubMed Central Google Scholar
• Holmes, G. R. et al. Repelled from the wound, or randomly dispersed? Reverse migration behaviour of neutrophils characterized by dynamic modelling. J. R. Soc., Interface 9, 3229–3239 (2012). This report provides evidence that reverse migration of zebrafish neutrophils in vivo may represent a stochastic redistribution.
  Google Scholar
• Sadik, C. D., Kim, N. D. & Luster, A. D. Neutrophils cascading their way to inflammation. Trends Immunol. 32, 452–460 (2011).
  CAS PubMed PubMed Central Google Scholar
• Tsukamoto, T., Chanthaphavong, R. S. & Pape, H.-C. C. Current theories on the pathophysiology of multiple organ failure after trauma. Injury 41, 21–26 (2010).
  PubMed Google Scholar
• Wu, D. et al. Reverse-migrated neutrophils regulated by JAM-C are involved in acute pancreatitis-associated lung injury. Sci. Rep. 6, 20545 (2016).
  CAS PubMed PubMed Central Google Scholar
• Hampton, H. R., Bailey, J., Tomura, M., Brink, R. & Chtanova, T. Microbe-dependent lymphatic migration of neutrophils modulates lymphocyte proliferation in lymph nodes. Nat. Commun. 6, 7139 (2015). This report shows that photoconverted neutrophils migrate from inflamed skin to lymph nodes via the lymphatic circulation.
  CAS PubMed PubMed Central Google Scholar
• Abadie, V. et al. Neutrophils rapidly migrate via lymphatics after Mycobacterium bovis BCG intradermal vaccination and shuttle live bacilli to the draining lymph nodes. Blood 106, 1843–1850 (2005).
  CAS PubMed Google Scholar
• Maletto, B. A. et al. Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood 108, 3094–3102 (2006).
  CAS PubMed Google Scholar
• Wright, H. L., Moots, R. J. & Edwards, S. W. The multifactorial role of neutrophils in rheumatoid arthritis. Nat. Rev. Rheumatol. 10, 593–601 (2014).
  CAS PubMed Google Scholar
• Cantin, A. M. M., Hartl, D., Konstan, M. W. & Chmiel, J. F. Inflammation in cystic fibrosis lung disease: Pathogenesis and therapy. J. Cyst. Fibros. 14, 419–430 (2015).
  CAS PubMed Google Scholar
• Cocco, G., Chu, D. C. C. & Pandolfi, S. Colchicine in clinical medicine. A guide for internists. Eur. J. Internal Med. 21, 503–508 (2010).
  CAS Google Scholar
• Lazaar, A. L. et al. SB-656933, a novel CXCR2 selective antagonist, inhibits ex vivo neutrophil activation and ozone-induced airway inflammation in humans. Br. J. Clin. Pharmacol. 72, 282–293 (2011).
  CAS PubMed PubMed Central Google Scholar
• Moss, R. B. et al. Safety and early treatment effects of the CXCR2 antagonist SB-656933 in patients with cystic fibrosis. J. Cyst. Fibros. 12, 241–248 (2013).
  CAS PubMed Google Scholar
• Horuk, R. Chemokine receptor antagonists: overcoming developmental hurdles. Nat. Rev. Drug Discov. 8, 23–33 (2009).
  CAS PubMed Google Scholar
• Dalli, J. et al. Resolvin D3 and aspirin-triggered resolvin D3 are potent immunoresolvents. Chem. Biol. 20, 188–201 (2013).
  CAS PubMed PubMed Central Google Scholar
• Eickmeier, O. et al. Aspirin-triggered resolvin D1 reduces mucosal inflammation and promotes resolution in a murine model of acute lung injury. Mucosal Immunol. 6, 256–266 (2013).
  CAS PubMed Google Scholar
• Schwab, J. M., Chiang, N., Arita, M. & Serhan, C. N. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447, 869–874 (2007).
  CAS PubMed PubMed Central Google Scholar
• Dovi, J. V., He, L.-K. K. & DiPietro, L. A. Accelerated wound closure in neutrophil-depleted mice. J. Leukoc. Biol. 73, 448–455 (2003).
  CAS PubMed Google Scholar
• Li, L., Yan, B., Shi, Y.-Q. Q., Zhang, W.-Q. Q. & Wen, Z.-L. L. Live imaging reveals differing roles of macrophages and neutrophils during zebrafish tail fin regeneration. J. Biol. Chem. 287, 25353–25360 (2012).
  CAS PubMed PubMed Central Google Scholar
• Paoliello-Paschoalato, A. B. et al. Isolation of healthy individuals' and rheumatoid arthritis patients' peripheral blood neutrophils by the gelatin and Ficoll-Hypaque methods: comparative efficiency and impact on the neutrophil oxidative metabolism and Fcγ receptor expression. J. Immunol. Methods 412, 70–77 (2014).
  CAS PubMed Google Scholar
• Collins, S. J., Ruscetti, F. W., Gallagher, R. E. & Gallo, R. C. Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc. Natl Acad. Sci. USA 75, 2458–2462 (1978).
  CAS PubMed Google Scholar
• Tucker, K. A., Lilly, M. B., Heck, L. & Rado, T. A. Characterization of a new human diploid myeloid leukemia cell line (PLB-985) with granulocytic and monocytic differentiating capacity. Blood 70, 372–378 (1987).
  CAS PubMed Google Scholar
• Berthier, E., Surfus, J., Verbsky, J., Huttenlocher, A. & Beebe, D. An arrayed high-content chemotaxis assay for patient diagnosis. Integr. Biol. 2, 630–638 (2010).
  CAS Google Scholar
• Montanez-Sauri, S. I., Beebe, D. J. & Sung, K. E. Microscale screening systems for 3D cellular microenvironments: platforms, advances, and challenges. Cell. Mol. Life Sci. 72, 237–249 (2015).
  CAS PubMed Google Scholar
• Boneschansker, L., Yan, J., Wong, E., Briscoe, D. M. & Irimia, D. Microfluidic platform for the quantitative analysis of leukocyte migration signatures. Nat. Commun. 5, 4787 (2014).
  CAS PubMed PubMed Central Google Scholar
• Yamahashi, Y. et al. Integrin associated proteins differentially regulate neutrophil polarity and directed migration in 2D and 3D. Biomed. Microdevices 17, 100 (2015).
  PubMed PubMed Central Google Scholar
• Mantopoulos, D., Cruzat, A. & Hamrah, P. In vivo imaging of corneal inflammation: new tools for clinical practice and research. Semin. Ophthalmol. 25, 178–185 (2010).
  PubMed PubMed Central Google Scholar
• Ley, K. et al. Sequential contribution of L- and P-selectin to leukocyte rolling in vivo. J. Exp. Med. 181, 669–675 (1995).
  CAS PubMed Google Scholar
• Zarbock, A., Lowell, C. A. & Ley, K. Spleen tyrosine kinase Syk is necessary for E-selectin-induced αLβ2 integrin-mediated rolling on intercellular adhesion molecule-1. Immunity 26, 773–783 (2007).
  CAS PubMed PubMed Central Google Scholar
• Emre, Y., Jemelin, S. & Imhof, B. A. Imaging neutrophils and monocytes in mesenteric veins by intravital microscopy on anaesthetized mice in real time. J. Vis. Exp. 105 http://dx.doi.org/10.3791/53314 (2015).
• Jenne, C. N., Wong, C. H., Petri, B. & Kubes, P. The use of spinning-disk confocal microscopy for the intravital analysis of platelet dynamics in response to systemic and local inflammation. PLoS ONE 6, e25109 (2011).
  CAS PubMed PubMed Central Google Scholar
• Looney, M. R. et al. Stabilized imaging of immune surveillance in the mouse lung. Nat. Methods 8, 91–96 (2011).
  CAS PubMed Google Scholar
• Wong, J. et al. A minimal role for selectins in the recruitment of leukocytes into the inflamed liver microvasculature. J. Clin. Invest. 99, 2782–2790 (1997).
  CAS PubMed PubMed Central Google Scholar
• Slaba, I. et al. Imaging the dynamic platelet-neutrophil response in sterile liver injury and repair in mice. Hepathology 62, 1593–1605 (2015).
  CAS Google Scholar
• Walters, K. B., Green, J. M., Surfus, J. C., Yoo, S. K. & Huttenlocher, A. Live imaging of neutrophil motility in a zebrafish model of WHIM syndrome. Blood 116, 2803–2811 (2010).
  CAS PubMed PubMed Central Google Scholar
• Deng, Q., Yoo, S. K., Cavnar, P. J., Green, J. M. & Huttenlocher, A. Dual roles for Rac2 in neutrophil motility and active retention in zebrafish hematopoietic tissue. Dev. Cell 21, 735–745 (2011).
  CAS PubMed PubMed Central Google Scholar
• Henry, K. M., Loynes, C. A., Whyte, M. K. & Renshaw, S. A. Zebrafish as a model for the study of neutrophil biology. J. Leukoc. Biol. 94, 633–642 (2013).
  CAS PubMed Google Scholar
• Lieschke, G. J., Oates, A. C., Crowhurst, M. O., Ward, A. C. & Layton, J. E. Morphologic and functional characterization of granulocytes and macrophages in embryonic and adult zebrafish. Blood 98, 3087–3096 (2001).
  CAS PubMed Google Scholar
• Harvie, E. A. & Huttenlocher, A. Neutrophils in host defense: new insights from zebrafish. J. Leukoc. Biol. 98, 523–537 (2015).
  CAS PubMed PubMed Central Google Scholar
• Berthier, E. et al. Low-volume toolbox for the discovery of immunosuppressive fungal secondary metabolites. PLoS Pathog. 9, e1003289 (2013).
  CAS PubMed PubMed Central Google Scholar
• Graziano, B. R. & Weiner, O. D. Self-organization of protrusions and polarity during eukaryotic chemotaxis. Curr. Opin. Cell Biol. 30, 60–67 (2014).
  CAS PubMed Google Scholar
• Deng, Q. & Huttenlocher, A. Leukocyte migration from a fish eye's view. J. Cell Sci. 125, 3949–3956 (2012).
  CAS PubMed PubMed Central Google Scholar
• Baker, M. J., Pan, D. & Welch, H. C. Small GTPases and their guanine-nucleotide exchange factors and GTPase-activating proteins in neutrophil recruitment. Curr. Opin. Hematol. 23, 44–54 (2016).
  CAS PubMed Google Scholar
• Mócsai, A., Walzog, B. & Lowell, C. A. Intracellular signalling during neutrophil recruitment. Cardiovasc. Res. 107, 373–385 (2015).
  PubMed PubMed Central Google Scholar
• Weiner, O. D. Regulation of cell polarity during eukaryotic chemotaxis: the chemotactic compass. Curr. Opin. Cell Biol. 14, 196–202 (2002).
  CAS PubMed PubMed Central Google Scholar
• Kölsch, V., Charest, P. G. & Firtel, R. A. The regulation of cell motility and chemotaxis by phospholipid signaling. J. Cell Sci. 121, 551–559 (2008).
  PubMed PubMed Central Google Scholar
• Afonso, P. V. & Parent, C. A. PI3K and chemotaxis: a priming issue? Sci. Signal. 4, pe22 (2011).
  PubMed Google Scholar
• Kunisaki, Y. et al. DOCK2 is a Rac activator that regulates motility and polarity during neutrophil chemotaxis. J. Cell Biol. 174, 647–652 (2006).
  CAS PubMed PubMed Central Google Scholar
• Welch, H. C. et al. P-Rex1, a PtdIns(3,4,5)P3- and Gβγ-regulated guanine-nucleotide exchange factor for Rac. Cell 108, 809–821 (2002).
  CAS PubMed Google Scholar
• Heit, B., Tavener, S., Raharjo, E. & Kubes, P. An intracellular signaling hierarchy determines direction of migration in opposing chemotactic gradients. J. Cell Biol. 159, 91–102 (2002).
  CAS PubMed PubMed Central Google Scholar
• Raghuwanshi, S. K. et al. The chemokine receptors CXCR1 and CXCR2 couple to distinct G protein-coupled receptor kinases to mediate and regulate leukocyte functions. J. Immunol. 189, 2824–2832 (2012).
  CAS PubMed PubMed Central Google Scholar
• Yoo, S. K. et al. Differential regulation of protrusion and polarity by PI3K during neutrophil motility in live zebrafish. Dev. Cell 18, 226–236 (2010).
  CAS PubMed PubMed Central Google Scholar
• Beerman, R. W. et al. Direct in vivo manipulation and imaging of calcium transients in neutrophils identify a critical role for leading-edge calcium flux. Cell Rep. 13, 2107–2117 (2015).
  CAS PubMed PubMed Central Google Scholar
• Hu, N. et al. Differential expression of granulopoiesis related genes in neutrophil subsets distinguished by membrane expression of CD177. PLoS ONE 9, e99671 (2014).
  PubMed PubMed Central Google Scholar
• Welin, A. et al. The human neutrophil subsets defined by the presence or absence of OLFM4 both transmigrate into tissue in vivo and give rise to distinct NETs in vitro. PLoS ONE 8, e69575 (2013).
  CAS PubMed PubMed Central Google Scholar
• Fridlender, Z. G. et al. Polarization of tumor-associated neutrophil phenotype by TGF-β: “N1” versus “N2” TAN. Cancer Cell 16, 183–194 (2009).
  CAS PubMed PubMed Central Google Scholar
• Hartl, D. et al. Infiltrated neutrophils acquire novel chemokine receptor expression and chemokine responsiveness in chronic inflammatory lung diseases. J. Immunol. 181, 8053–8067 (2008).
  CAS PubMed Google Scholar
• Tirouvanziam, R. et al. Profound functional and signaling changes in viable inflammatory neutrophils homing to cystic fibrosis airways. Proc. Natl Acad. Sci. USA 105, 4335–4339 (2008).
  CAS PubMed Google Scholar
• Bauer, S. et al. Proteinase 3 and CD177 are expressed on the plasma membrane of the same subset of neutrophils. J. Leukoc. Biol. 81, 458–464 (2007).
  CAS PubMed Google Scholar
• Carmona-Rivera, C. & Kaplan, M. J. Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin. Immunopathol. 35, 455–463 (2013).
  CAS PubMed PubMed Central Google Scholar
• Drifte, G., Dunn-Siegrist, I., Tissières, P. & Pugin, J. Innate immune functions of immature neutrophils in patients with sepsis and severe systemic inflammatory response syndrome. Crit. Care Med. 41, 820–832 (2013).
  CAS PubMed Google Scholar
• Bowers, N. L. et al. Immune suppression by neutrophils in HIV-1 infection: role of PD-L1/PD-1 pathway. PLoS Pathog. 10, e1003993 (2014).
  PubMed PubMed Central Google Scholar
• Cloke, T. et al. Phenotypic alteration of neutrophils in the blood of HIV seropositive patients. PLoS ONE 8, e72034 (2013).
  CAS PubMed PubMed Central Google Scholar
• Matsushima, H. et al. Neutrophil differentiation into a unique hybrid population exhibiting dual phenotype and functionality of neutrophils and dendritic cells. Blood 121, 1677–1689 (2013).
  CAS PubMed PubMed Central Google Scholar
• Nair, P. et al. Safety and efficacy of a CXCR2 antagonist in patients with severe asthma and sputum neutrophils: a randomized, placebo-controlled clinical trial. Clin. Exp. Allergy 42, 1097–1103 (2012).
  CAS PubMed Google Scholar
• Opfermann, P. et al. A pilot study on reparixin, a CXCR1/2 antagonist, to assess safety and efficacy in attenuating ischaemia-reperfusion injury and inflammation after on-pump coronary artery bypass graft surgery. Clin. Exp. Immunol. 180, 131–142 (2015).
  CAS PubMed PubMed Central Google Scholar
• Bertini, R. et al. Receptor binding mode and pharmacological characterization of a potent and selective dual CXCR1/CXCR2 non-competitive allosteric inhibitor. Br. J. Pharmacol. 165, 436–454 (2012).
  CAS PubMed PubMed Central Google Scholar
• Leaker, B. R., Barnes, P. J. & O'Connor, B. Inhibition of LPS-induced airway neutrophilic inflammation in healthy volunteers with an oral CXCR2 antagonist. Respiratory Res. 14, 137 (2013)
  Google Scholar
• Miller, B. E. et al. The pharmacokinetics and pharmacodynamics of danirixin (GSK1325756) —a selective CXCR2 antagonist —in healthy adult subjects. BMC Pharmacol. Toxicol. 16, 18 (2015).
  PubMed PubMed Central Google Scholar
• Jurcevic, S. et al. The effect of a selective CXCR2 antagonist (AZD5069) on human blood neutrophil count and innate immune functions. Br. J. Clin. Pharmacol. 80, 1324–1336 (2015).
  CAS PubMed PubMed Central Google Scholar
• Nicholls, D. J. et al. Pharmacological characterization of AZD5069, a slowly reversible CXC chemokine receptor 2 antagonist. J. Pharmacol. Exp. Ther. 353, 340–350 (2015).
  CAS PubMed Google Scholar
• US National Library of Medicine. ClinicalTrials.gov [online], (2016).
• US National Library of Medicine. ClinicalTrials.gov [online], (2015).