Neutrophil: A cell with many roles in inflammation or several cell types?

Frontiers in Physiology

Volumn 9, Issue FEB, 2018, Pages

  Rosales, Carlos ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Bacteria; Cancer; Infection; Inflammation; Neutrophil

Indexed keywords

BONE MARROW; CELL CYCLE; CELL DEATH; CELL FUNCTION; CELL HETEROGENEITY; CELL MIGRATION; CELL SUBPOPULATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CIRCULATION; CLEARANCE; EXTRACELLULAR TRAP; GRANULOPOIESIS; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOGENIC CELL; INFLAMMATION; LOW DENSITY NEUTROPHIL; MALIGNANT NEOPLASM; METABOLIC DISORDER; MICROFLORA; MYELOID-DERIVED SUPPRESSOR CELL; NEUTROPHIL; NEUTROPHIL EXIT; NONHUMAN; PHENOTYPE; REVIEW; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ASSOCIATED NEUTROPHIL;

EID: 85042213376     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2018.00113     Document Type: Review

References (200)

1. Aaes, T. L., Kaczmarek, A., Delvaeye, T., De Craene, B., De Koker, S., Heyndrickx, L., et al. (2016). Vaccination with necroptotic cancer cells induces efficient anti-tumor immunity. Cell Rep. 15, 274-287. doi: 10.1016/j.celrep.2016.03.037
2. Adrover, J. M., Nicolás-ávila, J. A., and Hidalgo, A. (2016). Aging: a temporal dimension for neutrophils. Trends Immunol. 37, 334-345. doi: 10.1016/j.it.2016.03.005
3. Beauvillain, C., Cunin, P., Doni, A., Scotet, M., Jaillon, S., Loiry, M. L., et al. (2011). CCR7 is involved in the migration of neutrophils to lymph nodes. Blood 117, 1196-1204. doi: 10.1182/blood-2009-11-254490
4. Berger-Achituv, S., Brinkmann, V., Abed, U. A., Kühn, L. I., Ben-Ezra, J., Elhasid, R., et al. (2013). A proposed role for neutrophil extracellular traps in cancer immunoediting. Front. Immunol. 4:48. doi: 10.3389/fimmu.2013.00048
5. Beyrau, M., Bodkin, J. V., and Nourshargh, S. (2012). Neutrophil heterogeneity in health and disease: a revitalized avenue in inflammation and immunity. Open Biol. 2:120134. doi: 10.1098/rsob.120134
6. Bezu, L., Gomes-de-Silva, L. C., Dewitte, H., Breckpot, K., Fucikova, J., Spisek, R., et al. (2015). Combinatorial strategies for the induction of immunogenic cell death. Front. Immunol. 6:187. doi: 10.3389/fimmu.2015.00187
7. Bianchi, M. E. (2007). DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol. 81, 1-5. doi: 10.1189/jlb.0306164
8. Bonaventura, A., Liberale, L., Carbone, F., Vecchié, A., Diaz-Cañestro, C., Camici, G. G., et al. (2018). The pathophysiological role of neutrophil extracellular traps in inflammatory diseases. Thromb. Haemost. 118, 6-27. doi: 10.1160/TH17-09-0630
9. Borregaard, N. (2010). Neutrophils, from marrow to microbes. Immunity 33, 657-670. doi: 10.1016/j.immuni.2010.11.011
10. Bournazou, I., Pound, J. D., Duffin, R., Bournazos, S., Melville, L. A., Brown, S. B., et al. (2009). Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin. J. Clin. Invest. 119, 20-32. doi: 10.1172/JCI36226
11. Böyum, A. (1968). Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand, J. Clin. Lab. Invest. Suppl. 97, 77-89
12. Braganza, J. M., Lee, S. H., McCloy, R. F., and McMahon, M. J. (2011). Chronic pancreatitis. Lancet 377, 1184-1197. doi: 10.1016/S0140-6736(10)61852-1
13. Brandau, S., Moses, K., and Lang, S. (2013). The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: cousins, siblings or twins? Semin. Cancer Biol. 23, 171-182. doi: 10.1016/j.semcancer.2013.02.007
14. Brandau, S., Trellakis, S., Bruderek, K., Schmaltz, D., Steller, G., Elian, M., et al. (2011). Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J. Leukoc. Biol. 89, 311-317. doi: 10.1189/jlb.0310162
15. Branzk, N., Lubojemska, A., Hardison, S. E., Wang, Q., Gutierrez, M. G., Brown, G. D., et al. (2014). Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat. Immunol. 15, 1017-1025. doi: 10.1038/ni.2987
16. Bratton, D. L., and Henson, P. M. (2011). Neutrophil clearance: when the party is over, clean-up begins. Trends Immunol. 32, 350-357. doi: 10.1016/j.it.2011.04.009
17. Brill, A., Fuchs, T. A., Savchenko, A. S., Thomas, G. M., Martinod, K., De Meyer, S. F., et al. (2012). Neutrophil extracellular traps promote deep vein thrombosis in mice. J. Thromb. Haemost. 10, 136-144. doi: 10.1111/j.1538-7836.2011.04544.x
18. Buckley, C. D., Ross, E. A., McGettrick, H. M., Osborne, C. E., Haworth, O., Schmutz, C., et al. (2006). 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. doi: 10.1189/jlb.0905496
19. Busso, N., and So, A. (2012). Microcrystals as DAMPs and their role in joint inflammation. Rheumatology 51, 1154-1160. doi: 10.1093/rheumatology/ker524
20. Carmona-Rivera, C., and Kaplan, M. J. (2013). Low-density granulocytes: a distinct class of neutrophils in systemic autoimmunity. Semin. Immunopathol. 35, 455-463. doi: 10.1007/s00281-013-0375-7
21. Caruso, R. A., Bellocco, R., Pagano, M., Bertoli, G., Rigoli, L., and Inferrera, C. (2002). Prognostic value of intratumoral neutrophils in advanced gastric carcinoma in a high-risk area in northern Italy. Mod. Pathol. 15, 831-837. doi: 10.1097/01.MP.0000020391.98998.6B
22. Casanova-Acebes, M., Pitaval, C., Weiss, L. A., Nombela-Arrieta, C., Chèvre, R., A-González, N., et al. (2013). Rhythmic modulation of the hematopoietic niche through neutrophil clearance. Cell 153, 1025-1035. doi: 10.1016/j.cell.2013.04.040
23. Cerutti, A., Puga, I., and Magri, G. (2013). The B cell helper side of neutrophils. J. Leukoc. Biol. 94, 677-682. doi: 10.1189/jlb.1112596
24. Chavakis, E., Choi, E. Y., and Chavakis, T. (2009). Novel aspects in the regulation of the leukocyte adhesion cascade. Thromb. Haemost. 102, 191-197. doi: 10.1160/TH08-12-0844
25. Chen, F., Wu, W., Millman, A., Craft, J. F., Chen, E., Patel, N., et al. (2014). Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion. Nat. Immunol. 15, 938-946. doi: 10.1038/ni.2984
26. Chistiakov, D. A., Bobryshev, Y. V., and Orekhov, A. N. (2015). Neutrophil's weapons in atherosclerosis. Exp. Mol. Pathol. 99, 663-671. doi: 10.1016/j.yexmp.2015.11.011
27. Clark, S. R., Ma, A. C., Tavener, S. A., McDonald, B., Goodarzi, Z., Kelly, M. M., et al. (2007). Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13, 463-469. doi: 10.1038/nm1565
28. Clarke, T. B., Davis, K. M., Lysenko, E. S., Zhou, A. Y., Yu, Y., and Weiser, J. N. (2010). Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16, 228-231. doi: 10.1038/nm.2087
29. Cloke, T., Munder, M., Taylor, G., Müller, I., and Kropf, P. (2012). Characterization of a novel population of low-density granulocytes associated with disease severity in HIV-1 infection. PLoS ONE 7:e48939. doi: 10.1371/journal.pone.0048939
30. Coffelt, S. B., Wellenstein, M. D., and de Visser, K. E. (2016). Neutrophils in cancer: neutral no more. Nat. Rev. Cancer 16, 431-446. doi: 10.1038/nrc.2016.52
31. Daley, J. M., Thomay, A. A., Connolly, M. D., Reichner, J. S., and Albina, J. E. (2008). Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J. Leukoc. Biol. 83, 64-70. doi: 10.1189/jlb.0407247
32. Damuzzo, V., Pinton, L., Desantis, G., Solito, S., Marigo, I., Bronte, V., et al. (2015). Complexity and challenges in defining myeloid-derived suppressor cells. Cytometry B Clin. Cytom. 88, 77-91. doi: 10.1002/cytob.21206
33. Dancey, J. T., Deubelbeiss, K. A., Harker, L. A., and Finch, C. A. (1976). Neutrophil kinetics in man. J. Clin. Invest. 58, 705-715. doi: 10.1172/JCI108517
34. Deng, Y., Ye, J., Luo, Q., Huang, Z., Peng, Y., Xiong, G., et al. (2016). Low-density granulocytes are elevated in mycobacterial infection and associated with the severity of tuberculosis. PLoS ONE 11:e0153567. doi: 10.1371/journal.pone.0153567
35. Denny, M. F., Yalavarthi, S., Zhao, W., Thacker, S. G., Anderson, M., Sandy, A. R., et al. (2010). A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J. Immunol. 184, 3284-3297. doi: 10.4049/jimmunol.0902199
36. Deshmukh, H. S., Liu, Y., Menkiti, O. R., Mei, J., Dai, N., O'Leary, C. E., et al. (2014). The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat. Med. 20, 524-530. doi: 10.1038/nm.3542
37. Devi, S., Wang, Y., Chew, W. K., Lima, R., A.-González, N., Mattar, C. N., et al. (2013). Neutrophil mobilization via plerixafor-mediated CXCR4 inhibition arises from lung demargination and blockade of neutrophil homing to the bone marrow. J. Exp. Med. 210, 2321-2336. doi: 10.1084/jem.20130056
38. Di Nisio, M., van Es, N., and Büller, H. R. (2016). Deep vein thrombosis and pulmonary embolism. Lancet 388, 3060-3073. doi: 10.1016/S0140-6736(16)30514-1
39. Döring, Y., Drechsler, M., Wantha, S., Kemmerich, K., Lievens, D., Vijayan, S., et al. (2012). Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ. Res. 110, 1052-1056. doi: 10.1161/CIRCRESAHA.112.265868
40. Döring, Y., Soehnlein, O., and Weber, C. (2017). Neutrophil extracellular traps in atherosclerosis and atherothrombosis. Circ. Res. 120, 736-743. doi: 10.1161/CIRCRESAHA.116.309692
41. Downey, G. P., Fukushima, T., Fialkow, L., and Waddell, T. K. (1995). Intracellular signaling in neutrophil priming and activation. Semin. Cell Biol. 6, 345-356. doi: 10.1016/S1043-4682(05)80005-4
42. Drechsler, M., Megens, R. T., van Zandvoort, M., Weber, C., and Soehnlein, O. (2010). Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 122, 1837-1845. doi: 10.1161/CIRCULATIONAHA.110.961714
43. Duffy, D., Perrin, H., Abadie, V., Benhabiles, N., Boissonnas, A., Liard, C., et al. (2012). Neutrophils transport antigen from the dermis to the bone marrow, initiating a source of memory CD8+ T cells. Immunity 37, 917-929. doi: 10.1016/j.immuni.2012.07.015
44. Dumitru, C. A., Moses, K., Trellakis, S., Lang, S., and Brandau, S. (2012). Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology. Cancer Immunol. Immunother. 61, 1155-1167. doi: 10.1007/s00262-012-1294-5
45. Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., and Schreiber, R. D. (2002). Cancer immunoediting: from immunosurveillance to tumor escape. Nat. Immunol. 3, 991-998. doi: 10.1038/ni1102-991
46. Eash, K. J., Greenbaum, A. M., Gopalan, P. K., and Link, D. C. (2010). CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J. Clin. Invest. 120, 2423-2431. doi: 10.1172/JCI41649
47. Eash, K. J., Means, J. M., White, D. W., and Link, D. C. (2009). CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood 113, 4711-4719. doi: 10.1182/blood-2008-09-177287
48. El-Benna, J., Hurtado-Nedelec, M., Marzaioli, V., Marie, J. C., Gougerot-Pocidalo, M. A., and Dang, P. M. (2016). Priming of the neutrophil respiratory burst: role in host defense and inflammation. Immunol. Rev. 273, 180-193. doi: 10.1111/imr.12447
49. Elliott, M. R., Chekeni, F. B., Trampont, P. C., Lazarowski, E. R., Kadl, A., Walk, S. F., et al. (2009). Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461, 282-286. doi: 10.1038/nature08296
50. Ericson, J. A., Duffau, P., Yasuda, K., Ortiz-Lopez, A., Rothamel, K., Rifkin, I. R., et al. (2014). Gene expression during the generation and activation of mouse neutrophils: implication of novel functional and regulatory pathways. PLoS ONE 9:e108553. doi: 10.1371/journal.pone.0108553
51. Eruslanov, E. B., Bhojnagarwala, P. S., Quatromoni, J. G., Stephen, T. L., Ranganathan, A., Deshpande, C., et al. (2014). Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J. Clin. Invest. 124, 5466-5480. doi: 10.1172/JCI77053
52. Eskan, M. A., Jotwani, R., Abe, T., Chmelar, J., Lim, J. H., Liang, S., et al. (2012). The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nat. Immunol. 13, 465-473. doi: 10.1038/ni.2260
53. Etulain, J., Martinod, K., Wong, S. L., Cifuni, S. M., Schattner, M., and Wagner, D. D. (2015). P-selectin promotes neutrophil extracellular trap formation in mice. Blood 126, 242-246. doi: 10.1182/blood-2015-01-624023
54. Faria, S. S., Fernandes, P. C. Jr., Silva, M. J., Lima, V. C., Fontes, W., Freitas-Junior, R., et al. (2016). The neutrophil-to-lymphocyte ratio: a narrative review. Ecancermedicalscience 10:702. doi: 10.3332/ecancer.2016.702
55. Favaloro, J., Liyadipitiya, T., Brown, R., Yang, S., Suen, H., Woodland, N., et al. (2014). Myeloid derived suppressor cells are numerically, functionally and phenotypically different in patients with multiple myeloma. Leuk. Lymphoma. 55, 2893-2900. doi: 10.3109/10428194.2014.904511
56. Fortunati, E., Kazemier, K. M., Grutters, J. C., Koenderman, L., and Van den Bosch, v. J. (2009). Human neutrophils switch to an activated phenotype after homing to the lung irrespective of inflammatory disease. Clin. Exp. Immunol. 155, 559-566. doi: 10.1111/j.1365-2249.2008.03791.x
57. Fridlender, Z. G., and Albelda, S. M. (2012). Tumor-associated neutrophils: friend or foe? Carcinogenesis 33, 949-955. doi: 10.1093/carcin/bgs123
58. Fridlender, Z. G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L., et al. (2009). Polarization of tumor-associated neutrophil phenotype by TGF-beta, "N1" versus "N2" TAN. Cancer Cell 16, 183-194. doi: 10.1016/j.ccr.2009.06.017
59. Fu, J., Tobin, M. C., and Thomas, L. L. (2014). Neutrophil-like low-density granulocytes are elevated in patients with moderate to severe persistent asthma. Ann. Allergy Asthma Immunol. 113, 635-640. doi: 10.1016/j.anai.2014.08.024
60. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241. doi: 10.1083/jcb.200606027
61. Fuchs, T. A., Brill, A., Duerschmied, D., Schatzberg, D., Monestier, M., Myers, D. D., et al. (2010). Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. U.S.A. 107, 15880-15885. doi: 10.1073/pnas.1005743107
62. Gaffen, S. L., Jain, R., Garg, A. V., and Cua, D. J. (2014). The IL-23-IL-17 immune axis: from mechanisms to therapeutic testing. Nat. Rev. Immunol. 14, 585-600. doi: 10.1038/nri3707
63. Galdiero, M. R., Garlanda, C., Jaillon, S., Marone, G., and Mantovani, A. (2013). Tumor associated macrophages and neutrophils in tumor progression. J. Cell. Physiol. 228, 1404-1412. doi: 10.1002/jcp.24260
64. Galluzzi, L., Senovilla, L., Zitvogel, L., and Kroemer, G. (2012). The secret ally: immunostimulation by anticancer drugs. Nat. Rev. Drug Discov. 11, 215-233. doi: 10.1038/nrd3626
65. García-García, E., Uribe-Querol, E., and Rosales, C. (2013). A simple and efficient method to detect nuclear factor activation in human neutrophils by flow cytometry. J. Vis. Exp. 74:e50410. doi: 10.3791/50410
66. Garcia-Romo, G. S., Caielli, S., Vega, B., Connolly, J., Allantaz, F., Xu, Z., et al. (2011). Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci. Transl. Med. 3:73ra20. doi: 10.1126/scitranslmed.3001201
67. Garg, A. D., and Agostinis, P. (2017). Cell death and immunity in cancer: from danger signals to mimicry of pathogen defense responses. Immunol. Rev. 280, 126-148. doi: 10.1111/imr.12574
68. Garg, A. D., Dudek-Peric, A. M., Romano, E., and Agostinis, P. (2015a). Immunogenic cell death. Int. J. Dev. Biol. 59, 131-140. doi: 10.1387/ijdb.150061pa
69. Garg, A. D., Galluzzi, L., Apetoh, L., Baert, T., Birge, R. B., Bravo-San Pedro, J. M., et al. (2015b). Molecular and translational classifications of DAMPs in immunogenic cell death. Front. Immunol. 6:588. doi: 10.3389/fimmu.2015.00588
70. Garg, A. D., Martin, S., Golab, J., and Agostinis, P. (2014). Danger signalling during cancer cell death: origins, plasticity and regulation. Cell Death Differ. 21, 26-38. doi: 10.1038/cdd.2013.48
71. Garg, A. D., More, S., Rufo, N., Mece, O., Sassano, M. L., Agostinis, P., et al. (2017a). Trial watch: immunogenic cell death induction by anticancer chemotherapeutics. Oncoimmunology 6:e1386829. doi: 10.1080/2162402X.2017.1386829
72. Garg, A. D., Romano, E., Rufo, N., and Agostinis, P. (2016). Immunogenic versus tolerogenic phagocytosis during anticancer therapy: mechanisms and clinical translation. Cell Death Differ. 23, 938-951. doi: 10.1038/cdd.2016.5
73. Garg, A. D., Vandenberk, L., Fang, S., Fasche, T., Van Eygen, S., Maes, J., et al. (2017b). Pathogen response-like recruitment and activation of neutrophils by sterile immunogenic dying cells drives neutrophil-mediated residual cell killing. Cell Death Differ. 24, 832-843. doi: 10.1038/cdd.2017.15
74. Garley, M., Jablonska, E., and Dabrowska, D. (2016). NETs in cancer. Tumour Biol. 37, 14355-14361. doi: 10.1007/s13277-016-5328-z
75. Gisterå, A., and Hansson, G. K. (2017). The immunology of atherosclerosis. Nat. Rev. Nephrol. 13, 368-380. doi: 10.1038/nrneph.2017.51
76. Gordy, C., Pua, H., Sempowski, G. D., and He, Y. W. (2011). Regulation of steady-state neutrophil homeostasis by macrophages. Blood 117, 618-629. doi: 10.1182/blood-2010-01-265959
77. Görgens, A., Radtke, S., Möllmann, M., Cross, M., Dürig, J., Horn, P. A., et al. (2013). Revision of the human hematopoietic tree: granulocyte subtypes derive from distinct hematopoietic lineages. Cell Rep. 3, 1539-1552. doi: 10.1016/j.celrep.2013.04.025
78. Gorlino, C. V., Ranocchia, R. P., Harman, M. F., García, I. A., Crespo, M. I., Morón, G., et al. (2014). Neutrophils exhibit differential requirements for homing molecules in their lymphatic and blood trafficking into draining lymph nodes. J. Immunol. 193, 1966-1974. doi: 10.4049/jimmunol.1301791
79. Grayson, P. C., Carmona-Rivera, C., Xu, L., Lim, N., Gao, Z., Asare, A. L., et al. (2015). Neutrophil-related gene expression and low-density granulocytes associated with disease activity and response to treatment in antineutrophil cytoplasmic antibody-associated vasculitis. Arthritis Rheumatol. 67, 1922-1932. doi: 10.1002/art.39153
80. Green, D. R., Ferguson, T., Zitvogel, L., and Kroemer, G. (2009). Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 9, 353-363. doi: 10.1038/nri2545
81. Greenlee-Wacker, M. C. (2016). Clearance of apoptotic neutrophils and resolution of inflammation. Immunol. Rev. 273, 357-370. doi: 10.1111/imr.12453
82. Gukovskaya, A. S., Pandol, S. J., and Gukovsky, I. (2016). New insights into the pathways initiating and driving pancreatitis. Curr. Opin. Gastroenterol. 32, 429-435. doi: 10.1097/MOG.0000000000000301
83. Gukovskaya, A. S., Vaquero, E., Zaninovic, V., Gorelick, F. S., Lusis, A. J., Brennan, M. L., et al. (2002). Neutrophils and NADPH oxidase mediate intrapancreatic trypsin activation in murine experimental acute pancreatitis. Gastroenterology 122, 974-984. doi: 10.1053/gast.2002.32409
84. Guthrie, G. J., Charles, K. A., Roxburgh, C. S., Horgan, P. G., McMillan, D. C., and Clarke, S. J. (2013). The systemic inflammation-based neutrophil-lymphocyte ratio: experience in patients with cancer. Crit. Rev. Oncol. Hematol. 88, 218-230. doi: 10.1016/j.critrevonc.2013.03.010
85. Hacbarth, E., and Kajdacsy-Balla, A. (1986). Low density neutrophils in patients with systemic lupus erythematosus, rheumatoid arthritis, and acute rheumatic fever. Arthritis Rheum. 29, 1334-1342. doi: 10.1002/art.1780291105
86. Häger, M., Cowland, J. B., and Borregaard, N. (2010). Neutrophil granules in health and disease. J. Intern. Med. 268, 25-34. doi: 10.1111/j.1365-2796.2010.02237.x
87. Hahn, J., Knopf, J., Maueröder, C., Kienhöfer, D., Leppkes, M., and Herrmann, M. (2016). Neutrophils and neutrophil extracellular traps orchestrate initiation and resolution of inflammation. Clin. Exp. Rheumatol. 34, 6-8
88. Hajishengallis, G., and Chavakis, T. (2013). Endogenous modulators of inflammatory cell recruitment. Trends Immunol. 34, 1-6. doi: 10.1016/j.it.2012.08.003
89. Halangk, W., Lerch, M. M., Brandt-Nedelev, B., Roth, W., Ruthenbuerger, M., Reinheckel, T., et al. (2000). Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J. Clin. Invest. 106, 773-781. doi: 10.1172/JCI9411
90. Hampton, H. R., and Chtanova, T. (2016). The lymph node neutrophil. Semin. Immunol. 28, 129-136. doi: 10.1016/j.smim.2016.03.008
91. Hansson, G. K., Libby, P., and Tabas, I. (2015). Inflammation and plaque vulnerability. J. Intern. Med. 278, 483-493. doi: 10.1111/joim.12406
92. Hergott, C. B., Roche, A. M., Tamashiro, E., Clarke, T. B., Bailey, A. G., Laughlin, A., et al. (2016). Peptidoglycan from the gut microbiota governs the lifespan of circulating phagocytes at homeostasis. Blood 127, 2460-2471. doi: 10.1182/blood-2015-10-675173
93. Jablonska, J., Leschner, S., Westphal, K., Lienenklaus, S., and Weiss, S. (2010). Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J. Clin. Invest. 120, 1151-1164. doi: 10.1172/JCI37223
94. Jaiswal, S., Jamieson, C. H., Pang, W. W., Park, C. Y., Chao, M. P., Majeti, R., et al. (2009). CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138, 271-285. doi: 10.1016/j.cell.2009.05.046
95. Jiao, J., Dragomir, A. C., Kocabayoglu, P., Rahman, A. H., Chow, A., Hashimoto, D., et al. (2014). Central role of conventional dendritic cells in regulation of bone marrow release and survival of neutrophils. J. Immunol. 192, 3374-3382. doi: 10.4049/jimmunol.1300237
96. Kanamaru, R., Ohzawa, H., Miyato, H., Matsumoto, S., Haruta, H., Kurashina, K., et al. (2018). Low density neutrophils (LDN) in postoperative abdominal cavity assist the peritoneal recurrence through the production of neutrophil extracellular traps (NETs). Sci. Rep. 8:632. doi: 10.1038/s41598-017-19091-2
97. Kepp, O., Senovilla, L., Vitale, I., Vacchelli, E., Adjemian, S., Agostinis, P., et al. (2014). Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology 3:e955691. doi: 10.4161/21624011.2014.955691
98. Keskinov, A. A., and Shurin, M. R. (2015). Myeloid regulatory cells in tumor spreading and metastasis. Immunobiology 220, 236-242. doi: 10.1016/j.imbio.2014.07.017
99. Kessenbrock, K., Krumbholz, M., Schönermarck, U., Back, W., Gross, W. L., Werb, Z., et al. (2009). Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15, 623-625. doi: 10.1038/nm.1959
100. Khandpur, R., Carmona-Rivera, C., Vivekanandan-Giri, A., Gizinski, A., Yalavarthi, S., Knight, J. S., et al. (2013). NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci. Transl. Med. 5:178ra40. doi: 10.1126/scitranslmed.3005580
101. Kim, H. K., De La Luz Sierra, M., Williams, C. K., Gulino, A. V., and Tosato, G. (2006). G-CSF down-regulation of CXCR4 expression identified as a mechanism for mobilization of myeloid cells. Blood 108, 812-820. doi: 10.1182/blood-2005-10-4162
102. Kingsbury, S. R., Conaghan, P. G., and McDermott, M. F. (2011). The role of the NLRP3 inflammasome in gout. J. Inflamm. Res. 4, 39-49. doi: 10.2147/JIR.S11330
103. Knight, J. S., Luo, W., O'Dell, A. A., Yalavarthi, S., Zhao, W., Subramanian, V., et al. (2014). Peptidylarginine deiminase inhibition reduces vascular damage and modulates innate immune responses in murine models of atherosclerosis. Circ. Res. 114, 947-956. doi: 10.1161/CIRCRESAHA.114.303312
104. Köhler, A., De Filippo, K., Hasenberg, M., van den Brandt, C., Nye, E., Hosking, M. P., et al. (2011). G-CSF-mediated thrombopoietin release triggers neutrophil motility and mobilization from bone marrow via induction of CXCR2 ligands. Blood 117, 4349-4357. doi: 10.1182/blood-2010-09-308387
105. Kolaczkowska, E., and Kubes, P. (2013). Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159-175. doi: 10.1038/nri3399
106. Kraakman, M. J., Lee, M. K., Al-Sharea, A., Dragoljevic, D., Barrett, T. J., Montenont, E., et al. (2017). Neutrophil-derived S100 calcium-binding proteins A8/A9 promote reticulated thrombocytosis and atherogenesis in diabetes. J. Clin. Invest. 127, 2133-2147. doi: 10.1172/JCI92450
107. Kropf, P., Baud, D., Marshall, S. E., Munder, M., Mosley, A., Fuentes, J. M., et al. (2007). Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur. J. Immunol. 37, 935-945. doi: 10.1002/eji.200636542
108. Lankisch, P. G., Apte, M., and Banks, P. A. (2015). Acute pancreatitis. Lancet 386, 85-96. doi: 10.1016/S0140-6736(14)60649-8
109. Lechner, M. G., Liebertz, D. J., and Epstein, A. L. (2010). Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J. Immunol. 185, 2273-2284. doi: 10.4049/jimmunol.1000901
110. Leppkes, M., Maueröder, C., Hirth, S., Nowecki, S., Günther, C., Billmeier, U., et al. (2016). Externalized decondensed neutrophil chromatin occludes pancreatic ducts and drives pancreatitis. Nat. Commun. 7:10973. doi: 10.1038/ncomms10973
111. Ley, K., Laudanna, C., Cybulsky, M. I., and Nourshargh, S. (2007). Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689. doi: 10.1038/nri2156
112. Lin, A. M., Rubin, C. J., Khandpur, R., Wang, J. Y., Riblett, M., Yalavarthi, S., et al. (2011). Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J. Immunol. 187, 490-500. doi: 10.4049/jimmunol.1100123
113. Mandruzzato, S., Brandau, S., Britten, C. M., Bronte, V., Damuzzo, V., Gouttefangeas, C., et al. (2016). Toward harmonized phenotyping of human myeloid-derived suppressor cells by flow cytometry: results from an interim study. Cancer. Immunol. Immunother. 65, 161-169. doi: 10.1007/s00262-015-1782-5
114. Manfredi, A. A., Covino, C., Rovere-Querini, P., and Maugeri, N. (2015). Instructive influences of phagocytic clearance of dying cells on neutrophil extracellular trap generation. Clin. Exp. Immunol. 179, 24-29. doi: 10.1111/cei.12320
115. Manohar, M., Verma, A. K., Venkateshaiah, S. U., Sanders, N. L., and Mishra, A. (2017). Pathogenic mechanisms of pancreatitis. World J. Gastrointest. Pharmacol. Ther. 8, 10-25. doi: 10.4292/wjgpt.v8.i1.10
116. Mansuy-Aubert, V., Zhou, Q. L., Xie, X., Gong, Z., Huang, J. Y., Khan, A. R., et al. (2013). Imbalance between neutrophil elastase and its inhibitor a1-antitrypsin in obesity alters insulin sensitivity, inflammation, and energy expenditure. Cell Metab. 17, 534-548. doi: 10.1016/j.cmet.2013.03.005
117. Martin, C., Burdon, P. C., Bridger, G., Gutierrez-Ramos, J. C., Williams, T. J., and Rankin, S. M. (2003). Chemokines acting via CXCR2 and CXCR4 control the release of neutrophils from the bone marrow and their return following senescence. Immunity 19, 583-593. doi: 10.1016/S1074-7613(03)00263-2
118. Massberg, S., Grahl, L., von Bruehl, M. L., Manukyan, D., Pfeiler, S., Goosmann, C., et al. (2010). Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat. Med. 16, 887-896. doi: 10.1038/nm.2184
119. Massena, S., Christoffersson, G., Vågesjö, E., Seignez, C., Gustafsson, K., Binet, F., et al. (2015). Identification and characterization of VEGF-A-responsive neutrophils expressing CD49d, VEGFR1, and CXCR4 in mice and humans. Blood 126, 2016-2026. doi: 10.1182/blood-2015-03-631572
120. Mathias, J. R., Perrin, B. J., Liu, T. X., Kanki, J., Look, A. T., and Huttenlocher, A. (2012). Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J. Leukoc. Biol. 80, 1281-1288. doi: 10.1189/jlb.0506346
121. Maueröder, C., Kienhöfer, D., Hahn, J., Schauer, C., Manger, B., Schett, G., et al. (2015). How neutrophil extracellular traps orchestrate the local immune response in gout. J. Mol. Med. 93, 727-734. doi: 10.1007/s00109-015-1295-x
122. Mayadas, T. N., Cullere, X., and Lowell, C. A. (2014). The multifaceted functions of neutrophils. Annu. Rev. Pathol. 9, 181-218. doi: 10.1146/annurev-pathol-020712-164023
123. Mazor, R., Shurtz-Swirski, R., Farah, R., Kristal, B., Shapiro, G., Dorlechter, F., et al. (2008). Primed polymorphonuclear leukocytes constitute a possible link between inflammation and oxidative stress in hyperlipidemic patients. Atherosclerosis 197, 937-943. doi: 10.1016/j.atherosclerosis.2007.08.014
124. McGary, C. T., Miele, M. E., and Welch, D. R. (1995). Highly metastatic 13762NF rat mammary adenocarcinoma cell clones stimulate bone marrow by secretion of granulocyte-macrophage colony-stimulating factor/interleukin-3 activity. Am. J. Pathol. 147, 1668-1681
125. Merza, M., Hartman, H., Rahman, M., Hwaiz, R., Zhang, E., Renström, E., et al. (2015). Neutrophil extracellular traps induce trypsin activation, inflammation, and tissue damage in mice with severe acute pancreatitis. Gastroenterology 149, 1920-1931. doi: 10.1053/j.gastro.2015.08.026
126. Michels, A., Albánez, S., Mewburn, J., Nesbitt, K., Gould, T. J., Liaw, P. C., et al. (2016). Histones link inflammation and thrombosis through the induction of Weibel-Palade body exocytosis. J. Thromb. Haemost. 14, 2274-2286. doi: 10.1111/jth.13493
127. Mishalian, I., Bayuh, R., Levy, L., Zolotarov, L., Michaeli, J., and Fridlender, Z. G. (2013). Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol. Immunother. 62, 1745-1756. doi: 10.1007/s00262-013-1476-9
128. Mishalian, I., Granot, Z., and Fridlender, Z. G. (2017). The diversity of circulating neutrophils in cancer. Immunobiology 222, 82-88. doi: 10.1016/j.imbio.2016.02.001
129. Morisaki, T., Goya, T., Ishimitsu, T., and Torisu, M. (1992). The increase of low density subpopulations and CD10 (CALLA) negative neutrophils in severely infected patients. Surg. Today. 22, 322-327. doi: 10.1007/BF00308740
130. Nagaraj, S., Schrum, A. G., Cho, H. I., Celis, E., and Gabrilovich, D. (2010). Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J. Immunol. 184, 3106-3116. doi: 10.4049/jimmunol.0902661
131. Nagase, H., Miyamasu, M., Yamaguchi, M., Imanishi, M., Tsuno, N. H., Matsushima, K., et al. (2002). Cytokine-mediated regulation of CXCR4 expression in human neutrophils. J. Leukoc. Biol. 71, 711-717. doi: 10.1189/jlb.71.4.711
132. Nauseef, W. M., and Borregaard, N. (2014). Neutrophils at work. Nat. Immunol. 15, 602-611. doi: 10.1038/ni.2921
133. Netea, M. G., Joosten, L. A., Latz, E., Mills, K. H., Natoli, G., Stunnenberg, H. G., et al. (2016). Trained immunity: a program of innate immune memory in health and disease. Science 352:aaf1098. doi: 10.1126/science.aaf1098
134. Nourshargh, S., Renshaw, S. A., and Imhof, B. A. (2016). Reverse migration of neutrophils: where, when, how, and why? Trends Immunol. 37, 273-286. doi: 10.1016/j.it.2016.03.006
135. Pandol, S. J., Saluja, A. K., Imrie, C. W., and Banks, P. A. (2007). Acute pancreatitis: bench to the bedside. Gastroenterology 132, 1127-1151. doi: 10.1053/j.gastro.2007.01.055
136. Paramanathan, A., Saxena, A., and Morris, D. L. (2014). A systematic review and meta-analysis on the impact of pre-operative neutrophil lymphocyte ratio on long term outcomes after curative intent resection of solid tumours. Surg. Oncol. 23, 31-39. doi: 10.1016/j.suronc.2013.12.001
137. Pelletier, M., Maggi, L., Micheletti, A., Lazzeri, E., Tamassia, N., Costantini, C., et al. (2010). Evidence for a cross-talk between human neutrophils and Th17 cells. Blood 115, 335-343. doi: 10.1182/blood-2009-04-216085
138. Peng, B., Wang, Y. H., Liu, Y. M., and Ma, L. X. (2015). Prognostic significance of the neutrophil to lymphocyte ratio in patients with non-small cell lung cancer: a systemic review and meta-analysis. Int. J. Clin. Exp. Med. 8, 3098-3106
139. Peranzoni, E., Zilio, S., Marigo, I., Dolcetti, L., Zanovello, P., Mandruzzato, S., et al. (2010). Myeloid-derived suppressor cell heterogeneity and subset definition. Curr. Opin. Immunol. 22, 238-244. doi: 10.1016/j.coi.2010.01.021
140. Petit, I., Szyper-Kravitz, M., Nagler, A., Lahav, M., Peled, A., Habler, L., et al. (2002). G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat. Immunol. 3, 687-694. doi: 10.1038/ni813
141. Pillay, J., Kamp, V. M., van Hoffen, E., Visser, T., Tak, T., Lammers, J. W., et al. (2012). A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. J. Clin. Invest. 122, 327-336. doi: 10.1172/JCI57990
142. Pillay, J., Tak, T., Kamp, V. M., and Koenderman, L. (2013). Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell. Mol. Life Sci. 70, 3813-3827. doi: 10.1007/s00018-013-1286-4
143. Puga, I., Cols, M., Barra, C. M., He, B., Cassis, L., Gentile, M., et al. (2011). B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat. Immunol. 13, 170-180. doi: 10.1038/ni.2194
144. Qi, H., Yang, S., and Zhang, L. (2017). Neutrophil extracellular traps and endothelial dysfunction in atherosclerosis and thrombosis. Front. Immunol. 8:928. doi: 10.3389/fimmu.2017.00928
145. Raber, P. L., Thevenot, P., Sierra, R., Wyczechowska, D., Halle, D., Ramirez, M. E., et al. (2014). Subpopulations of myeloid-derived suppressor cells impair T cell responses through independent nitric oxide-related pathways. Int. J. Cancer 134, 2853-2864. doi: 10.1002/ijc.28622
146. Raber, P., Ochoa, A. C., and Rodríguez, P. C. (2012). Metabolism of L-arginine by myeloid-derived suppressor cells in cancer: mechanisms of T cell suppression and therapeutic perspectives. Immunol. Invest. 41, 614-634. doi: 10.3109/08820139.2012.680634
147. Ramacciotti, E., Hawley, A. E., Farris, D. M., Ballard, N. E., Wrobleski, S. K., Myers, D. D. Jr., et al. (2009). Leukocyte-and platelet-derived microparticles correlate with thrombus weight and tissue factor activity in an experimental mouse model of venous thrombosis. Thromb. Haemost. 101, 748-754. doi: 10.1160/TH08-09-0620
148. Rocha, B. C., Marques, P. E., Leoratti, F. M. S., Junqueira, C., Pereira, D. B., Antonelli, L. R., et al. (2015). Type I interferon transcriptional signature in neutrophils and low-density granulocytes are associated with tissue damage in malaria. Cell Rep. 13, 2829-2841. doi: 10.1016/j.celrep.2015.11.055
149. Rodriguez, P. C., Quiceno, D. G., Zabaleta, J., Ortiz, B., Zea, A. H., Piazuelo, M. B., et al. (2004). Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res. 64, 5839-5849. doi: 10.1158/0008-5472.CAN-04-0465
150. Saffarzadeh, M., Juenemann, C., Queisser, M. A., Lochnit, G., Barreto, G., Galuska, S. P., et al. (2012). Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS ONE 7:e32366. doi: 10.1371/journal.pone.0032366
151. Sagiv, J. Y., Michaeli, J., Assi, S., Mishalian, I., Kisos, H., Levy, L., et al. (2015). Phenotypic diversity and plasticity in circulating neutrophil subpopulations in cancer. Cell Rep. 10, 562-573. doi: 10.1016/j.celrep.2014.12.039
152. Sagiv, J. Y., Voels, S., and Granot, Z. (2016). Isolation and characterization of low-vs. high-density neutrophils in cancer. Methods Mol. Biol. 1458, 179-193. doi: 10.1007/978-1-4939-3801-8_13
153. Scapini, P., and Cassatella, M. A. (2014). Social networking of human neutrophils within the immune system. Blood 124, 710-719. doi: 10.1182/blood-2014-03-453217
154. Schauer, C., Janko, C., Munoz, L. E., Zhao, Y., Kienhöfer, D., Frey, B., et al. (2014). Aggregated neutrophil extracellular traps limit inflammation by degrading cytokines and chemokines. Nat. Med. 20, 511-517. doi: 10.1038/nm.3547
155. Scheiermann, C., Kunisaki, Y., and Frenette, P. S. (2013). Circadian control of the immune system. Nat. Rev. Immunol. 13, 190-198. doi: 10.1038/nri3386
156. Scheiermann, C., Kunisaki, Y., Lucas, D., Chow, A., Jang, J. E., Zhang, D., et al. (2012). Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37, 290-301. doi: 10.1016/j.immuni.2012.05.021
157. Schmidt, H., Bastholt, L., Geertsen, P., Christensen, I. J., Larsen, S., Gehl, J., et al. (2005). Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br. J. Cancer 93, 273-278. doi: 10.1038/sj.bjc.6602702
158. Schorn, C., Frey, B., Lauber, K., Janko, C., Strysio, M., Keppeler, H., et al. (2011). Sodium overload and water influx activate the NALP3 inflammasome. J. Biol. Chem. 286, 35-41. doi: 10.1074/jbc. M110.139048
159. Schreiber, R. D., Old, L. J., and Smyth, M. J. (2011). Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 331, 1565-1570. doi: 10.1126/science.1203486
160. Semerad, C. L., Christopher, M. J., Liu, F., Short, B., Simmons, P. J., Winkler, I., et al. (2005). G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood 106, 3020-3027. doi: 10.1182/blood-2004-01-0272
161. Shah, K., Spear, J., Nathanson, L. A., McCauley, J., and Edlow, J. A. (2007). Does the presence of crystal arthritis rule out septic arthritis? J. Emerg. Med. 32, 23-26. doi: 10.1016/j.jemermed.2006.07.019
162. Silvestre-Roig, C., Hidalgo, A., and Soehnlein, O. (2016). Neutrophil heterogeneity: implications for homeostasis and pathogenesis. Blood 127, 2173-2181. doi: 10.1182/blood-2016-01-688887
163. Sionov, R. V., Fridlender, Z. G., and Granot, Z. (2015). The multifaceted roles neutrophils play in the tumor microenvironment. Cancer Microenviron. 8, 125-158. doi: 10.1007/s12307-014-0147-5
164. So, A. K., and Martinon, F. (2017). Inflammation in gout: mechanisms and therapeutic targets. Nat. Rev. Rheumatol. 13, 639-647. doi: 10.1038/nrrheum.2017.155
165. So, A., and Busso, N. (2014). The concept of the inflammasome and its rheumatologic implications. Joint Bone Spine 81, 398-402. doi: 10.1016/j.jbspin.2014.02.009
166. Solito, S., Pinton, L., and Mandruzzato, S. (2017). In Brief: myeloid-derived suppressor cells in cancer. J. Pathol. 242, 7-9. doi: 10.1002/path.4876
167. Spanier, B. W., Dijkgraaf, M. G., and Bruno, M. J. (2008). Epidemiology, aetiology and outcome of acute and chronic pancreatitis: an update. Best Pract. Res. Clin. Gastroenterol. 22, 45-63. doi: 10.1016/j.bpg.2007.10.007
168. Ssemaganda, A., Kindinger, L., Bergin, P., Nielsen, L., Mpendo, J., Ssetaala, A., et al. (2014). Characterization of neutrophil subsets in healthy human pregnancies. PLoS ONE 9:e85696. doi: 10.1371/journal.pone.0085696
169. Stakos, D. A., Kambas, K., Konstantinidis, T., Mitroulis, I., Apostolidou, E., Arelaki, S., et al. (2015). Expression of functional tissue factor by neutrophil extracellular traps in culprit artery of acute myocardial infarction. Eur. Heart J. 36, 1405-1414. doi: 10.1093/eurheartj/ehv007
170. Stark, M. A., Huo, Y., Burcin, T. L., Morris, M. A., Olson, T. S., and Ley, K. (2005). Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22, 285-294. doi: 10.1016/j.immuni.2005.01.011
171. Stephenson, H. N., Herzig, A., and Zychlinsky, A. (2016). Beyond the grave: when is cell death critical for immunity to infection? Curr. Opin. Immunol. 38, 59-66. doi: 10.1016/j.coi.2015.11.004
172. Summers, C., Rankin, S. M., Condliffe, A. M., Singh, N., Peters, A. M., and Chilvers, E. R. (2010). Neutrophil kinetics in health and disease. Trends Immunol. 31, 318-324. doi: 10.1016/j.it.2010.05.006
173. Swierczak, A., Mouchemore, K. A., Hamilton, J. A., and Anderson, R. L. (2015). Neutrophils: important contributors to tumor progression and metastasis. Cancer Metastasis Rev. 34, 735-751. doi: 10.1007/s10555-015-9594-9
174. Talukdar, S., Oh, D. Y., Bandyopadhyay, G., Li, D., Xu, J., McNelis, J., et al. (2012). Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase. Nat. Med. 18, 1407-1412. doi: 10.1038/nm.2885
175. Tecchio, C., and Cassatella, M. A. (2016). Neutrophil-derived chemokines on the road to immunity. Semin. Immunol. 28, 119-128. doi: 10.1016/j.smim.2016.04.003
176. Tecchio, C., Micheletti, A., and Cassatella, M. A. (2014). Neutrophil-derived cytokines: facts beyond expression. Front. Immunol. 5:508. doi: 10.3389/fimmu.2014.00508
177. Templeton, A. J., McNamara, M. G., Šeruga, B., Vera-Badillo, F. E., Aneja, P., Ocaña, A., et al. (2014). Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J. Natl. Cancer Inst. 106:dju124. doi: 10.1093/jnci/dju124
178. Terkeltaub, R., Baird, S., Sears, P., Santiago, R., and Boisvert, W. (1998). The murine homolog of the interleukin-8 receptor CXCR-2 is essential for the occurrence of neutrophilic inflammation in the air pouch model of acute urate crystal-induced gouty synovitis. Arthritis Rheum. 41, 900-909. doi: 10.1002/1529-0131(199805)41:5<900::AID-ART18>3.0.CO;2-K
179. Tsuda, Y., Takahashi, H., Kobayashi, M., Hanafusa, T., Herndon, D. N., and Suzuki, F. (2004). Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity 21, 215-226. doi: 10.1016/j.immuni.2004.07.006
180. Ueda, Y., Cain, D. W., Kuraoka, M., Kondo, M., and Kelsoe, G. (2009). IL-1R type I-dependent hemopoietic stem cell proliferation is necessary for inflammatory granulopoiesis and reactive neutrophilia. J. Immunol. 182, 6477-6484. doi: 10.4049/jimmunol.0803961
181. Uribe-Querol, E., and Rosales, C. (2015). Neutrophils in cancer: two sides of the same coin. J. Immunol. Res. 2015:983698. doi: 10.1155/2015/983698
182. Van Acker, G. J., Saluja, A. K., Bhagat, L., Singh, V. P., Song, A. M., and Steer, M. L. (2002). Cathepsin B inhibition prevents trypsinogen activation and reduces pancreatitis severity. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G794-G800. doi: 10.1152/ajpgi.00363.2001
183. Villanueva, E., Yalavarthi, S., Berthier, C. C., Hodgin, J. B., Khandpur, R., Lin, A. M., et al. (2011). Netting neutrophils induce endothelial damage, infiltrate tissues, and expose immunostimulatory molecules in systemic lupus erythematosus. J. Immunol. 187, 538-552. doi: 10.4049/jimmunol.1100450
184. von Vietinghoff, S., and Ley, K. (2008). Homeostatic regulation of blood neutrophil counts. J. Immunol. 181, 5183-5188. doi: 10.4049/jimmunol.181.8.5183
185. von Vietinghoff, S., and Ley, K. (2009). IL-17A controls IL-17F production and maintains blood neutrophil counts in mice. J. Immunol. 183, 865-873. doi: 10.4049/jimmunol.0804080
186. Wang, J., Sjöberg, S., Tang, T. T., Oörni, K., Wu, W., Liu, C., et al. (2014). Cathepsin G activity lowers plasma LDL and reduces atherosclerosis. Biochim. Biophys. Acta 1842, 2174-2183. doi: 10.1016/j.bbadis.2014.07.026
187. Warnatsch, A., Ioannou, M., Wang, Q., and Papayannopoulos, V. (2015). Inflammation. Neutrophil extracellular traps licensemacrophages for cytokine production in atherosclerosis. Science 349, 316-320. doi: 10.1126/science.aaa8064
188. Weaver, C. T., Elson, C. O., Fouser, L. A., and Kolls, J. K. (2013). The Th17 pathway and inflammatory diseases of the intestines, lungs, and skin. Annu. Rev. Pathol. 8, 477-512. doi: 10.1146/annurev-pathol-011110-130318
189. Wong, S. L., Demers, M., Martinod, K., Gallant, M., Wang, Y., Goldfine, A. B., et al. (2015). Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat. Med. 21, 815-819. doi: 10.1038/nm.3887
190. Woodfin, A., Voisin, M. B., Beyrau, M., Colom, B., Caille, D., Diapouli, F. M., et al. (2011). The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12, 761-769. doi: 10.1038/ni.2062
191. Wu, P., Wu, D., Ni, C., Ye, J., Chen, W., Hu, G., et al. (2014). dT17 cells promote the accumulation and expansion of myeloid-derived suppressor cells in human colorectal cancer. Immunity 40, 785-800. doi: 10.1016/j.immuni.2014.03.013
192. Xiang, M., Yuan, Y., Fan, L., Li, Y., Li, A., Yin, L., et al. (2012). Role of macrophages in mobilization of hematopoietic progenitor cells from bone marrow after hemorrhagic shock. Shock 37, 518-523. doi: 10.1097/SHK.0b013e318249b81d
193. Xu, S., Li, X., LaPenna, K. B., Yokota, S. D., Huke, S., and He, P. (2017). New insights into shear stress-induced endothelial signalling and barrier function: cell-free fluid versus blood flow. Cardiovasc. Res. 113, 508-518. doi: 10.1093/cvr/cvx021
194. Yan, J., Kloecker, G., Fleming, C., Bousamra, M. II., Hansen, R., Hu, X., et al. (2014). Human polymorphonuclear neutrophils specifically recognize and kill cancerous cells. Oncoimmunology 3:e950163. doi: 10.4161/15384101.2014.950163
195. Yang, F., Feng, C., Zhang, X., Lu, J., and Zhao, Y. (2017). The diverse biological functions of neutrophils, beyond the defense against Infections. Inflammation 40, 311-323. doi: 10.1007/s10753-016-0458-4
196. Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., et al. (2012). Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 18, 1386-1393. doi: 10.1038/nm.2847
197. Youn, J. I., Nagaraj, S., Collazo, M., and Gabrilovich, D. I. (2008). Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J. Immunol. 181, 5791-5802. doi: 10.4049/jimmunol.181.8.5791
198. Zenobia, C., and Hajishengallis, G. (2015). Basic biology and role of interleukin-17 in immunity and inflammation. Periodontol. 2000 69, 142-159. doi: 10.1111/prd.12083
199. Zhang, D., Chen, G., Manwani, D., Mortha, A., Xu, C., Faith, J. J., et al. (2015). Neutrophil ageing is regulated by the microbiome. Nature 525, 528-532. doi: 10.1038/nature15367
200. Zitvogel, L., Kepp, O., and Kroemer, G. (2010). Decoding cell death signals in inflammation and immunity. Cell 140, 798-804. doi: 10.1016/j.cell.2010.02.015