The enigmatic neutrophil: what we do not know

Cell and Tissue Research

Volumn 371, Issue 3, 2018, Pages 399-406

  Kubes, Paul ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Healing; Imaging; Inflammation; Neutrophil extracellular traps aggregates; Neutrophil killing mechanisms

Indexed keywords

ADAPTIVE IMMUNITY; BLOOD; CELL DEATH; CELL DIFFERENTIATION; CELL SUBPOPULATION; CYTOKINE PRODUCTION; DISEASES; HUMAN; IMMUNITY; LEUKOCYTE FUNCTION; NEUTROPHIL; NONHUMAN; PATHOGEN CLEARANCE; PRIORITY JOURNAL; REVIEW; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; IMMUNOLOGY;

ANIMALS; CELL DEATH; HUMANS; NEUTROPHILS; ORGAN SPECIFICITY;

EID: 85042231405     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-018-2790-5     Document Type: Review

References (57)

1. Afonso PV, Janka-Junttila M, Lee YJ, McCann CP, Oliver CM, Aamer KA, Losert W, Cicerone MT, Parent CA (2012) LTB4 is a signal-relay molecule during neutrophil chemotaxis. Dev Cell 22:1079–1091
2. Bodey GP, Buckley M, Sathe YS, Freireich EJ (1966) Quantitative relationships between circulating leukocytes and infection in patients with acute leukemia. Ann Intern Med 64:328–340
3. Bogoslowski A, Butcher EC, Kubes P (2018) Neutrophils recruited through high endothelial venules of the lymph node via PNAd intercept disseminating Staphylococcus aureus. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.1715756115
4. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303:1532–1535
5. Campbell EJ, Senior RM, McDonald JA, Cox DL, Greco JM, Landis JA (1982) Proteolysis by neutrophils. J Clin Invest 70:845–852
6. Christoffersson G, Vagesjo E, Vandooren J, Liden M, Massena S, Reinert RB, Brissova M, Powers AC, Opdenakker G, Phillipson M (2012) VEGF-A recruits a proangiogenic MMP-9-delivering neutrophil subset that induces angiogenesis in transplanted hypoxic tissue. Blood 120:4653–4662
7. Chtanova T, Schaeffer M, Han SJ, van Dooren GG, Nollmann M, Herzmark P, Chan SW, Satija H, Camfield K, Aaron H, Striepen B, Robey EA (2008) Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29:487–496
8. Clemmensen SN, Bohr CT, Rorvig S, Glenthoj A, Mora-Jensen H, Cramer EP, Jacobsen LC, Larsen MT, Cowland JB, Tanassi JT, Heegaard NH, Wren JD, Silahtaroglu AN, Borregaard N (2012) Olfactomedin 4 defines a subset of human neutrophils. J Leukoc Biol 91:495–500
9. Davis JM, Albert JD, Tracy KJ, Calvano SE, Lowry SF, Shires GT, Yurt RW (1991) Increased neutrophil mobilization and decreased chemotaxis during cortisol and epinephrine infusions. J Trauma 31:725–731
10. Deniset JF, Surewaard BG, Lee WY, Kubes P (2017) Splenic Ly6Ghigh mature and Ly6Gint immature neutrophils contribute to eradication of S. pneumoniae. J Exp Med 214:1333–1350
11. Denny MF, Yalavarthi S, Zhao W, Thacker SG, Anderson M, Sandy AR, McCune WJ, Kaplan MJ (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
12. Devi S, Wang Y, Chew WK, Lima R, Gonzalez NA, Mattar CNZ, Chong SZ, Schlitzer A, Bakocevic N, Chew S, Keeble JL, Goh CC, Li JLY, Evrard M, Malleret B, Larbi A, Renia L, Haniffa M, Tan SM, Chan JKY, Balabanian K, Nagasawa T, Bachelerie F, Hidalgo A, Ginhoux F, Kubes P, Ng LG (2013) Neutrophil mobilization via plerixafor-mediated CXCR4 inhibition arises from llung demargination and blockade of neutrophil homing to the bone marrow. J Exp Med 210:2321–2336
13. Downey GP, Worthen GS, Henson PM, Hyde DM (1993) Neutrophil sequestration and migration in localized pulmonary inflammation. Capillary localization and migration across the interalveolar septum. Am Rev Respir Dis 147:168–176
14. Elting LS, Rubenstein EB, Rolston KV, Bodey GP (1997) Outcomes of bacteremia in patients with cancer and neutropenia: observations from two decades of epidemiological and clinical trials. Clin Infect Dis 25:247–259
15. Fantone JC, Ward PA (1985) Polymorphonuclear leukocyte-mediated cell and tissue injury: oxygen metabolites and their relations to human disease. Hum Pathol 16:973–978
16. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 16:183–194
17. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176:231–241
18. Gao JL, Lee EJ, Murphy PM (1999) Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J Exp Med 189:657–662
19. Garg AD, Agostinis P (2017) Cell death and immunity in cancer: from danger signals to mimicry of pathogen defense responses. Immunol Rev 280:126–148
20. Jorch SK, Kubes P (2017) An emerging role for neutrophil extracellular traps in noninfectious disease. Nat Med 23:279–287
21. Keelan ETM, Licence ST, Peters AM, Binns RM, Haskard DO (1994) Characterization of E-selectin expression in vivo with use of a radiolabeled monoclonal antibody. Am J Phys 266:H279–H290
22. Kobayashi SD, Malachowa N, Deleo FR (2017) Influence of microbes on neutrophil life and death. Front Cell Infect Microbiol 7:159
23. Kolaczkowska E, Kubes P (2013) Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13:159–175
24. Landzberg M, Doering H, Aboodi GM, Tenenbaum HC, Glogauer M (2015) Quantifying oral inflammatory load: oral neutrophil counts in periodontal health and disease. J Periodontal Res 50:330–336
25. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7:678–689
26. Li KW, Turner SM, Emson CL, Hellerstein MK, Dale DC (2011) Deuterium and neutrophil kinetics. Blood 117:6052–6053
27. Lood C, Blanco LP, Purmalek MM, Carmona-Rivera C, De Ravin SS, Smith CK, Malech HL, Ledbetter JA, Elkon KB, Kaplan MJ (2016) Neutrophil extracellular traps enriched in oxidized mitochondrial DNA are interferogenic and contribute to lupus-like disease. Nat Med 22:146–153
28. Martin C, Burdon PC, Bridger G, Gutierrez-Ramos JC, Williams TJ, Rankin SM (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
29. Mathias JR, Perrin BJ, Liu TX, Kanki J, Look AT, Huttenlocher A (2006) Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. J Leukoc Biol 80:1281–1288
30. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, Waterhouse CC, Beck PL, Muruve DA, Kubes P (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330:362–366
31. Ng LG, Qin JS, Roediger B, Wang Y, Jain R, Cavanagh LL, Smith AL, Jones CA, de VM GMA, Meeusen EN, Weninger W (2011) Visualizing the neutrophil response to sterile tissue injury in mouse dermis reveals a three-phase cascade of events. J Invest Dermatol 131:2058–2068
32. Papayannopoulos V (2017) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18(2):134–147
33. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, Kamhawi S, Lawyer P, Fay MP, Germain RN, Sacks D (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321:970–974
34. Petri B, Phillipson M, Kubes P (2008) The physiology of leukocyte recruitment: an in vivo perspective. J Immunol 180:6439–6446
35. Phillipson M, Kubes P (2011) The neutrophil in vascular inflammation. Nat Med 17:1381–1390
36. Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JA, Tesselaar K, Koenderman L (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116:625–627
37. Pilsczek FH, Salina D, Poon KK, Fahey C, Yipp BG, Sibley CD, Robbins SM, Green FH, Surette MG, Sugai M, Bowden MG, Hussain M, Zhang K, Kubes P (2010) A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185:7413–7425
38. Postnikoff CK, Nichols KK (2017) Neutrophil and T-cell homeostasis in the closed eye. Invest Ophthalmol Vis Sci 58:6212–6220
39. Puga I, Cols M, Barra CM, He B, Cassis L, Gentile M, Comerma L, Chorny A, Shan M, Xu W, Magri G, Knowles DM, Tam W, Chiu A, Bussel JB, Serrano S, Lorente JA, Bellosillo B, Lloreta J, Juanpere N, Alameda F, Baro T, de Heredia CD, Toran N, Catala A, Torrebadell M, Fortuny C, Cusi V, Carreras C, Diaz GA, Blander JM, Farber CM, Silvestri G, Cunningham-Rundles C, Calvillo M, Dufour C, Notarangelo LD, Lougaris V, Plebani A, Casanova JL, Ganal SC, Diefenbach A, Arostegui JI, Juan M, Yague J, Mahlaoui N, Donadieu J, Chen K, Cerutti A (2011) B cell-helper neutrophils stimulate the diversification and production of immunoglobulin in the marginal zone of the spleen. Nat Immunol 13:170–180
40. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195
41. Schiwon M, Weisheit C, Franken L, Gutweiler S, Dixit A, Meyer-Schwesinger C, Pohl JM, Maurice NJ, Thiebes S, Lorenz K, Quast T, Fuhrmann M, Baumgarten G, Lohse MJ, Opdenakker G, Bernhagen J, Bucala R, Panzer U, Kolanus W, Grone HJ, Garbi N, Kastenmuller W, Knolle PA, Kurts C, Engel DR (2014) Crosstalk between sentinel and helper macrophages permits neutrophil migration into infected uroepithelium. Cell 156:456–468
42. Shaul ME, Levy L, Sun J, Mishalian I, Singhal S, Kapoor V, Horng W, Fridlender G, Albelda SM, Fridlender ZG (2016) Tumor-associated neutrophils display a distinct N1 profile following TGFbeta modulation: a transcriptomics analysis of pro- vs. antitumor TANs. Oncoimmunology 5:e1232221
43. Slaba I, Wang J, Kolaczkowska E, McDonald B, Lee WY, Kubes P (2015) Imaging the dynamic platelet-neutrophil response in sterile liver injury and repair in mice. Hepatology 62:1593–1605
44. Soehnlein O, Lindbom L (2010) Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol 10:427–439
45. Stark MA, Huo Y, Burcin TL, Morris MA, Olson TS, Ley K (2005) Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22:285–294
46. Tecchio C, Micheletti A, Cassatella MA (2014) Neutrophil-derived cytokines: facts beyond expression. Front Immunol 5:508
47. Treffers LW, Hiemstra IH, Kuijpers TW, van den Berg TK, Matlung HL (2016) Neutrophils in cancer. Immunol Rev 273:312–328
48. Uchida T, Nemoto T, Yui T, Matsuda S, Kariyone S (1979) Use of technetium-99m as a radioactive label to study migratory patterns of leukocytes. J Nucl Med 20:1197–1200
49. Wang J, Hossain M, Thanabalasuriar A, Gunzer M, Meininger C, Kubes P (2017) Visualizing the function and fate of neutrophils in sterile injury and repair. Science 358:111–116
50. Woodfin A, Voisin MB, Beyrau M, Colom B, Caille D, Diapouli FM, Nash GB, Chavakis T, Albelda SM, Rainger GE, Meda P, Imhof BA, Nourshargh S (2011) The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat Immunol 12:761–769
51. Wu Z, Liang R, Ohnesorg T, Cho V, Lam W, Abhayaratna WP, Gatenby PA, Perera C, Zhang Y, Whittle B, Sinclair A, Goodnow CC, Field M, Andrews TD, Cook MC (2016) Heterogeneity of human Neutrophil CD177 expression results from CD177P1 Pseudogene conversion. PLoS Genet 12:e1006067
52. Yipp BG, Kim JH, Lima R, Zbytnuik LD, Petri B, Swanlund N, Ho M, Szeto VG, Tak T, Koenderman L, Pickkers P, Tool ATJ, Kuijpers TW, van den Berg TK, Looney MR, Krummel MF, Kubes P (2017) The Lung is a Host Defense Niche for Immediate Neutrophil-Mediated Vascular Protection. Sci Immunol. https://doi.org/10.1126/sciimmunol.aam8929
53. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, de Boisfleury CA, Zhang K, Conly J, Kubes P (2012) Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 18:1386–1393
54. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU (2009) Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 16:1438–1444
55. Zhang D, Chen G, Manwani D, Mortha A, Xu C, Faith JJ, Burk RD, Kunisaki Y, Jang JE, Scheiermann C, Merad M, Frenette PS (2015) Neutrophil ageing is regulated by the microbiome. Nature 525:528–532
56. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W, Brohi K, Itagaki K, Hauser CJ (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464:104–107
57. Zhou GX, Liu ZJ (2017) Potential roles of neutrophils in regulating intestinal mucosal inflammation of inflammatory bowel disease. J Dig Dis 18:495–503