Paradoxical roles of the neutrophil in sepsis: Protective and deleterious

Frontiers in Immunology

Volumn 7, Issue APR, 2016, Pages

  Sônego, Fabiane ^a,b   Castanheira, Fernanda Vargas e Silva ^a   Ferreira, Raphael Gomes ^a   Kanashiro, Alexandre ^a   Leite, Caio Abner Vitorino Gonçalves ^a   Nascimento, Daniele Carvalho ^a   Colón, David Fernando ^a   Borges, Vanessa de Fátima ^a   Alves Filho, José Carlos ^a   Cunha, Fernando Queiróz ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUT PASTEUR   (France)

Author keywords

Chemotactic receptors; Neutrophil migration; Organ dysfunction; Sepsis; Toll like receptors

Indexed keywords

CATHEPSIN G; CHEMOKINE; CHEMOKINE RECEPTOR CCR; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR2; CPG OLIGODEOXYNUCLEOTIDE; CXCL2 CHEMOKINE; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYSTATHIONINE BETA SYNTHASE; CYSTATHIONINE GAMMA LYASE; CYSTEINE; ELASTASE; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR KINASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 33; LIPOPOLYSACCHARIDE; MYELOPEROXIDASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PROTEIN ARGININE DEIMINASE; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

BACTERIAL INFECTION; CELL DAMAGE; CELL INFILTRATION; CELL MIGRATION; ENDOTHELIAL DYSFUNCTION; HUMAN; HYPOTENSION; HYPOXEMIA; INFECTION; INFLAMMATION; INNATE IMMUNITY; MORTALITY RATE; MYCOSIS; NEUTROPHIL; NONHUMAN; ORGAN INJURY; PHAGOCYTOSIS; PROTEIN EXPRESSION; SEPSIS; SEQUENTIAL ORGAN FAILURE ASSESSMENT SCORE; SHORT SURVEY; SURVIVAL RATE;

EID: 84966709115     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2016.00155     Document Type: Short Survey

References (81)

1. Horeczko T, Green JP, Panacek EA. Epidemiology of the Systemic Inflammatory Response Syndrome (SIRS) in the emergency department. West J Emerg Med (2014) 15:329-36. doi: 10.5811/westjem.2013.9.18064
2. Kumar G, Kumar N, Taneja A, Kaleekal T, Tarima S, McGinley E, et al. Nationwide trends of severe sepsis in the 21st century (2000-2007). Chest (2011) 140:1223-31. doi:10.1378/chest.11-0352
3. Bone RC, Sibbald WJ, Sprung CL. The ACCP-SCCM consensus conference on sepsis and organ failure. Chest (1992) 101:1481-3. doi:10.1378/chest.101.6.1481
4. Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol (2011) 12:1035-44. doi:10.1038/ni.2109
5. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol (2013) 13:159-75. doi:10.1038/nri3399
6. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol (2011) 11:519-31. doi:10.1038/nri3024
7. Ermert D, Zychlinsky A, Urban C. Fungal and bacterial killing by neutrophils. Methods Mol Biol (2009) 470:293-312. doi:10.1007/978-1-59745-204-5_21
8. Robertson CM, Perrone EE, McConnell KW, Dunne WM, Boody B, Brahmbhatt T, et al. Neutrophil depletion causes a fatal defect in murine pulmonary Staphylococcus aureus clearance. J Surg Res (2008) 150:278-85. doi:10.1016/j.jss.2008.02.009
9. Bouma G, Ancliff PJ, Thrasher AJ, Burns SO. Recent advances in the understanding of genetic defects of neutrophil number and function. Br J Haematol (2010) 151:312-26. doi:10.1111/j.1365-2141.2010.08361.x
10. Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med (2012) 4:165rv113. doi:10.1126/scitranslmed.3004404
11. Swamydas M, Gao JL, Break TJ, Johnson MD, Jaeger M, Rodriguez CA, et al. CXCR1-mediated neutrophil degranulation and fungal killing promote Candida clearance and host survival. Sci Transl Med (2016) 8:322ra310. doi:10.1126/scitranslmed.aac7718
12. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol (2006) 6:173-82. doi:10.1038/nri1785
13. Bardoel BW, Kenny EF, Sollberger G, Zychlinsky A. The balancing act of neutrophils. Cell Host Microbe (2014) 15:526-36. doi:10.1016/j.chom.2014.04.011
14. Benjamim CF, Silva JS, Fortes ZB, Oliveira MA, Ferreira SH, Cunha FQ. Inhibition of leukocyte rolling by nitric oxide during sepsis leads to reduced migration of active microbicidal neutrophils. Infect Immun (2002) 70:3602-10. doi:10.1128/IAI.70.7.3602-3610.2002
15. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol (2007) 81:1-5. doi:10.1189/jlb.0306164
16. Luster AD. Chemokines-chemotactic cytokines that mediate inflammation. N Engl J Med (1998) 338:436-45. doi:10.1056/nejm199802123380706
17. Graham GJ. D6 and the atypical chemokine receptor family: novel regulators of immune and inflammatory processes. Eur J Immunol (2009) 39:342-51. doi:10.1002/eji.200838858
18. Rollins BJ. Chemokines. Blood (1997) 90:909-28
19. Mantovani A, Bonecchi R, Locati M. Tuning inflammation and immunity by chemokine sequestration: decoys and more. Nat Rev Immunol (2006) 6:907-18. doi:10.1038/nri1964
20. Sonego F, Alves-Filho JC, Cunha FQ. Targeting neutrophils in sepsis. Expert Rev Clin Immunol (2014) 10:1019-28. doi:10.1586/1744666X.2014.922876
21. Alves-Filho JC, de Freitas A, Spiller F, Souto FO, Cunha FQ. The role of neutrophils in severe sepsis. Shock (2008) 30(Suppl 1):3-9. doi:10.1097/SHK.0b013e3181818466
22. Chishti AD, Shenton BK, Kirby JA, Baudouin SV. Neutrophil chemotaxis and receptor expression in clinical septic shock. Intensive Care Med (2004) 30:605-11. doi:10.1007/s00134-004-2175-y
23. Arraes SM, Freitas MS, da Silva SV, de Paula Neto HA, Alves-Filho JC, Auxiliadora Martins M, et al. Impaired neutrophil chemotaxis in sepsis associates with GRK expression and inhibition of actin assembly and tyrosine phosphorylation. Blood (2006) 108:2906-13. doi:10.1182/blood-2006-05-024638
24. Rios-Santos F, Alves-Filho JC, Souto FO, Spiller F, Freitas A, Lotufo CM, et al. Down-regulation of CXCR2 on neutrophils in severe sepsis is mediated by inducible nitric oxide synthase-derived nitric oxide. Am J Respir Crit Care Med (2007) 175:490-7. doi:10.1164/rccm.200601-103OC
25. Tavares-Murta BM, Zaparoli M, Ferreira RB, Silva-Vergara ML, Oliveira CH, Murta EF, et al. Failure of neutrophil chemotactic function in septic patients. Crit Care Med (2002) 30:1056-61. doi:10.1097/00003246-200205000-00017
26. Alves-Filho JC, Freitas A, Souto FO, Spiller F, Paula-Neto H, Silva JS, et al. Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc Natl Acad Sci U S A (2009) 106:4018-23. doi:10.1073/pnas.0900196106
27. Secher T, Vasseur V, Poisson DM, Mitchell JA, Cunha FQ, Alves-Filho JC, et al. Crucial role of TNF receptors 1 and 2 in the control of polymicrobial sepsis. J Immunol (2009) 182:7855-64. doi:10.4049/jimmunol.0804008
28. Martin EL, Souza DG, Fagundes CT, Amaral FA, Assenzio B, Puntorieri V, et al. Phosphoinositide-3 kinase gamma activity contributes to sepsis and organ damage by altering neutrophil recruitment. Am J Respir Crit Care Med (2010) 182:762-73. doi:10.1164/rccm.201001-0088OC
29. Paula-Neto HA, Alves-Filho JC, Souto FO, Spiller F, Amendola RS, Freitas A, et al. Inhibition of guanylyl cyclase restores neutrophil migration and maintains bactericidal activity increasing survival in sepsis. Shock (2011) 35:17-27. doi:10.1097/SHK.0b013e3181e37ea8
30. Murdoch C, Finn A. Chemokine receptors and their role in inflammation and infectious diseases. Blood (2000) 95:3032-43
31. Moore CA, Milano SK, Benovic JL. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol (2007) 69:451-82. doi:10.1146/annurev.physiol.69.022405.154712
32. Lefkowitz RJ, Shenoy SK. Transduction of receptor signals by beta-arrestins. Science (2005) 308:512-7. doi:10.1126/science.1109237
33. Alves-Filho JC, Sonego F, Souto FO, Freitas A, Verri WA Jr, Auxiliadora-Martins M, et al. Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med (2010) 16:708-12. doi:10.1038/nm.2156
34. Trevelin SC, Alves-Filho JC, Sonego F, Turato W, Nascimento DC, Souto FO, et al. Toll-like receptor 9 activation in neutrophils impairs chemotaxis and reduces sepsis outcome. Crit Care Med (2012) 40:2631-7. doi:10.1097/CCM.0b013e318258fb70
35. Lee SK, Kim SD, Kook M, Lee HY, Ghim J, Choi Y, et al. Phospholipase D2 drives mortality in sepsis by inhibiting neutrophil extracellular trap formation and down-regulating CXCR2. J Exp Med (2015) 212:1381-90. doi:10.1084/jem.20141813
36. Alves-Filho JC, de Freitas A, Russo M, Cunha FQ. Toll-like receptor 4 signaling leads to neutrophil migration impairment in polymicrobial sepsis*. Crit Care Med (2006) 34:461-70. doi:10.1097/01.ccm.0000198527.71819.e1
37. Le HT, Tran VG, Kim W, Kim J, Cho HR, Kwon B. IL-33 priming regulates multiple steps of the neutrophil-mediated anti-Candida albicans response by modulating TLR and dectin-1 signals. J Immunol (2012) 189:287-95. doi:10.4049/jimmunol.1103564
38. Sonego F, Castanheira FV, Czaikoski PG, Kanashiro A, Souto FO, Franca RO, et al. MyD88-, but not Nod1- and/or Nod2-deficient mice, show increased susceptibility to polymicrobial sepsis due to impaired local inflammatory response. PLoS One (2014) 9:e103734. doi:10.1371/journal.pone.0103734
39. Dal-Secco D, Freitas A, Abreu MA, Garlet TP, Rossi MA, Ferreira SH, et al. Reduction of ICAM-1 expression by carbon monoxide via soluble guanylate cyclase activation accounts for modulation of neutrophil migration. Naunyn Schmiedebergs Arch Pharmacol (2010) 381:483-93. doi:10.1007/s00210-010-0500-2
40. Cunha FQ, Assreuy J, Moss DW, Rees D, Leal LM, Moncada S, et al. Differential induction of nitric oxide synthase in various organs of the mouse during endotoxaemia: role of TNF-alpha and IL-1-beta. Immunology (1994) 81:211-5
41. Sakai K, Suzuki H, Oda H, Akaike T, Azuma Y, Murakami T, et al. Phosphoinositide 3-kinase in nitric oxide synthesis in macrophage: critical dimerization of inducible nitric-oxide synthase. J Biol Chem (2006) 281:17736-42. doi:10.1074/jbc.M601896200
42. Szabo C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov (2007) 6:917-35. doi:10.1038/nrd2425
43. Spiller F, Orrico MI, Nascimento DC, Czaikoski PG, Souto FO, Alves-Filho JC, et al. Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. Am J Respir Crit Care Med (2010) 182:360-8. doi:10.1164/rccm.200907-1145OC
44. Mestriner FL, Spiller F, Laure HJ, Souto FO, Tavares-Murta BM, Rosa JC, et al. Acute-phase protein alpha-1-acid glycoprotein mediates neutrophil migration failure in sepsis by a nitric oxide-dependent mechanism. Proc Natl Acad Sci U S A (2007) 104:19595-600. doi:10.1073/pnas.0709681104
45. Torres-Duenas D, Celes MR, Freitas A, Alves-Filho JC, Spiller F, Dal-Secco D, et al. Peroxynitrite mediates the failure of neutrophil migration in severe polymicrobial sepsis in mice. Br J Pharmacol (2007) 152:341-52. doi:10.1038/sj.bjp.0707393
46. Wu Z, Sawamura T, Kurdowska AK, Ji HL, Idell S, Fu J. LOX-1 deletion improves neutrophil responses, enhances bacterial clearance, and reduces lung injury in a murine polymicrobial sepsis model. Infect Immun (2011) 79:2865-70. doi:10.1128/IAI.01317-10
47. Freitas A, Alves-Filho JC, Victoni T, Secher T, Lemos HP, Sonego F, et al. IL-17 receptor signaling is required to control polymicrobial sepsis. J Immunol (2009) 182:7846-54. doi:10.4049/jimmunol.0803039
48. Reddy RC, Narala VR, Keshamouni VG, Milam JE, Newstead MW, Standiford TJ. Sepsis-induced inhibition of neutrophil chemotaxis is mediated by activation of peroxisome proliferator-activated receptor-{gamma}. Blood (2008) 112:4250-8. doi:10.1182/blood-2007-12-128967
49. Ferreira AE, Sisti F, Sonego F, Wang S, Filgueiras LR, Brandt S, et al. PPAR-gamma/IL-10 axis inhibits MyD88 expression and ameliorates murine polymicrobial sepsis. J Immunol (2014) 192:2357-65. doi:10.4049/jimmunol.1302375
50. Alves-Filho JC, Spiller F, Cunha FQ. Neutrophil paralysis in sepsis. Shock (2010) 34(Suppl 1):15-21. doi:10.1097/SHK.0b013e3181e7e61b
51. Kovach MA, Standiford TJ. The function of neutrophils in sepsis. Curr Opin Infect Dis (2012) 25:321-7. doi:10.1097/QCO.0b013e3283528c9b
52. Hoesel LM, Neff TA, Neff SB, Younger JG, Olle EW, Gao H, et al. Harmful and protective roles of neutrophils in sepsis. Shock (2005) 24:40-7. doi:10.1097/01.shk.0000170353.80318.d5
53. Brown KA, Brain SD, Pearson JD, Edgeworth JD, Lewis SM, Treacher DF. Neutrophils in development of multiple organ failure in sepsis. Lancet (2006) 368:157-69. doi:10.1016/s0140-6736(06)69005-3
54. Zhang S, Rahman M, Qi Z, Thorlacius H. Simvastatin antagonizes CD40L secretion, CXC chemokine formation, and pulmonary infiltration of neutrophils in abdominal sepsis. J Leukoc Biol (2011) 89:735-42. doi:10.1189/jlb.0510279
55. Hwaiz R, Rahman M, Syk I, Zhang E, Thorlacius H. Rac1-dependent secretion of platelet-derived CCL5 regulates neutrophil recruitment via activation of alveolar macrophages in septic lung injury. J Leukoc Biol (2015) 97:975-84. doi:10.1189/jlb.4A1214-603R
56. Johnston B, Burns AR, Suematsu M, Issekutz TB, Woodman RC, Kubes P. Chronic inflammation upregulates chemokine receptors and induces neutrophil migration to monocyte chemoattractant protein-1. J Clin Invest (1999) 103:1269-76. doi:10.1172/JCI5208
57. Speyer CL, Gao H, Rancilio NJ, Neff TA, Huffnagle GB, Sarma JV, et al. Novel chemokine responsiveness and mobilization of neutrophils during sepsis. Am J Pathol (2004) 165:2187-96. doi:10.1016/S0002-9440(10)63268-3
58. Hartl D, Krauss-Etschmann S, Koller B, Hordijk PL, Kuijpers TW, Hoffmann F, et al. Infiltrated neutrophils acquire novel chemokine receptor expression and chemokine responsiveness in chronic inflammatory lung diseases. J Immunol (2008) 181:8053-67. doi:10.4049/jimmunol.181.11.8053
59. Souto FO, Alves-Filho JC, Turato WM, Auxiliadora-Martins M, Basile-Filho A, Cunha FQ. Essential role of CCR2 in neutrophil tissue infiltration and multiple organ dysfunction in sepsis. Am J Respir Crit Care Med (2011) 183:234-42. doi:10.1164/rccm.201003-0416OC
60. Talbot J, Bianchini FJ, Nascimento DC, Oliveira RD, Souto FO, Pinto LG, et al. CCR2 expression in neutrophils plays a critical role in their migration into the joints in rheumatoid arthritis. Arthritis Rheumatol (2015) 67:1751-9. doi:10.1002/art.39117
61. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science (2004) 303:1532-5. doi:10.1126/science.1092385
62. Luo L, Zhang S, Wang Y, Rahman M, Syk I, Zhang E, et al. Proinflammatory role of neutrophil extracellular traps in abdominal sepsis. Am J Physiol Lung Cell Mol Physiol (2014) 307:L586-96. doi:10.1152/ajplung.00365.2013
63. Martinod K, Fuchs TA, Zitomersky NL, Wong SL, Demers M, Gallant M, et al. PAD4-deficiency does not affect bacteremia in polymicrobial sepsis and ameliorates endotoxemic shock. Blood (2015) 125:1948-56. doi:10.1182/blood-2014-07-587709
64. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe (2012) 12:324-33. doi:10.1016/j.chom.2012.06.011
65. Czaikoski PG, Mota JM, Nascimento DC, Sonego F, Castanheira FV, Melo PH, et al. Neutrophil extracellular traps induce organ damage during experimental and clinical sepsis. PLoS One (2016) 11:e0148142. doi:10.1371/journal.pone.0148142
66. Liu FC, Chuang YH, Tsai YF, Yu HP. Role of neutrophil extracellular traps following injury. Shock (2014) 41:491-8. doi:10.1097/shk.0000000000000146
67. Gupta AK, Joshi MB, Philippova M, Erne P, Hasler P, Hahn S, et al. Activated endothelial cells induce neutrophil extracellular traps and are susceptible to NETosis-mediated cell death. FEBS Lett (2010) 584:3193-7. doi:10.1016/j.febslet.2010.06.006
68. Gao X, Hao S, Yan H, Ding W, Li K, Li J. Neutrophil extracellular traps contribute to the intestine damage in endotoxemic rats. J Surg Res (2015) 195:211-8. doi:10.1016/j.jss.2014.12.019
69. Tanaka K, Koike Y, Shimura T, Okigami M, Ide S, Toiyama Y, et al. In vivo characterization of neutrophil extracellular traps in various organs of a murine sepsis model. PLoS One (2014) 9:e111888. doi:10.1371/journal.pone.0111888
70. Clark SR, Ma AC, Tavener SA, McDonald B, Goodarzi Z, Kelly MM, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med (2007) 13:463-9. doi:10.1038/nm1565
71. Scheibner KA, Lutz MA, Boodoo S, Fenton MJ, Powell JD, Horton MR. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol (2006) 177:1272-81. doi:10.4049/jimmunol.177.2.1272
72. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, et al. Extracellular histones are major mediators of death in sepsis. Nat Med (2009) 15:1318-21. doi:10.1038/nm.2053
73. Allam R, Scherbaum CR, Darisipudi MN, Mulay SR, Hagele H, Lichtnekert J, et al. Histones from dying renal cells aggravate kidney injury via TLR2 and TLR4. J Am Soc Nephrol (2012) 23:1375-88. doi:10.1681/asn.2011111077
74. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One (2012) 7:e32366. doi:10.1371/journal.pone.0032366
75. Brealey D, Singer M. Multi-organ dysfunction in the critically ill: effects on different organs. J R Coll Physicians Lond (2000) 34:428-31. doi:10.7861/jroycollphys.34-5-428
76. Windsor AC, Mullen PG, Fowler AA, Sugerman HJ. Role of the neutrophil in adult respiratory distress syndrome. Br J Surg (1993) 80:10-7. doi:10.1002/bjs.1800800106
77. Astiz ME, DeGent GE, Lin RY, Rackow EC. Microvascular function and rheologic changes in hyperdynamic sepsis. Crit Care Med (1995) 23:265-71. doi:10.1097/00003246-199502000-00011
78. Fink MP, Evans TW. Mechanisms of organ dysfunction in critical illness: report from a Round Table Conference held in Brussels. Intensive Care Med (2002) 28:369-75. doi:10.1007/s00134-001-1205-2
79. Aird WC. The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood (2003) 101:3765-77. doi:10.1182/blood-2002-06-1887
80. Rees DD, Monkhouse JE, Cambridge D, Moncada S. Nitric oxide and the haemodynamic profile of endotoxin shock in the conscious mouse. Br J Pharmacol (1998) 124:540-6. doi:10.1038/sj.bjp.0701815
81. Kooy NW, Lewis SJ, Royall JA, Ye YZ, Kelly DR, Beckman JS. Extensive tyrosine nitration in human myocardial inflammation: evidence for the presence of peroxynitrite. Crit Care Med (1997) 25:812-9. doi:10.1097/00003246-199705000-00017