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PLOS ONE  2014 

TRAIL Induces Neutrophil Apoptosis and Dampens Sepsis-Induced Organ Injury in Murine Colon Ascendens Stent Peritonitis

DOI: 10.1371/journal.pone.0097451

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Abstract:

TNF-related apoptosis inducing ligand (TRAIL) influences several inflammatory reactions by partially still unknown mechanisms. TRAIL is produced and expressed by several cells of the immune system. Murine Colon Ascendens Stent Peritonitis (CASP) represents a hyperinflammatory model of diffuse peritonitis. As we have shown previously, TRAIL strongly improves survival in murine CASP. This is accompanied by a significantly reduced infiltration of neutrophils in the associated lymphoid tissue. Additionally, it is known that TRAIL induces apoptosis in neutrophils and acceleration of neutrophil apoptosis enhances resolution of inflammatory reactions. In this study, we investigated the correlation of the protective effect of TRAIL in sepsis and its influence on neutrophils. We found that neutrophils infiltrating the lymphoid organs express the TRAIL-receptor DR5 at high density. Furthermore, we demonstrated that TRAIL-treatment enhances apoptosis of neutrophils in the spleen, lung and liver and decreases organ injury during sepsis. To further examine a role for neutrophils in TRAIL-mediated protection in CASP, we have depleted neutrophils 24 hours prior to CASP. In these depleted mice, administration of TRAIL was ineffective. We conclude that TRAIL induces apoptosis in tissue-infiltrating neutrophils thereby protecting organs from sepsis-induced injury.

References

[1]  Salomao R, Brunialti MK, Rapozo MM, Baggio-Zappia GL, Galanos C, et al. (2012) Bacterial sensing, cell signaling, and modulation of the immune response during sepsis. Shock 38: 227–242. doi: 10.1097/shk.0b013e318262c4b0
[2]  Remick DG, Bolgos G, Copeland S, Siddiqui J (2005) Role of interleukin-6 in mortality from and physiologic response to sepsis. Infect Immun 73: 2751–2757. doi: 10.1128/iai.73.5.2751-2757.2005
[3]  Buras JA, Holzmann B, Sitkovsky M (2005) Animal models of sepsis: setting the stage. Nat Rev Drug Discov 4: 854–865. doi: 10.1038/nrd1854
[4]  Hotchkiss RS, Coopersmith CM, Karl IE (2005) Prevention of lymphocyte apoptosis–a potential treatment of sepsis? Clin Infect Dis 41 Suppl 7: S465–469. doi: 10.1086/431998
[5]  Muenzer JT, Davis CG, Chang K, Schmidt RE, Dunne WM, et al. (2010) Characterization and modulation of the immunosuppressive phase of sepsis. Infect Immun 78: 1582–1592. doi: 10.1128/iai.01213-09
[6]  Cziupka K, Busemann A, Partecke LI, Potschke C, Rath M, et al. (2010) Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) improves the innate immune response and enhances survival in murine polymicrobial sepsis. Crit Care Med. doi: 10.1097/ccm.0b013e3181eedaa8
[7]  Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, et al. (1997) Control of TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 277: 818–821. doi: 10.1126/science.277.5327.818
[8]  Renshaw SA, Parmar JS, Singleton V, Rowe SJ, Dockrell DH, et al. (2003) Acceleration of human neutrophil apoptosis by TRAIL. J Immunol 170: 1027–1033. doi: 10.4049/jimmunol.170.2.1027
[9]  Xiao H, Wang S, Miao R, Kan W (2011) TRAIL is associated with impaired regulation of CD4+CD25? T cells by regulatory T cells in patients with rheumatoid arthritis. J Clin Immunol 31: 1112–1119. doi: 10.1007/s10875-011-9559-x
[10]  Hayakawa Y, Screpanti V, Yagita H, Grandien A, Ljunggren HG, et al. (2004) NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol 172: 123–129. doi: 10.4049/jimmunol.172.1.123
[11]  Collison A, Foster PS, Mattes J (2009) Emerging role of tumour necrosis factor-related apoptosis-inducing ligand (TRAIL) as a key regulator of inflammatory responses. Clin Exp Pharmacol Physiol 36: 1049–1053. doi: 10.1111/j.1440-1681.2009.05258.x
[12]  Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23: 197–223. doi: 10.1146/annurev.immunol.23.021704.115653
[13]  Almyroudis NG, Grimm MJ, Davidson BA, Rohm M, Urban CF, et al. (2013) NETosis and NADPH oxidase: at the intersection of host defense, inflammation, and injury. Front Immunol 4: 45. doi: 10.3389/fimmu.2013.00045
[14]  Frasch SC, Fernandez-Boyanapalli RF, Berry KZ, Leslie CC, Bonventre JV, et al. (2011) Signaling via macrophage G2A enhances efferocytosis of dying neutrophils by augmentation of Rac activity. J Biol Chem 286: 12108–12122. doi: 10.1074/jbc.m110.181800
[15]  McGrath EE, Marriott HM, Lawrie A, Francis SE, Sabroe I, et al. (2011) TNF-related apoptosis-inducing ligand (TRAIL) regulates inflammatory neutrophil apoptosis and enhances resolution of inflammation. J Leukoc Biol 90: 855–865. doi: 10.1189/jlb.0211062
[16]  Sarangi PP, Hyun YM, Lerman YV, Pietropaoli AP, Kim M (2012) Role of beta1 integrin in tissue homing of neutrophils during sepsis. Shock 38: 281–287. doi: 10.1097/shk.0b013e31826136f8
[17]  Hotchkiss RS, Tinsley KW, Swanson PE, Chang KC, Cobb JP, et al. (1999) Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc Natl Acad Sci U S A 96: 14541–14546. doi: 10.1073/pnas.96.25.14541
[18]  Hoesel LM, Neff TA, Neff SB, Younger JG, Olle EW, et al. (2005) Harmful and protective roles of neutrophils in sepsis. Shock 24: 40–47. doi: 10.1097/01.shk.0000170353.80318.d5
[19]  Wu Z, Sawamura T, Kurdowska AK, Ji HL, Idell S, et al. (2011) LOX-1 deletion improves neutrophil responses, enhances bacterial clearance, and reduces lung injury in a murine polymicrobial sepsis model. Infect Immun 79: 2865–2870. doi: 10.1128/iai.01317-10
[20]  Lum JJ, Bren G, McClure R, Badley AD (2005) Elimination of senescent neutrophils by TNF-related apoptosis-inducing [corrected] ligand. J Immunol 175: 1232–1238. doi: 10.4049/jimmunol.175.2.1232
[21]  Hoffmann O, Priller J, Prozorovski T, Schulze-Topphoff U, Baeva N, et al. (2007) TRAIL limits excessive host immune responses in bacterial meningitis. J Clin Invest 117: 2004–2013. doi: 10.1172/jci30356
[22]  Maier S, Traeger T, Entleutner M, Westerholt A, Kleist B, et al. (2004) Cecal ligation and puncture versus colon ascendens stent peritonitis: two distinct animal models for polymicrobial sepsis. Shock 21: 505–511. doi: 10.1097/01.shk.0000126906.52367.dd
[23]  Zantl N, Uebe A, Neumann B, Wagner H, Siewert JR, et al. (1998) Essential role of gamma interferon in survival of colon ascendens stent peritonitis, a novel murine model of abdominal sepsis. Infect Immun 66: 2300–2309.
[24]  Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE (2008) Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64–70. doi: 10.1189/jlb.0407247
[25]  Gurung P, Rai D, Condotta SA, Babcock JC, Badovinac VP, et al. (2011) Immune unresponsiveness to secondary heterologous bacterial infection after sepsis induction is TRAIL dependent. J Immunol 187: 2148–2154. doi: 10.4049/jimmunol.1101180
[26]  Unsinger J, Kazama H, McDonough JS, Griffith TS, Hotchkiss RS, et al. (2010) Sepsis-induced apoptosis leads to active suppression of delayed-type hypersensitivity by CD8+ regulatory T cells through a TRAIL-dependent mechanism. J Immunol 184: 6766–6772. doi: 10.4049/jimmunol.0904054
[27]  Barrera G, Landoni V, Martire-Greco D, Chiarella P, Meiss R, et al. (2011) Model of polymicrobial peritonitis that induces the proinflammatory and immunosuppressive phases of sepsis. Infect Immun 79: 1280–1288. doi: 10.1128/iai.01127-10
[28]  Simon HU (2003) Neutrophil apoptosis pathways and their modifications in inflammation. Immunol Rev 193: 101–110. doi: 10.1034/j.1600-065x.2003.00038.x
[29]  Kelly KJ, Sandoval RM, Dunn KW, Molitoris BA, Dagher PC (2003) A novel method to determine specificity and sensitivity of the TUNEL reaction in the quantitation of apoptosis. Am J Physiol Cell Physiol 284: C1309–1318. doi: 10.1152/ajpcell.00353.2002

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