Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 37, 2012, Pages 14983-14988

  El Kebira, Driss ^a   Gjorstrup, Per ^b   Filepa, János G ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b Resolvyx Pharmaceuticals   (United States)

Author keywords

Efferocytosis; Innate immunity; Leukocytes; Resolution of inflammation

Indexed keywords

BACTERIAL DNA; CARRAGEENAN; CASPASE 3; CASPASE 8; ICOSAPENTAENOIC ACID; LEUKOTRIENE B4 RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MYELOPEROXIDASE; OMEGA 3 FATTY ACID; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RESOLVIN E1; SERUM AMYLOID A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DRUG ACTIVITY; ENZYME ACTIVATION; ESCHERICHIA COLI; FEMALE; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PNEUMONIA; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; YEAST;

AMINO ACID CHLOROMETHYL KETONES; ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; CASPASE 3; CASPASE 8; CELLS, CULTURED; EICOSAPENTAENOIC ACID; ESCHERICHIA COLI; HUMANS; MICE; MITOCHONDRIA; NEUTROPHILS; PHAGOCYTOSIS; PNEUMONIA; REACTIVE OXYGEN SPECIES; RECEPTORS, LEUKOTRIENE B4; STATISTICS, NONPARAMETRIC; YEASTS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MUS;

EID: 84866295321     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206641109     Document Type: Article

References (41)

1. Nathan C, Ding A (2010) Nonresolving inflammation. Cell 140:871-882.
2. Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: Dual anti-inflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8:349-361.
3. Ware LB, Matthay MA (2000) The acute respiratory distress syndrome. N Engl J Med 342:1334-1349.
4. Savill JS, et al. (1989) Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J Clin Invest 83:865-875.
5. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: Clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2:965-975.
6. El KebirD, József L, Pan W, Filep JG(2008) Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation. Circ Res 103:352-359.
7. Rossi AG, et al. (2006) Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat Med 12:1056-1064.
8. Koedel U, et al. (2009) Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog 5:e1000461.
9. El Kebir D, et al. (2009) 15-epi-lipoxin A4 inhibits myeloperoxidase signaling and enhances resolution of acute lung injury. Am J Respir Crit Care Med 180:311-319.
10. Matute-Bello G, et al. (1997) Neutrophil apoptosis in the acute respiratory distress syndrome. Am J Respir Crit Care Med 156:1969-1977.
11. Keel M, et al. (1997) Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis. Blood 90:3356-3363.
12. Serhan CN, et al. (2000) Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from ω-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med 192:1197-1204.
13. Oh SF, Pillai PS, Recchiuti A, Yang R, Serhan CN (2011) Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation. J Clin Invest 121:569-581.
14. Arita M, et al. (2005) Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med 201:713-722.
15. Arita M, et al. (2007) Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J Immunol 178:3912-3917.
16. Haworth O, Cernadas M, Yang R, Serhan CN, Levy BD (2008) Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat Immunol 9:873-879.
17. Schwab JM, Chiang N, Arita M, Serhan CN (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447:869-874.
18. Seki H, et al. (2010) The anti-inflammatory and proresolving mediator resolvin E1 protects mice from bacterial pneumonia and acute lung injury. J Immunol 184:836-843.
19. Aoki H, et al. (2008) Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem Biophys Res Commun 367:509-515.
20. Haworth O, Cernadas M, Levy BD (2011) NK cells are effectors for resolvin E1 in the timely resolution of allergic airway inflammation. J Immunol 186:6129-6135.
21. Zhang B, Hirahashi J, Cullere X, Mayadas TN (2003) Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: Cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J Biol Chem 278:28443-28454.
22. Xu Y, Loison F, Luo HR (2010) Neutrophil spontaneous death is mediated by down-regulation of autocrine signaling through GPCR, PI3Kgamma, ROS, and actin. Proc Natl Acad Sci USA 107:2950-2955.
23. Brovkovych V, et al. (2008) Augmented iNOS expression and increased NO production reduce sepsis-induced lung injury and mortality in myeloperoxidase-null mice. Am J Physiol Lung Cell Mol Physiol 295:L96-L103.
24. 4 to mediate glucocorticoid refractory lung inflammation in chronic obstructive pulmonary disease. Proc Natl Acad Sci USA 109:935-940.
25. Schwartz DA, et al. (1997) CpG motifs in bacterial DNA cause inflammation in the lower respiratory tract. J Clin Invest 100:68-73.
26. El Kebir D, et al. (2007) Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid A in human neutrophils: A novel mechanism for resolution of inflammation. J Immunol 179:616-622.
27. József L, Khreiss T, Filep JG (2004) CpG motifs in bacterial DNA delay apoptosis of neutrophil granulocytes. FASEB J 18:1776-1778.
28. Maianski NA, et al. (2004) Functional characterization of mitochondria in neutrophils: A role restricted to apoptosis. Cell Death Differ 11:143-153.
29. Moulding DA, Quayle JA, Hart CA, Edwards SW (1998) Mcl-1 expression in human neutrophils: Regulation by cytokines and correlation with cell survival. Blood 92:2495-2502.
30. Coxon A, et al. (1996) A novel role for the beta 2 integrin CD11b/CD18 in neutrophil apoptosis: A homeostatic mechanism in inflammation. Immunity 5:653-666.
31. Serhan CN, Petasis NA (2011) Resolvins and protectins in inflammation resolution. Chem Rev 111:5922-5943.
32. McLeish KR, Klein JB, Coxon PY, Head KZ, Ward RA (1998) Bacterial phagocytosis activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase cascades in human neutrophils. J Leukoc Biol 64:835-844.
33. Cash JL, et al. (2008) Synthetic chemerin-derived peptides suppress inflammation through ChemR23. J Exp Med 205:767-775.
34. Campbell EL, et al. (2007) Resolvin E1 promotes mucosal surface clearance of neutrophils: A new paradigm for inflammatory resolution. FASEB J 21:3162-3170.
35. Gadek JE, et al.; Enteral Nutrition in ARDS Study Group (1999) Effect of enteral feeding with eicosapentaenoic acid, γ-linolenic acid, and antioxidants in patients withacute respiratory distress syndrome. Crit Care Med 27:1409-1420.
36. Pontes-Arruda A, Aragão AM, Albuquerque JD (2006) Effects of enteral feeding with eicosapentaenoic acid, γ-linoleic acid, and antioxidants in mechanically ventilatedpatients with severe sepsis and septic shock. Crit Care Med 34:2325-2333.
37. Pacht ER, et al. (2003) Enteral nutrition with eicosapentaenoic acid, γ-linolenic acid,and antioxidants reduces alveolar inflammatory mediators and protein influx in patients with acute respiratory distress syndrome. Crit Care Med 31:491-500.
38. Gilroy DW, Lawrence T, Perretti M, Rossi AG (2004) Inflammatory resolution: New opportunities for drug discovery. Nat Rev Drug Discov 3:401-416.
39. Hasturk H, et al. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 179:7021-7029.
40. Hong S, et al. (2008) Resolvin E1 metabolome in local inactivation during inflammation-resolution. J Immunol 180:3512-3519.
41. McGrath EE, et al. (2011) TNF-related apoptosis-inducing ligand (TRAIL) regulates inflammatory neutrophil apoptosis and enhances resolution of inflammation. J Leukoc Biol 90:855-865.