The role of neutrophils in inflammation resolution

Seminars in Immunology

Volumn 28, Issue 2, 2016, Pages 137-145

  Jones, Hefin R ^a   Robb, Calum T ^b   Perretti, Mauro ^a   Rossi, Adriano G ^b  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Inflammation; Neutrophil; Repair; Resolution

Indexed keywords

CHEMOKINE; CYTOKINE; INTERLEUKIN 10; AUTACOID; BIOLOGICAL MARKER;

APOPTOSIS; HOMEOSTASIS; HUMAN; INFLAMMATION; MEDIATOR RELEASE; MICROENVIRONMENT; NEUTROPHIL; NONHUMAN; REVIEW; TISSUE REPAIR; WOUND HEALING; ANIMAL; IMMUNOLOGY; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BIOMARKERS; CYTOKINES; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATION MEDIATORS; NEUTROPHIL ACTIVATION; NEUTROPHIL INFILTRATION; NEUTROPHILS; SIGNAL TRANSDUCTION; WOUND HEALING;

EID: 84968909116     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2016.03.007     Document Type: Review

References (115)

1. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D.S., et al. Neutrophil extracellular traps kill bacteria. Science 2004, 303:1532-1535. 10.1126/science.1092385.
2. Fuchs T.A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., et al. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007, 176:231-241. 10.1083/jcb.200606027.
3. Robb C.T., Dyrynda E.A., Gray R.D., Rossi A.G., Smith V.J. Invertebrate extracellular phagocyte traps show that chromatin is an ancient defence weapon. Nat. Commun. 2014, 5:4627. 10.1038/ncomms5627.
4. Perretti M., Croxtall J.D., Wheller S.K., Goulding N.J., Hannon R., Flower R.J. Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat. Med. 1996, 2:1259-1262. (accessed 09.05.15). http://www.ncbi.nlm.nih.gov/pubmed/8898757.
5. Perretti M., Christian H., Wheller S.K., Aiello I., Mugridge K.G., Morris J.F., et al. Annexin I is stored within gelatinase granules of human neutrophil and mobilized on the cell surface upon adhesion but not phagocytosis. Cell Biol. Int. 2000, 24:163-174. 10.1006/cbir.1999.0468.
6. Traverso V., Morris J.F., Flower R.J., Buckingham J. Lipocortin 1 (annexin 1) in patches associated with the membrane of a lung adenocarcinoma cell line and in the cell cytoplasm. J. Cell Sci. 1998, 111(Pt. 1):1405-1418. (accessed 09.05.15). http://www.ncbi.nlm.nih.gov/pubmed/9570758.
7. Solito E., Nuti S., Parente L. Dexamethasone-induced translocation of lipocortin (annexin) 1 to the cell membrane of U-937 cells. Br. J. Pharmacol. 1994, 112:347-348. (accessed 09.05.15). http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1910349%26tool=pmcentrez%26rendertype=abstract.
8. Babiychuk E.B., Monastyrskaya K., Draeger A. Fluorescent annexin A1 reveals dynamics of ceramide platforms in living cells. Traffic 2008, 9:1757-1775. 10.1111/j.1600-0854.2008.00800.x.
9. Scannell M., Maderna P. Lipoxins and annexin-1: resolution of inflammation and regulation of phagocytosis of apoptotic cells. Sci. World J. 2006, 6:1555-1573. 10.1100/tsw.2006.259.
10. McArthur S., Gobbetti T., Kusters D.H.M., Reutelingsperger C.P., Flower R.J., Perretti M. Definition of a novel pathway centered on lysophosphatidic acid to recruit monocytes during the resolution phase of tissue inflammation. J. Immunol. 2015, 195:1139-1151. 10.4049/jimmunol.1500733.
11. Gobbetti T., Coldewey S.M., Chen J., McArthur S., le Faouder P., Cenac N., et al. Nonredundant protective properties of FPR2/ALX in polymicrobial murine sepsis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:18685-18690. 10.1073/pnas.1410938111.
12. Dalli J., Norling L.V., Renshaw D., Cooper D., Leung K.-Y., Perretti M. Annexin 1 mediates the rapid anti-inflammatory effects of neutrophil-derived microparticles. Blood 2008, 112:2512-2519. 10.1182/blood-2008-02-140533.
13. Levy B.D., Clish C.B., Schmidt B., Gronert K., Serhan C.N. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2001, 2:612-619. 10.1038/89759.
14. Fierro I.M., Colgan S.P., Bernasconi G., Petasis N.A., Clish C.B., Arita M., et al. Lipoxin A4 and aspirin-Triggered 15-epi-Lipoxin A4 inhibit human neutrophil migration: comparisons between synthetic 15 epimers in chemotaxis and transmigration with microvessel endothelial cells and epithelial cells. J. Immunol. 2003, 170:2688-2694. 10.4049/jimmunol.170.5.2688.
15. Godson C., Mitchell S., Harvey K., Petasis N.A., Hogg N., Brady H.R. Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J. Immunol. 2000, 164:1663-1667. (accessed 09.05.15). http://www.ncbi.nlm.nih.gov/pubmed/10657608.
16. El Kebir D., Filep J.G. Modulation of neutrophil apoptosis and the resolution of inflammation through β2 integrins. Front. Immunol. 2013, 4:60. 10.3389/fimmu.2013.00060.
17. Ferracini M., Rios F.J.O., Pecenin M., Jancar S. Clearance of apoptotic cells by macrophages induces regulatory phenotype and involves stimulation of cd36 and platelet-activating factor receptor. Mediators Inflamm. 2013, 10.1155/2013/950273.
18. Buckley C.D., Gilroy D.W., Serhan C.N. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 2014, 40:315-327. 10.1016/j.immuni.2014.02.009.
19. Dalli J., Chiang N., Serhan C.N. Elucidation of novel 13-series resolvins that increase with atorvastatin and clear infections. Nat. Med. 2015, 21:1071-1075. 10.1038/nm.3911.
20. Bourke E., Cassetti A., Villa A., Fadlon E., Colotta F., Mantovani A. IL-1 beta scavenging by the type II IL-1 decoy receptor in human neutrophils. J. Immunol. 2003, 170:5999-6005. (accessed 30.11.15). http://www.ncbi.nlm.nih.gov/pubmed/12794127.
21. Crepaldi L., Silveri L., Calzetti F., Pinardi C., Cassatella M.A. Molecular basis of the synergistic production of IL-1 receptor antagonist by human neutrophils stimulated with IL-4 and IL-10. Int. Immunol. 2002, 14:1145-5153. (accessed 30.11.15). http://www.ncbi.nlm.nih.gov/pubmed/12356680.
22. Martin P., Palmer G., Vigne S., Lamacchia C., Rodriguez E., Talabot-Ayer D., et al. Mouse neutrophils express the decoy type 2 interleukin-1 receptor (IL-1R2) constitutively and in acute inflammatory conditions. J. Leukoc. Biol. 2013, 94:791-802. 10.1189/jlb.0113035.
23. Ariel A., Fredman G., Sun Y.-P., Kantarci A., Van Dyke T.E., Luster A.D., et al. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat. Immunol. 2006, 7:1209-1216. 10.1038/ni1392.
24. McKimmie C.S., Fraser A.R., Hansell C., Gutiérrez L., Philipsen S., Connell L., et al. Hemopoietic cell expression of the chemokine decoy receptor D6 is dynamic and regulated by GATA1. J. Immunol. 2008, 181:3353-3363. (accessed 30.11.15). http://www.ncbi.nlm.nih.gov/pubmed/18714007.
25. De Santo C., Arscott R., Booth S., Karydis I., Jones M., Asher R., et al. Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat. Immunol. 2010, 11:1039-1046. 10.1038/ni.1942.
26. Romani L., Mencacci A., Cenci E., Spaccapelo R., Del Sero G., Nicoletti I., et al. Neutrophil production of IL-12 and IL-10 in candidiasis and efficacy of IL-12 therapy in neutropenic mice. J. Immunol. 1997, 158:5349-5356. (accessed 21.11.15). http://www.ncbi.nlm.nih.gov/pubmed/9164955.
27. Hoffman S.J., Polack F.P., Hauer D.A., Griffin D.E. Measles virus infection of rhesus macaques affects neutrophil expression of IL-12 and IL-10. Viral Immunol. 2003, 16:369-379. 10.1089/088282403322396163.
28. Kasten K.R., Muenzer J.T., Caldwell C.C. Neutrophils are significant producers of IL-10 during sepsis. Biochem. Biophys. Res. Commun. 2010, 393:28-31. 10.1016/j.bbrc.2010.01.066.
29. Ocuin L.M., Bamboat Z.M., Balachandran V.P., Cavnar M.J., Obaid H., Plitas G., et al. Neutrophil IL-10 suppresses peritoneal inflammatory monocytes during polymicrobial sepsis. J. Leukoc. Biol. 2011, 89:423-432. 10.1189/jlb.0810479.
30. Davey M.S., Tamassia N., Rossato M., Bazzoni F., Calzetti F., Bruderek K., et al. Failure to detect production of IL-10 by activated human neutrophils. Nat. Immunol. 2011, 12:1017-1018. author reply 1018-1020. 10.1038/ni.2111.
31. Tamassia N., Zimmermann M., Castellucci M., Ostuni R., Bruderek K., Schilling B., et al. Cutting edge: an inactive chromatin configuration at the IL-10 locus in human neutrophils. J. Immunol. 2013, 190:1921-1925. 10.4049/jimmunol.1203022.
32. Voll R.E., Herrmann M., Roth E.A., Stach C., Kalden J.R., Girkontaite I. Immunosuppressive effects of apoptotic cells. Nature 1997, 390:350-351. 10.1038/37022.
33. Michlewska S., Dransfield I., Megson I.L., Rossi A.G. Macrophage phagocytosis of apoptotic neutrophils is critically regulated by the opposing actions of pro-inflammatory and anti-inflammatory agents: key role for TNF-alpha. FASEB J. 2009, 23:844-854. 10.1096/fj08-121228.
34. Ward C., Murray J., Clugston A., Dransfield I., Haslett C., Rossi A.G. Interleukin-10 inhibits lipopolysaccharide-induced survival and extracellular signal-regulated kinase activation in human neutrophils. Eur. J. Immunol. 2005, 35:2728-2737. 10.1002/eji.200425561.
35. Yáñez-Mó M., Siljander P.R.-M., Andreu Z., Zavec A.B., Borràs F.E., Buzas E.I., et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles 2015, 4. (accessed 22.05.15). http://www.journalofextracellularvesicles.net/index.php/jev/article/view/27066/xml_13.
36. Headland S.E., Jones H.R., D'sa A.S.V., Perretti M., Norling L.V. Cutting-Edge analysis of extracellular microparticles using ImageStreamX imaging flow cytometry. Sci. Rep. 2014, 4. 10.1038/srep05237.
37. Gasser O., Schifferli J.A. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 2004, 104:2543-2548. 10.1182/blood-2004-01-0361.
38. Eken C., Gasser O., Zenhaeusern G., Oehri I., Hess C., Schifferli J.A. Polymorphonuclear neutrophil-derived ectosomes interfere with the maturation of monocyte-derived dendritic cells. J. Immunol. 2008, 180:817-824. (accessed 10.05.13). http://www.ncbi.nlm.nih.gov/pubmed/18178820.
39. Eken C., Martin P.J., Sadallah S., Treves S., Schaller M., Schifferli J.A. Ectosomes released by polymorphonuclear neutrophils induce a MerTK-dependent anti-inflammatory pathway in macrophages. J. Biol. Chem. 2010, 285:39914-39921. 10.1074/jbc.M110.126748.
40. Timár C.I., Lorincz A.M., Csépányi-Kömi R., Vályi-Nagy A., Nagy G., Buzás E.I., et al. Antibacterial effect of microvesicles released from human neutrophilic granulocytes. Blood 2013, 121:510-518. 10.1182/blood-2012-05-431114.
41. Leitch A.E., Duffin R., Haslett C., Rossi A.G. Relevance of granulocyte apoptosis to resolution of inflammation at the respiratory mucosa. Mucosal Immunol. 2008, 1:350-363. 10.1038/mi.2008.31.
42. Hallett J.M., Leitch A.E., Riley N.A., Duffin R., Haslett C., Rossi A.G. Novel pharmacological strategies for driving inflammatory cell apoptosis and enhancing the resolution of inflammation. Trends Pharmacol. Sci. 2008, 29:250-257. 10.1016/j.tips.2008.03.002.
43. Rossi A.G., Sawatzky D.A., Walker A., Ward C., Sheldrake T.A., Riley N.A., et al. Cyclin-dependent kinase inhibitors enhance the resolution of inflammation by promoting inflammatory cell apoptosis. Nat. Med. 2006, 12:1056-1064. 10.1038/nm1468.
44. Leitch A.E., Riley N.A., Sheldrake T.A., Festa M., Fox S., Duffin R., et al. The cyclin-dependent kinase inhibitor R-roscovitine down-regulates Mcl-1 to override pro-inflammatory signalling and drive neutrophil apoptosis. Eur. J. Immunol. 2010, 40:1127-1138. 10.1002/eji.200939664.
45. Leitch A.E., Lucas C.D., Marwick J.A., Duffin R., Haslett C., Rossi A.G. Cyclin-dependent kinases 7 and 9 specifically regulate neutrophil transcription and their inhibition drives apoptosis to promote resolution of inflammation. Cell Death Differ. 2012, 19:1950-1961. 10.1038/cdd.2012.80.
46. Lucas C.D., Dorward D.A., Tait M.A., Fox S., Marwick J.A., Allen K.C., et al. Downregulation of Mcl-1 has anti-inflammatory pro-resolution effects and enhances bacterial clearance from the lung. Mucosal Immunol. 2014, 7:857-868. 10.1038/mi.2013.102.
47. Ward C., Chilvers E.R., Lawson M.F., Pryde J.G., Fujihara S., Farrow S.N., et al. NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J. Biol. Chem. 1999, 274:4309-4318. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/9933632.
48. Lucas C.D., Allen K.C., Dorward D.A., Hoodless L.J., Melrose L.A., Marwick J.A., et al. Flavones induce neutrophil apoptosis by down-regulation of Mcl-1 via a proteasomal-dependent pathway. FASEB J. 2013, 27:1084-1094. 10.1096/fj.12-218990.
49. Ward C., Dransfield I., Chilvers E.R., Haslett C., Rossi A.G. Pharmacological manipulation of granulocyte apoptosis: potential therapeutic targets. Trends Pharmacol. Sci. 1999, 20:503-509. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/10603493.
50. Hannah S., Mecklenburgh K., Rahman I., Bellingan G.J., Greening A., Haslett C., et al. Hypoxia prolongs neutrophil survival in vitro. FEBS Lett. 1995, 372:233-237. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/7556675.
51. Murray J., WalmsleY S.R., Mecklenburgh K.I., Cowburn A.S., White J.F., Rossi A.G., et al. Hypoxic regulation of neutrophil apoptosis role: of reactive oxygen intermediates in constitutive and tumor necrosis factor α-Induced cell death. Ann. N. Y. Acad. Sci. 2003, 1010:417-425. 10.1196/annals.1299.075.
52. K. Mecklenburgh, J. Murray, T. Brazil, C. Ward, A.G. Rossi, E.R. Chilvers, Role of neutrophil apoptosis in the resolution of pulmonary inflammation., Monaldi Arch. Chest Dis. = Arch. Monaldi per Le Mal. Del Torace/Fond. Clin. Del Lav. IRCCS [and] Ist. Di Clin. Tisiol. E Mal. Appar. Respir. Univ. Di Napoli, Second. Ateneo. 54 (1999) 345-9. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/10546479.
53. Walmsley S.R., Print C., Farahi N., Peyssonnaux C., Johnson R.S., Cramer T., et al. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 2005, 201:105-115. 10.1084/jem.20040624.
54. Walmsley S.R., Chilvers E.R., Thompson A.A., Vaughan K., Marriott H.M., Parker L.C., et al. Prolyl hydroxylase 3 (PHD3) is essential for hypoxic regulation of neutrophilic inflammation in humans and mice. J. Clin. Invest. 2011, 121:1053-1063. 10.1172/JCI43273.
55. Cox G., Gauldie J., Jordana M. Bronchial epithelial cell-derived cytokines (G-CSF and GM-CSF) promote the survival of peripheral blood neutrophils in vitro. Am. J. Respir. Cell Mol. Biol. 1992, 7:507-513. 10.1165/ajrcmb/7.5.507.
56. Lee A., Whyte M.K., Haslett C. Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J. Leukoc. Biol. 1993, 54:283-288. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/8409750.
57. Gilroy D.W., Lawrence T., Perretti M., Rossi A.G. Inflammatory resolution: new opportunities for drug discovery. Nat. Rev. Drug Discov. 2004, 3:401-416. 10.1038/nrd1383.
58. Kato T., Takeda Y., Nakada T., Sendo F. Inhibition by dexamethasone of human neutrophil apoptosis in vitro. Nat. Immun. 1995, 14:198-208. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/8696009.
59. Cox G. Glucocorticoid treatment inhibits apoptosis in human neutrophils. Separation of survival and activation outcomes., J. Immunol. 1995, 154:4719-4725. (accessed 09.02.16). http://www.ncbi.nlm.nih.gov/pubmed/7722324.
60. Meagher L.C., Cousin J.M., Seckl J.R., Haslett C. Opposing effects of glucocorticoids on the rate of apoptosis in neutrophilic and eosinophilic granulocytes. J. Immunol. 1996, 156:4422-4428. (accessed 09.02.16). http://www.ncbi.nlm.nih.gov/pubmed/8666816.
61. Marwick J.A., Dorward D.A., Lucas C.D., Jones K.O., Sheldrake T.A., Fox S., et al. Oxygen levels determine the ability of glucocorticoids to influence neutrophil survival in inflammatory environments. J. Leukoc. Biol. 2013, 94:1285-1292. 10.1189/jlb.0912462.
62. Alessandri A.L., Sousa L.P., Lucas C.D., Rossi A.G., Pinho V., Teixeira M.M. Resolution of inflammation: mechanisms and opportunity for drug development. Pharmacol. Ther. 2013, 139:189-212. 10.1016/j.pharmthera.2013.04.006.
63. Miles K., Clarke D.J., Lu W., Sibinska Z., Beaumont P.E., Davidson D.J., et al. Dying and necrotic neutrophils are anti-inflammatory secondary to the release of alpha-defensins. J. Immunol. 2009, 183:2122-2132. 10.4049/jimmunol.0804187.
64. Rock K.L., Kono H. The inflammatory response to cell death. Annu. Rev. Pathol. 2008, 3:99-126. 10.1146/annurev.pathmechdis.3.121806.151456.
65. Parnaik R., Raff M.C., Scholes J. Differences between the clearance of apoptotic cells by professional and non-professional phagocytes. Curr. Biol. 2000, 10:857-860. (accessed 08.12.15). http://www.ncbi.nlm.nih.gov/pubmed/10899007.
66. Monks J., Smith-Steinhart C., Kruk E.R., Fadok V.A., Henson P.M. Epithelial cells remove apoptotic epithelial cells during post-lactation involution of the mouse mammary gland. Biol. Reprod. 2008, 78:586-594. 10.1095/biolreprod.107.065045.
67. Dalli J., Serhan C.N. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood. 2012, 120:e60-e72. 10.1182/blood-2012-04-423525.
68. Novak M.L., Thorp E.B. Shedding light on impaired efferocytosis and nonresolving inflammation. Circ. Res. 2013, 113:9-12. 10.1161/CIRCRESAHA.113.301583.
69. Lu J., Cao Q., Zheng D., Sun Y., Wang C., Yu X., et al. Discrete functions of M2a and M2c macrophage subsets determine their relative efficacy in treating chronic kidney disease. Kidney Int. 2013, 84:745-755. 10.1038/ki.2013.135.
70. Liu Y., Cousin J.M., Hughes J., Van Damme J., Seckl J.R., Haslett C., et al. Glucocorticoids promote nonphlogistic phagocytosis of apoptotic leukocytes. J. Immunol. 1999, 162:3639-3646. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/10092825.
71. Leibovich S.J., Chen J.-F., Pinhal-Enfield G., Belem P.C., Elson G., Rosania A., et al. Synergistic up-regulation of vascular endothelial growth factor expression in murine macrophages by adenosine A(2A) receptor agonists and endotoxin. Am. J. Pathol. 2002, 160:2231-2244. 10.1016/S0002-9440(10) 61170-4.
72. Scapini P., Calzetti F., Cassatella M.A. On the detection of neutrophil-derived vascular endothelial growth factor (VEGF). J. Immunol. Methods. 1999, 232:121-129. 10.1016/S0022-1759(99) 00170-2.
73. Scapini P., Morini M., Tecchio C., Minghelli S., Di Carlo E., Tanghetti E., et al. CXCL1/macrophage inflammatory protein-2-induced angiogenesis in vivo is mediated by neutrophil-derived vascular endothelial growth factor-A. J. Immunol. 2004, 172:5034-5040. (accessed 29.02.16). http://www.ncbi.nlm.nih.gov/pubmed/15067085.
74. Gaudry M., Brégerie O., Andrieu V., El Benna J., Pocidalo M.A., Hakim J. Intracellular pool of vascular endothelial growth factor in human neutrophils. Blood. 1997, 90:4153-4161. (abstract, accessed 29.02.16). http://www.bloodjournal.org/content/90/10/4153.
75. Koedel U., Frankenberg T., Kirschnek S., Obermaier B., Häcker H., Paul R., et al. Apoptosis is essential for neutrophil functional shutdown and determines tissue damage in experimental pneumococcal meningitis. PLoS Pathog. 2009, 5:e1000461. 10.1371/journal.ppat.1000461.
76. Huynh M.-L.N., Fadok V.A., Henson P.M. Phosphatidylserine-dependent ingestion of apoptotic cells promotes TGF-beta1 secretion and the resolution of inflammation. J. Clin. Invest. 2002, 109:41-50. 10.1172/JCI11638.
77. Lee Y.-J., Moon C., Lee S.H., Park H.-J., Seoh J.-Y., Cho M.-S., et al. Apoptotic cell instillation after bleomycin attenuates lung injury through hepatocyte growth factor induction. Eur. Respir. J. 2012, 40:424-435. 10.1183/09031936.00096711.
78. Ren Y., Xie Y., Jiang G., Fan J., Yeung J., Li W., et al. Apoptotic cells protect mice against lipopolysaccharide-induced shock. J. Immunol. 2008, 180:4978-4985. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/18354223.
79. Bijl M., Reefman E., Horst G., Limburg P.C., Kallenberg C.G.M. Reduced uptake of apoptotic cells by macrophages in systemic lupus erythematosus: correlates with decreased serum levels of complement. Ann. Rheum. Dis. 2006, 65:57-63. 10.1136/ard.2005.035733.
80. Eltboli O., Bafadhel M., Hollins F., Wright A., Hargadon B., Kulkarni N., et al. COPD exacerbation severity and frequency is associated with impaired macrophage efferocytosis of eosinophils. BMC Pulm. Med. 2014, 14:112. 10.1186/1471-2466-14-112.
81. Barker R.N., Erwig L.-P., Hill K.S.K., Devine A., Pearce W.P., Rees A.J. Antigen presentation by macrophages is enhanced by the uptake of necrotic, but not apoptotic, cells. Clin. Exp. Immunol. 2002, 127:220-225. (accessed 21.02.16). http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1906351%26tool=pmcentrez%26rendertype=abstract.
82. Mevorach D., Zhou J.L., Song X., Elkon K.B. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J. Exp. Med. 1998, 188:387-392. (accessed 21.02.16). http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2212450%26tool=pmcentrez%26rendertype=abstract.
83. Harel-Adar T., Ben Mordechai T., Amsalem Y., Feinberg M.S., Leor J., Cohen S. Modulation of cardiac macrophages by phosphatidylserine-presenting liposomes improves infarct repair. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1827-1832. 10.1073/pnas.1015623108.
84. Ramos G.C., Fernandes D., Charão C.T., Souza D.G., Teixeira M.M., Assreuy J. Apoptotic mimicry: phosphatidylserine liposomes reduce inflammation through activation of peroxisome proliferator-activated receptors (PPARs) in vivo. Br. J. Pharmacol. 2007, 151:844-850. 10.1038/sj.bjp.0707302.
85. McGrath E.E., Marriott H.M., Lawrie A., Francis S.E., Sabroe I., Renshaw S.A., et al. TNF-related apoptosis-inducing ligand (TRAIL) regulates inflammatory neutrophil apoptosis and enhances resolution of inflammation. J. Leukoc. Biol. 2011, 90:855-865. 10.1189/jlb.0211062.
86. Alessandri A.L., Duffin R., Leitch A.E., Lucas C.D., Sheldrake T.A., Dorward D.A., et al. Induction of eosinophil apoptosis by the cyclin-dependent kinase inhibitor AT7519 promotes the resolution of eosinophil-dominant allergic inflammation. PLoS One 2011, 6:e25683. 10.1371/journal.pone.0025683.
87. Lucas C.D., Dorward D.A., Sharma S., Rennie J., Felton J.M., Alessandri A.L., et al. Wogonin induces eosinophil apoptosis and attenuates allergic airway inflammation. Am. J. Respir. Crit. Care Med. 2015, 191:626-636. 10.1164/rccm.201408-1565OC.
88. Felton J.M., Lucas C.D., Rossi A.G., Dransfield I. Eosinophils in the lung-modulating apoptosis and efferocytosis in airway inflammation. Front. Immunol. 2014, 5:302. 10.3389/fimmu.2014.00302.
89. Poon I.K.H., Lucas C.D., Rossi A.G., Ravichandran K.S. Apoptotic cell clearance: basic biology and therapeutic potential. Nat. Rev. Immunol. 2014, 14:166-180. 10.1038/nri3607.
90. Watson R.W., Redmond H.P., Wang J.H., Condron C., Bouchier-Hayes D. Neutrophils undergo apoptosis following ingestion of Escherichia coli. J. Immunol. 1996, 156:3986-3992. (accessed 08.12.15). http://www.ncbi.nlm.nih.gov/pubmed/8621940.
91. El Kebir D., Gjorstrup P., Filep J.G. Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:14983-14988. 10.1073/pnas.1206641109.
92. Horckmans M., Ring L., Duchene J., Santovito D., Schloss M.J., Drechsler M., et al. Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype. Eur. Heart J. 2016, 10.1093/eurheartj/ehw002.
93. Brannigan A.E., O'Connell P.R., Hurley H., O'Neill A., Brady H.R., Fitzpatrick J.M., et al. Neutrophil apoptosis is delayed in patients with inflammatory bowel disease. Shock. 2000, 13:361-366. (accessed 01.02.16). http://www.ncbi.nlm.nih.gov/pubmed/10807010.
94. Gamonal J., Sanz M., O'Connor A., Acevedo A., Suarez I., Sanz A., et al. Delayed neutrophil apoptosis in chronic periodontitis patients. J. Clin. Periodontol. 2003, 30:616-623. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/12834499.
95. O'Neill S., O'Neill A.J., Conroy E., Brady H.R., Fitzpatrick J.M., Watson R.W.G. Altered caspase expression results in delayed neutrophil apoptosis in acute pancreatitis. J. Leukoc. Biol. 2000, 68:15-20. (long, accessed 21.02.16). http://www.jleukbio.org/content/68/1/15.
96. Pérez-Ladaga A., Muñoz M.A., Mastora C., Sola A. HIF-1α provokes delayed neutrophil apoptosis by decreasing 24P3 expression and intracellular iron content. Eur. J. Inflamm. 2014, 12:53-65. 10.1177/1721727X1401200106.
97. Teixeira C.F.P., Zamunér S.R., Zuliani J.P., Fernandes C.M., Cruz-Hofling M.A., Fernandes I., et al. Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom. Muscle Nerve. 2003, 28:449-459. 10.1002/mus.10453.
98. Theilgaard-Monch K., Knudsen S., Follin P., Borregaard N. The transcriptional activation program of human neutrophils in skin lesions supports their important role in wound healing. J. Immunol. 2004, 172:7684-7693. 10.4049/jimmunol.172.12.7684.
99. Dovi J.V. Accelerated wound closure in neutrophil-depleted mice. J. Leukoc. Biol. 2003, 73:448-455. 10.1189/jlb.0802406.
100. Campbell E.L.L., Bruyninckx W.J.J., Kelly C.J.J., Glover L.E.E., McNamee E.N.N., Bowers B.E.E., et al. Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity. 2014, 40:66-77. 10.1016/j.immuni.2013.11.020.
101. Zindl C.L., Lai J.-F., Lee Y.K., Maynard C.L., Harbour S.N., Ouyang W., et al. IL-22-producing neutrophils contribute to antimicrobial defense and restitution of colonic epithelial integrity during colitis. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:12768-12773. 10.1073/pnas.1300318110.
102. Aarbiou J., Ertmann M., van Wetering S., van Noort P., Rook D., Rabe K.F., et al. Human neutrophil defensins induce lung epithelial cell proliferation in vitro. J. Leukoc. Biol. 2002, 72:167-174. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/12101277.
103. Ginzberg H.H., Cherapanov V., Dong Q., Cantin A., McCulloch C.A., Shannon P.T., et al. Neutrophil-mediated epithelial injury during transmigration: role of elastase. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281:G705-G7017. (accessed 21.02.16). http://www.ncbi.nlm.nih.gov/pubmed/11518683.
104. Suzuki T., Moraes T.J., Vachon E., Ginzberg H.H., Huang T.-T., Matthay M.A., et al. Proteinase-activated receptor-1 mediates elastase-induced apoptosis of human lung epithelial cells. Am. J. Respir. Cell Mol. Biol. 2005, 33:231-247. 10.1165/rcmb.2005-0109OC.
105. Lungarella G., Cavarra E., Lucattelli M., Martorana P.A. The dual role of neutrophil elastase in lung destruction and repair. Int. J. Biochem. Cell Biol. 2008, 40:1287-1296. 10.1016/j.biocel.2007.12.008.
106. Zemans R.L., Briones N., Campbell M., McClendon J., Young S.K., Suzuki T., et al. Neutrophil transmigration triggers repair of the lung epithelium via beta-catenin signaling. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:15990-15995. 10.1073/pnas.1110144108.
107. Zemans R.L., McClendon J., Aschner Y., Briones N., Young S.K., Lau L.F., et al. Role of β-catenin-regulated CCN matricellular proteins in epithelial repair after inflammatory lung injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 2013, 304:L415-L427. 10.1152/ajplung.00180.2012.
108. Rieger M.E., Zhou B., Solomon N., Sunohara M., Li C., Nguyen C., et al. P300/β-catenin interactions regulate adult progenitor cell differentiation downstream of Wnt5a/protein kinase C (PKC). J. Biol. Chem. 2016, (M115.706416). 10.1074/jbc.M115.706416.
109. Wilson R., Cohen J.M., Jose R.J., de Vogel C., Baxendale H., Brown J.S. Protection against Streptococcus pneumoniae lung infection after nasopharyngeal colonization requires both humoral and cellular immune responses. Mucosal Immunol. 2015, 8:627-639. 10.1038/mi.2014.95.
110. Headland S.E., Jones H.R., Norling L.V., Kim A., Souza P.R., Corsiero E., et al. Neutrophil-derived microvesicles enter cartilage and protect the joint in inflammatory arthritis. Sci. Transl. Med. 2015, 7. (315ra190-315ra190). 10.1126/scitranslmed.aac5608.
111. Damazo A.S., Yona S., Flower R.J., Perretti M., Oliani S.M. Spatial and temporal profiles for anti-Inflammatory gene expression in leukocytes during a resolving model of peritonitis. J. Immunol. 2006, 176:4410-4418. 10.4049/jimmunol.176.7.4410.
112. Tsuda Y., Takahashi H., Kobayashi M., Hanafusa T., Herndon D.N., Suzuki F. Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity 2004, 21:215-226. 10.1016/j.immuni.2004.07.006.
113. Fridlender Z.G., Sun J., Kim S., Kapoor V., Cheng G., Ling L., et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: N1 versus N2 TAN. Cancer Cell. 2009, 16:183-194. 10.1016/j.ccr.2009.06.017.
114. Neely C.J., Kartchner L.B., Mendoza A.E., Linz B.M., Frelinger J.A., Wolfgang M.C., et al. Flagellin treatment prevents increased susceptibility to systemic bacterial infection after injury by inhibiting anti-inflammatory IL-10+ IL-12- neutrophil polarization. PLoS One 2014, 9:e85623. 10.1371/journal.pone.0085623.
115. Nadkarni S., Dalli J., Hollywood J., Mason J.C., Dasgupta B., Perretti M. Investigational analysis reveals a potential role for neutrophils in giant-cell arteritis disease progression. Circ. Res. 2014, 114:242-248. 10.1161/CIRCRESAHA.114.301374.