Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation
Open accessAbstract
Inappropriate neutrophil activation contributes to the pathogenesis of acute lung injury (ALI). Apoptosis is essential for removal of neutrophils from inflamed tissues and timely resolution of inflammation. Resolvin E1 (RvE1) is an endogenous lipid mediator derived from the ω-3 polyunsaturated fatty acid eicosapentaenoic acid that displays proresolving actions. Because the balance of prosurvival and proapoptosis signals determines the fate of neutrophils, we investigated the impact of RvE1 on neutrophil apoptosis and the outcome of neutrophil-mediated pulmonary inflammation in mice. Culture of human neutrophils with RvE1 accelerated apoptosis evoked by phagocytosis of opsonized Escherichia coli or yeast. RvE1 through the leukotriene B 4 receptor BLT1 enhanced NADPH oxidase-derived reactive oxygen species generation and subsequent activation of caspase-8 and caspase-3. RvE1 also attenuated ERK and Akt-mediated apoptosis-suppressing signals from myeloperoxidase, serum amyloid A, and bacterial DNA, shifting the balance of pro- and anti-survival signals toward apoptosis via induction of mitochondrial dysfunction. In mice, RvE1 treatment enhanced the resolution of established neutrophil-mediated pulmonary injury evoked by intratracheal instillation or i.p. administration of live E. coli or intratracheal instillation of carrageenan plus myeloperoxidase via facilitating neutrophil apoptosis and their removal by macrophages. The actions of RvE1 were prevented by the pan-caspase inhibitor zVAD-fmk. These results identify a mechanism, promotion of phagocytosis-induced neutrophil apoptosis and mitigation of potent anti-apoptosis signals, by which RvE1 could enhance resolution of acute lung inflammation.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
RvE1 limits neutrophil-mediated inflammation by promoting neutrophil apoptosis and efferocytosis.
“The EPA-derived SPM RvE1 limits neutrophil-mediated inflammation by promoting neutrophil apoptosis and efferocytosis113.”
From Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities (2019) · cites this paper as [113]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Acute Respiratory Distress Syndrome
Matthay, M. A. (1996) · New England Journal of Medicine · doi:10.1056/nejm199605303342209 · Cited by 4,924 · see citing works
The Acute Respiratory Distress Syndrome
Ware, L. B., & Matthay, M. A. (2000) · New England Journal of Medicine · doi:10.1056/nejm200005043421806 · Cited by 4,666 · see citing works
Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators
Serhan, C. N., Chiang, N., & Van Dyke, T. E. (2008) · Nature Reviews Immunology · doi:10.1038/nri2294 · Cited by 2,932 · see citing works
Nathan, C., & Ding, A. (2010) · Cell · doi:10.1016/j.cell.2010.02.029 · Cited by 2,183 · see citing works
A blast from the past: clearance of apoptotic cells regulates immune responses
Savill, J., Dransfield, I., Gregory, C. D., & Haslett, C. (2002) · Nature reviews. Immunology · doi:10.1038/nri957 · Cited by 1,574 · see citing works
Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M., & Haslett, C. (1989) · Journal of Clinical Investigation · doi:10.1172/jci113970 · Cited by 1,536 · see citing works
Serhan, C. N., Clish, C. B., Brannon, J., Colgan, S. P., Chiang, N., & Gronert, K. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.192.8.1197 · Cited by 1,189 · see citing works
Resolvin E1 and protectin D1 activate inflammation-resolution programmes
Schwab, J. M., Chiang, N., Arita, M., & Serhan, C. N. (2007) · Nature · doi:10.1038/nature05877 · Cited by 1,188 · see citing works
Resolvins and protectins in inflammation resolution
Serhan, C. N., & Petasis, N. A. (2011) · Chemical Reviews · doi:10.1021/cr100396c · Cited by 996 · see citing works
Arita, M., Bianchini, F., Aliberti, J., Sher, A., Chiang, N., Hong, S., Yang, R., Petasis, N. A., & Serhan, C. N. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20042031 · Cited by 926 · see citing works
Inflammatory Resolution: new opportunities for drug discovery
Gilroy, D. W., Lawrence, T., Perretti, M., & Rossi, A. G. (2004) · Nature Reviews Drug Discovery · doi:10.1038/nrd1383 · Cited by 772 · see citing works
Gadek, J. E., DeMichele, S. J., Karlstad, M. D., Pacht, E. R., Donahoe, M., Albertson, T. E., Van Hoozen, C., Wennberg, A. K., Nelson, J. L., & Noursalehi, M. (1999) · Critical Care Medicine · doi:10.1097/00003246-199908000-00001 · Cited by 757 · see citing works
Arita, M., Ohira, T., Sun, Y., Elangovan, S., Chiang, N., & Serhan, C. N. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.6.3912 · Cited by 636 · see citing works
Coxon, A., Rieu, P., Barkalow, F. J., Askari, S., Sharpe, A. H., von Andrian, U. H., Arnaout, M. A., & Mayadas, T. N. (1996) · Immunity · doi:10.1016/s1074-7613(00)80278-2 · Cited by 627 · see citing works
Rossi, A. G., Sawatzky, D. A., Walker, A., Ward, C., Sheldrake, T. A., Riley, N. A., Caldicott, A., Martínez‐Losa, M., Walker, T. R., Duffin, R., et al. (2006) · Nature Medicine · doi:10.1038/nm1468 · Cited by 506 · see citing works
Hastürk, H., Kantarcı, A., Goguet, E., Blackwood, A., Andry, C., Serhan, C. N., & Dyke, T. E. V. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.10.7021 · Cited by 462 · see citing works
Haworth, O., Cernadas, M., Yang, R., Serhan, C. N., & Levy, B. D. (2008) · Nature Immunology · doi:10.1038/ni.1627 · Cited by 425 · see citing works
Pontes-Arruda, A., Aragão, A. M. A., & Albuquerque, J. D. (2006) · Critical Care Medicine · doi:10.1097/01.ccm.0000234033.65657.b6 · Cited by 423 · see citing works
Neutrophil Apoptosis in the Acute Respiratory Distress Syndrome
Matute‐Bello, G., Liles, W. C., Radella, F., Steinberg, K. P., RUZINSKI, J. T., Jonas, M., CHI, E. Y., Hudson, L. D., & MARTIN, T. R. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.156.6.96-12081 · Cited by 394 · see citing works
Functional characterization of mitochondria in neutrophils: a role restricted to apoptosis
Mayanskiy, N. A., Geissler, J., Srinivasula, S. M., Alnemri, E. S., Roos, D., & Kuijpers, T. W. (2003) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4401320 · Cited by 385 · see citing works
Synthetic chemerin-derived peptides suppress inflammation through ChemR23
Cash, J. L., Hart, R., Russ, A., Dixon, J. P. C., Colledge, W. H., Doran, J., Hendrick, A. G., Carlton, M. B. L., & Greaves, D. R. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20071601 · Cited by 372 · see citing works
Mcl-1 Expression in Human Neutrophils: Regulation by Cytokines and Correlation With Cell Survival
MOULDING, D. A., Quayle, J. A., Hart, C. A., & Edwards, S. W. (1998) · Blood · doi:10.1182/blood.v92.7.2495 · Cited by 356 · see citing works
Oh, S. F., Pillai, P. S., Recchiuti, A., Yang, R., & Serhan, C. N. (2011) · Journal of Clinical Investigation · doi:10.1172/jci42545 · Cited by 292 · see citing works
Keel, M. J. B., Ungethüm, U., Steckholzer, U., Niederer, E. M., Härtung, T., Trentz, O., & Ertel, W. (1997) · Blood · doi:10.1182/blood.v90.9.3356 · Cited by 291 · see citing works
CpG motifs in bacterial DNA cause inflammation in the lower respiratory tract.
Schwartz, D. A., Quinn, T. J., Thorne, P. S., Sayeed, S., Yi, A., & KRIEG, A. M. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119523 · Cited by 250 · see citing works
Elucidation of Molecular Events Leading to Neutrophil Apoptosis following Phagocytosis
Zhang, B., Hirahashi, J., Culleré, X., & Mayadas, T. N. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210727200 · Cited by 242 · see citing works
Seki, H., Fukunaga, K., Arita, M., Arai, H., Nakanishi, H., Taguchi, R., Miyasho, T., Takamiya, R., Asano, K., Ishizaka, A., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901809 · Cited by 221 · see citing works
15-Epi-lipoxin A4 Inhibits Myeloperoxidase Signaling and Enhances Resolution of Acute Lung Injury
Kebir, D. E., József, L., Pan, W., Wang, L., Petasis, N. A., Serhan, C. N., & Filep, J. G. (2009) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200810-1601oc · Cited by 206 · see citing works
Self-citationCampbell, E. L., Louis, N. A., Tomassetti, S. E., Canny, G. O., Arita, M., Serhan, C. N., & Colgan, S. P. (2007) · The FASEB Journal · doi:10.1096/fj.07-8473com · Cited by 205 · see citing works
Myeloperoxidase Delays Neutrophil Apoptosis Through CD11b/CD18 Integrins and Prolongs Inflammation
Kebir, D. E., József, L., Pan, W., & Filep, J. G. (2008) · Circulation Research · doi:10.1161/01.res.0000326772.76822.7a · Cited by 191 · see citing works
Self-citationPacht, E. R., DeMichele, S. J., Nelson, J. L., Hart, J., Wennberg, A. K., & Gadek, J. E. (2003) · Critical Care Medicine · doi:10.1097/01.ccm.0000049952.96496.3e · Cited by 191 · see citing works
Koedel, U., Frankenberg, T., Kirschnek, S., Obermaier, B., Häcker, H., Paul, R. H., & Häcker, G. A. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000461 · Cited by 179 · see citing works
Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma
Aoki, H., Hisada, T., Ishizuka, T., Utsugi, M., Kawata, T., Shimizu, Y., Okajima, F., Dobashi, K., & Mori, M. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.01.012 · Cited by 172 · see citing works
Bozinovski, S., Uddin, M., Vlahos, R., Thompson, M., McQualter, J. L., Merritt, A.-S., Wark, P. A. B., Hutchinson, A., Irving, L. B., Levy, B. D., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1109382109 · Cited by 163 · see citing works
NK Cells Are Effectors for Resolvin E1 in the Timely Resolution of Allergic Airway Inflammation
Haworth, O., Cernadas, M., & Levy, B. D. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1004007 · Cited by 144 · see citing works
McGrath, E. E., Marriott, H. M., Lawrie, A., Francis, S., Sabroe, I., Renshaw, S. A., Dockrell, D. H., & Whyte, M. K. B. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0211062 · Cited by 138 · see citing works
Kebir, D. E., József, L., Khreiss, T., Pan, W., Petasis, N. A., Serhan, C. N., & Filep, J. G. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.1.616 · Cited by 136 · see citing works
Self-citationMcLeish, K. R., Klein, J. B., Coxon, P. Y., Head, K. Z., & Ward, R. A. (1998) · Journal of Leukocyte Biology · doi:10.1002/jlb.64.6.835 · Cited by 110 · see citing works
Resolvin E1 Metabolome in Local Inactivation during Inflammation-Resolution
Hong, S., Porter, T. F., Lu, Y., Oh, S. F., Pillai, P. S., & Serhan, C. N. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.5.3512 · Cited by 107 · see citing works
CpG motifs in bacterial DNA delay apoptosis of neutrophil granulocytes
József, L., Khreiss, T., & Filep, J. G. (2004) · The FASEB Journal · doi:10.1096/fj.04-2048fje · Cited by 95 · see citing works
Self-citationBrovkovych, V. M., Gao, X.-P., Ong, E., Brovkovych, S. D., Brennan, M., Su, X., Hazen, S. L., Malik, A. B., & Skidgel, R. A. (2008) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00450.2007 · Cited by 74 · see citing works
Xu, Y., Loison, F., & Luo, H. R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912717107 · Cited by 72 · see citing works
Mcl-1 Expression in Human Neutrophils: Regulation by Cytokines and Correlation With Cell Survival
MOULDING, D. A., Quayle, J. A., Hart, C. A., et al. (1998) · Blood · doi:10.1182/blood.v92.7.2495.2495_2495_2502 · Cited by 42 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Pro-resolving lipid mediators are leads for resolution physiology
Serhan, C. N. (2014) · Nature · doi:10.1038/nature13479 · Cited by 3,041 · see citing works
Resolvins in inflammation: emergence of the pro-resolving superfamily of mediators
Serhan, C. N., & Levy, B. D. (2018) · Journal of Clinical Investigation · doi:10.1172/jci97943 · Cited by 1,344 · see citing works
Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities
Bäck, M., Yurdagul, A., Tabas, I., Öörni, K., & Kovanen, P. T. (2019) · Nature Reviews Cardiology · doi:10.1038/s41569-019-0169-2 · Cited by 1,341 · see citing works
Apoptotic cell clearance: basic biology and therapeutic potential
Poon, I. K. H., Lucas, C. D., Rossi, A. G., & Ravichandran, K. S. (2014) · Nature Reviews Immunology · doi:10.1038/nri3607 · Cited by 1,223 · see citing works
Targeting inflammation in atherosclerosis — from experimental insights to the clinic
Soehnlein, O., & Libby, P. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00198-1 · Cited by 1,042 · see citing works
Resolution of inflammation: a new therapeutic frontier
Fullerton, J. N., & Gilroy, D. W. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.39 · Cited by 937 · see citing works
Specialized pro-resolving mediators: endogenous regulators of infection and inflammation
Basil, M. C., & Levy, B. D. (2015) · Nature reviews. Immunology · doi:10.1038/nri.2015.4 · Cited by 805 · see citing works
Neutrophils in chronic inflammatory diseases
Herrero-Cervera, A., Soehnlein, O., & Kenne, E. M. (2022) · Cellular and Molecular Immunology · doi:10.1038/s41423-021-00832-3 · Cited by 719 · see citing works
The resolution code of acute inflammation: Novel pro-resolving lipid mediators in resolution
Serhan, C. N., Chiang, N., & Dalli, J. (2015) · Seminars in Immunology · doi:10.1016/j.smim.2015.03.004 · Cited by 583 · see citing works
Neutrophil chemoattractant receptors in health and disease: Double-edged swords
Metzemaekers, M., Gouwy, M., & Proost, P. (2020) · Cellular & Molecular Immunology · doi:10.1038/s41423-020-0412-0 · Cited by 570 · see citing works
Nutrition, immunity and COVID-19
Calder, P. C. (2020) · BMJ Nutrition Prevention & Health · doi:10.1136/bmjnph-2020-000085 · Cited by 587 · see citing works
Serhan, C. N. (2017) · The FASEB Journal · doi:10.1096/fj.201601222r · Cited by 553 · see citing works
Lipid Mediators in the Resolution of InflammationPreprint
Serhan, C. N., Chiang, N., Dalli, J., & Levy, B. D. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016311 · Cited by 545 · see citing works
Resolvins, Specialized Proresolving Lipid Mediators, and Their Potential Roles in Metabolic Diseases
Spite, M., Clària, J., & Serhan, C. N. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2013.10.006 · Cited by 464 · see citing works
Natural resolution of inflammation
Freire, M., & Dyke, T. E. V. (2013) · Periodontology 2000 · doi:10.1111/prd.12034 · Cited by 391 · see citing works
Identification of resolvin D2 receptor mediating resolution of infections and organ protection
Chiang, N., Dalli, J., Colas, R. A., & Serhan, C. N. (2015) · The Journal of Experimental Medicine · doi:10.1084/jem.20150225 · Cited by 388 · see citing works
Cell Death in the Lung: The Apoptosis–Necroptosis Axis
Sauler, M., Bazan, I. S., & Lee, P. J. (2018) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020518-114320 · Cited by 325 · see citing works
Chiang, N., & Serhan, C. N. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.03.005 · Cited by 330 · see citing works
The role of neutrophils in inflammation resolution
Jones, H. R., Robb, C. T., Perretti, M., & Rossi, A. G. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.03.007 · Cited by 298 · see citing works
GPR37 regulates macrophage phagocytosis and resolution of inflammatory pain
Bang, S., Xie, Y., Zhang, Z., Wang, Z., Xu, Z., & Ji, R. (2018) · Journal of Clinical Investigation · doi:10.1172/jci99888 · Cited by 288 · see citing works
Neutrophils in innate and adaptive immunity
Jaillon, S., Galdiero, M. R., Prete, D. D., Cassatella, M. A., Garlanda, C., & Mantovani, A. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0374-8 · Cited by 284 · see citing works
Dobrev, D., Heijman, J., Hiram, R., Li, N., & Nattel, S. (2022) · Nature Reviews Cardiology · doi:10.1038/s41569-022-00759-w · Cited by 272 · see citing works
The role of non-resolving inflammation in atherosclerosis
Kasikara, C., Doran, A. C., Cai, B., & Tabas, I. (2018) · Journal of Clinical Investigation · doi:10.1172/jci97950 · Cited by 266 · see citing works
Serhan, C. N. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.03.001 · Cited by 266 · see citing works
Potey, P. M., Rossi, A. G., Lucas, C. D., & Dorward, D. A. (2018) · The Journal of Pathology · doi:10.1002/path.5221 · Cited by 248 · see citing works
New pro-resolving n-3 mediators bridge resolution of infectious inflammation to tissue regeneration
Serhan, C. N., Chiang, N., & Dalli, J. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.08.002 · Cited by 246 · see citing works
Resolvin D3 and Aspirin-Triggered Resolvin D3 Are Potent Immunoresolvents
Dalli, J., Winkler, J. W., Colas, R. A., Arnardottir, H. H., Cheng, C.-Y. C., Chiang, N., Petasis, N. A., & Serhan, C. N. (2013) · Chemistry & Biology · doi:10.1016/j.chembiol.2012.11.010 · Cited by 246 · see citing works
Sansbury, B. E., & Spite, M. R. (2016) · Circulation Research · doi:10.1161/circresaha.116.307308 · Cited by 226 · see citing works
Omega-3 fatty acid-derived mediators that control inflammation and tissue homeostasis
Ishihara, T., Yoshida, M., & Arita, M. (2019) · International Immunology · doi:10.1093/intimm/dxz001 · Cited by 218 · see citing works
Resolution of inflammation: Mechanisms and opportunity for drug development
Alessandri, A. L., Sousa, L. P., Lucas, C. D., Rossi, A. G., Pinho, V., & Teixeira, M. M. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.04.006 · Cited by 217 · see citing works
Hsiao, H.-M., Sapinoro, R., Thatcher, T. H., Croasdell, A., Levy, E. P., Fulton, R. A., Olsen, K. C., Pollock, S. J., Serhan, C. N., Phipps, R. P., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058258 · Cited by 212 · see citing works
Production of hydroxy fatty acids by microbial fatty acid-hydroxylation enzymes
Kim, K.-R., & Oh, D. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.07.004 · Cited by 187 · see citing works
Roles of neutrophil granule proteins in orchestrating inflammation and immunity
Othman, A., Sekheri, M., & Filep, J. G. (2021) · FEBS Journal · doi:10.1111/febs.15803 · Cited by 184 · see citing works
Self-citationResolvin E1 Reverses Experimental Periodontitis and Dysbiosis
Lee, C.-T., Teles, R. P., Kantarcı, A., Chen, T., McCafferty, J., Starr, J. R., Brito, L. C. N., Paster, B. J., & Dyke, T. E. V. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600859 · Cited by 176 · see citing works
Lipoxin and Resolvin Receptors Transducing the Resolution of Inflammation in Cardiovascular Disease
Pirault, J., & Bäck, M. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01273 · Cited by 167 · see citing works
Sorokin, A. V., Karathanasis, S. K., Yang, Z., Freeman, L. A., Kotani, K., & Remaley, A. T. (2020) · The FASEB Journal · doi:10.1096/fj.202001451 · Cited by 166 · see citing works
Satyanarayanan, S. K., Kebir, D. E., Soboh, S., Butenko, S., Sekheri, M., Saadi, J., Peled, N., Assi, S., Othman, A., Schif‐Zuck, S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10903-9 · Cited by 160 · see citing works
Self-citationNeutrophil and remnant clearance in immunity and inflammation
Singhal, A., & Kumar, S. (2021) · Immunology · doi:10.1111/imm.13423 · Cited by 158 · see citing works
Interplay between intestinal alkaline phosphatase, diet, gut microbes and immunity
Estaki, M. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i42.15650 · Cited by 146 · see citing works
Dalli, J., & Serhan, C. N. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14336 · Cited by 138 · see citing works
Efferocytosis and Lung Disease
McCubbrey, A. L., & Curtis, J. L. (2013) · CHEST Journal · doi:10.1378/chest.12-2413 · Cited by 130 · see citing works
Li, Y., Dalli, J., Chiang, N., Baron, R. M., Quintana, C., & Serhan, C. N. (2013) · Immunity · doi:10.1016/j.immuni.2013.10.011 · Cited by 126 · see citing works
Immune resolution mechanisms in inflammatory arthritis
Perretti, M., Cooper, D., Dalli, J., & Norling, L. V. (2017) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2016.193 · Cited by 126 · see citing works
Targeting Neutrophils for Promoting the Resolution of Inflammation
Filep, J. G. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.866747 · Cited by 128 · see citing works
Self-citationSercundes, M. K., Ortolan, L. D. S., Debone, D., Pereira, P. V. S., Gomes, E., Aitken, E. H., Condino‐Neto, A., Russo, M., Lima, M. R. D., Álvarez, J. M., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1006054 · Cited by 123 · see citing works
Modulation of Neutrophil Apoptosis and the Resolution of Inflammation through β2 Integrins
Kebir, D. E., & Filep, J. G. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00060 · Cited by 121 · see citing works
Self-citationLee, H., & Surh, Y. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.002 · Cited by 119 · see citing works
Chiang, N., Shinohara, M., Dalli, J., Mirakaj, V., Kibi, M., Choi, A. M. K., & Serhan, C. N. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202969 · Cited by 117 · see citing works
Human health benefits of very-long-chain polyunsaturated fatty acids from microalgae
Lupette, J., & Christoph Benning, A. (2020) · Biochimie · doi:10.1016/j.biochi.2020.04.022 · Cited by 117 · see citing works
Sekheri, M., Kebir, D. E., Edner, N. M., & Filep, J. G. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1920193117 · Cited by 113 · see citing works
Self-citationNovel proresolving and tissue‐regenerative resolvin and protectin sulfido‐conjugated pathways
Dalli, J., Ramon, S., Norris, P. C., Colas, R. A., & Serhan, C. N. (2015) · The FASEB Journal · doi:10.1096/fj.14-268441 · Cited by 111 · see citing works
Resolvins: Emerging Players in Autoimmune and Inflammatory Diseases
Abdolmaleki, F., Kovanen, P. T., Mardani, R., Hayat, S. M. G., Bo, S., & Sahebkar, A. (2019) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-019-08754-9 · Cited by 104 · see citing works
Husson, M.-O., Ley, D., Portal, C., Aumar, M., Hueso, T., Desseyn, J., & Gottrand, F. (2016) · Journal of Infection · doi:10.1016/j.jinf.2016.10.001 · Cited by 103 · see citing works
The role of pro‐resolution lipid mediators in infectious disease
Russell, C. D., & Schwarze, J. (2013) · Immunology · doi:10.1111/imm.12206 · Cited by 101 · see citing works
Gelman, A. E., Fisher, A. J., Huang, H. J., Baz, M. A., Shaver, C. M., Egan, T. M., & Mulligan, M. S. (2017) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2017.07.014 · Cited by 100 · see citing works
Resolvin D4 stereoassignment and its novel actions in host protection and bacterial clearance
Winkler, J. W., Orr, S. K., Dalli, J., Cheng, C.-Y. C., Sanger, J. M., Chiang, N., Petasis, N. A., & Serhan, C. N. (2016) · Scientific Reports · doi:10.1038/srep18972 · Cited by 99 · see citing works
Maresin conjugates in tissue regeneration biosynthesis enzymes in human macrophages
Dalli, J., Vlasakov, I., Riley, I. R., Rodrı́guez, A. R., Spur, B. W., Petasis, N. A., Chiang, N., & Serhan, C. N. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1607003113 · Cited by 99 · see citing works
Resolvin D4 attenuates the severity of pathological thrombosis in mice
Cherpokova, D., Jouvene, C. C., Libreros, S., DeRoo, E., Chu, L., de la Rosa, X., Norris, P. C., Wagner, D. D., & Serhan, C. N. (2019) · Blood · doi:10.1182/blood.2018886317 · Cited by 97 · see citing works
Lipid mediators in immune dysfunction after severe inflammation
Fullerton, J. N., O'Brien, A. J., & Gilroy, D. W. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.10.008 · Cited by 87 · see citing works
Neutrophil Resolvin E1 Receptor Expression and Function in Type 2 Diabetes
Freire, M., Dalli, J., Serhan, C. N., & Dyke, T. E. V. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1601543 · Cited by 90 · see citing works
Targeting Neutrophil Apoptosis for Enhancing the Resolution of Inflammation
Kebir, D. E., & Filep, J. G. (2013) · Cells · doi:10.3390/cells2020330 · Cited by 89 · see citing works
Self-citationSpecialized Proresolving Mediators in Innate and Adaptive Immune Responses in Airway Diseases
Krishnamoorthy, N., Abdulnour, R.-E. E., Walker, K. H., Engstrom, B. D., & Levy, B. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00026.2017 · Cited by 84 · see citing works
Hong, S., & Lü, Y. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00013 · Cited by 85 · see citing works
Extracellular Vesicles as Conveyors of Membrane-Derived Bioactive Lipids in Immune System
Sagini, K., Costanzi, E., Emiliani, C., Buratta, S., & Urbanelli, L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19041227 · Cited by 85 · see citing works
Pathways mediating resolution of inflammation: when enough is too much
Fullerton, J. N., O'Brien, A. J., & Gilroy, D. W. (2013) · The Journal of Pathology · doi:10.1002/path.4232 · Cited by 81 · see citing works
Inflammatory processes during acute respiratory distress syndrome: a complex system
Reiss, L. K., Schuppert, A., & Uhlig, S. (2017) · Current Opinion in Critical Care · doi:10.1097/mcc.0000000000000472 · Cited by 81 · see citing works
Role of Resolvins in the Inflammatory Resolution of Neurological Diseases
Li, C., Wu, X., Liu, S., Shen, D., Zhu, J., & Liu, K. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00612 · Cited by 80 · see citing works
Proresolving actions of a new resolvin D1 analog mimetic qualifies as an immunoresolvent
Orr, S. K., Colas, R. A., Dalli, J., Chiang, N., & Serhan, C. N. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00370.2014 · Cited by 80 · see citing works
Resolution of inflammation in inflammatory bowel disease
Rogler, G. (2017) · The Lancet Gastroenterology & Hepatology · doi:10.1016/s2468-1253(17)30031-6 · Cited by 79 · see citing works
Stotts, C., Corrales‐Medina, V., & Rayner, K. J. (2023) · Circulation Research · doi:10.1161/circresaha.122.321636 · Cited by 86 · see citing works
Permissive and protective roles for neutrophils in leishmaniasis
Carlsen, E. D., Liang, Y., Shelite, T. R., Walker, D. H., Melby, P. C., & Soong, L. (2015) · Clinical & Experimental Immunology · doi:10.1111/cei.12674 · Cited by 78 · see citing works
Filep, J. G., & Ariel, A. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00181.2020 · Cited by 75 · see citing works
Self-citationЛи, Б., Zeng, M., He, W., Huang, X., Luo, L., Zhang, H., & Deng, D. Y. B. (2014) · Endocrinology · doi:10.1210/en.2014-1539 · Cited by 76 · see citing works
Emerging Concepts in the Resolution of Periodontal Inflammation: A Role for Resolvin E1
Balta, M. G., Loos, B. G., & Nicu, E. A. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01682 · Cited by 76 · see citing works
Motwani, M. P., Colas, R. A., George, M. J., Flint, J., Dalli, J., Richard-Loendt, A., Maeyer, R. P. H. D., Serhan, C. N., & Gilroy, D. W. (2018) · JCI Insight · doi:10.1172/jci.insight.94463 · Cited by 74 · see citing works
Bui, T. M., Mascarenhas, L., & Sumagin, R. (2018) · Tissue Barriers · doi:10.1080/21688370.2018.1431038 · Cited by 73 · see citing works
Trilleaud, C., Gauttier, V., Biteau, K., Girault, I., Belarif, L., Mary, C., Pengam, S., Teppaz, G., Thépenier, V., Danger, R., et al. (2021) · Science Advances · doi:10.1126/sciadv.abd1453 · Cited by 73 · see citing works
Colas, R. A., Souza, P. R., Walker, M. E., Burton, M., Zasłona, Z., Curtis, A. M., Marques, R. M., & Dalli, J. (2018) · Circulation Research · doi:10.1161/circresaha.117.312472 · Cited by 71 · see citing works
Flesher, R. P., Herbert, C. A., & Kumar, R. K. (2013) · Clinical Science · doi:10.1042/cs20130623 · Cited by 70 · see citing works
Specialized pro‐resolving mediators: biosynthesis and biological role in bacterial infections
Jordan, P. M., & Werz, O. (2021) · FEBS Journal · doi:10.1111/febs.16266 · Cited by 69 · see citing works
Types of necroinflammation, the effect of cell death modalities on sterile inflammation
Mázló, A., Jenei, V., Sára, B., Molnár, T., Bácsi, A., & Koncz, G. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-04883-w · Cited by 65 · see citing works
Omega 3 Fatty Acid and Skin Diseases
Sawada, Y., Saito‐Sasaki, N., & Nakamura, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.623052 · Cited by 68 · see citing works
Redox signaling in innate immunity and inflammation: focus on macrophages and neutrophils
Braunstein, I., Motohashi, H., Dallenga, T. K., Schaible, U. E., & Benhar, M. (2025) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2025.06.006 · Cited by 72 · see citing works
Identification and Actions of a Novel Third Maresin Conjugate in Tissue Regeneration: MCTR3
Dalli, J., Sanger, J. M., Rodrı́guez, A. R., Chiang, N., Spur, B. W., & Serhan, C. N. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149319 · Cited by 67 · see citing works
Fungal sensing of host environment
Braunsdorf, C., Mailänder‐Sánchez, D., & Schaller, M. (2016) · Cellular Microbiology · doi:10.1111/cmi.12610 · Cited by 66 · see citing works
Chen, F., Fan, X., Wu, Y., Zhu, J., Wang, F., Bo, L., Li, J. B., Bao, R., & Deng, X. M. (2013) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-1978-6 · Cited by 64 · see citing works
Kalish, B. T., Mattè, A., Andolfo, I., Iolascon, A., Weinberg, O. K., Ghigo, A., Cimino, J., Siciliano, A., Hirsch, E., Federti, E., et al. (2015) · Haematologica · doi:10.3324/haematol.2015.124586 · Cited by 63 · see citing works
Serhan, C. N., de la Rosa, X., & Jouvene, C. C. (2018) · Journal of Internal Medicine · doi:10.1111/joim.12871 · Cited by 63 · see citing works
Sulijaya, B., Takahashi, N., & Yamazaki, K. (2019) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2019.07.002 · Cited by 65 · see citing works
Li, C., Bo, L., Liu, W., Lü, X., & Jin, F. (2015) · Nutrients · doi:10.3390/nu7075239 · Cited by 63 · see citing works
Pharmacological strategies to resolve acute inflammation
Sousa, L. P., Alessandri, A. L., Pinho, V., & Teixeira, M. M. (2013) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2013.03.007 · Cited by 63 · see citing works
Beyond host defense and tissue injury: the emerging role of neutrophils in tissue repair
Rizo-Téllez, S. A., & Filep, J. G. (2024) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00652.2023 · Cited by 62 · see citing works
Self-citationLevy, B. D. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00390 · Cited by 60 · see citing works
PDn-3 DPA Pathway Regulates Human Monocyte Differentiation and Macrophage Function
Pistorius, K., Souza, P. R., Matteis, R. D., Austin‐Williams, S., Primdahl, K. G., Vik, A., Mazzacuva, F., Colas, R. A., Marques, R. M., Hansen, T. V., et al. (2018) · Cell chemical biology · doi:10.1016/j.chembiol.2018.04.017 · Cited by 60 · see citing works
Kotlyarov, S. N., & Котлярова, А. А. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312803 · Cited by 58 · see citing works
Quirós, M., & Nusrat, A. (2018) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020518-114504 · Cited by 47 · see citing works
Duvall, M. G., Brüggemann, T. R., & Levy, B. D. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.04.003 · Cited by 57 · see citing works
Welty, F. K., Schulte, F., Alfaddagh, A., Elajami, T. K., Bistrian, B. R., & Hardt, M. (2021) · The FASEB Journal · doi:10.1096/fj.202002471r · Cited by 57 · see citing works
Yang, A., Wu, Y., Yu, G., & Wang, H. (2021) · Respiratory Research · doi:10.1186/s12931-021-01792-y · Cited by 56 · see citing works
Roles of resolvins in the resolution of acute inflammation
Qu, Q., Xuan, W., & Fan, G.-H. (2014) · Cell Biology International · doi:10.1002/cbin.10345 · Cited by 57 · see citing works
- Authors
- El Kebir, D., Gjorstrup, P., & Filep, J. G.
- Affiliations
- Research Center, Maisonneuve-Rosemont Hospital, and Department of Pathology and Cell Biology, University of Montréal, Montréal, QC, Canada H1T 2M4; and
- Resolvyx Pharmaceuticals, Cambridge, MA 02142
- Hôpital Maisonneuve-Rosemont (CA)
- ORCID
- Filep, János G.
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2012-08-27
- Volume
- 109
- Issue
- 37
- Pages
- 14983-14988
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3443132
- OpenAlex
- W2050362957
- Cited by
- 289
- References
- 42
- Citations by year
- 2026: 11 · 2025: 22 · 2024: 18 · 2023: 20 · 2022: 25 · 2021: 23 · 2020: 18 · 2019: 15 · 2018: 26 · 2017: 22 · 2016: 16 · 2015: 22 · 2014: 19 · 2013: 31 · 2012: 1
- FWCI
- 21.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Canadian Institutes of Health Research (MOP‐97742)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Fatty Acid Research and Health
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Keywords
- resolvin E1, neutrophil apoptosis, phagocytosis, inflammation resolution, acute lung injury, reactive oxygen species, caspase-8, caspase-3, myeloperoxidase, serum amyloid A, bacterial DNA, mitochondrial dysfunction, eicosapentaenoic acid
- MeSH terms
- Amino Acid Chloromethyl Ketones, Analysis of Variance, Animals, Cells, Cultured, Escherichia coli, Humans, Mitochondria, Neutrophils, Phagocytosis, Pneumonia, Yeasts, Eicosapentaenoic Acid, Apoptosis, Reactive Oxygen Species, Receptors, Leukotriene B4, Statistics, Nonparametric, Mice, Caspase 3, Caspase 8
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review