{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T02:23:08Z","timestamp":1788402188770,"version":"build-2803163510"},"reference-count":44,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2017,1,6]],"date-time":"2017-01-06T00:00:00Z","timestamp":1483660800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Death Differ"],"published-print":{"date-parts":[[2017,3]]},"DOI":"10.1038\/cdd.2016.159","type":"journal-article","created":{"date-parts":[[2017,1,6]],"date-time":"2017-01-06T15:39:02Z","timestamp":1483717142000},"page":"559-570","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":65,"title":["CD73 regulates anti-inflammatory signaling between apoptotic cells and endotoxin-conditioned tissue macrophages"],"prefix":"10.1038","volume":"24","author":[{"given":"Patrick S","family":"Murphy","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jing","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2330-4691","authenticated-orcid":false,"given":"Samir P","family":"Bhagwat","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua C","family":"Munger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William J","family":"Janssen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Terry W","family":"Wright","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0642-482X","authenticated-orcid":false,"given":"Michael R","family":"Elliott","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2017,1,6]]},"reference":[{"key":"BFcdd2016159_CR1","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1038\/nri2779","volume":"10","author":"O Soehnlein","year":"2010","unstructured":"Soehnlein O, Lindbom L . Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol 2010; 10: 427\u2013439.","journal-title":"Nat Rev Immunol"},{"key":"BFcdd2016159_CR2","first-page":"4","volume":"3","author":"A Ariel","year":"2012","unstructured":"Ariel A, Serhan CN . New lives given by cell death: macrophage differentiation following their encounter with apoptotic leukocytes during the resolution of inflammation. Front Immunol 2012; 3: 4.","journal-title":"Front Immunol"},{"key":"BFcdd2016159_CR3","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.smim.2015.05.003","volume":"27","author":"D Gilroy","year":"2015","unstructured":"Gilroy D, De Maeyer R . New insights into the resolution of inflammation. Semin Immunol 2015; 27: 161\u2013168.","journal-title":"Semin Immunol"},{"key":"BFcdd2016159_CR4","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1038\/sj.cdd.4402271","volume":"15","author":"DV Krysko","year":"2007","unstructured":"Krysko DV, Vandenabeele P . From regulation of dying cell engulfment to development of anti-cancer therapy. Cell Death Differ 2007; 15: 29\u201338.","journal-title":"Cell Death Differ"},{"key":"BFcdd2016159_CR5","doi-asserted-by":"publisher","first-page":"1059","DOI":"10.1083\/jcb.201004096","volume":"189","author":"MR Elliott","year":"2010","unstructured":"Elliott MR, Ravichandran KS . Clearance of apoptotic cells: implications in health and disease. J Cell Biol 2010; 189: 1059\u20131070.","journal-title":"J Cell Biol"},{"key":"BFcdd2016159_CR6","doi-asserted-by":"publisher","first-page":"1055","DOI":"10.2217\/imt.13.103","volume":"5","author":"P Saas","year":"2013","unstructured":"Saas P, Kaminski S, Perruche S . Prospects of apoptotic cell-based therapies for transplantation and inflammatory diseases. Immunotherapy 2013; 5: 1055\u20131073.","journal-title":"Immunotherapy"},{"key":"BFcdd2016159_CR7","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1016\/j.cell.2010.02.014","volume":"140","author":"S Nagata","year":"2010","unstructured":"Nagata S, Hanayama R, Kawane K . Autoimmunity and the clearance of dead cells. Cell 2010; 140: 619\u2013630.","journal-title":"Cell"},{"key":"BFcdd2016159_CR8","first-page":"139","volume":"6","author":"LE Mu\u00f1oz","year":"2015","unstructured":"Mu\u00f1oz LE, Berens C, Lauber K, Gaipl US, Herrmann M . Apoptotic cell clearance and its role in the origin and resolution of chronic inflammation. Front Immunol 2015; 6: 139.","journal-title":"Front Immunol"},{"key":"BFcdd2016159_CR9","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1038\/37022","volume":"390","author":"RE Voll","year":"1997","unstructured":"Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, Girkontaite I . Immunosuppressive effects of apoptotic cells. Nature 1997; 390: 350\u2013351.","journal-title":"Nature"},{"key":"BFcdd2016159_CR10","doi-asserted-by":"publisher","first-page":"890","DOI":"10.1172\/JCI1112","volume":"101","author":"VA Fadok","year":"1998","unstructured":"Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM . Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine\/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Investig 1998; 101: 890\u2013898.","journal-title":"J Clin Investig"},{"key":"BFcdd2016159_CR11","doi-asserted-by":"publisher","first-page":"2610","DOI":"10.4049\/jimmunol.171.5.2610","volume":"171","author":"M Lucas","year":"2003","unstructured":"Lucas M, Stuart LM, Savill J, Lacy-Hulbert A . Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J Immunol 2003; 171: 2610\u20132615.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR12","doi-asserted-by":"publisher","first-page":"4852","DOI":"10.4049\/jimmunol.1303377","volume":"192","author":"N Ipseiz","year":"2014","unstructured":"Ipseiz N, Uderhardt S, Scholtysek C, Steffen M, Schabbauer G, Bozec A et al. The nuclear receptor Nr4a1 mediates anti-inflammatory effects of apoptotic cells. J Immunol 2014; 192: 4852\u20134858.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR13","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1038\/cdd.2016.13","volume":"23","author":"CB Medina","year":"2016","unstructured":"Medina CB, Ravichandran KS . Do not let death do us part: \u2018find-me\u2019 signals in communication between dying cells and the phagocytes. Cell Death Differ 2016; 23: 979\u2013989.","journal-title":"Cell Death Differ"},{"key":"BFcdd2016159_CR14","doi-asserted-by":"publisher","first-page":"e02172","DOI":"10.7554\/eLife.02172","volume":"3","author":"H Yamaguchi","year":"2014","unstructured":"Yamaguchi H, Maruyama T, Urade Y, Nagata S . Immunosuppression via adenosine receptor activation by adenosine monophosphate released from apoptotic cells. Elife 2014; 3: e02172.","journal-title":"Elife"},{"key":"BFcdd2016159_CR15","doi-asserted-by":"publisher","first-page":"7144","DOI":"10.4049\/jimmunol.1002284","volume":"186","author":"K Koroskenyi","year":"2011","unstructured":"Koroskenyi K, Duro E, Pallai A, Sarang Z, Kloor D, Ucker DS et al. Involvement of adenosine A2A receptors in engulfment-dependent apoptotic cell suppression of inflammation. J Immunol 2011; 186: 7144\u20137155.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR16","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1038\/nri.2016.4","volume":"16","author":"C Cekic","year":"2016","unstructured":"Cekic C, Linden J . Purinergic regulation of the immune system. Nat Rev Immunol 2016; 16: 177\u2013192.","journal-title":"Nat Rev Immunol"},{"key":"BFcdd2016159_CR17","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1007\/s11302-012-9309-4","volume":"8","author":"H Zimmermann","year":"2012","unstructured":"Zimmermann H, Zebisch M, Str\u00e4ter N . Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 2012; 8: 437\u2013502.","journal-title":"Purinergic Signal"},{"key":"BFcdd2016159_CR18","doi-asserted-by":"publisher","first-page":"832","DOI":"10.1016\/j.cell.2014.04.016","volume":"157","author":"Y Okabe","year":"2014","unstructured":"Okabe Y, Medzhitov R . Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 2014; 157: 832\u2013844.","journal-title":"Cell"},{"key":"BFcdd2016159_CR19","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1126\/science.1251414","volume":"344","author":"M Rosas","year":"2014","unstructured":"Rosas M, Davies LC, Giles PJ, Liao C-T, Kharfan B, Stone TC et al. The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 2014; 344: 645\u2013648.","journal-title":"Science"},{"key":"BFcdd2016159_CR20","doi-asserted-by":"publisher","first-page":"6780","DOI":"10.4049\/jimmunol.177.10.6780","volume":"177","author":"JJ Kobie","year":"2006","unstructured":"Kobie JJ, Shah PR, Yang L, Rebhahn JA, Fowell DJ, Mosmann TR . T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5'-adenosine monophosphate to adenosine. J Immunol 2006; 177: 6780\u20136786.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR21","doi-asserted-by":"publisher","first-page":"4256","DOI":"10.4049\/jimmunol.1003379","volume":"187","author":"G Hasko","year":"2011","unstructured":"Hasko G, Csoka B, Koscso B, Chandra R, Pacher P, Thompson LF et al. Ecto-5'-nucleotidase (CD73) decreases mortality and organ injury in sepsis. J Immunol 2011; 187: 4256\u20134267.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR22","doi-asserted-by":"publisher","first-page":"L1313","DOI":"10.1152\/ajplung.00130.2015","volume":"309","author":"F Aeffner","year":"2015","unstructured":"Aeffner F, Woods PS, Davis IC . Ecto-5'-nucleotidase CD73 modulates the innate immune response to influenza infection but is not required for development of influenza-induced acute lung injury. Am J Physiol Lung Cell Mol Physiol 2015; 309: L1313\u2013L1322.","journal-title":"Am J Physiol Lung Cell Mol Physiol"},{"key":"BFcdd2016159_CR23","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1016\/j.it.2009.07.009","volume":"30","author":"SK Biswas","year":"2009","unstructured":"Biswas SK, L\u00f3pez-Collazo E . Endotoxin tolerance: new mechanisms, molecules and clinical significance. Trends Immunol 2009; 30: 475\u2013487.","journal-title":"Trends Immunol"},{"key":"BFcdd2016159_CR24","doi-asserted-by":"publisher","first-page":"4047","DOI":"10.4049\/jimmunol.177.6.4047","volume":"177","author":"M Lucas","year":"2006","unstructured":"Lucas M, Stuart LM, Zhang A, Hodivala-Dilke K, Febbraio M, Silverstein R et al. Requirements for apoptotic cell contact in regulation of macrophage responses. J Immunol 2006; 177: 4047\u20134054.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR25","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1038\/nature08296","volume":"461","author":"MR Elliott","year":"2009","unstructured":"Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461: 282\u2013286.","journal-title":"Nature"},{"key":"BFcdd2016159_CR26","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1038\/nature09413","volume":"467","author":"FB Chekeni","year":"2010","unstructured":"Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, Lazarowski ER et al. Pannexin 1 channels mediate \u2018find-me\u2019 signal release and membrane permeability during apoptosis. Nature 2010; 467: 863\u2013867.","journal-title":"Nature"},{"key":"BFcdd2016159_CR27","doi-asserted-by":"publisher","first-page":"6553","DOI":"10.4049\/jimmunol.1100478","volume":"186","author":"Y Qu","year":"2011","unstructured":"Qu Y, Misaghi S, Newton K, Gilmour LL, Louie S, Cupp JE et al. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol 2011; 186: 6553\u20136561.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR28","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1038\/nri2938","volume":"11","author":"WG Junger","year":"2011","unstructured":"Junger WG . Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 2011; 11: 201\u2013212.","journal-title":"Nat Rev Immunol"},{"key":"BFcdd2016159_CR29","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1038\/nature13085","volume":"509","author":"M Idzko","year":"2014","unstructured":"Idzko M, Ferrari D, Eltzschig HK . Nucleotide signalling during inflammation. Nature 2014; 509: 310\u2013317.","journal-title":"Nature"},{"key":"BFcdd2016159_CR30","doi-asserted-by":"publisher","first-page":"2065","DOI":"10.1096\/fj.99-0508com","volume":"14","author":"G Hasko","year":"2000","unstructured":"Hasko G, Kuhel DG, Chen JF, Schwarzschild MA, Deitch EA, Mabley JG et al. Adenosine inhibits IL-12 and TNF-[alpha] production via adenosine A2a receptor-dependent and independent mechanisms. FASEB J 2000; 14: 2065\u20132074.","journal-title":"FASEB J"},{"key":"BFcdd2016159_CR31","doi-asserted-by":"publisher","first-page":"575","DOI":"10.1042\/BJ20050888","volume":"391","author":"LJ Murphree","year":"2005","unstructured":"Murphree LJ, Sullivan GW, Marshall MA, Linden J . Lipopolysaccharide rapidly modifies adenosine receptor transcripts in murine and human macrophages: role of NF-\u03baB in A2A adenosine receptor induction. Biochem J 2005; 391: 575.","journal-title":"Biochem J"},{"key":"BFcdd2016159_CR32","doi-asserted-by":"publisher","first-page":"1935","DOI":"10.1182\/blood-2013-04-496216","volume":"122","author":"HB Cohen","year":"2013","unstructured":"Cohen HB, Briggs KT, Marino JP, Ravid K, Robson SC, Mosser DM . TLR stimulation initiates a CD39-based autoregulatory mechanism that limits macrophage inflammatory responses. Blood 2013; 122: 1935\u20131945.","journal-title":"Blood"},{"key":"BFcdd2016159_CR33","doi-asserted-by":"publisher","first-page":"172","DOI":"10.1124\/jpet.105.096016","volume":"317","author":"LM Kreckler","year":"2006","unstructured":"Kreckler LM, Wan TC, Ge Z-D, Auchampach JA . Adenosine inhibits tumor necrosis factor-alpha release from mouse peritoneal macrophages via A2A and A2B but not the A3 adenosine receptor. J Pharmacol Exp Ther 2006; 317: 172\u2013180.","journal-title":"J Pharmacol Exp Ther"},{"key":"BFcdd2016159_CR34","doi-asserted-by":"publisher","first-page":"2568","DOI":"10.1073\/pnas.0915000107","volume":"107","author":"EEB Ghosn","year":"2010","unstructured":"Ghosn EEB, Cassado AA, Govoni GR, Fukuhara T, Yang Y, Monack DM et al. Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc Natl Acad Sci USA 2010; 107: 2568\u20132573.","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFcdd2016159_CR35","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1038\/gene.2012.60","volume":"14","author":"G Elson","year":"2013","unstructured":"Elson G, Eisenberg M, Garg C, Outram S, Ferrante CJ, Hasko G et al. Induction of murine adenosine A2A receptor expression by LPS: analysis of the 5\u2032 upstream promoter. Genes Immun 2013; 14: 147\u2013153.","journal-title":"Genes Immun"},{"key":"BFcdd2016159_CR36","doi-asserted-by":"publisher","first-page":"1884","DOI":"10.4049\/jimmunol.179.3.1884","volume":"179","author":"MD Desrosiers","year":"2007","unstructured":"Desrosiers MD, Cembrola KM, Fakir MJ, Stephens LA, Jama FM, Shameli A et al. Adenosine deamination sustains dendritic cell activation in inflammation. J Immunol 2007; 179: 1884\u20131892.","journal-title":"J Immunol"},{"key":"BFcdd2016159_CR37","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1038\/nri957","volume":"2","author":"J Savill","year":"2002","unstructured":"Savill J, Dransfield I, Gregory C, Haslett C . A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2002; 2: 965\u2013975.","journal-title":"Nat Rev Immunol"},{"key":"BFcdd2016159_CR38","doi-asserted-by":"publisher","first-page":"1191","DOI":"10.1038\/ni1276","volume":"6","author":"CN Serhan","year":"2005","unstructured":"Serhan CN, Savill J . Resolution of inflammation: the beginning programs the end. Nat Immunol 2005; 6: 1191\u20131197.","journal-title":"Nat Immunol"},{"key":"BFcdd2016159_CR39","doi-asserted-by":"publisher","first-page":"1118","DOI":"10.1038\/ni.2419","volume":"13","author":"EL Gautier","year":"2012","unstructured":"Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 2012; 13: 1118\u20131128.","journal-title":"Nat Immunol"},{"key":"BFcdd2016159_CR40","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.coi.2010.01.003","volume":"22","author":"MB Torchinsky","year":"2010","unstructured":"Torchinsky MB, Garaude J, Blander JM . Infection and apoptosis as a combined inflammatory trigger. Curr Opin Immunol 2010; 22: 55\u201362.","journal-title":"Curr Opin Immunol"},{"key":"BFcdd2016159_CR41","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1172\/JCI0210649","volume":"109","author":"DJ Pinsky","year":"2002","unstructured":"Pinsky DJ, Broekman MJ, Peschon JJ, Stocking KL, Fujita T, Ramasamy R et al. Elucidation of the thromboregulatory role of CD39\/ectoapyrase in the ischemic brain. J Clin Investig 2002; 109: 1031\u20131040.","journal-title":"J Clin Investig"},{"key":"BFcdd2016159_CR42","doi-asserted-by":"publisher","first-page":"1341","DOI":"10.1002\/j.1460-2075.1994.tb06387.x","volume":"13","author":"M Takata","year":"1994","unstructured":"Takata M, Sabe H, Hata A, Inazu T, Homma Y, Nukada T et al. Tyrosine kinases Lyn and Syk regulate B cell receptor-coupled Ca2+ mobilization through distinct pathways. EMBO J 1994; 13: 1341\u20131349.","journal-title":"EMBO J"},{"key":"BFcdd2016159_CR43","doi-asserted-by":"publisher","first-page":"18019","DOI":"10.1073\/pnas.1415864111","volume":"111","author":"SR DeVito","year":"2014","unstructured":"DeVito SR, Ortiz-Ria\u00f1o E, Mart\u00ednez-Sobrido L, Munger J . Cytomegalovirus-mediated activation of pyrimidine biosynthesis drives UDP-sugar synthesis to support viral protein glycosylation. Proc Natl Acad Sci USA 2014; 111: 18019\u201318024.","journal-title":"Proc Natl Acad Sci USA"},{"key":"BFcdd2016159_CR44","doi-asserted-by":"publisher","first-page":"6062","DOI":"10.4049\/jimmunol.1303348","volume":"192","author":"C Stevenson","year":"2014","unstructured":"Stevenson C, la Rosa de G, Anderson CS, Murphy PS, Capece T, Kim M et al. Essential role of elmo1 in dock2-dependent lymphocyte migration. J Immunol 2014; 192: 6062\u20136070.","journal-title":"J Immunol"}],"container-title":["Cell Death & Differentiation"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/cdd2016159.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/cdd2016159","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/cdd2016159.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T13:10:47Z","timestamp":1684415447000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/cdd2016159"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,1,6]]},"references-count":44,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2017,3]]}},"alternative-id":["BFcdd2016159"],"URL":"https:\/\/doi.org\/10.1038\/cdd.2016.159","relation":{},"ISSN":["1350-9047","1476-5403"],"issn-type":[{"value":"1350-9047","type":"print"},{"value":"1476-5403","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,1,6]]},"assertion":[{"value":"5 October 2016","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 December 2016","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 December 2016","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 January 2017","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no conflict of interest.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}]}}