2,248
Views
42
CrossRef citations to date
0
Altmetric
Original Research

The ecto-ATPDase CD39 is involved in the acquisition of the immunoregulatory phenotype by M-CSF-macrophages and ovarian cancer tumor-associated macrophages: Regulatory role of IL-27

, , , , , , , , , , , , & show all
Article: e1178025 | Received 04 Sep 2015, Accepted 06 Apr 2016, Published online: 30 Jun 2016

References

  • Romagnani P, Annunziato F, Piccinni MP, Maggi E, Romagnani S. Th1/Th2 cells, their associated molecules and role in pathophysiology. Eur Cytokine Netw 2000; 11:510-1; PMID:11203198
  • Lacey DC, Achuthan A, Fleetwood AJ, Dinh H, Roiniotis J, Scholz GM, Chang MW, Beckman SK, Cook AD, Hamilton JA. Defining GM-CSF- and macrophage-CSF-dependent macrophage responses by in vitro models. J Immunol 2012; 188:5752-65; PMID:22547697; http://dx.doi.org/10.4049/jimmunol.1103426
  • Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 2012; 122:787-95; PMID:22378047; http://dx.doi.org/10.1172/JCI59643
  • Duluc D, Corvaisier M, Blanchard S, Catala L, Descamps P, Gamelin E, Ponsoda S, Delneste Y, Hebbar M, Jeannin P. Interferon-gamma reverses the immunosuppressive and protumoral properties and prevents the generation of human tumor-associated macrophages. Int J Cancer 2009; 125:367-73; PMID:19378341; http://dx.doi.org/10.1002/ijc.24401
  • Foucher ED, Blanchard S, Preisser L, Garo E, Ifrah N, Guardiola P, Delneste Y, Jeannin P. IL-34 induces the differentiation of human monocytes into immunosuppressive macrophages. antagonistic effects of GM-CSF and IFNgamma. PLoS One 2013; 8:e56045; PMID:23409120; http://dx.doi.org/10.1371/journal.pone.0056045
  • Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005; 5:263-74; PMID:15776005; http://dx.doi.org/10.1038/nrc1586
  • Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG, Rimoldi M, Biswas SK, Allavena P, Mantovani A. Macrophage polarization in tumour progression. Semin Cancer Biol 2008; 18:349-55; PMID:18467122; http://dx.doi.org/10.1016/j.semcancer.2008.03.004
  • Mantovani A, Allavena P, Sica A. Tumour-associated macrophages as a prototypic type II polarised phagocyte population: role in tumour progression. Eur J Cancer 2004; 40:1660-7; PMID:15251154; http://dx.doi.org/10.1016/j.ejca.2004.03.016
  • Motz GT, Coukos G. Deciphering and reversing tumor immune suppression. Immunity 2013; 39:61-73; PMID:23890064; http://dx.doi.org/10.1016/j.immuni.2013.07.005
  • Duluc D, Delneste Y, Tan F, Moles MP, Grimaud L, Lenoir J, Preisser L, Anegon I, Catala L, Ifrah N et al. Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood 2007; 110:4319-30; PMID:17848619; http://dx.doi.org/10.1182/blood-2007-02-072587
  • Metcalf D. Control of granulocytes and macrophages: molecular, cellular, and clinical aspects. Science 1991; 25:529-33; PMID:1948028; http://dx.doi.org/10.1126/science.1948028
  • Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H, Portela Catani JP, Hannani D, Duret H, Steegh K et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013; 38:729-41; PMID:23562161; http://dx.doi.org/10.1016/j.immuni.2013.03.003
  • Ma YT, Adjemian S, Yang H, Catani JPP, Hannani D, Martins I, Michaud M, Kepp O, Sukkurwala AQ, Vacchelli E et al. ATP-dependent recruitment, survival and differentiation of dendritic cell precursors in the tumor bed after anticancer chemotherapy. Onco Immunol 2013; 2:e24568; PMID:23894718; http://dx.doi.org/10.4161/onci.24568
  • Idzko M, Ferrari D, Eltzschig HK. Nucleotide signalling during inflammation. Nature 2014; 509:310-7; PMID:24828189; http://dx.doi.org/10.1038/nature13085
  • Netea MG, Nold-Petry CA, Nold MF, Joosten LAB, Opitz B, van der Meer JHM, van de Veerdonk FL, Ferwerda G, Heinhuis B, Devesa I et al. Differential requirement for the activation of the inflammasome for processing and release of IL-1beta in monocytes and macrophages. Blood 2009; 113:2324-35; PMID:19104081; http://dx.doi.org/10.1182/blood-2008-03-146720
  • Piccini A, Carta S, Tassi S, Lasiglie D, Fossati G, Rubartelli A. ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc Natl Acad Sci U S A 2008; 105:8067-72; PMID:18523012; http://dx.doi.org/10.1073/pnas.0709684105
  • Lazarowski ER, Sesma JI, Seminario-Vidal L, Kreda SM. Molecular mechanisms of purine and pyrimidine nucleotide release. Adv Pharmacol 2011; 61:221-61; PMID:21586361; http://dx.doi.org/10.1016/B978-0-12-385526-8.00008-4
  • Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, Park D, Woodson RI, Ostankovich M, Sharma P et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461:282-U165; PMID:19741708; http://dx.doi.org/10.1038/nature08296
  • Aymeric L, Apetoh L, Ghiringhelli F, Tesniere A, Martins I, Kroemer G, Smyth MJ, Zitvogel L. Tumor cell death and ATP release prime dendritic cells and efficient anticancer immunity. Cancer Res 2010; 70:855-8; PMID:20086177; http://dx.doi.org/10.1158/0008-5472.CAN-09-3566
  • Ohta A, Gorelik E, Prasad SJ, Ronchese F, Lukashev D, Wong MMK, Huang XJ, Cladwell S, Liu KB, Smith P. A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci U S A 2006; Aug 29; 103:13132-7; PMID:16916931; http://dx.doi.org/10.1073/pnas.0605251103
  • Ohta A, Sitkovsky M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 2001; 414:916-20; PMID:11780065; http://dx.doi.org/10.1038/414916a
  • Hasko G, Kuhel DG, Chen JF, Schwarzschild MA, Deitch EA, Mabley JG, Marton A, Szabo C. Adenosine inhibits IL-12 and TNF-α production via adenosine A(2a) receptor-dependent and independent mechanisms. Faseb J 2000; 14:2065-74; PMID:11023991; http://dx.doi.org/10.1096/fj.99-0508com
  • Hasko G, Szabo C, Nemeth ZH, Kvetan V, Pastores SM, Vizi ES. Adenosine receptor agonists differentially regulate IL-10, TNF-α and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J Immunol 1996; 157:4634-40; PMID:8906843
  • Eltzschig HK, Ibla JC, Furuta GT, Leonard MO, Jacobson KA, Enjyoji K, Robson SC, Colgan SP. Coordinated adenine nucleotide phosphohydrolysis and nucleoside signaling in posthypoxic endothelium: role of ectonucleotidases and adenosine A2B receptors. J Exp Med 2003; 198:783-96; PMID:12939345; http://dx.doi.org/10.1084/jem.20030891
  • Hasko G, Pacher P. Regulation of macrophage function by adenosine. Arterioscler Thromb Vasc Biol 2012; 32:865-9; PMID:22423038; http://dx.doi.org/10.1161/ATVBAHA.111.226852
  • Hasko G, Cronstein BN. Adenosine: an endogenous regulator of innate immunity. Trends Immunol 2004; 25:33-9; PMID:14698282; http://dx.doi.org/10.1016/j.it.2003.11.003
  • Hasko G, Linden J, Cronstein B, Pacher P. Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 2008; 7:759-70; PMID:18758473; http://dx.doi.org/10.1038/nrd2638
  • Sitkovsky MV, Lukashev D, Apasov S, Kojima H, Koshiba M, Caldwell C, Ohta A, Thiel M. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu Rev Immunol 2004; 22:657-82; PMID:15032592; http://dx.doi.org/10.1146/annurev.immunol.22.012703.104731
  • Antonioli L, Pacher P, Vizi ES, Hasko G. CD39 and CD73 in immunity and inflammation. Trends Mol Med 2013; 19:355-67; PMID:23601906; http://dx.doi.org/10.1016/j.molmed.2013.03.005
  • Resta R, Yamashita Y, Thompson LF. Ecto-enzyme and signaling functions of lymphocyte CD73. Immunol Rev 1998; 161:95-109; PMID:9553767; http://dx.doi.org/10.1111/j.1600-065X.1998.tb01574.x
  • Stagg J, Smyth MJ. Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 2010; 29:5346-58; PMID:20661219; http://dx.doi.org/10.1038/onc.2010.292
  • Odashima M, Bamias G, Rivera-Nieves J, Linden J, Nast CC, Moskaluk CA, Marini M, Sugawara K, Kozaiwa K, Otaka M et al. Activation of A2A adenosine receptor attenuates intestinal inflammation in animal models of inflammatory bowel disease. Gastroenterology 2005; 129:26-33; PMID:16012931; http://dx.doi.org/10.1053/j.gastro.2005.05.032
  • Odashima M, Otaka M, Jin M, Komatsu K, Wada I, Matsuhashi T, Horikawa Y, Hatakeyama N, Oyake J, Ohba R et al. Selective A2A adenosine agonist ATL-146e attenuates acute lethal liver injury in mice. J Gastroenterol 2005; 40:526-9; PMID:15942719; http://dx.doi.org/10.1007/s00535-005-1609-9
  • Huang S, Apasov S, Koshiba M, Sitkovsky M. Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood 1997; 90:1600-10; PMID:9269779
  • Cekic C, Day YJ, Sag D, Linden J. Myeloid expression of adenosine A2A receptor suppresses T and NK cell responses in the solid tumor microenvironment. Cancer Res 2014; 74:7250-9; PMID:25377469; http://dx.doi.org/10.1158/0008-5472.CAN-13-3583
  • Sitkovsky MV, Kjaergaard J, Lukashev D, Ohta A. Hypoxia-adenosinergic immunosuppression: tumor protection by T regulatory cells and cancerous tissue hypoxia. Clin Cancer Res 2008; Oct 1:5947; PMID:18829471; http://dx.doi.org/10.1158/1078-0432.CCR-08-0229
  • Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, Denoyer D, Dwyer KM, Smyth MJ. Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A 2010; 107:1547-52; PMID:20080644; http://dx.doi.org/10.1073/pnas.0908801107
  • Bastid J, Cottalorda-Regairaz A, Alberici G, Bonnefoy N, Eliaou JF, Bensussan A. ENTPD1/CD39 is a promising therapeutic target in oncology. Oncogene 2013; 32:1743-51; PMID:22751118; http://dx.doi.org/10.1038/onc.2012.269
  • Hausler SF, Del Barrio IM, Diessner J, Stein RG, Strohschein J, Honig A, Dietl J, Wischhusen J. Anti-CD39 and anti-CD73 antibodies A1 and 7G2 improve targeted therapy in ovarian cancer by blocking adenosine-dependent immune evasion. Am J Transl Res 2014; 6:129-39; PMID:24489992
  • Young A, Mittal D, Stagg J, Smyth MJ. Targeting cancer-derived adenosine: new therapeutic approaches. Cancer Discov 2014; 4:879; PMID:25035124; http://dx.doi.org/10.1158/2159-8290.CD-14-0341
  • Beavis PA, Milenkovsky N, Henderson Ma, John LB, Allard B, Loi S, Kershaw MH, Stagg J, Darcy PK. Adenosine receptor 2A blockade increase the eficacy of anti-PD-1 through enhanced antitumor T-cell responses. Cancer Immunol Res 2015; 3:506; PMID:25672397; http://dx.doi.org/10.1158/2326-6066.CIR-14-0211
  • Allard B, Pommey S, Smyth MJ, Stagg J. Targeting CD73 enhances the antitumor activity of anti-PD-1 and anti-CTLA-4 mAbs. Clin Cancer Res 2013; 19:5626; PMID:23983257; http://dx.doi.org/10.1158/1078-0432.CCR-13-0545
  • Bastid J, Regairaz A, Bonnefoy N, Dejou C, Giustiniani J, Laheurte C, Cochaud S, Laprevotte E, Funck-Brentano E, Hemon P et al. Inhibition of CD39 enzymatic function at the surface of tumor cells alleviates their immunosuppressive activity. Cancer Immunol Res 2015; 3:254-65; PMID:25403716; http://dx.doi.org/10.1158/2326-6066.CIR-14-0018
  • Zhang B, Cheng B, Li F, Ding J, Feng Y, Zhuo G, Wei H, Zhao K. High expression of CD39/ENTPD1 in malignant epithelial cells of human rectal adenocarcinoma. Tumor Biol 2015; 36:9411-9; PMID:26113408; http://dx.doi.org/10.1007/s13277-015-3683-9
  • Sun X, Wu Y, Gao W, Enjyoji K, Csizmadia E, Muller CE, Murakami T, Robson SC. CD39/ENTPD1 expression by CD4+Foxp3+ regulatory T cells promotes hepatic metastatic tumor growth in mice. Gastroenterol 2010; 139:1030-40; PMID:20546740; http://dx.doi.org/10.1053/j.gastro.2010.05.007
  • Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, Erat A, Chen JF, Enjyoji K, Linden J, Oukka M et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 2007; 204:1257-65; PMID:17502665; http://dx.doi.org/10.1084/jem.20062512
  • Zanin RF, Braganhol E, Bergamin LS, Campesato LF, Filho AZ, Moreira JC, Morrone FB, Sevigny J, Schetinger MR, de Souza Wyse AT et al. Differential macrophage activation alters the expression profile of NTPDase and ecto-5′-nucleotidase. PLoS One 2012; 7:e31205; PMID:22348056; http://dx.doi.org/10.1371/journal.pone.0031205
  • Thibaudin M, Chaix M, Boidot R, Vegran F, Derangere V, Limagne E, Berger H, Ladoire S, Apetoh L, Ghiringhelli F. Human ectonucleotidase-expressing CD25high Th17 cells accumulate in breast cancer tumors and exert immunosuppressive functions. Onco Immunol 2016; 5:e1055444; PMID:26942062; http://dx.doi.org/10.1080/2162402X.2015.1055444
  • Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006; 440:237-41; PMID:16407889; http://dx.doi.org/10.1038/nature04516
  • Foucher ED, Blanchard S, Preisser L, Descamps P, Ifrah N, Delneste Y, Jeannin P. IL-34- and M-CSF-induced macrophages switch memory T cells into Th17 cells via membrane IL-1alpha. Eur J Immunol 2014; 45(4):1092-102; PMID:25545357; http://dx.doi.org/10.1002/eji.201444606
  • Hasko G, Pacher P, Deitch EA, Vizi ES. Shaping of monocyte and macrophage function by adenosine receptors. Pharmacol Ther 2007; 113:264-75; PMID:17056121; http://dx.doi.org/10.1016/j.pharmthera.2006.08.003
  • Mascanfroni ID, Yeste A, Vieira SM, Burns EJ, Patel B, Sloma I, Wu Y, Mayo L, Ben-Hamo R, Efroni S et al. IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat Immunol 2013; 14:1054-63; PMID:23995234; http://dx.doi.org/10.1038/ni.2695
  • Sekar D, Hahn C, Brune B, Roberts E, Weigert A. Apoptotic tumor cells induce IL-27 release from human DCs to activate Treg cells that express CD69 and attenuate cytotoxicity. Eur J Immunol 2012; 42:1585-98; PMID:22678911; http://dx.doi.org/10.1002/eji.201142093
  • 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; 122:1935-45; PMID:23908469; http://dx.doi.org/10.1182/blood-2013-04-496216
  • Dubois-Colas N, Petit-Jentreau L, Barreiro LB, Durand S, Soubigou G, Lecointe C, Klibi J, Rezai K, Lokiec F, Coppee JY et al. Extracellular Adenosine Triphosphate Affects the Response of Human Macrophages Infected With Mycobacterium tuberculosis. J Infect Dis 2014; 210:824-33; PMID:24604822; http://dx.doi.org/10.1093/infdis/jiu135
  • Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 2009; 27:519-50; PMID:19302047; http://dx.doi.org/10.1146/annurev.immunol.021908.132612
  • Riteau N, Baron L, Villeret B, Guillou N, Savigny F, Ryffel B, Rassendren F, Le Bert M, Gombault A, Couillin I. ATP release and purinergic signaling: a common pathway for particle-mediated inflammasome activation. Cell Death Dis 2012; 3:e403; PMID:23059822; http://dx.doi.org/10.1038/cddis.2012.144
  • Levesque SA, Kukulski F, Enjyoji K, Robson SC, Sevigny J. NTPDase1 governs P2X7-dependent functions in murine macrophages. Eur J Immunol 2010; 40:1473-85; PMID:20201036; http://dx.doi.org/10.1002/eji.200939741
  • Hausler SF, Montalban del Barrio I, Strohschein J, Anoop Chandran P, Engel JB, Honig A, Ossadnik M, Horn E, Fischer B, Krockenberger M et al. Ectonucleotidases CD39 and CD73 on OvCA cells are potent adenosine-generating enzymes responsible for adenosine receptor 2A-dependent suppression of T cell function and NK cell cytotoxicity. Cancer Immunol Immunother 2011; 60:1405-18; PMID:21638125; http://dx.doi.org/10.1007/s00262-011-1040-4
  • Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41:49-61; PMID:25035953; http://dx.doi.org/10.1016/j.immuni.2014.06.010
  • Eichin D, Laurila JP, Jalkanen S, Salmi M. CD73 activity is dispensable for the polarization of M2 macrophages. PLoS One 2015; 10:e0134721; PMID:26258883; http://dx.doi.org/10.1371/journal.pone.0134721
  • Hunter CA, Kastelein R. Interleukin-27: balancing protective and pathological immunity. Immunity 2012; 37:960-9; PMID:23244718; http://dx.doi.org/10.1016/j.immuni.2012.11.003
  • Apetoh L, Quintana FJ, Pot C, Joller N, Xiao S, Kumar D, Burns EJ, Sherr DH, Weiner HL, Kuchroo VK. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 2010; 11:854-61; PMID:20676095; http://dx.doi.org/10.1038/ni.1912
  • Kido M, Takeuchi S, Sugiyama N, Esaki H, Nakashima H, Yoshida H, Furue M. T cell-specific overexpression of interleukin-27 receptor α subunit (WSX-1) prevents spontaneous skin inflammation in MRL/lpr mice. Br J Dermatol 2011; 164:1214-20; PMID:21332454; http://dx.doi.org/10.1111/j.1365-2133.2011.10244.x
  • Jung JY, Robinson CM. IL-12 and IL-27 regulate the phagolysosomal pathway in mycobacteria-infected human macrophages. Cell Commun Signal 2014; 12:16; PMID:24618498; http://dx.doi.org/10.1186/1478-811X-12-16
  • Kalliolias GD, Ivashkiv LB. IL-27 activates human monocytes via STAT1 and suppresses IL-10 production but the inflammatory functions of IL-27 are abrogated by TLRs and p38. J Immunol 2008; 180:6325-33; http://dx.doi.org/10.4049/jimmunol.180.9.6325
  • Zhang Z, Zhou B, Wu Y, Gao Q, Zhang K, Song Y, Zhang L, Xi M. Prognostic value of IL-27 polymorphisms and the susceptibility to epithelial ovarian cancer in a Chinese population. Immuno Genetics 2014; 66:85-92; PMID:24352695; http://dx.doi.org/10.1007/s00251-013-0753-2
  • Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; http://dx.doi.org/10.1056/NEJMoa1200694
  • Duraiswamy J, Freeman GJ, Coukos G. Therapeutic PD-1 pathway blockade augments with other modalities of immunotherapy T-cell function to prevent immune decline in ovarian cancer. Cancer Res 2013; 73:6900-12; PMID:23975756; http://dx.doi.org/10.1158/0008-5472.CAN-13-1550
  • Abiko K, Mandai M, Hamanishi J, Yoshioka Y, Matsumura N, Baba T, Yamaguchi K, Murakami R, Yamamoto A, Kharma B et al. PD-L1 on tumor cells is induced in ascites and promotes peritoneal dissemination of ovarian cancer through CTL dysfunction. Clin Cancer Res 2013; 19:1363-74; PMID:23340297; http://dx.doi.org/10.1158/1078-0432.CCR-12-2199
  • Maine CJ, Aziz NH, Chatterjee J, Hayford C, Brewig N, Whilding L, George AJ, Ghaem-Maghami S. Programmed death ligand-1 over-expression correlates with malignancy and contributes to immune regulation in ovarian cancer. Cancer Immunol Immunotherapy 2014; 63:215-24; PMID:24297569; http://dx.doi.org/10.1007/s00262-013-1503-x
  • Levitt B, Head RJ, Westfall DP. High-pressure liquid chromatographic-fluorometric detection of adenosine and adenine nucleotides: application to endogenous content and electrically induced release of adenyl purines in guinea pig vas deferens. Anal Biochem 1984; 137:93-100; PMID:6731811; http://dx.doi.org/10.1016/0003-2697(84)90352-X

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.