Transcriptional and metabolic reprogramming induce an inflammatory phenotype in non-medullary thyroid carcinoma-induced macrophages

OncoImmunology

Volumn 5, Issue 12, 2016, Pages

  Arts, Rob J W ^a   Plantinga, Theo S ^a   Tuit, Sander ^b   Ulas, Thomas ^b   Heinhuis, Bas ^a   Tesselaar, Marika ^a   Sloot, Yvette ^a   Adema, Gosse J ^c   Joosten, Leo A B ^a   Smit, Johannes W A ^a   Netea, Mihai G ^a   Schultze, Joachim L ^b,d   Netea Maier, Romana T ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF BONN   (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

Cytokines; epigenetics; immunometabolism; lactate; thyroid cancer; tumor associated macrophages

Indexed keywords

CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; LACTIC ACID; MONOCYTE CHEMOTACTIC PROTEIN 1; RAPAMYCIN; TOLL LIKE RECEPTOR; TRANSCRIPTOME; TUMOR NECROSIS FACTOR; VASCULOTROPIN;

ARTICLE; CELL METABOLISM; EPIGENETICS; HISTONE METHYLATION; HUMAN; IMMUNOHISTOCHEMISTRY; OXYGEN CONSUMPTION; PHENOTYPE; THYROID CARCINOMA; TUMOR ASSOCIATED LEUKOCYTE;

EID: 84999748146     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.1080/2162402X.2016.1229725     Document Type: Article

References (38)

1. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454:436-44; PMID:18650914; http://dx.doi.org/10.1038/nature07205
2. 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
3. Colegio OR, Chu NQ, Szabo AL, Chu T, Rhebergen AM, Jairam V, Cyrus N, Brokowski CE, Eisenbarth SC, Phillips GM, et al. Functional polarization of tumour-associated macrophages by tumour-derived lactic acid. Nature 2014; 513:559-63; PMID:25043024; http://dx.doi.org/10.1038/nature13490
4. Sica A, Mantovani A. Macrophage plasticity and polarization:in vivo veritas. J Clin Investig 2012; 122:787-95; PMID:22378047; http://dx.doi.org/10.1172/JCI59643
5. Davies L, Welch HG. Current thyroid cancer trends in the United States. JAMA Otolaryngol Head Neck Surg 2014; 140:317-22; PMID:24557566; http://dx.doi.org/10.1001/jamaoto.2014.1
6. Ryder M, Ghossein RA, Ricarte-Filho JC, Knauf JA, Fagin JA. Increased density of tumor-associated macrophages is associated with decreased survival in advanced thyroid cancer. Endocrine-related cancer 2008; 15:1069-74; PMID:18719091; http://dx.doi.org/10.1677/ERC-08-0036
7. Caillou B, Talbot M, Weyemi U, Pioche-Durieu C, Al Ghuzlan A, Bidart JM, Chouaib S, Schlumberger M, Dupuy C. Tumor-associated macrophages (TAMs) form an interconnected cellular supportive network in anaplastic thyroid carcinoma. PloS one 2011; 6:e22567; PMID:21811634; http://dx.doi.org/10.1371/journal.pone.0022567
8. Ryder M, Gild M, Hohl TM, Pamer E, Knauf J, Ghossein R, Joyce JA, Fagin JA. Genetic and pharmacological targeting of CSF-1/CSF-1R inhibits tumor-associated macrophages and impairs BRAF-induced thyroid cancer progression. PloS one 2013; 8:e54302; PMID:23372702; http://dx.doi.org/10.1371/journal.pone.0054302
9. Liberzon A. A description of the Molecular Signatures Database (MSigDB) Web site. Methods Mol Biol 2014; 1150:153-60; PMID:24743996; http://dx.doi.org/10.1007/978-1-4939-0512-6_9
10. Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, Giamarellos-Bourboulis EJ, Martens JH, Rao NA, Aghajanirefah A, et al. mTOR- and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 2014; 345:1250684; PMID:25258083; http://dx.doi.org/10.1126/science.1250684
11. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, Frezza C, Bernard NJ, Kelly B, Foley NH, et al. Succinate is an inflammatory signal that induces IL-1beta through HIF-1alpha. Nature 2013; 496:238-42; PMID:23535595; http://dx.doi.org/10.1038/nature11986
12. Mauro C, Leow SC, Anso E, Rocha S, Thotakura AK, Tornatore L, Moretti M, De Smaele E, Beg AA, Tergaonkar V, et al. NF-kappaB controls energy homeostasis and metabolic adaptation by upregulating mitochondrial respiration. Nat Cell Biol 2011; 13:1272-9; PMID:21968997; http://dx.doi.org/10.1038/ncb2324
13. Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F, Cheng SC, Ratter J, Berentsen K, van der Ent MA, et al. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 2014; 345:1251086; PMID:25258085; http://dx.doi.org/10.1126/science.1251086
14. Kimura H. Histone modifications for human epigenome analysis. J Human Genet 2013; 58:439-45; PMID:23739122; http://dx.doi.org/10.1038/jhg.2013.66
15. Arts RJ, Blok BA, van Crevel R, Joosten LA, Aaby P, Benn CS, Netea MG. Vitamin A induces inhibitory histone methylation modifications and down-regulates trained immunity in human monocytes. J Leukoc Biol 2015; 98:129-36; PMID:25934925; http://dx.doi.org/10.1189/jlb.6AB0914-416R
16. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages:functional diversity, clinical significance, and open questions. Semin Immunopathol 2013; 35:585-600; PMID:23657835; http://dx.doi.org/10.1007/s00281-013-0367-7
17. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010; 141:39-51; PMID:20371344; http://dx.doi.org/10.1016/j.cell.2010.03.014
18. Murdoch C, Muthana M, Coffelt SB, Lewis CE. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008; 8:618-31; PMID:18633355; http://dx.doi.org/10.1038/nrc2444
19. Ajjan RA, Watson PF, Findlay C, Metcalfe RA, Crisp M, Ludgate M, Weetman AP. The sodium iodide symporter gene and its regulation by cytokines found in autoimmunity. J Endocrinol 1998; 158:351-8; PMID:9846164; http://dx.doi.org/10.1677/joe.0.1580351
20. Huijbers A, Plantinga TS, Joosten LA, Aben KK, Gudmundsson J, den Heijer M, Kiemeney LA, Netea MG, Hermus AR, Netea-Maier RT. The effect of the ATG16L1 Thr300Ala polymorphism on susceptibility and outcome of patients with epithelial cell-derived thyroid carcinoma. Endocrine-related Cancer 2012; 19:L15-8; PMID:22302078; http://dx.doi.org/10.1530/ERC-11-0302
21. Plantinga TS, Costantini I, Heinhuis B, Huijbers A, Semango G, Kusters B, Netea MG, Hermus AR, Smit JW, Dinarello CA, et al. A promoter polymorphism in human interleukin-32 modulates its expression and influences the risk and the outcome of epithelial cell-derived thyroid carcinoma. Carcinogenesis 2013; 34:1529-35; PMID:23486016; http://dx.doi.org/10.1093/carcin/bgt092
22. De Rosa V, Galgani M, Porcellini A, Colamatteo A, Santopaolo M, Zuchegna C, Romano A, De imone S, Procaccini C, La Rocca C, et al. Glycolysis controls the induction of human regulatory T cells by modulating the expression of FOXP3 exon 2 splicing variants. Nat Immunol 2015; 16:1174-84; PMID:26414764; http://dx.doi.org/10.1038/ni.3269
23. Liu Y, Yun X, Gao M, Yu Y, Li X. Analysis of regulatory T cells frequency in peripheral blood and tumor tissues in papillary thyroid carcinoma with and without Hashimoto's thyroiditis. Clin Translat Oncol 2015; 17:274-80; PMID:25387566; http://dx.doi.org/10.1007/s12094-014-1222-6
24. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-8; PMID:16648838; http://dx.doi.org/10.1038/nature04753
25. Savage ND, de Boer T, Walburg KV, Joosten SA, van Meijgaarden K, Geluk A, Ottenhoff TH. Human anti-inflammatory macrophages induce Foxp3+ GITR+ CD25+ regulatory T cells, which suppress via membrane-bound TGFbeta-1. J Immunol 2008; 181:2220-6; PMID:18641362; http://dx.doi.org/10.4049/jimmunol.181.3.2220
26. Hu X, Liu G, Hou Y, Shi J, Zhu L, Jin D, Peng J, Zhao Y. Induction of M2-like macrophages in recipient NOD-scid mice by allogeneic donor CD4(+)CD25(+) regulatory T cells. Cell Mol Immunol 2012; 9:464-72; PMID:23085944; http://dx.doi.org/10.1038/cmi.2012.47
27. Van Dyken SJ, Locksley RM. Interleukin-4- and interleukin-13-mediated alternatively activated macrophages:roles in homeostasis and disease. Ann Rev Immunol 2013; 31:317-43; PMID:23298208; http://dx.doi.org/10.1146/annurev-immunol-032712-095906
28. Odegaard JI, Chawla A. Alternative macrophage activation and metabolism. Ann Rev Pathol 2011; 6:275-97; PMID:21034223; http://dx.doi.org/10.1146/annurev-pathol-011110-130138
29. Xue J, Schmidt SV, Sander J, Draffehn A, Krebs W, Quester I, De Nardo D, Gohel TD, Emde M, Schmidleithner L, et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 2014; 40:274-88; PMID:24530056; http://dx.doi.org/10.1016/j.immuni.2014.01.006
30. Nold-Petry CA, Lo CY, Rudloff I, Elgass KD, Li S, Gantier MP, Lotz-Havla AS, Gersting SW, Cho SX, Lao JC, et al. IL-37 requires the receptors IL-18Ralpha and IL-1R8 (SIGIRR) to carry out its multifaceted anti-inflammatory program upon innate signal transduction. Nat Immunol 2015; 16:354-65; PMID:25729923; http://dx.doi.org/10.1038/ni.3103
31. Dinarello CA, Nold-Petry C, Nold M, Fujita M, Li S, Kim S, Bufler P. Suppression of innate inflammation and immunity by interleukin-37. Eur J Immunol 2016; 46:1067-81; PMID:27060871; http://dx.doi.org/10.1002/eji.201545828
32. Kaelin WG, Jr, McKnight SL. Influence of metabolism on epigenetics and disease. Cell 2013; 153:56-69; PMID:23540690; http://dx.doi.org/10.1016/j.cell.2013.03.004
33. Johnson C, Warmoes MO, Shen X, Locasale JW. Epigenetics and cancer metabolism. Cancer letters 2015; 356:309-14; PMID:24125862; http://dx.doi.org/10.1016/j.canlet.2013.09.043
34. Lu C, Ward PS, Kapoor GS, Rohle D, Turcan S, Abdel-Wahab O, Edwards CR, Khanin R, Figueroa ME, Melnick A, et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 2012; 483:474-8; PMID:22343901; http://dx.doi.org/10.1038/nature10860
35. Cluntun AA, Huang H, Dai L, Liu X, Zhao Y, Locasale JW. The rate of glycolysis quantitatively mediates specific histone acetylation sites. Cancer Metabolism 2015; 3:10; PMID:26401273; http://dx.doi.org/10.1186/s40170-015-0135-3
36. Pavlides S, Whitaker-Menezes D, Castello-Cros R, Flomenberg N, Witkiewicz AK, Frank PG, Casimiro MC, Wang C, Fortina P, Addya S, et al. The reverse Warburg effect:aerobic glycolysis in cancer associated fibroblasts and the tumor stroma. Cell cycle 2009; 8:3984-4001; PMID:19923890; http://dx.doi.org/10.4161/cc.8.23.10238
37. Ertel A, Tsirigos A, Whitaker-Menezes D, Birbe RC, Pavlides S, Martinez-Outschoorn UE, Pestell RG, Howell A, Sotgia F, Lisanti MP. Is cancer a metabolic rebellion against host aging? In the quest for immortality, tumor cells try to save themselves by boosting mitochondrial metabolism. Cell Cycle 2012; 11:253-63; PMID:22234241; http://dx.doi.org/10.4161/cc.11.2.19006
38. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC, et al. Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals cross-contamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 2008; 93:4331-41; PMID:18713817; http://dx.doi.org/10.1210/jc.2008-1102