Tet2 restrains inflammatory gene expression in macrophages

Experimental Hematology

Volumn 55, Issue , 2017, Pages 56-70.e13

  Cull, Alyssa H ^a   Snetsinger, Brooke ^a   Buckstein, Rena ^b   Wells, Richard A ^b   Rauh, Michael J ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b DEPARTMENT OF RADIATION ONCOLOGY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MESSENGER RNA; ARG1 PROTEIN, MOUSE; ARGINASE; DNA BINDING PROTEIN; ONCOPROTEIN; TET2 PROTEIN, HUMAN; TET2 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TET2 GENE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CHRONIC MYELOMONOCYTIC LEUKEMIA; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTATION; MYELODYSPLASTIC SYNDROME; PATHOLOGY;

ANIMALS; ARGINASE; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; LEUKEMIA, MYELOMONOCYTIC, CHRONIC; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; MYELODYSPLASTIC SYNDROMES; PROTO-ONCOGENE PROTEINS;

EID: 85030628840     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2017.08.001     Document Type: Article

References (62)

1. Claus, R., Lubbert, M., Epigenetic targets in hematopoietic malignancies. Oncogene 22 (2003), 6489–6496.
2. Issa, J.P., Epigenetic changes in the myelodysplastic syndrome. Hematol Oncol Clin North Am 24 (2010), 317–330.
3. Toyota, M., Issa, J.P., Epigenetic changes in solid and hematopoietic tumors. Semin Oncol 32 (2005), 521–530.
4. Delhommeau, F., Dupont, S., Della Valle, V., et al. Mutation in TET2 in myeloid cancers. N Engl J Med 360 (2009), 2289–2301.
5. Langemeijer, S.M., Kuiper, R.P., Berends, M., et al. Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat Genet 41 (2009), 838–842.
6. Tefferi, A., Lim, K.H., Abdel-Wahab, O., et al. Detection of mutant TET2 in myeloid malignancies other than myeloproliferative neoplasms: CMML, MDS, MDS/MPN and AML. Leukemia 23 (2009), 1343–1345.
7. Itzykson, R., Kosmider, O., Renneville, A., et al. Prognostic score including gene mutations in chronic myelomonocytic leukemia. J Clin Oncol 31 (2013), 2428–2436.
8. Grossmann, V., Kohlmann, A., Eder, C., et al. Molecular profiling of chronic myelomonocytic leukemia reveals diverse mutations in >80% of patients with TET2 and EZH2 being of high prognostic relevance. Leukemia 25 (2011), 877–879.
9. Kohlmann, A., Grossmann, V., Klein, H.U., et al. Next-generation sequencing technology reveals a characteristic pattern of molecular mutations in 72.8% of chronic myelomonocytic leukemia by detecting frequent alterations in TET2, CBL, RAS, and RUNX1. J Clin Oncol 28 (2010), 3858–3865.
10. Papaemmanuil, E., Gerstung, M., Malcovati, L., et al. Clinical and biological implications of driver mutations in myelodysplastic syndromes. Blood 122 (2013), 3616–3627 quiz 3699.
11. Jaiswal, S., Fontanillas, P., Flannick, J., et al. Age-related clonal hematopoiesis associated with adverse outcomes. N Engl J Med 371 (2014), 2488–2498.
12. Yamazaki, J., Jelinek, J., Lu, Y., et al. TET2 mutations affect Non-CpG island DNA methylation at enhancers and transcription factor-binding sites in chronic myelomonocytic leukemia. Cancer Res 75 (2015), 2833–2843.
13. Rasmussen, K.D., Jia, G., Johansen, J.V., et al. Loss of TET2 in hematopoietic cells leads to DNA hypermethylation of active enhancers and induction of leukemogenesis. Genes Dev 29 (2015), 910–922.
14. Moran-Crusio, K., Reavie, L., Shih, A., et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20 (2011), 11–24.
15. Quivoron, C., Couronne, L., Della Valle, V., et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20 (2011), 25–38.
16. Ko, M., Bandukwala, H.S., An, J., et al. Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc Natl Acad Sci USA 108 (2011), 14566–14571.
17. Li, Z., Cai, X., Cai, C.L., et al. Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118 (2011), 4509–4518.
18. Ganan-Gomez, I., Wei, Y., Starczynowski, D.T., et al. Deregulation of innate immune and inflammatory signaling in myelodysplastic syndromes. Leukemia 29 (2015), 1458–1469.
19. Cull, A.H., Rauh, M.J., Success in bone marrow failure? Novel therapeutic directions based on the immune environment of myelodysplastic syndromes. J Leukoc Biol 102 (2017), 209–219.
20. Fuster, J.J., MacLauchlan, S., Zuriaga, M.A., et al. Clonal hematopoiesis associated with Tet2 deficiency accelerates atherosclerosis development in mice. Science 355 (2017), 842–847.
21. Jaiswal, S., Natarajan, P., Silver, A.J., et al. Clonal hematopoiesis and risk of atherosclerotic cardiovascular disease. N Engl J Med 377 (2017), 111–121.
22. Phinney, D.G., Di Giuseppe, M., Njah, J., et al. Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs. Nat Commun, 6, 2015, 8472.
23. Rigolin, G.M., Cuneo, A., Roberti, M.G., Bardi, A., Castoldi, G., Myelodysplastic syndromes with monocytic component: hematologic and cytogenetic characterization. Haematologica 82 (1997), 25–30.
24. Singh, Z.N., Post, G.R., Kiwan, E., Maddox, A.M., Cytopenia, dysplasia, and monocytosis: a precursor to chronic myelomonocytic leukemia or a distinct subgroup? Case reports and review of literature. Clin Lymphoma Myeloma Leuk 11 (2011), 293–297.
25. Weisser, S.B., McLarren, K.W., Kuroda, E., Sly, L.M., Generation and characterization of murine alternatively activated macrophages. Methods Mol Biol 946 (2013), 225–239.
26. Rauh, M.J., Ho, V., Pereira, C., et al. SHIP represses the generation of alternatively activated macrophages. Immunity 23 (2005), 361–374.
27. Ring, B.A., Ferreira Lacerda, A., Drummond, D.J., et al. Frog virus 3 open reading frame 97R localizes to the endoplasmic reticulum and induces nuclear invaginations. J Virol 87 (2013), 9199–9207.
28. Coomes, S.M., Pelly, V.S., Kannan, Y., et al. IFNγ and IL-12 restrict Th2 responses during helminth/plasmodium co-infection and promote IFNγ from Th2 cells. PLoS Pathog, 11, 2015, e1004994.
29. Chen, W., Han, C., Xie, B., et al. Induction of Siglec-G by RNA viruses inhibits the innate immune response by promoting RIG-I degradation. Cell 152 (2013), 467–478.
30. Chang, H.Y., Lee, H.N., Kim, W., Surh, Y.J., Docosahexaenoic acid induces M2 macrophage polarization through peroxisome proliferator-activated receptor γ activation. Life Sci 120 (2015), 39–47.
31. Ariffin, J.K., Kapetanovic, R., Schaale, K., et al. The E3 ubiquitin ligase RNF144B is LPS-inducible in human, but not mouse, macrophages and promotes inducible IL-1β expression. J Leukoc Biol 100 (2016), 155–161.
32. Zimmermann, M., Arruda-Silva, F., Bianchetto-Aguilera, F., et al. IFNα enhances the production of IL-6 by human neutrophils activated via TLR8. Sci Rep, 6, 2016, 19674.
33. Stephens, A.S., Stephens, S.R., Morrison, N.A., Internal control genes for quantitative RT-PCR expression analysis in mouse osteoblasts, osteoclasts and macrophages. BMC Res Notes, 4, 2011, 410.
34. Zhou, Z., Wu, Y., Chen, L., et al. Heat shock protein 10 of Chlamydophila pneumoniae induces proinflammatory cytokines through Toll-like receptor (TLR) 2 and TLR4 in human monocytes THP-1. In Vitro Cell Dev Biol Anim 47 (2011), 541–549.
35. Hoaglin, D.C., Iglewicz, B., Fine-tuning some resistant rules for outlier labeling. J Am Stat Assoc 82 (1987), 1147–1149.
36. Sekeres, M.A., Othus, M., List, A.F., et al. Randomized phase II study of azacitidine alone or in combination with lenalidomide or with vorinostat in higher-risk myelodysplastic syndromes and chronic myelomonocytic leukemia: North American Intergroup Study SWOG S1117. J Clin Oncol 35 (2017), 2745–2753.
37. Bagger, F.O., Sasivarevic, D., Sohi, S.H., et al. BloodSpot: a database of gene expression profiles and transcriptional programs for healthy and malignant haematopoiesis. Nucleic Acids Res 44 (2016), D917–D924.
38. Heng, T.S., Painter, M.W., Immunological Genome Project Consortium. The Immunological Genome Project: networks of gene expression in immune cells. Nat Immunol 9 (2008), 1091–1094.
39. Zhang, Q., Zhao, K., Shen, Q., et al. Tet2 is required to resolve inflammation by recruiting Hdac2 to specifically repress IL-6. Nature 525 (2015), 389–393.
40. Foster, S.L., Hargreaves, D.C., Medzhitov, R., Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447 (2007), 972–978.
41. Nemeth, Z.H., Leibovich, S.J., Deitch, E.A., Vizi, E.S., Szabo, C., Hasko, G., cDNA microarray analysis reveals a nuclear factor-kappaB-independent regulation of macrophage function by adenosine. J Pharmacol Exp Ther 306 (2003), 1042–1049.
42. El Kasmi, K.C., Qualls, J.E., Pesce, J.T., et al. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol 9 (2008), 1399–1406.
43. Murray, P.J., Allen, J.E., Biswas, S.K., et al. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41 (2014), 14–20.
44. Ko, M., An, J., Pastor, W.A., Koralov, S.B., Rajewsky, K., Rao, A., TET proteins and 5-methylcytosine oxidation in hematological cancers. Immunol Rev 263 (2015), 6–21.
45. An, J., Gonzalez-Avalos, E., Chawla, A., et al. Acute loss of TET function results in aggressive myeloid cancer in mice. Nat Commun, 6, 2015, 10071.
46. Kitagawa, M., Saito, I., Kuwata, T., et al. Overexpression of tumor necrosis factor (TNF)-alpha and interferon (IFN)-gamma by bone marrow cells from patients with myelodysplastic syndromes. Leukemia 11 (1997), 2049–2054.
47. Flores-Figueroa, E., Gutierrez-Espindola, G., Montesinos, J.J., Arana-Trejo, R.M., Mayani, H., In vitro characterization of hematopoietic microenvironment cells from patients with myelodysplastic syndrome. Leuk Res 26 (2002), 677–686.
48. Pang, W.W., Pluvinage, J.V., Price, E.A., et al. Hematopoietic stem cell and progenitor cell mechanisms in myelodysplastic syndromes. Proc Natl Acad Sci USA 110 (2013), 3011–3016.
49. Velegraki, M., Papakonstanti, E., Mavroudi, I., et al. Impaired clearance of apoptotic cells leads to HMGB1 release in the bone marrow of patients with myelodysplastic syndromes and induces TLR4-mediated cytokine production. Haematologica 98 (2013), 1206–1215.
50. Yang, L., Qian, Y., Eksioglu, E., Epling-Burnette, P.K., Wei, S., The inflammatory microenvironment in MDS. Cell Mol Life Sci 72 (2015), 1959–1966.
51. Braun, T., Fenaux, P., Myelodysplastic Syndromes (MDS) and autoimmune disorders (AD): Cause or consequence?. Best Pract Res Clin Haematol 26 (2013), 327–336.
52. Zambetti, N.A., Ping, Z., Chen, S., et al. Mesenchymal inflammation drives genotoxic stress in hematopoietic stem cells and predicts disease evolution in human pre-leukemia. Cell Stem Cell 19 (2016), 613–627.
53. Basiorka, A.A., McGraw, K.L., Eksioglu, E.A., et al. The NLRP3 inflammasome functions as a driver of the myelodysplastic syndrome phenotype. Blood 128 (2016), 2960–2975.
54. Walter, M.J., Shen, D., Shao, J., et al. Clonal diversity of recurrently mutated genes in myelodysplastic syndromes. Leukemia 27 (2013), 1275–1282.
55. Haferlach, T., Nagata, Y., Grossmann, V., et al. Landscape of genetic lesions in 944 patients with myelodysplastic syndromes. Leukemia 28 (2014), 241–247.
56. Kallin, E.M., Rodriguez-Ubreva, J., Christensen, J., et al. Tet2 facilitates the derepression of myeloid target genes during CEBPα-induced transdifferentiation of pre-B cells. Mol Cell 48 (2012), 266–276.
57. de la Rica, L., Rodriguez-Ubreva, J., Garcia, M., et al. PU.1 target genes undergo Tet2-coupled demethylation and DNMT3b-mediated methylation in monocyte-to-osteoclast differentiation. Genome Biol, 14, 2013, R99.
58. Bocker, M.T., Tuorto, F., Raddatz, G., et al. Hydroxylation of 5-methylcytosine by TET2 maintains the active state of the mammalian HOXA cluster. Nat Commun, 3, 2012, 818.
59. Ichiyama, K., Chen, T., Wang, X., et al. The methylcytosine dioxygenase Tet2 promotes DNA demethylation and activation of cytokine gene expression in T cells. Immunity 42 (2015), 613–626.
60. Yasukawa, H., Ohishi, M., Mori, H., et al. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 4 (2003), 551–556.
61. Qin, H., Holdbrooks, A.T., Liu, Y., Reynolds, S.L., Yanagisawa, L.L., Benveniste, E.N., SOCS3 deficiency promotes M1 macrophage polarization and inflammation. J Immunol 189 (2012), 3439–3448.
62. Su, X., Li, S., Meng, M., et al. TNF receptor-associated factor-1 (TRAF1) negatively regulates Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF)-mediated signaling. Eur J Immunol 36 (2006), 199–206.