Epigenetic modification of TLR4 promotes activation of NF-κB by regulating methyl-CpG-binding domain protein 2 and Sp1 in gastric cancer

Oncotarget

Volumn 7, Issue 4, 2016, Pages 4195-4209

  Kim, Tae Woo ^a,b   Lee, Seon Jin ^a,b   Oh, Byung Moo ^a,b   Lee, Heesoo ^a,b   Uhm, Tae Gi ^a   Min, Jeong Ki ^a   Park, Young Jun ^a   Yoon, Suk Ran ^a   Kim, Bo Yeon ^a   Kim, Jong Wan ^c   Choe, Yong Kyung ^a   Lee, Hee Gu ^a,b  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

^c Dankook University   (South Korea)

Author keywords

Gastric cancer; Methyl CpG binding domain protein 2; Methylation; Sp1; Toll like receptor 4

Indexed keywords

DECITABINE; HISTONE DEACETYLASE 1; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; METHYL CPG BINDING PROTEIN 2; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN; TOLL LIKE RECEPTOR 4; VENETOCLAX; HDAC1 PROTEIN, HUMAN; HISTONE; MECP2 PROTEIN, HUMAN; MESSENGER RNA; SP1 PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SP1;

ARTICLE; BINDING SITE; CANCER STAGING; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STOMACH CANCER; TLR4 GENE; APOPTOSIS; CELL PROLIFERATION; ENZYME IMMUNOASSAY; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOMACH TUMOR; TISSUE MICROARRAY; TUMOR CELL CULTURE;

APOPTOSIS; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HISTONE DEACETYLASE 1; HISTONES; HUMANS; IMMUNOENZYME TECHNIQUES; METHYL-CPG-BINDING PROTEIN 2; NF-KAPPA B; PROMOTER REGIONS, GENETIC; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SP1 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; TISSUE ARRAY ANALYSIS; TOLL-LIKE RECEPTOR 4; TUMOR CELLS, CULTURED;

EID: 84957991409     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6549     Document Type: Article

References (63)

1. Nishimura M and Naito S. Tissue-specific mRNA expression profiles of human toll-like receptors and related genes. Biol Pharm Bull. 2005;28:886-892.
2. Wang J, Lin D, Peng H, Shao J and Gu J. Cancer-derived immunoglobulin G promotes LPS-induced proinflammatory cytokine production via binding to TLR4 in cervical cancer cells. Oncotarget. 2014;5:9727-9743. doi: 10.18632/oncotarget.2359.
3. Yu L, Wang L, Li M, Zhong J, Wang Z and Chen S. Expression of toll-like receptor 4 is downregulated during progression of cervical neoplasia. Cancer Immunol Immunother. 2010;59:1021-1028.
4. Zhan Z, Xie X, Cao H, Zhou X, Zhang XD, Fan H and Liu Z. Autophagy facilitates TLR4-and TLR3-triggered migration and invasion of lung cancer cells through the promotion of TRAF6 ubiquitination. Autophagy. 2013;10:257-268.
5. Yu L and Chen S. Toll-like receptors expressed in tumor cells: targets for therapy. Cancer Immunol Immunother. 2008;57:1271-1278.
6. Federico Feroze Tak. The PGE2-EP receptor axis in cololectal cancer and angiogenesis.Journal of Tumor. 2014;2:208-218.
7. Liao SJ, Zhou YH, Yuan Y, Li D, Wu FH, Wang Q, Zhu JH, Yan B, Wei JJ, Zhang GM and Feng ZH. Triggering of Toll-like receptor 4 on metastatic breast cancer cells promotes αvβ3-mediated adhesion and invasive migration. Breast Cancer Res Treat. 2012;133:853-863.
8. He W, Liu Q, Wang L, Chen W, Li N and Cao X. TLR4 signaling promotes immune escape of human lung cancer cells by inducing immunosuppressive cytokines and apoptosis resistance. Mol Immunol. 2007;44:2850-2859.
9. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S, Miyake K, Shibuya M, Akira S, Aburatani H and Maru Y. The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol. 2008;10:1349-1355.
10. Takahashi K, Sugi Y, Hosono A and Kaminogawa S. Epigenetic regulation of TLR4 gene expression in intestinal epithelial cells for the maintenance of intestinal homeostasis. Journal of Immunology. 2009;183: 6522-6529.
11. Nephew KP and Huang TH. Epigenetic gene silencing in cancer initiation and progression. Cancer Letter. 2003; 190: 125-133.
12. Nagy E, Gajjar KB, Patel LL, Taylor S, Martin-Hirsch PL, Stringfellow HF, Martin FL and Phillips DH. MGMT promoter hypermethylation and K-RAS, PTEN and TP53 mutations in tamoxifen-exposed and non-exposed endometrial cancer cases. Br J Cancer. 2014;110: 2874-2880.
13. Zampetaki A, Xiao Q, Zeng L, Hu Y and Xu Q. TLR4 expression in mouse embryonic stem cells and in stem cell-derived vascular cells is regulated by epigenetic modifications. Biochem Biophys Res Commun. 2006; 347: 89-99.
14. Takahashi K, Sugi Y, Nakano K, Tsuda M, Kurihara K, Hosono A and Kaminogawa S. Epigenetic control of the host gene by commensal bacteria in large intestinal epithelial cells. J Biol Chem. 2011; 286: 35755-35762.
15. Comb M and Goodman HM. CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Res. 1990;18: 3975-3982.
16. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN and Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature. 1998;393: 386-389.
17. Wasiluk KR, McCulloch KA, Banton KL and Dunn DL. Sp1 elements regulate transcriptional activity within the murine Toll-like receptor 4 promoter. Surg Infect (Larchmt). 2006;7: 489-499.
18. Holler M, Westin G, Jirincy J and Schaffner W. Sp1 transcription factor binds DNA and activates transcription even when the binding site is CpG methylated. Genes Dev. 1998; 2: 1127-1135.
19. Cao YX, Jean JC and Williams MC. Cytosine methylation of an Sp1 site contributes to organ-specific and cell-specific regulation of expression of the lung epithelial gene t1alpha. Biochem J. 2000;350: 883-890.
20. Simonsson S and Gurdon J. DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol. 2004;6: 984-990.
21. Baylin SB. DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol. 2005;2: S4-S11.
22. Chen H, Cowan MJ, Hasday JD, Vogel SN and Medvedev AE. Tobacco smoking inhibits expression of proinflammatory cytokines and activation of IL-1R-associated kinase, p38, and NF-kappaB in alveolar macrophages stimulated with TLR2 and TLR4 agonists. J Immunol. 2007;179: 6097-6106.
23. Dobrovolskaia MA, Medvedev AE, Thomas KE, Cuesta N, Toshchakov V, Ren T, Cody MJ, Michalek SM, Rice NR and Vogel SN. Induction of in vitro reprogramming by Toll-like receptor (TLR)2 and TLR4 agonists in murine macrophage: effects of TLR "homotolerance" versus "heterotolerance" on NF-kappa B signaling pathway components. J Immunol. 2003;170: 508-519.
24. Bird AP and Wolffe AP. Methylation-induced repression-belts, braces, and chromatin. Cell. 1999;99: 451-454.
25. Kemp CJ, Moore JM, Moser R, Bernard B, Teater M, smith LE, Rabaia NA, Gurley KE, Guinney J, Busch SE, Shaknovich R, Lobanenkov VV, Lighitt D, Shmulevich I, Melnick A and Filippova GN. CTCF haploinsufficiency destabilizes DNA methylation and predisposes to cancer. Cell Rep. 2014;7: 1020-1029.
26. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J and Wolffe AP. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet. 1998;19: 187-191.
27. Cassel S, Carouge D, Gensburger C, Anglard P, Burgun C, Dietrich JB, Aunis D and Zwiller J. Fluoxetine and cocaine induce the epigenetic factors MeCP2 and MBD1 in adult rat brain, Mol Pharmacol. 2006;70: 487-492.
28. Abuhatzira L, Shemer R and Razin A. MeCP2 involvement in the regulation of neuronal alpha-tubulin production. Hum Mol Genet. 2009;18: 1415-1423.
29. Hendrich B and Tweedie S. The methyl-CpG binding domain and the evolving role of DNA methylation in animals. Trends Genet. 2003;19: 269-277.
30. Liu L, Li YH, Niu YB, Sun Y, Guo ZJ, Li Q, Li C, Feng J, Cao SS and Mei QB. An apple oligogalactan prevents against inflammation and carcinogenesis by targeting LPS/TLR4/NF-kB pathway in a mouse model of colitis-associated colon cancer. Carcinogenesis. 2010;31: 1822-1832.
31. Szajnik M, Szczepanski MJ, Czystowska M, Elishaev E, Mandapathil M, Nowak-Markwitz E, Spaczynski M and Whiteside TL. TLR4 signaling induced by lipopolysaccharide or paclitaxel regulates tumor survival and chemoresistance in ovarian cancer. Oncogene. 2009; 28: 4353-4363.
32. Jiang Q, Akashi S, Miyake K and Petty HR. Lipopolysaccharide induces physical proximity between CD14 and toll-like receptor 4 (TLR4) prior to nuclear translocation of NF-kappa B. J Immunol. 2000;165: 3541-3544.
33. Aderem A and Ulevitch RJ. Toll-like receptors in the induction of the innate immune response. Nature. 2000;406:782-787.
34. Hua D, Liu MY, Cheng ZD, Qin XJ, Zhang HM, Chen Y, Qin GJ, Li JN, Han XF and Liu DX. Small interfering RNA-directed targeting of Toll-like receptor 4 inhibits human prostate cancer cell invasion, survival, and tumorigenicity. Mol. Immunol. 2009;46:2876-2884.
35. Gonzalez-Reyes S, Marin L, Gonzalez L, Gonzalez LO, del Casar JM, Lamelas ML, Gonzalez-Quintana JM and Vizoso FJ. Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis. BMC Cancer. 2010;10:665.
36. Cammarota R, Bertolini V, Pennesi G, Bucci EO, Gottardi O, Garlanda C, Laghi L, Barberis MC, Sessa F, Noonan DM and Albini A. The tumor microenvironment of colorectal cancer: stromal TLR-4 expression as a potential prognostic marker. J Transl Med. 2010;8: 112.
37. Velazquez RF, Rodriguez M, Navascues CA, Linares A, Perez R, Sotorrios NG, Martinez I and Rodrigo L. Prospective analysis of risk factors for hepatocellular carcinoma in patients with liver cirrhosis. Hepatology. 2003;37:520-527.
38. Broering R, Wu J, Meng Z, Hilgard P, Lu M, Trippler M, Szczeponek A, Gerken G and Schlaak JF. Toll-like receptor-stimulated non-parenchymal liver cells can regulate hepatitis C virus replication. J Hepatol. 2008;48:914-922.
39. Wu J, Lu M, Meng Z, Trippler M, Broering R, Szczeponek A, Krux F, Dittmer U, Roggendorf M, Gerken G and Schlaak JF. Toll-like receptor-mediated control of HBV replication by nonparenchymal liver cells in mice. Hepatology. 2007;46:1769-1778.
40. Ferrero RL. Innate immune recognition of the extracellular mucosal pathogen, Helicobacter pylori. Mol Immunol. 2005;42:879-885.
41. Uno K, Kato K, Atsumi T, Suzuki T, Yoshitake J, Morita H, Ohara S, Kotake Y, Shimosegawa T and Yoshimura T. Toll-like receptor (TLR) 2 induced through TLR4 signaling initiated by Helicobacter pylori cooperatively amplifies iNOS induction in gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007;293:G1004-G1012.
42. Yang R, Murillo FM, Cui H, Blosser R, Uematsu S, Takeda K, Akira S, Viscidi RP and Roden RB. Papillomavirus-like particles stimulate murine bone marrow-derived dendritic cells to produce a interferon and Th1 immune responses via MyD88. J Virol. 2004;78:11152-11160.
43. Otto F, Schmid P, Mackensen A, Wehr U, Seiz A, Braun M, Galanos C, Mertelsmann R and Engelhardt R. Phase II trial of intravenous endotoxin in patients with colorectal and non-small cell lung cancer. Eur J Cancer. 1996;32A:1712-1718.
44. Garay RP, Viens P, Bauer J, Normier G, Bardou M, Jeannin JF and Chiavaroli C. Cancer relapse under chemotherapy: why TLR2/4 receptor agonists can help. Eur J Pharmacol. 2007;563:1-17.
45. Goto Y, Arigami T, Kitago M, Nguyen SL, Narita N, Ferrone S, Morton DL, Irie RF and Hoon DS. Activation of Toll-like receptors 2, 3, and 4 on human melanoma cells induces inflammatory factors. Mol Cancer Ther. 2008;7:3642-3653.
46. Lee CH, Wu CL and Shiau AL. Toll-like receptor 4 signaling promotes tumor growth. J Immunother. 2010;33:73-82.
47. Ling GS, Bennett J, Woollard KJ, Szajna M, Fossati-Jimack L, Taylor PR, Scott D, Franzoso G, Cook HT and Botto M. Integrin CD11b Positively regulates TLR4-induced signalling pathways in dendritic cells but not inmacrophages. Nat Commun. 2014; doi: 10.1038/ncomms 4039.
48. Xia X, Cui J, Wang HY, Zhu L, Matsueda S, Wang Q, Yang X, Hong J, Songyang Z, Chen ZJ and Wang RF. NLRX1 Negatively Regulates TLR-Induced NF-kB Signaling by Targeting TRAF6 and IKK. Immunity. 2011; 34:843-853.
49. Shukla S, Meeran SM and Katiyar SK. Epigenetic regulation by selected dietary phytochemicals in cancer chemoprevention. Cancer Lett. 2014;355:9-17.
50. Jones PA and Baylin SB, The fundamental role of epigenetic events in cancer. Nat Rev Genet. 2002;3:415-428.
51. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, Motiwala T and Jacob ST. 5-Aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Mol Cell Biol. 2005;25:4727-4741.
52. Drewell RA, Goddard CJ, Thomas JO and Surani MA. Methylation-dependent silencing at the H19 imprinting control region by MeCP2. Nucleic Acids Res. 2002;30: 1139-1144.
53. Fuks F, Hurd PJ, Deplus R and Kouzarides T. The DNA methyltransferase associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 2003;31: 2305-2312.
54. Dandrea M, Donadell M, Costanzo C, Scarpa A and Palmieri M. MeCP2/H3meK9 are involved in IL-6 gene silencing in pancreatic adenocarcinoma cell lines. Nucleic Acids Res. 2009;37:6681-6690.
55. Jinawath N, Furukawa Y, Hasegawa S, Li M, Tsunoda T, Yamaguchi T, Imamura H, Inoue M, Shiozaki H and Nakamura Y. Comparison of gene-expression profiles between between diffuse-and intestinal-type gastric cancers using a genome-wide cDNA microarray. Oncogene. 2004;23:6830-6844.
56. Yang H, Zhou H, Feng P, Zhou X, Wen H, Xie X, Shen H and Zhu X. Reduced expression of Toll-like receptor 4 inhibits human breast cancer cells proliferation and inflammatory cytokines secretion. J Exp Clin Cancer Res. 2010;29:92.
57. De Oliveira NF, Andia DC, Planello AC, Pasetto S, Marques MR, Nociti FH Jr, Line SR and De Souza AP. TLR2 and TLR4 gene promoter methylation status during chronic periodontitis, J Clin Periodontol. 2011;38:975-983.
58. Brandeis M, Frank D, Keshet I, Siegfried Z, Mendelsohn M, Nemes A, Temper V, Razin A and Cedar H. Sp1 elements protect a CpG island from de novo methylation. Nature. 1994;371:435-438.
59. Meehan RR, Lewis JD and Bird AP. Characterization of MeCP2, a vertebrate DNA binding protein with affinity for methylated DNA. Nucleic Acids Res. 1992;20:5085-5092.
60. Feinberg AP and Tycko B. The history of cancer epigenetics. Nat Rey Cancer. 2004;4: 143-153.
61. Ballestar E and Wolffe AP. Methyl-CpG-binding proteins. Targeting specific gene repression. Eur J Biochem. 2001;268:1-6.
62. Bienvenu T and Chelly J. Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat Rev Genet. 2006;7:415-426.
63. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP and Kouzarides T. The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem. 2003;278: 4035-4040.