Functional cell surface expression of toll-like receptor 9 promotes cell proliferation and survival in human hepatocellular carcinomas

International Journal of Oncology

Volumn 37, Issue 4, 2010, Pages 805-814

  Tanaka, Junichiro ^a   Sugimoto, Kazushi ^a   Shiraki, Katsuya ^a   Tameda, Masahiko ^a   Kusagawa, Satoko ^a   Nojiri, Keiichiro ^a   Beppu, Tetsuya ^a   Yoneda, Kentaro ^a   Yamamoto, Norihiko ^a   Uchida, Kazuhiko ^b   Kojima, Takahiro ^b   Takei, Yoshiyuki ^a  

^a MIE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Hepatocellular carcinomas; Toll like receptor

Indexed keywords

CISPLATIN; CPG OLIGODEOXYNUCLEOTIDE; DOXORUBICIN; FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; INTERFERON REGULATORY FACTOR 7; PROTEIN BCL XL; SURVIVIN; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR; X LINKED INHIBITOR OF APOPTOSIS;

ANKRD20B GENE; ARTICLE; BIRC6 GENE; CANCER GROWTH; CARCINOGENESIS; CELL MEMBRANE; CELL PROLIFERATION; CELL SURFACE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CRYAA GENE; CYTOPLASM; CYTOTOXICITY; DRUG EFFECT; FUNCTIONAL PROTEOMICS; GDF5OS GENE; GRAP GENE; HSPB8 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; HUWE1 GENE; IMMUNOHISTOCHEMISTRY; KLF5 GENE; LIVER CELL CARCINOMA; MALAT1 GENE; MICROARRAY ANALYSIS; NDRG4 GENE; NUCLEOTIDE SEQUENCE; NXN GENE; ONCOGENE; PRIORITY JOURNAL; PRKDC GENE; PROTEIN EXPRESSION; PSPN GENE; PTPLA GENE; RELN GENE; REX01L1 GENE; SCARNA7 GENE; SETBP1 GENE; SETD8 GENE; SIGNAL TRANSDUCTION; SMG1 GENE; SNORD116 2 GENE; SNRPN GENE; SURFACE PROPERTY; UPREGULATION; WESTERN BLOTTING;

EID: 77956500014     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000730     Document Type: Article

References (43)

1. Takeda K, Kaisho T and Akira S: Toll-like receptors. Annu Rev Immunol 21: 335-376, 2003.
2. Takeda K and Akira S: Toll-like receptors in innate immunity. Int Immunol 17: 1-14, 2005.
3. Beutler B, Jiang Z, Georgel P, Crozat K, Croker B, Rutschmann S, Du X and Hoebe K: Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu Rev Immunol 24: 353-389, 2006.
4. Kopp E and Medzhitov R: Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol 15: 396-401, 2003. (Pubitemid 36930075)
5. Akira S, Uematsu S and Takeuchi O: Pathogen recognition and innate immunity. Cell 124: 783-801, 2006.
6. Becker MN, Diamond G, Verghese MW and Randell SH: CD14-dependent lipopolysaccharide-induced beta-defensin-2 expression in human tracheobronchial epithelium. J Biol Chem 275: 29731-29736, 2000.
7. Muzio M, Bosisio D, Polentarutti N, D'Amico G, Stoppacciaro A, Mancinelli R, van't Veer C, Penton-Rol G, Ruco LP, Allavena P and Mantovani A: Differential expression and regulation of toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol 164: 5998-6004, 2000.
8. Faure E, Thomas L, Xu H, Medvedev A, Equils O and Arditi M: Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-kappa B activation. J Immunol 166: 2018-2024, 2001.
9. Visintin A, Mazzoni A, Spitzer JH, Wyllie DH, Dower SK and Segal DM: Regulation of Toll-like receptors in human monocytes and dendritic cells. J Immunol 166: 249-255, 2001.
10. Barton GM, Kagan JC and Medzhitov R: Intracellular localization of Toll-like receptor 9 prevents recognition of self-DNA but facilitates access to viral DNA. Nat Immunol 7: 49-56, 2006.
11. Matsumura T, Degawa T, Takii T, Hayashi H, Okamoto T, Inoue J and Onozaki K: TRAF6-NF-kappaB pathway is essential for interleukin-1-induced TLR2 expression and its functional response to TLR2 ligand in murine hepatocytes. Immunology 109: 127-136, 2003. (Pubitemid 36577983)
12. Harada K, Ohira S, Isse K, Ozaki S, Zen Y, Sato Y and Nakanuma Y: Lipopolysaccharide activates nuclear factor-kappaB through toll-like receptors and related molecules in cultured biliary epithelial cells. Lab Invest 83: 1657-1667, 2003.
13. Uhrig A, Banafsche R, Kremer M, Hegenbarth S, Hamann A, Neurath M, Gerken G, Limmer A and Knolle PA: Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver. J Leukoc Biol 77: 626-633, 2005. (Pubitemid 40628742)
14. Bauer S, Kirschning CJ, Häcker H, Redecke V, Hausmann S, Akira S, Wagner H and Lipford GB: Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci USA 98: 9237-9242, 2001.
15. McHutchison JG, Bacon BR, Gordon SC, Lawitz E, Shiffman M, Afdhal NH, Jacobson IM, Muir A, Al-Adhami M, Morris ML, Lekstrom-Himes JA, Efler SM and Davis HL: Phase 1B, randomized, double-blind, dose-escalation trial of CpG 10101 in patients with chronic hepatitis C virus. Hepatology 46: 1341-1349, 2007.
16. Chen R, Alvero AB, Silasi DA, Steffensen KD and Mor G: Cancers take their Toll-the function and regulation of Toll-like receptors in cancer cells. Oncogene 27: 225-233, 2008.
17. Huang B, Zhao J, Unkeless JC, Feng ZH and Xiong H: TLR signaling by tumor and immune cells: a double-edged sword. Oncogene 27: 218-224, 2008.
18. Salaun B, Coste I, Rissoan MC, Lebecque SJ and Renno T: TLR3 can directly trigger apoptosis in human cancer cells. J Immunol 176: 4894-4901, 2006.
19. Kelly MG, Alvero AB, Chen R, Silasi DA, Abrahams VM, Chan S, Visintin I, Rutherford T and Mor G: TLR-4 signaling promotes tumor growth and paclitaxel chemoresistance in ovarian cancer. Cancer Res 66: 3859-3868, 2006.
20. Huang B, Zhao J, Li H, He KL, Chen Y, Chen SH, Mayer L, Unkeless JC and Xiong H: Toll-like receptors on tumor cells facilitate evasion of immune surveillance. Cancer Res 65: 5009-5014, 2005.
21. Merrell MA, Ilvesaro JM, Lehtonen N, Sorsa T, Gehrs B, Rosenthal E, Chen D, Shackley B, Harris KW and Selander KS: Toll-like receptor 9 agonists promote cellular invasion by increasing matrix metalloproteinase activity. Mol Cancer Res 4: 437-447, 2006.
22. El Andaloussi A, Sonabend AM, Han Y and Lesniak MS: Stimulation of TLR9 with CpG ODN enhances apoptosis of glioma and prolongs the survival of mice with experimental brain tumors. Glia 54: 526-535, 2006. (Pubitemid 44449333)
23. Droemann D, Albrecht D, Gerdes J, Ulmer AJ, Branscheid D, Vollmer E, Dalhoff K, Zabel P and Goldmann T: Human lung cancer cells express functionally active Toll-like receptor 9. Respir Res 6: 1, 2005.
24. Schmausser B, Andrulis M, Endrich S, Müller-Hermelink HK and Eck M: Toll-like receptors TLR4, TLR5 and TLR9 on gastric carcinoma cells: an implication for interaction with Helicobacter pylori. Int J Med Microbiol 295: 179-185, 2005.
25. Ilvesaro JM, Merrell MA, Swain TM, Davidson J, Zayzafoon M, Harris KW and Selander KS: Toll-like receptor-9 agonists stimulate prostate cancer invasion in vitro. Prostate 67: 774-781, 2007.
26. Ludwig L, Oswald F, Hoang-Vu C, Dralle H, Hildt E, Schmid RM and Karges W: Expression of the Grb2-related RET adapter protein Grap-2 in human medullary thyroid carcinoma. Cancer Lett 275: 194-197, 2009.
27. Yoneda K, Sugimoto K, Shiraki K, Tanaka J, Beppu T, Fuke H, Yamamoto N, Masuya M, Horie R, Uchida K and Takei Y: Dual topology of functional Toll-like receptor 3 expression in human hepatocellular carcinoma: differential signaling mechanisms of TLR3-induced NF-κB activation and apoptosis. Int J Oncol 33: 929-936, 2008.
28. Leifer CA, Kennedy MN, Mazzoni A, Lee C, Kruhlak MJ and Segal DM: TLR9 is localized in the endoplasmic reticulum prior to stimulation. J Immunol 173: 1179-1183, 2004. (Pubitemid 38924294)
29. Brinkmann MM, Spooner E, Hoebe K, Beutler B, Ploegh HL and Kim YM: The interaction between the ER membrane protein UNC93B and TLR3, 7 and 9 is crucial for TLR signaling. J Cell Biol 177: 265-275, 2007.
30. Kim YM, Brinkmann MM, Paquet ME and Ploegh HL: UNC93B1 delivers nucleotide-sensing toll-like receptors to endolysosomes. Nature 452: 234-238, 2008.
31. Ewald SE, Lee BL, Lau L, Wickliffe KE, Shi GP, Chapman HA and Barton GM: The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 456: 658-662, 2008.
32. Ren T, Xu L, Jiao S, Wang Y, Cai Y, Liang Y, Zhou Y, Zhou H and Wen Z: TLR9 signaling promotes tumor progression of human lung cancer cell in vivo. Pathol Oncol Res 15: 623-630, 2009.
33. Honda K, Yanai H, Mizutani T, Negishi H, Shimada N, Suzuki N, Ohba Y, Takaoka A, Yeh WC and Taniguchi T: Role of a transductional- transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc Natl Acad Sci USA 101: 15416-15421, 2004.
34. Kawai T, Sato S, Ishii KJ, Coban C, Hemmi H, Yamamoto M, Terai K, Matsuda M, Inoue J, Uematsu S, Takeuchi O and Akira S: Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat Immunol 5: 1061-1068, 2004.
35. Kawai T and Akira S: TLR signaling. Cell Death Differ 13: 816-825, 2006.
36. Baldwin AS Jr: Series introduction: the transcription factor NF-κB and human disease. J Clin Invest 107: 3-6, 2001.
37. Karin M, Cao Y, Greten FR and Li ZW: NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2: 301-310, 2002.
38. Ghosh S and Karin M: Missing pieces in the NF-κB puzzle. Cell 109: S81-S96, 2002.
39. Ji P, Diederichs S, Wang W, Böing S, Metzger R, Schneider PM, Tidow N, Brandt B, Buerger H, Bulk E, Thomas M, Berdel WE, Serve H and Müller-Tidow C: MALAT-1, a novel non-coding RNA, and thymosin β4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 22: 8031-8041, 2003.
40. Lin R, Maeda S, Liu C, Karin M and Edgington TS: A large non-coding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas. Oncogene 26: 851-858, 2007. (Pubitemid 46245738)
41. Luo JH, Ren B, Keryanov S, Tseng GC, Rao UN, Monga SP, Strom S, Demetris AJ, Nalesnik M, Yu YP, Ranganathan S and Michalopoulos GK: Transcriptomic and genomic analysis of human hepatocellular carcinomas and hepatoblastomas. Hepatology 44: 1012-1024, 2006.
42. Bateman NW, Tan D, Pestell RG, Black JD and Black AR: Intestinal tumor progression is associated with altered function of KLF5. J Biol Chem 279: 12093-12101, 2004.
43. Zhao J, Wu G, Bu F, Lu B, Liang A, Cao L, Tong X, Lu X, Wu M and Guo Y: Epigenetic silence of ankyrin-repeat-containing, SH3-domain-containing, and proline-rich-region-containing protein 1 (ASPP1) and ASPP2 genes promotes tumor growth in hepatitis B virus-positive hepatocellular carcinoma. Hepatology 51: 142-153, 2010.