Toll-like receptor-4 is a target for suppression of proliferation and chemoresistance in HepG2 hepatoblastoma cells

Cancer Letters

Volumn 368, Issue 1, 2015, Pages 144-152

  Hsiao, Chih Cheng ^a   Chen, Po Han ^b   Cheng, Cheng I ^a   Tsai, Ming Shian ^b   Chang, Chih Yang ^b   Lu, Shang Chieh ^b   Hsieh, Ming Chu ^b   Lin, Yu Chun ^b   Lee, Po Huang ^b   Kao, Ying Hsien ^b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b E DA HOSPITAL   (Taiwan)

Author keywords

Lipopolysaccharide; Nitric oxide production; Nitric oxide synthase; Signal transduction; Small interfering RNA

Indexed keywords

CISPLATIN; DOXORUBICIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 4; PROTEIN KINASE INHIBITOR; TLR4 PROTEIN, HUMAN;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA MODIFICATION; DRUG EFFICACY; DRUG MECHANISM; DRUG RESISTANCE; GENETIC TRANSFECTION; HEPATOCELLULAR CARCINOMA CELL LINE; HEPG2 CELL LINE; HUH 7 CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SK HEP1 CELL LINE; UPREGULATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; GENE SILENCING; GENETICS; HEPATOBLASTOMA; LIVER TUMOR; METABOLISM; PATHOLOGY; RNA INTERFERENCE; TIME;

CELL PROLIFERATION; CISPLATIN; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; HEP G2 CELLS; HEPATOBLASTOMA; HUMANS; LIPOPOLYSACCHARIDES; LIVER NEOPLASMS; MITOGEN-ACTIVATED PROTEIN KINASES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 4; TRANSFECTION;

EID: 84940744632     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.08.004     Document Type: Article

References (57)

1. Cherfils-Vicini J., Platonova S., Gillard M., Laurans L., Validire P., Caliandro R., et al. Triggering of TLR7 and TLR8 expressed by human lung cancer cells induces cell survival and chemoresistance. J. Clin. Invest 2010, 120:1285-1297.
2. Wang E.L., Qian Z.R., Nakasono M., Tanahashi T., Yoshimoto K., Bando Y., et al. High expression of Toll-like receptor 4/myeloid differentiation factor 88 signals correlates with poor prognosis in colorectal cancer. Br. J. Cancer 2010, 102:908-915.
3. Gatti G., Quintar A.A., Andreani V., Nicola J.P., Maldonado C.A., Masini-Repiso A.M., et al. Expression of Toll-like receptor 4 in the prostate gland and its association with the severity of prostate cancer. Prostate 2009, 69:1387-1397.
4. Yang H., Zhou H., Feng P., Zhou X., Wen H., Xie X., et al. Reduced expression of Toll-like receptor 4 inhibits human breast cancer cells proliferation and inflammatory cytokines secretion. J. Exp. Clin. Cancer Res 2010, 29:92-99.
5. Lee J.W., Choi J.J., Seo E.S., Kim M.J., Kim W.Y., Choi C.H., et al. Increased toll-like receptor 9 expression in cervical neoplasia. Mol. Carcinog 2007, 46:941-947.
6. Goto Y., Arigami T., Kitago M., Nguyen S.L., Narita N., Ferrone S., et al. Activation of Toll-like receptors 2, 3, and 4 on human melanoma cells induces inflammatory factors. Mol. Cancer Ther 2008, 7:3642-3653.
7. Sato Y., Goto Y., Narita N., Hoon D.S. Cancer cells expressing toll-like receptors and the tumor microenvironment. Cancer Microenviron 2009, 2(Suppl. 1):205-214.
8. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
9. Basith S., Manavalan B., Yoo T.H., Kim S.G., Choi S. Roles of toll-like receptors in cancer: a double-edged sword for defense and offense. Arch. Pharm. Res 2012, 35:1297-1316.
10. He W., Liu Q., Wang L., Chen W., Li N., 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.
11. Huang B., Zhao J., Unkeless J.C., Feng Z.H., Xiong H. TLR signaling by tumor and immune cells: a double-edged sword. Oncogene 2008, 27:218-224.
12. Ilvesaro J.M., Merrell M.A., Li L., Wakchoure S., Graves D., Brooks S., et al. Toll-like receptor 9 mediates CpG oligonucleotide-induced cellular invasion. Mol. Cancer Res 2008, 6:1534-1543.
13. Szajnik M., Szczepanski M.J., Czystowska M., Elishaev E., Mandapathil M., Nowak-Markwitz E., et al. TLR4 signaling induced by lipopolysaccharide or paclitaxel regulates tumor survival and chemoresistance in ovarian cancer. Oncogene 2009, 28:4353-4363.
14. Machida K., Feldman D.E., Tsukamoto H. TLR4-dependent tumor-initiating stem cell-like cells (TICs) in alcohol-associated hepatocellular carcinogenesis. Adv. Exp. Med. Biol 2015, 815:131-144.
15. Shehata M.A., Abou El-Enein A., El-Sharnouby G.A. Significance of toll-like receptors 2 and 4 mRNA expression in chronic hepatitis C virus infection. Egypt. J. Immunol 2006, 13:141-152.
16. Mozer-Lisewska I., Sluzewski W., Kaczmarek M., Jenek R., Szczepanski M., Figlerowicz M., et al. Tissue localization of Toll-like receptors in biopsy specimens of liver from children infected with hepatitis C virus. Scand. J. Immunol 2005, 62:407-412.
17. Machida K., Cheng K.T., Sung V.M., Levine A.M., Foung S., Lai M.M. Hepatitis C virus induces toll-like receptor 4 expression, leading to enhanced production of beta interferon and interleukin-6. J. Virol 2006, 80:866-874.
18. Eiro N., Altadill A., Juarez L.M., Rodriguez M., Gonzalez L.O., Atienza S., et al. Toll-like receptors 3, 4 and 9 in hepatocellular carcinoma: relationship with clinicopathological characteristics and prognosis. Hepatol. Res 2014, 44:769-778.
19. Dapito D.H., Mencin A., Gwak G.Y., Pradere J.P., Jang M.K., Mederacke I., et al. Promotion of hepatocellular carcinoma by the intestinal microbiota and TLR4. Cancer Cell 2012, 21:504-516.
20. Garcia-Tsao G., Wiest R. Gut microflora in the pathogenesis of the complications of cirrhosis. Best Pract. Res. Clin. Gastroenterol 2004, 18:353-372.
21. Albillos A., de la Hera A., Gonzalez M., Moya J.L., Calleja J.L., Monserrat J., et al. Increased lipopolysaccharide binding protein in cirrhotic patients with marked immune and hemodynamic derangement. Hepatology 2003, 37:208-217.
22. Wang L., Zhu R., Huang Z., Li H., Zhu H. Lipopolysaccharide-induced toll-like receptor 4 signaling in cancer cells promotes cell survival and proliferation in hepatocellular carcinoma. Dig. Dis. Sci 2013, 58:2223-2236.
23. Li H., Li Y., Liu D., Liu J. LPS promotes epithelial-mesenchymal transition and activation of TLR4/JNK signaling. Tumour Biol 2014, 35:10429-10435.
24. Jing Y.Y., Han Z.P., Sun K., Zhang S.S., Hou J., Liu Y., et al. Toll-like receptor 4 signaling promotes epithelial-mesenchymal transition in human hepatocellular carcinoma induced by lipopolysaccharide. BMC Med 2012, 10:98.
25. Liu W.T., Jing Y.Y., Yu G.F., Han Z.P., Yu D.D., Fan Q.M., et al. Toll like receptor 4 facilitates invasion and migration as a cancer stem cell marker in hepatocellular carcinoma. Cancer Lett 2015, 358:136-143.
26. Kelly M.G., Alvero A.B., Chen R., Silasi D.A., Abrahams V.M., Chan S., et al. TLR-4 signaling promotes tumor growth and paclitaxel chemoresistance in ovarian cancer. Cancer Res 2006, 66:3859-3868.
27. Fukumura D., Kashiwagi S., Jain R.K. The role of nitric oxide in tumour progression. Nat. Rev. Cancer 2006, 6:521-534.
28. Cheng H., Wang L., Mollica M., Re A.T., Wu S., Zuo L. Nitric oxide in cancer metastasis. Cancer Lett 2014, 353:1-7.
29. Kishikawa T., Otsuka M., Tan P.S., Ohno M., Sun X., Yoshikawa T., et al. Decreased miR122 in hepatocellular carcinoma leads to chemoresistance with increased arginine. Oncotarget 2015, 6:8339-8352.
30. Puglisi M.A., Cenciarelli C., Tesori V., Cappellari M., Martini M., Di Francesco A.M., et al. High nitric oxide production, secondary to inducible-nitric oxide synthase expression, is essential for regulation of the tumour-initiating properties of colon cancer stem cells. J. Pathol 2015, 236:479-490.
31. Ishak K.G., Glunz P.R. Hepatoblastoma and hepatocarcinoma in infancy and childhood. Report of 47 cases. Cancer 1967, 20:396-422.
32. Hsiao C.C., Kao Y.H., Huang S.C., Chuang J.H. Toll-like receptor-4 agonist inhibits motility and invasion of hepatoblastoma HepG2 cells in vitro. Pediatr. Blood Cancer 2013, 60:248-253.
33. Hsieh M.C., Hu W.P., Yu H.S., Wu W.C., Chang L.S., Kao Y.H., et al. A DC-81-indole conjugate agent suppresses melanoma A375 cell migration partially via interrupting VEGF production and stromal cell-derived factor-1alpha-mediated signaling. Toxicol. Appl. Pharmacol 2011, 255:150-159.
34. Kao Y.H., Yu C.L., Chang L.W., Yu H.S. Low concentrations of arsenic induce vascular endothelial growth factor and nitric oxide release and stimulate angiogenesis in vitro. Chem. Res. Toxicol 2003, 16:460-468.
35. Sokolowska M., Rokita H., Wlodek L. Activation of DNA biosynthesis in human hepatoblastoma HEPG2 cells by the nitric oxide donor, sodium nitroprusside. Fundam. Clin. Pharmacol 2003, 17:599-607.
36. Tang X.Y., Zhu Y.Q., Wei B., Wang H. Expression and functional research of TLR4 in human colon carcinoma. Am. J. Med. Sci 2010, 339:319-326.
37. Molteni M., Marabella D., Orlandi C., Rossetti C. Melanoma cell lines are responsive in vitro to lipopolysaccharide and express TLR-4. Cancer Lett 2006, 235:75-83.
38. Matsumura T., Ito A., Takii T., Hayashi H., Onozaki K. Endotoxin and cytokine regulation of toll-like receptor (TLR) 2 and TLR4 gene expression in murine liver and hepatocytes. J. Interferon Cytokine Res 2000, 20:915-921.
39. Nanbo A., Nishimura H., Muta T., Nagasawa S. Lipopolysaccharide stimulates HepG2 human hepatoma cells in the presence of lipopolysaccharide-binding protein via CD14. Eur. J. Biochem 1999, 260:183-191.
40. Luo J.H., Ren B., Keryanov S., Tseng G.C., Rao U.N., Monga S.P., et al. Transcriptomic and genomic analysis of human hepatocellular carcinomas and hepatoblastomas. Hepatology 2006, 44:1012-1024.
41. Fisher D.T., Appenheimer M.M., Evans S.S. The two faces of IL-6 in the tumor microenvironment. Semin. Immunol 2014, 26:38-47.
42. Yu L.X., Yan H.X., Liu Q., Yang W., Wu H.P., Dong W., et al. Endotoxin accumulation prevents carcinogen-induced apoptosis and promotes liver tumorigenesis in rodents. Hepatology 2010, 52:1322-1333.
43. Earl T.M., Nicoud I.B., Pierce J.M., Wright J.P., Majoras N.E., Rubin J.E., et al. Silencing of TLR4 decreases liver tumor burden in a murine model of colorectal metastasis and hepatic steatosis. Ann. Surg. Oncol 2009, 16:1043-1050.
44. Akita K., Okuno M., Enya M., Imai S., Moriwaki H., Kawada N., et al. Impaired liver regeneration in mice by lipopolysaccharide via TNF-alpha/kallikrein-mediated activation of latent TGF-beta. Gastroenterology 2002, 123:352-364.
45. Chen C.L., Tsukamoto H., Liu J.C., Kashiwabara C., Feldman D., Sher L., et al. Reciprocal regulation by TLR4 and TGF-beta in tumor-initiating stem-like cells. J. Clin. Invest 2013, 123:2832-2849.
46. Chew V., Tow C., Teo M., Wong H.L., Chan J., Gehring A., et al. Inflammatory tumour microenvironment is associated with superior survival in hepatocellular carcinoma patients. J. Hepatol 2010, 52:370-379.
47. Okamoto M., Oshikawa T., Tano T., Ohe G., Furuichi S., Nishikawa H., et al. Involvement of Toll-like receptor 4 signaling in interferon-gamma production and antitumor effect by streptococcal agent OK-432. J. Natl Cancer Inst 2003, 95:316-326.
48. Yu P., Cheng X., Guo J., Wang X. Toll-like receptors 2/4 agonists: a potential strategy for preventing invasion and metastasis of hepatocellular carcinoma. Gut 2010, 59:1447-1448. author reply 1448-1449.
49. Yu P., Cheng X., Du Y., Huang L., Dong R. TAK-242 can be the potential agents for preventing invasion and metastasis of hepatocellular carcinoma. Med. Hypotheses 2013, 81:653-655.
50. Wang Y., Tu Q., Yan W., Xiao D., Zeng Z., Ouyang Y., et al. CXC195 suppresses proliferation and inflammatory response in LPS-induced human hepatocellular carcinoma cells via regulating TLR4-MyD88-TAK1-mediated NF-kappaB and MAPK pathway. Biochem. Biophys. Res. Commun 2015, 456:373-379.
51. Guo H., Marroquin C.E., Wai P.Y., Kuo P.C. Nitric oxide-dependent osteopontin expression induces metastatic behavior in HepG2 cells. Dig. Dis. Sci 2005, 50:1288-1298.
52. Harmey J.H., Bucana C.D., Lu W., Byrne A.M., McDonnell S., Lynch C., et al. Lipopolysaccharide-induced metastatic growth is associated with increased angiogenesis, vascular permeability and tumor cell invasion. Int. J. Cancer 2002, 101:415-422.
53. Ying H., Da L., Yu-xiu S., Yu X., Li-xia L., Li-mei X., et al. TLR4 mediates MAPK-STAT3 axis activation in bladder epithelial cells. Inflammation 2013, 36:1064-1074.
54. Doan H.Q., Bowen K.A., Jackson L.A., Evers B.M. Toll-like receptor 4 activation increases Akt phosphorylation in colon cancer cells. Anticancer Res 2009, 29:2473-2478.
55. Hua D., Liu M.Y., Cheng Z.D., Qin X.J., Zhang H.M., Chen Y., et al. 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.
56. Jiang Z.C., Tang X.M., Zhao Y.R., Zheng L. A functional variant at miR-34a binding site in toll-like receptor 4 gene alters susceptibility to hepatocellular carcinoma in a Chinese Han population. Tumour Biol 2014, 35:12345-12352.
57. Tesniere A., Schlemmer F., Boige V., Kepp O., Martins I., Ghiringhelli F., et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010, 29:482-491.