Ginsenoside Rg3 induces FUT4-mediated apoptosis in H. pylori CagA-treated gastric cancer cells by regulating SP1 and HSF1 expressions

Toxicology in Vitro

Volumn 31, Issue , 2016, Pages 158-166

  Aziz, Faisal ^a   Wang, Xiaoqi ^b   Liu, Jiwei ^a   Yan, Qiu ^a  

^a DALIAN MEDICAL UNIVERSITY   (China)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Fucosyltransferase IV; Gastric cancer; Helicobacter pylori CagA; HSF1; Rg3; SP1

Indexed keywords

CAGA PROTEIN; CASPASE 3; CASPASE 8; CASPASE 9; FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE 4; GINSENOSIDE RG 3; HEAT SHOCK TRANSCRIPTION FACTOR 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; CAGA PROTEIN, HELICOBACTER PYLORI; CD15 ANTIGEN; DNA BINDING PROTEIN; FUT4 PROTEIN, HUMAN; GINSENOSIDE; HEAT SHOCK TRANSCRIPTION FACTOR; SP1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GASTRIC CANCER CELL LINE; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; PROTEIN EXPRESSION; SGC 7901 CELL LINE; STOMACH CANCER; UPREGULATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; STOMACH TUMOR; TUMOR CELL LINE;

ANTIGENS, BACTERIAL; ANTIGENS, CD15; ANTINEOPLASTIC AGENTS; APOPTOSIS; BACTERIAL PROTEINS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; FUCOSYLTRANSFERASES; GINSENOSIDES; HUMANS; SP1 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS; TRANSCRIPTION FACTORS;

EID: 84949994685     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2015.09.025     Document Type: Article

References (62)

1. Ahn J, Lee JS, Yang KM. Ultrafine particles of Ulmus davidiana var, 2014. Japonica induce apoptosis of gastric cancer cells via activation of caspase and endoplasmic reticulum stress, Arch Pharm Res. [Epub ahead of print].
2. Aziz F., Qiu Y. The role of anti-LeY antibody in the downregulation of MAPKs/COX-2 pathway in gastric cancer. Curr. Drug Targets 2014, 15:469-476.
3. Aziz F., Sherwani S.K., Akhtar S.S., Kazmi S.U. Development of an in-house enzyme-linked immunosorbent assay based on surface whole cell antigen for diagnosis of Helicobacter pylori infection in patients with gastroduodenal ulcer disease. World J. Microbiol. Biotechnol. 2014, 30:305-315.
4. Aziz F., Yang X., Wang X., Yan Q. Anti-LeY antibody enhances therapeutic efficacy of celecoxib against gastric cancer by downregulation ofMAPKs/COX-2 signaling pathway: correlation with clinical study. J. Cancer Res. Clin. Oncol. 2014, 141(7):1221-1235.
5. Aziz F., Chen X., Yang X., Yan Q. Prevalence and correlation with clinical diseases of Helicobacter pylori cagA and vacA genotype among gastric patients from Northeast China. Biomed. Res. Int. 2014, 2014:142980.
6. Bauer K., Porzsolt F., Henne-Bruns D. Can perioperative chemotherapy for advanced gastric cancer be recommended on the basis of current research? A critical analysis. J. Gastric Cancer 2014, 14:39-46.
7. Beck I.M., Drebert Z.J., Hoya-Arias R., Bahar A.A., Devos M., Clarisse D., et al. Compound A, a selective glucocorticoid receptor modulator, enhances heat shock protein Hsp70 gene promoter activation. PLoS ONE 2013, 8.
8. Björk J.K., Åkerfelt M., Joutsen J., Puustinen M.C., Cheng F., Sistonen L., et al. Heat-shock factor 2 is a suppressor of prostate cancer invasion. Oncogene 2015, 10.1038/onc.2015.241.
9. Björkholm B., Falk P., Engstrand L., Nyrén O. Helicobacter pylori: resurrection of the cancer link. J. Intern. Med. 2003, 253:2-19.
10. Cen H., Zheng S., Fang Y.M., Tang X.P., Dong Q. Induction of HSF1 expression is associated with sporadic colorectal cancer. World J. Gastroenterol. 2004, 10:3122-3126.
11. Cui Q.L., Shao M., Shu Q.J. Study on inhibitory effect of aqueous extract of Taxus chinensis var. mairei on growth of A549 lung cancer xenografts in nude mice and its mechanism. Zhongguo Zhong Yao Za Zhi 2013, 38:3549-3553.
12. Geng M., Wang L., Li P. Correlation between chemosensitivity to anticancer drugs and Bcl-2 expression in gastric cancer. Int. J. Clin. Exp. Pathol. 2013, 6:2554-2559.
13. Gomes J., Magalhães A., Carvalho A.S., Hernandez G.E., Papp S.L., Head S.R., et al. Glycophenotypic alterations induced by Pteridium aquilinum in mice gastric mucosa: synergistic effect with Helicobacter pylori infection. PLoS ONE 2012, 7.
14. Gomes C., Osório H., Pinto M.T., Campos D., Oliveira M.J., Reis C.A. Expression of ST3GAL4 leads to SLe(x) expression and induces c-Met activation and an invasive phenotype in gastric carcinoma cells. PLoS One 2013, 8(6).
15. Hartgrink H.H., van de Velde C.J., Putter H., et al. Extended lymph node dissection for gastric cancer: who may benefit? Final results of the randomized Dutch gastric cancer group trial. J. Clin. Oncol. 2004, 22:2069-2077.
16. Hatakeyama M., Higashi H. Helicobacter pylori CagA: a new paradigm for bacterial carcinogenesis. Cancer Sci. 2005, 96:35-43.
17. Ilver D., Arnqvist A., Ogren J., Frick I.M., Kersulyte D., Incecik E.T., et al. Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998, 279:73-77.
18. Jian J., Hu Z.F., Huang Y. Effect of ginsenoside Rg3 on Pim-3 and Bad proteins in human pancreatic cancer cell line PANC-1. Ai Zheng 2009, 28:461-465.
19. Kanai M., Wei D., Li Q., Jia Z., Ajani J., Le X., et al. Loss of Kruppel-like factor 4 expression contributes to SP1 overexpression and human gastric cancer development and progression. Clin. Cancer Res. 2006, 12:6395-6402.
20. Kang L.J., Choi Y.J., Lee S.G. Stimulation of TRAF6/TAK1 degradation and inhibition of JNK/AP-1 signalling by ginsenoside Rg3 attenuates hepatitis B virus replication. Int. J. Biochem. Cell Biol. 2013, 45:2612-2621.
21. Kim B.J., Nah S.Y., Jeon J.H., So I., Kim S.J. Transient receptor potential melastatin 7 channels are involved in ginsenoside Rg3-induced apoptosis in gastric cancer cells. Basic Clin. Pharmacol. Toxicol. 2011, 109:233-239.
22. Kim J.W., Jung S.Y., Kwon Y.H., Lee J.H., Lee Y.M., Lee B.Y., Kwon S.M. Ginsenoside Rg3 attenuates tumor angiogenesis via inhibiting bioactivities of endothelial progenitor cells. Cancer Biol. Ther. 2012, 13:504-515.
23. Lee J.O., Moon J.W., Lee S.K., Kim S.M., Kim N., Ko S.G., et al. Rhus verniciflua extract modulates survival of MCF-7 breast cancer cells through the modulation of AMPK-pathway. Biol. Pharm. Bull. 2014, 37(5):794-801.
24. Li T., Chen C.L., Wang J.D., Cui S.D., Cui D.Y., Guo W. Expression of heat-shock transcription factor 1 and X-linked inhibitor of apoptosis protein-associated factor-1 in gastrointestinal cancer. Nan Fang Yi Ke Da Xue Xue Bao 2008, 28:487-490.
25. Li S., Wang Q., Qiang Q., Shan H., Shi M., Chen B., et al. Sp1-mediated transcriptional regulation of MALAT1 plays a critical role in tumor. J. Cancer Res. Clin. Oncol. 2015, 141(11):1909-1920.
26. Lin W.C., Tsai H.F., Kuo S.H., Wu M.S., Lin C.W., Hsu P.I., et al. Translocation of Helicobacter pylori CagA into human B lymphocytes, the origin of mucosa-associated lymphoid tissue lymphoma. Cancer Res. 2010, 70:5740-5748.
27. Lin W., Zheng L., Zhuang Q., Zhao J., Cao Z., Zeng J., et al. Spica prunellae promotes cancer cell apoptosis, inhibits cell proliferation and tumor angiogenesis in a mouse model of colorectal cancer via suppression of stat3 pathway. BMC Complement. Altern Med. 2013, 13:144.
28. Liu J.P., Lu D., Zhao Y., Li P.Y., Li X. A new semisynthetic ocotillol-type saponin and resuscitation of haemorrhagic shock. J. Asian Nat. Prod. Res. 2007, 9:103-113.
29. Liu C., Pan Y., Wang X., Lu J., Huang B., Li X. Activation of RASSF2A by p300 induces late apoptosis through histone hyperacetylation. Cell Biol. Int. 2010, 34:1133-1139.
30. Menaker R.J., Ceponis P.J., Jones N.L. Helicobacter pylori induces apoptosis of macrophages in association with alterations in the mitochondrial pathway. Infect. Immun. 2004, 72:89-98.
31. Mendillo M.L., Santagata S., Koeva M., Bell G.W., Hu R., Tamimi R.M., et al. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers. Cell 2012, 150:549-562.
32. Meng D., Newburg D.S., Young C., Baker A., Tonkonogy S.L., Sartor R.B., et al. Bacterial symbionts induce a FUT2-dependent fucosylated niche on colonic epithelium via ERK and JNK signaling. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:80-87.
33. Mimuro H., Suzuki T., Nagai S., Rieder G., Suzuki M., Nagai T., et al. Helicobacter pylori dampens gut epithelial self-renewal by inhibiting apoptosis, a bacterial strategy to enhance colonization of the stomach. Cell Host Microbe 2007, 2:250-263.
34. Miyoshi E., Moriwaki K., Nakagawa T. Biological function of fucosylation in cancer biology. J. Biochem. 2008, 14:725-729.
35. Moriwaki K., Miyoshi E. Fucosylation and gastrointestinal cancer. World J. Hepatol. 2010, 2(4):151-161.
36. Pan X.Y., Guo H., Han J., Hao F., An Y., Xu Y., et al. Ginsenoside Rg3 attenuates cell migration via inhibition of aquaporin 1 expression in PC-3M prostate cancer cells. Eur. J. Pharmacol. 2012, 683:27-34.
37. Park S.A., Kim E.H., Na H.K., Surh Y.J. KG-135 inhibits COX-2 expression by blocking the activation of JNK and AP-1 in phorbol ester-stimulated human breast epithelial cells. Ann. N. Y. Acad. Sci. 2007, 1095:545-553. (2007 Jan).
38. Cancer Incidence in Five Continents 2002, Vol. VIII(International Agency for Research on Cancer).
39. Reis C.A., Osorio H., Silva L., Gomes C., David L. Alteration in glycosylation as biomarkers for cancer detection. J. Clin. Pathol. 2010, 3(4):322-329.
40. Schulz R., Streller F., Scheel A.H., Rüschoff J., Reinert M.C., Dobbelstein M., et al. HER2/ErbB2 activates HSF1 and thereby controls HSP90 clients including MIF in HER2-overexpressing breast cancer. Cell Death Dis. 2014, 2(5):e980.
41. Shan X., Fu Y.S., Aziz F., Wang X.Q., Yang Q., Liu J.W. Ginsenoside Rg3 inhibits melanoma cell proliferation through down regulation of histone deacetylase 3 (HDAC3) and increase of p53 acetylation. PLoS ONE 2014, 9.
42. Shan X., Aziz F., Tian L.L., Wang X.Q., Yan Q., Liu J.W. Ginsenoside Rg3-induced EGFR/MAPK pathway deactivation inhibits melanoma cell proliferation by decreasing FUT4/LeY expression. Int. J. Oncol. 2015, 46(4):1667-1676.
43. Songun I., Putter H., Kranenbarg E.M., et al. Surgical treatment of gastric cancer: 15-year follow-up results of the randomised nationwide Dutch D1D2 trial. Lancet Oncol. 2010, 11:439-449.
44. Targosz A., Brzozowski T., Pierzchalski P., Szczyrk U., Ptak-Belowska A., Konturek S.J., Pawlik W. Helicobacter pylori promotes apoptosis, activates cyclooxygenase (COX)-2 and inhibits heat shock protein HSP70 in gastric cancer epithelial cells. Inflamm. Res. 2012, 61:955-966.
45. Wang L., Wei D., Huang S., Peng Z., Le X., Wu T.T., et al. Transcription factor SP1 expression is a significant predictor of survival in human gastric cancer. Clin. Cancer Res. 2003, 9:6371-6380.
46. Wang J., He H., Yu L., Xia H.H., Lin M.C., Gu Q., et al. HSF1 down-regulates XAF1 through transcriptional regulation. J. Biol. Chem. 2006, 28:2451-2459.
47. Wang T., Xuan X., Li M., Gao P., Zheng Y., Zang W., Zhao G. Astragalus saponins affect proliferation, invasion and apoptosis of gastric cancer BGC-823 cells. Diagn. Pathol. 2013, 8:179.
48. Xu Y., Zhao F., Wang Z., Song Y., Luo Y., Zhang X., et al. MicroRNA-335 acts as a metastasis suppressor in gastric cancer by targeting Bcl-w and specificity protein 1. Oncogene 2012, 31:1398-1407.
49. Xu T.P., Liu X.X., Xia R., Yin L., Kong R., Chen W.M., et al. SP1-induced upregulation of the long noncoding RNA TINCR regulates cell proliferation and apoptosis by affecting KLF2 mRNA stability in gastric cancer. Oncogene 2015, 10.1038/onc.2015.18.
50. Xue G., Zou X., Zhou J.Y., Sun W., Wu J., Xu J.L., Wang R.P. Raddeanin A induces human gastric cancer cells apoptosis and inhibits their invasion in vitro. Biochem. Biophys. Res. Commun. 2013, 439:196-202.
51. Yan X., Lin Y., Liu S., Aziz F., Yan Q. Fucosyltransferase IV (FUT4) as an effective biomarker for the diagnosis of breast cancer. Biomed. Pharmacother. 2015, 70:299-304.
52. Yang X., Liu S., Liu Y., Liu J., Liu T., Wang X., Yan Q. Overexpression of fucosyltransferase IV promotes A431 cell proliferation through activation MAPK and P13K/Akt signaling pathways. J. Cell. Physiol. 2010, 225:612-619.
53. Yang X., Wang J., Liu S., Yan Q. HSF1 and SP1are involved in the regulation of FUT4 gene expression and cell proliferation in breast cancer cells. J. Cell. Biochem. 2014, 115:168-178.
54. Yao Y., Hu J., Shen Z., Yao R., Liu S., Li Y., et al. MiR-200b expression in breast cancer: a prognostic marker and act on cell proliferation and apoptosis by targeting Sp1. J. Cell. Mol. Med. 2015, 19:760-769.
55. Ye Y.W., Hu S., Shi Y.Q., Zhang X.F., Zhou Y., Zhao C.L., et al. Combination of the FGFR4 inhibitor PD173074 and 5-fluorouracil reduces proliferation and promotes apoptosis in gastric cancer. Oncol. Rep. 2013, 30:2777-2784.
56. Yih L.H., Hsu N.C., Kuo H.H., Wu Y.C. Inhibition of the heat shock response by PI103 enhances the cytotoxicity of arsenic trioxide. Toxicol. Sci. 2012, 128:126-136.
57. Yoshima T., Yura T., Yanagi H. Heat shock factor 1 mediates hemin-induced hsp70 gene transcription in K562 erythroleukemia cells. Biol. Chem. 1998, 273:25466-25471.
58. Zhang J., Zhu Z.G., Ji J., Yuan F., Yu Y.Y., Liu B.Y., Lin Y.Z. Transcription factor SP1 expression in gastric cancer and its relationship to long-term prognosis. World J. Gastroenterol. 2005, 11:2213-2217.
59. Zhang Z., Sun P., Liu J., Fu L., Yan J., Liu Y., et al. Suppression of FUT1/FUT4 expression by siRNA inhibits tumor growth. Biochim Biophys Acta. 2008, 1783(2):287-296.
60. Zhang C., Liu L., Yu Y., Chen B., Tang C., Li X. Antitumor effects of ginsenoside Rg3 on human hepatocellular carcinoma cells. Mol. Med. Rep. 2012, 5:1295-1298.
61. Zhao Y., Zhang W., Guo Z., Ma F., Wu Y., Bai Y., et al. Inhibition of the transcription factor SP1 suppresses colon cancer stem cell growth and induces apoptosis in vitro and in nude mouse xenografts. Oncol. Rep. 2013, 30:1782-1792.
62. Zhu Y., Zhong X., Zheng S., Du Q., Xu W. Transformed immortalized gastric epithelial cells by virulence factor cagA of Helicobacter pylori through Erk mitogen-activated protein kinase pathway. Oncogene 2005, 24:3886-3895.