Antitumorigenic effect of plumbagin by induction of SH2-containing protein tyrosine phosphatase 1 in human gastric cancer cells

International Journal of Oncology

Volumn 46, Issue 6, 2015, Pages 2380-2388

  Joo, Moon Kyung ^a   Park, Jong Jae ^a   Kim, Sung Ho ^a   Yoo, Hyo Soon ^a   Lee, Beom Jae ^a   Chun, Hoon Jai ^b   Lee, Sang Woo ^a   Bak, Young Tae ^a  

^a Korea University College of Medicine   (South Korea)

^b College of Medicine   (South Korea)

Author keywords

Janus kinase 2; Plumbagin; SH2 containing protein tyrosine phosphatase 1; Signal transducer and activator of transcription 3

Indexed keywords

CYCLIN D1; GELATINASE B; INTERLEUKIN 6; JANUS KINASE 2; PERVANADATE; PLUMBAGIN; PROTEIN BCL XL; PROTEIN TYROSINE PHOSPHATASE SHP 1; STAT3 PROTEIN; SURVIVIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH FACTOR 1; VASCULOTROPIN; ANTINEOPLASTIC AGENT; JAK2 PROTEIN, HUMAN; NAPHTHOQUINONE; PTPN6 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN;

ANNEXIN V ASSAY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; ASSAY; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; DOSE TIME EFFECT RELATION; DOWN REGULATION; GASTRIC CANCER CELL LINE; GENE EXPRESSION; HUMAN; HUMAN CELL; MATRIGEL INVASION ASSAY; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WOUND CLOSURE; WOUND CLOSURE ASSAY; WST-1 ASSAY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PHOSPHORYLATION; STOMACH TUMOR; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JANUS KINASE 2; NAPHTHOQUINONES; PHOSPHORYLATION; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STOMACH NEOPLASMS;

EID: 84928560787     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2015.2935     Document Type: Article

References (48)

1. Sandur SK, Ichikawa H, Sethi G, Ahn KS and Aggarwal BB: Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) suppresses NF-kappaB activation and NF-kappaB-regulated gene products through modulation of p65 and IkappaBalpha kinase activation, leading to potentiation of apoptosis induced by cytokine and chemotherapeutic agents. J Biol Chem 281: 17023-17033, 2006.
2. Sugie S, Okamoto K, Rahman KM, Tanaka T, Kawai K, Yamahara J and Mori H: Inhibitory effects of plumbagin and juglone on azoxymethane-induced intestinal carcinogenesis in rats. Cancer Lett 127: 177-183, 1998.
3. Kuo PL, Hsu YL and Cho CY: Plumbagin induces G2-M arrest and autophagy by inhibiting the AKT/mammalian target of rapamycin pathway in breast cancer cells. Mol Cancer Ther 5: 3209-3221, 2006.
4. Hsu YL, Cho CY, Kuo PL, Huang YT and Lin CC: Plumbagin (5-hydroxy-2-methyl-1,4-naphthoquinone) induces apoptosis and cell cycle arrest in A549 cells through p53 accumulation via c-Jun NH2-terminal kinase-mediated phosphorylation at serine 15 in vitro and in vivo. J Pharmacol Exp Ther 318: 484-494, 2006.
5. Wang CC, Chiang YM, Sung SC, Hsu YL, Chang JK and Kuo PL: Plumbagin induces cell cycle arrest and apoptosis through reactive oxygen species/c-Jun N-terminal kinase pathways in human melanoma A375.S2 cells. Cancer Lett 259: 82-98, 2008.
6. Powolny AA and Singh SV: Plumbagin-induced apoptosis in human prostate cancer cells is associated with modulation of cellular redox status and generation of reactive oxygen species. Pharm Res 25: 2171-2180, 2008.
7. Hafeez BB, Jamal MS, Fischer JW, Mustafa A and Verma AK: Plumbagin, a plant derived natural agent inhibits the growth of pancreatic cancer cells in in vitro and in vivo via targeting EGFR, Stat3 and NF-κB signaling pathways. Int J Cancer 131: 2175-2186, 2012.
8. Manu KA, Shanmugam MK, Rajendran P, Li F, Ramachandran L, Hay HS, Kannaiyan R, Swamy SN, Vali S, Kapoor S, et al: Plumbagin inhibits invasion and migration of breast and gastric cancer cells by downregulating the expression of chemokine receptor CXCR4. Mol Cancer 10: 107, 2011.
9. Li J, Shen L, Lu FR, Qin Y, Chen R, Li J, Li Y, Zhan HZ and He YQ: Plumbagin inhibits cell growth and potentiates apoptosis in human gastric cancer cells in vitro through the NF-κB signaling pathway. Acta Pharmacol Sin 33: 242-249, 2012.
10. Sandur SK, Pandey MK, Sung B and Aggarwal BB: 5-hydroxy-2-methyl-1,4-naphthoquinone, a vitamin K3 analogue, suppresses STAT3 activation pathway through induction of protein tyrosine phosphatase, SHP-1: Potential role in chemosensitization. Mol Cancer Res 8: 107-118, 2010.
11. Huang Z, Lee H, Lee E, Kang SK, Nam JM and Lee M: Responsive nematic gels from the self-assembly of aqueous nanofibres. Nat Commun 2: 459, 2011.
12. Dallol A, Agathanggelou A, Tommasi S, Pfeifer GP, Maher ER and Latif F: Involvement of the RASSF1A tumor suppressor gene in controlling cell migration. Cancer Res 65: 7653-7659, 2005.
13. Xiong H, Chen ZF, Liang QC, Du W, Chen HM, Su WY, Chen GQ, Han ZG and Fang JY: Inhibition of DNA methyltransferase induces G2 cell cycle arrest and apoptosis in human colorectal cancer cells via inhibition of JAK2/STAT3/STAT5 signalling. J Cell Mol Med 13: 3668-3679, 2009.
14. Lin MT, Lin BR, Chang CC, Chu CY, Su HJ, Chen ST, Jeng YM and Kuo ML: IL-6 induces AGS gastric cancer cell invasion via activation of the c-Src/RhoA/ROCK signaling pathway. Int J Cancer 120: 2600-2608, 2007.
15. Zhu BH, Chen HY, Zhan WH, Wang CY, Cai SR, Wang Z, Zhang CH and He YL: (-)-Epigallocatechin-3-gallate inhibits VEGF expression induced by IL-6 via Stat3 in gastric cancer. World J Gastroenterol 17: 2315-2325, 2011.
16. Rhee YH, Jeong SJ, Lee HJ, Lee HJ, Koh W, Jung JH, Kim SH and Sung-Hoon K: Inhibition of STAT3 signaling and induction of SHP1 mediate antiangiogenic and antitumor activities of ergosterol peroxide in U266 multiple myeloma cells. BMC Cancer 12: 28, 2012.
17. Lee JH, Chiang SY, Nam D, Chung WS, Lee J, Na YS, Sethi G and Ahn KS: Capillarisin inhibits constitutive and inducible STAT3 activation through induction of SHP-1 and SHP-2 tyrosine phosphatases. Cancer Lett 345: 140-148, 2014.
18. Jackson CB and Giraud AS: STAT3 as a prognostic marker in human gastric cancer. J Gastroenterol Hepatol 24: 505-507, 2009.
19. Kim JA, Lee EK, Park SJ, Kim ND, Hyun DH, Lee CG, Lee JH, Yang KM, Heo K and Son TG: Novel anti-cancer role of naphthazarin in human gastric cancer cells. Int J Oncol 40: 157-162, 2012.
20. Chen J, Wang J, Lin L, He L, Wu Y, Zhang L, Yi Z, Chen Y, Pang X and Liu M: Inhibition of STAT3 signaling pathway by nitidine chloride suppressed the angiogenesis and growth of human gastric cancer. Mol Cancer Ther 11: 277-287, 2012.
21. Jia Y, Liu D, Xiao D, Ma X, Han S, Zheng Y, Sun S, Zhang M, Gao H, Cui X, et al: Expression of AFP and STAT3 is involved in arsenic trioxide-induced apoptosis and inhibition of proliferation in AFP-producing gastric cancer cells. PLoS One 8: e54774, 2013.
22. Kim MJ, Nam HJ, Kim HP, Han SW, Im SA, Kim TY, Oh DY and Bang YJ: OPB-31121, a novel small molecular inhibitor, disrupts the JAK2/STAT3 pathway and exhibits an antitumor activity in gastric cancer cells. Cancer Lett 335: 145-152, 2013.
23. Katsha A, Arras J, Soutto M, Belkhiri A and El-Rifai W: AURKA regulates JAK2-STAT3 activity in human gastric and esophageal cancers. Mol Oncol 8: 1419-1428, 2014.
24. López-Ruiz P, Rodriguez-Ubreva J, Cariaga AE, Cortes MA and Colás B: SHP-1 in cell-cycle regulation. Anticancer Agents Med Chem 11: 89-98, 2011.
25. Zhang J, Somani AK and Siminovitch KA: Roles of the SHP-1 tyrosine phosphatase in the negative regulation of cell signalling. Semin Immunol 12: 361-378, 2000.
26. Wu C, Sun M, Liu L and Zhou GW: The function of the protein tyrosine phosphatase SHP-1 in cancer. Gene 306: 1-12, 2003.
27. Han Y, Amin HM, Franko B, Frantz C, Shi X and Lai R: Loss of SHP1 enhances JAK3/STAT3 signaling and decreases proteosome degradation of JAK3 and NPM-ALK in ALK+ anaplastic large-cell lymphoma. Blood 108: 2796-2803, 2006.
28. Oka T, Ouchida M, Koyama M, Ogama Y, Takada S, Nakatani Y, Tanaka T, Yoshino T, Hayashi K, Ohara N, et al: Gene silencing of the tyrosine phosphatase SHP1 gene by aberrant methylation in leukemias/lymphomas. Cancer Res 62: 6390-6394, 2002.
29. Koyama M, Oka T, Ouchida M, Nakatani Y, Nishiuchi R, Yoshino T, Hayashi K, Akagi T and Seino Y: Activated proliferation of B-cell lymphomas/leukemias with the SHP1 gene silencing by aberrant CpG methylation. Lab Invest 83: 1849-1858, 2003.
30. Chim CS, Fung TK, Cheung WC, Liang R and Kwong YL: SOCS1 and SHP1 hypermethylation in multiple myeloma: Implications for epigenetic activation of the Jak/STAT pathway. Blood 103: 4630-4635, 2004.
31. Ruchusatsawat K, Wongpiyabovorn J, Shuangshoti S, Hirankarn N and Mutirangura A: SHP-1 promoter 2 methylation in normal epithelial tissues and demethylation in psoriasis. J Mol Med (Berl) 84: 175-182, 2006.
32. Bernal C, Aguayo F, Villarroel C, Vargas M, Díaz I, Ossandon FJ, Santibáñez E, Palma M, Aravena E, Barrientos C, et al: Reprimo as a potential biomarker for early detection in gastric cancer. Clin Cancer Res 14: 6264-6269, 2008.
33. Ksiaa F, Ziadi S, Amara K, Korbi S and Trimeche M: Biological significance of promoter hypermethylation of tumor-related genes in patients with gastric carcinoma. Clin Chim Acta 404: 128-133, 2009.
34. Giraud AS, Menheniott TR and Judd LM: Targeting STAT3 in gastric cancer. Expert Opin Ther Targets 16: 889-901, 2012.
35. Souma Y, Nishida T, Serada S, Iwahori K, Takahashi T, Fujimoto M, Ripley B, Nakajima K, Miyazaki Y, Mori M, et al: Antiproliferative effect of SOCS-1 through the suppression of STAT3 and p38 MAPK activation in gastric cancer cells. Int J Cancer 131: 1287-1296, 2012.
36. Inagaki-Ohara K, Mayuzumi H, Kato S, Minokoshi Y, Otsubo T, Kawamura YI, Dohi T, Matsuzaki G and Yoshimura A: Enhancement of leptin receptor signaling by SOCS3 deficiency induces development of gastric tumors in mice. Oncogene 33: 74-84, 2014.
37. Tenev T, Böhmer SA, Kaufmann R, Frese S, Bittorf T, Beckers T and Böhmer FD: Perinuclear localization of the protein-tyrosine phosphatase SHP-1 and inhibition of epidermal growth factor-stimulated STAT1/3 activation in A431 cells. Eur J Cell Biol 79: 261-271, 2000.
38. Kim H and Baumann H: Dual signaling role of the protein tyrosine phosphatase SHP-2 in regulating expression of acute-phase plasma proteins by interleukin-6 cytokine receptors in hepatic cells. Mol Cell Biol 19: 5326-5338, 1999.
39. Gunaje JJ and Bhat GJ: Involvement of tyrosine phosphatase PTP1D in the inhibition of interleukin-6-induced Stat3 signaling by alpha-thrombin. Biochem Biophys Res Commun 288: 252-257, 2001.
40. Irie-Sasaki J, Sasaki T, Matsumoto W, Opavsky A, Cheng M, Welstead G, Griffiths E, Krawczyk C, Richardson CD, Aitken K, et al: CD45 is a JAK phosphatase and negatively regulates cytokine receptor signalling. Nature 409: 349-354, 2001.
41. Lee IO, Kim JH, Choi YJ, Pillinger MH, Kim SY, Blaser MJ and Lee YC: Helicobacter pylori CagA phosphorylation status determines the gp130-activated SHP2/ERK and JAK/STAT signal transduction pathways in gastric epithelial cells. J Biol Chem 285: 16042-16050, 2010.
42. Jiang J, Jin MS, Kong F, Wang YP, Jia ZF, Cao DH, Ma HX, Suo J and Cao XY: Increased expression of tyrosine phosphatase SHP-2 in Helicobacter pylori-infected gastric cancer. World J Gastroenterol 19: 575-580, 2013.
43. Kim JS, Shin OR, Kim HK, Cho YS, An CH, Lim KW and Kim SS: Overexpression of protein phosphatase non-receptor type 11 (PTPN11) in gastric carcinomas. Dig Dis Sci 55: 1565-1569, 2010.
44. Jiménez DJ, Montaña JS, Alvarez D and Baena S: A novel cold active esterase derived from Colombian high Andean forest soil metagenome. World J Microbiol Biotechnol 28: 361-370, 2012.
45. Gu X, Cun Y, Li M, Qing Y, Jin F, Zhong Z, Dai N, Qian C, Sui J and Wang D: Human apurinic/apyrimidinic endonuclease siRNA inhibits the angiogenesis induced by X-ray irradiation in lung cancer cells. Int J Med Sci 10: 870-882, 2013.
46. McTavish N, Copeland LA, Saville MK, Perkins ND and Spruce BA: Proenkephalin assists stress-activated apoptosis through transcriptional repression of NF-kappaB- and p53-regulated gene targets. Cell Death Differ 14: 1700-1710, 2007.
47. Takei Y, Kadomatsu K, Yuzawa Y, Matsuo S and Muramatsu T: A small interfering RNA targeting vascular endothelial growth factor as cancer therapeutics. Cancer Res 64: 3365-3370, 2004.
48. Rivera MN, Kim WJ, Wells J, Stone A, Burger A, Coffman EJ, Zhang J and Haber DA: The tumor suppressor WTX shuttles to the nucleus and modulates WT1 activity. Proc Natl Acad Sci USA 106: 8338-8343, 2009.