Arctigenin enhances chemosensitivity of cancer cells to cisplatin through inhibition of the STAT3 signaling pathway

Journal of Cellular Biochemistry

Volumn 112, Issue 10, 2011, Pages 2837-2849

  Yao, Xiangyang ^a   Zhu, Fenfen ^a   Zhao, Zhihui ^a   Liu, Chang ^a   Luo, Lan ^b   Yin, Zhimin ^a  

^a NANJING NORMAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

arctigenin; chemosensitivity; cisplatin; STAT3

Indexed keywords

ARCTIGENIN; CISPLATIN; CYCLIN D1; INTERLEUKIN 6; JANUS KINASE 1; JANUS KINASE 2; MYC PROTEIN; PERVANADATE; PROTEIN BCL 2; PROTEIN MCL 1; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE SHP 2; STAT3 PROTEIN;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE G1 PHASE; CELL DEATH; CHEMOSENSITIVITY; DOWN REGULATION; DRUG POTENTIATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; CISPLATIN; CYCLIN D1; FLOW CYTOMETRY; FURANS; G1 PHASE; HELA CELLS; HEP G2 CELLS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; JANUS KINASE 1; JANUS KINASE 2; LIGNANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

ARCTIUM LAPPA; IPOMOEA; TORREYA NUCIFERA;

EID: 79960178328     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23198     Document Type: Article

References (54)

1. Aggarwal BB, Kunnumakkara AB, Harikumar KB, Gupta SR, Tharakan ST, Koca C, Dey S, Sung B,. 2009. Signal transducer and activator of transcription-3, inflammation, and cancer: How intimate is the relationship? Ann NY Acad Sci 1171: 59-76.
2. Ahn KS, Sethi G, Sung B, Goel A, Ralhan R, Aggarwal BB,. 2008. Guggulsterone, a farnesoid X receptor antagonist, inhibits constitutive and inducible STAT3 activation through induction of a protein tyrosine phosphatase SHP-1. Cancer Res 68: 4406-4415.
3. Aziz MH, Hafeez BB, Sand JM, Pierce DB, Aziz SW, Dreckschmidt NE, Verma AK,. 2010. Protein kinase Cvarepsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene 29: 3100-3109.
4. Barre B, Vigneron A, Perkins N, Roninson IB, Gamelin E, Coqueret O,. 2007. The STAT3 oncogene as a predictive marker of drug resistance. Trends Mol Med 13: 4-11. (Pubitemid 46027724)
5. Bhattacharya S, Schindler C,. 2003. Regulation of Stat3 nuclear export. J Clin Invest 111: 553-559. (Pubitemid 36228012)
6. Bhattacharya S, Ray RM, Johnson LR,. 2005. STAT3-mediated transcription of Bcl-2, Mcl-1 and c-IAP2 prevents apoptosis in polyamine-depleted cells. Biochem J 392: 335-344. (Pubitemid 41796522)
7. Bowman T, Garcia R, Turkson J, Jove R,. 2000. STATs in oncogenesis. Oncogene 19: 2474-2488. (Pubitemid 30339203)
8. Catlett-Falcone R, Landowski TH, Oshiro MM, Turkson J, Levitzki A, Savino R, Ciliberto G, Moscinski L, Fernandez-Luna JL, Nunez G, Dalton WS, Jove R,. 1999. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity 10: 105-115. (Pubitemid 29077388)
9. Chen R-H, Chang M-C, Su Y-H, Tsai Y-T, Kuo M-L,. 1999. Interleukin-6 inhibits transforming growth factor-β-induced apoptosis through the phosphatidylinositol 3-kinase/Akt and signal transducers and activators of transcription 3 pathways. J Biol Chem 274: 23013-23019.
10. Cho MK, Park JW, Jang YP, Kim YC, Kim SG,. 2002. Potent inhibition of lipopolysaccharide-inducible nitric oxide synthase expression by dibenzylbutyrolactone lignans through inhibition of I-kappa B alpha phosphorylation and of p65 nuclear translocation in macrophages. Int Immunopharmacol 2: 105-116. (Pubitemid 33086808)
11. Daino H, Matsumura I, Takada K, Odajima J, Tanaka H, Ueda S, Shibayama H, Ikeda H, Hibi M, Machii T, Hirano T, Kanakura Y,. 2000. Induction of apoptosis by extracellular ubiquitin in human hematopoietic cells: Possible involvement of STAT3 degradation by proteasome pathway in interleukin 6-dependent hematopoietic cells. Blood 95: 2577-2585. (Pubitemid 30210536)
12. Decker T, Kovarik P,. 2000. Serine phosphorylation of STATs. Oncogene 19: 2628-2637. (Pubitemid 30339219)
13. Digicaylioglu M, Lipton SA,. 2001. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-[kappa]B signalling cascades. Nature 412: 641-647. (Pubitemid 32772276)
14. Epling-Burnette PK, Liu JH, Catlett-Falcone R, Turkson J, Oshiro M, Kothapalli R, Li Y, Wang JM, Yang-Yen HF, Karras J, Jove R, Loughran TP, Jr., 2001. Inhibition of STAT3 signaling leads to apoptosis of leukemic large granular lymphocytes and decreased Mcl-1 expression. J Clin Invest 107: 351-362.
15. Garcia R, Bowman TL, Niu G, Yu H, Minton S, Muro-Cacho CA, Cox CE, Falcone R, Fairclough R, Parsons S, Laudano A, Gazit A, Levitzki A, Kraker A, Jove R,. 2001. Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells. Oncogene 20: 2499-2513. (Pubitemid 32531347)
16. Han Y, Amin HM, Franko B, Frantz C, Shi X, Lai R,. 2006. 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.
17. Jaganathan S, Yue P, Turkson J,. 2010. Enhanced sensitivity of pancreatic cancer cells to concurrent inhibition of aberrant signal transducer and activator of transcription 3 and epidermal growth factor receptor or Src. J Pharmacol Exp Ther 333: 373-381.
18. Kelland L,. 2007. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 7: 573-584. (Pubitemid 47106628)
19. Kim JY, Hwang JH, Cha MR, Yoon MY, Son ES, Tomida A, Ko B, Song SW, Shin-Ya K, Hwang YI, Park HR,. 2010. Arctigenin blocks the unfolded protein response and shows therapeutic antitumor activity. J Cell Physiol 224: 33-40.
20. Kiuchi N, Nakajima K, Ichiba M, Fukada T, Narimatsu M, Mizuno K, Hibi M, Hirano T,. 1999. STAT3 is required for the gp130-mediated full activation of the c-myc gene. J Exp Med 189: 63-73. (Pubitemid 29047027)
21. Krasilnikov M, Ivanov VN, Dong J, Ronai Z,. 2003. ERK and PI3K negatively regulate STAT-transcriptional activities in human melanoma cells: Implications towards sensitization to apoptosis. Oncogene 22: 4092-4101. (Pubitemid 36819649)
22. Lee H, Herrmann A, Deng JH, Kujawski M, Niu G, Li Z, Forman S, Jove R, Pardoll DM, Yu H,. 2009. Persistently activated Stat3 maintains constitutive NF-kappaB activity in tumors. Cancer Cell 15: 283-293.
23. Leslie K, Lang C, Devgan G, Azare J, Berishaj M, Gerald W, Kim YB, Paz K, Darnell JE, Albanese C, Sakamaki T, Pestell R, Bromberg J,. 2006. Cyclin D1 is transcriptionally regulated by and required for transformation by activated signal transducer and activator of transcription 3. Cancer Res 66: 2544-2552.
24. Li F, Fernandez PP, Rajendran P, Hui KM, Sethi G,. 2010a. Diosgenin, a steroidal saponin, inhibits STAT3 signaling pathway leading to suppression of proliferation and chemosensitization of human hepatocellular carcinoma cells. Cancer Lett 292: 197-207.
25. Li F, Rajendran P, Sethi G,. 2010b. Thymoquinone inhibits proliferation, induces apoptosis and chemosensitizes human multiple myeloma cells through suppression of signal transducer and activator of transcription 3 activation pathway. Br J Pharmacol 161: 541-554.
26. Liu H, Ma Y, Cole SM, Zander C, Chen KH, Karras J, Pope RM,. 2003. Serine phosphorylation of STAT3 is essential for Mcl-1 expression and macrophage survival. Blood 102: 344-352. (Pubitemid 36759675)
27. Liu T, Peng H, Zhang M, Deng Y, Wu Z,. 2010. Cucurbitacin B, a small molecule inhibitor of the Stat3 signaling pathway, enhances the chemosensitivity of laryngeal squamous cell carcinoma cells to cisplatin. Eur J Pharmacol 641: 15-22.
28. Nam S, Buettner R, Turkson J, Kim D, Cheng JQ, Muehlbeyer S, Hippe F, Vatter S, Merz KH, Eisenbrand G, Jove R,. 2005. Indirubin derivatives inhibit Stat3 signaling and induce apoptosis in human cancer cells. Proc Natl Acad Sci USA 102: 5998-6003. (Pubitemid 40594244)
29. Ohtani T, Ishihara K, Atsumi T, Nishida K, Kaneko Y, Miyata T, Itoh S, Narimatsu M, Maeda H, Fukada T, Itoh M, Okano H, Hibi M, Hirano T,. 2000. Dissection of signaling cascades through gp130 in vivo: Reciprocal roles for STAT3- and SHP2-mediated signals in immune responses. Immunity 12: 95-105. (Pubitemid 30069218)
30. Pao LI, Badour K, Siminovitch KA, Neel BG,. 2007. Nonreceptor protein-tyrosine phosphatases in immune cell signaling. Annu Rev Immunol 25: 473-523. (Pubitemid 46697915)
31. Real PJ, Sierra A, De Juan A, Segovia JC, Lopez-Vega JM, Fernandez-Luna JL,. 2002. Resistance to chemotherapy via Stat3-dependent overexpression of Bcl-2 in metastatic breast cancer cells. Oncogene 21: 7611-7618. (Pubitemid 35398808)
32. Reich NC, Liu L,. 2006. Tracking STAT nuclear traffic. Nat Rev Immunol 6: 602-612. (Pubitemid 44134093)
33. Saydmohammed M, Joseph D, Syed V,. 2010. Curcumin suppresses constitutive activation of STAT-3 by up-regulating protein inhibitor of activated STAT-3 (PIAS-3) in ovarian and endometrial cancer cells. J Cell Biochem 110: 447-456.
34. Selvendiran K, Koga H, Ueno T, Yoshida T, Maeyama M, Torimura T, Yano H, Kojiro M, Sata M,. 2006. Luteolin promotes degradation in signal transducer and activator of transcription 3 in human hepatoma cells: An implication for the antitumor potential of flavonoids. Cancer Res 66: 4826-4834.
35. Shi R-X, Ong C-N, Shen H-M,. 2005. Protein kinase C inhibition and X-linked inhibitor of apoptosis protein degradation contribute to the sensitization effect of luteolin on tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in cancer cells. Cancer Res 65: 7815-7823. (Pubitemid 41297257)
36. Shin D-S, Kim H-N, Shin KD, Yoon YJ, Kim S-J, Han DC, Kwon B-M,. 2009. Cryptotanshinone inhibits constitutive signal transducer and activator of transcription 3 function through blocking the dimerization in DU145 prostate cancer cells. Cancer Res 69: 193-202.
37. Sims JT, Ganguly S, Fiore LS, Holler CJ, Park ES, Plattner R,. 2009. STI571 sensitizes breast cancer cells to 5-fluorouracil, cisplatin and camptothecin in a cell type-specific manner. Biochem Pharmacol 78: 249-260.
38. Song JI, Grandis JR,. 2000. STAT signaling in head and neck cancer. Oncogene 19: 2489-2495. (Pubitemid 30339204)
39. Song H, Sondak VK, Barber DL, Reid TJ, Lin J,. 2004. Modulation of Janus kinase 2 by cisplatin in cancer cells. Int J Oncol 24: 1017-1026.
40. Turkson J, Zhang S, Palmer J, Kay H, Stanko J, Mora LB, Sebti S, Yu H, Jove R,. 2004. Inhibition of constitutive signal transducer and activator of transcription 3 activation by novel platinum complexes with potent antitumor activity. Mol Cancer Ther 3: 1533-1542. (Pubitemid 40136708)
41. Turkson J, Zhang S, Mora LB, Burns A, Sebti S, Jove R,. 2005. A novel platinum compound inhibits constitutive Stat3 signaling and induces cell cycle arrest and apoptosis of malignant cells. J Biol Chem 280: 32979-32988. (Pubitemid 41368347)
42. Wen Z, Zhong Z, Darnell JE, Jr., 1995. Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82: 241-250.
43. Wormald S, Hilton DJ,. 2004. Inhibitors of cytokine signal transduction. J Biol Chem 279: 821-824. (Pubitemid 38082600)
44. Wu ZZ, Lu HP, Chao CC,. 2010. Identification and functional analysis of genes which confer resistance to cisplatin in tumor cells. Biochem Pharmacol 80: 262-276.
45. Yang C-F, Shen H-M, Ong C-N,. 1999. Protective effect of ebselen against hydrogen peroxide-induced cytotoxicity and DNA damage in HepG2cells. Biochem Pharmacol 57: 273-279. (Pubitemid 29056205)
46. Yang J, Liao X, Agarwal MK, Barnes L, Auron PE, Stark GR,. 2007. Unphosphorylated STAT3 accumulates in response to IL-6 and activates transcription by binding to NFkappaB. Genes Dev 21: 1396-1408. (Pubitemid 46871042)
47. Yilmaz T, Jiffar T, de la Garza G, Lin H, Milas Z, Takahashi Y, Hanna E, Macintyre T, Brown JL, Myers JN, Kupferman ME,. 2010. Theraputic targeting of Trk supresses tumor proliferation and enhances cisplatin activity in HNSCC. Cancer Biol Ther 10: 644-653.
48. Yoshikawa H, Matsubara K, Qian GS, Jackson P, Groopman JD, Manning JE, Harris CC, Herman JG,. 2001. SOCS-1, a negative regulator of the JAK/STAT pathway, is silenced by methylation in human hepatocellular carcinoma and shows growth-suppression activity. Nat Genet 28: 29-35. (Pubitemid 32405812)
49. You M, Yu DH, Feng GS,. 1999. Shp-2 tyrosine phosphatase functions as a negative regulator of the interferon-stimulated Jak/STAT pathway. Mol Cell Biol 19: 2416-2424. (Pubitemid 29098299)
50. Yu H, Jove R,. 2004. The STATs of cancer-New molecular targets come of age. Nat Rev Cancer 4: 97-105. (Pubitemid 38198738)
51. Yu CL, Meyer DJ, Campbell GS, Larner AC, Carter-Su C, Schwartz J, Jove R,. 1995. Enhanced DNA-binding activity of a Stat3-related protein in cells transformed by the Src oncoprotein. Science 269: 81-83.
52. Yu H, Kortylewski M, Pardoll D,. 2007. Crosstalk between cancer and immune cells: Role of STAT3 in the tumour microenvironment. Nat Rev Immunol 7: 41-51. (Pubitemid 46020826)
53. Zhang Q, Raghunath PN, Xue L, Majewski M, Carpentieri DF, Odum N, Morris S, Skorski T, Wasik MA,. 2002. Multilevel dysregulation of STAT3 activation in anaplastic lymphoma kinase-positive T/null-cell lymphoma. J Immunol 168: 466-474. (Pubitemid 34014150)
54. Zhao S, Venkatasubbarao K, Lazor JW, Sperry J, Jin C, Cao L, Freeman JW,. 2008. Inhibition of STAT3 Tyr705 phosphorylation by Smad4 suppresses transforming growth factor beta-mediated invasion and metastasis in pancreatic cancer cells. Cancer Res 68: 4221-4228.