Brassinin inhibits STAT3 signaling pathway through modulation of PIAS-3 and SOCS-3 expression and sensitizes human lung cancer xenograft in nude mice to paclitaxel

Oncotarget

Volumn 6, Issue 8, 2015, Pages 6386-6405

  Lee, Jong Hyun ^a   Kim, Chulwon ^a   Sethi, Gautam ^b   Ahn, Kwang Seok ^a  

^a Kyung Hee University   (South Korea)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Apoptosis; Brassinin; PIAS 3; SOCS 3; STAT3

Indexed keywords

BRASSININ; CD31 ANTIGEN; INTERLEUKIN 6; KI 67 ANTIGEN; PACLITAXEL; PHYTOALEXIN; PIAS 3; PROTEIN INHIBITOR OF ACTIVATED STAT; SMALL INTERFERING RNA; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; CHAPERONE; INDOLE DERIVATIVE; PIAS3 PROTEIN, HUMAN; SOCS3 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN; SUPPRESSOR OF CYTOKINE SIGNALING; THIOCARBAMIC ACID DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL INVASION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG SENSITIZATION; DRUG STRUCTURE; FEMALE; GENE INDUCTION; GENE PRODUCT; GENE SILENCING; HUMAN; HUMAN CELL; MOUSE; MOUSE MODEL; NON SMALL CELL LUNG CANCER; NONHUMAN; NUDE MOUSE; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR GROWTH; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; GENETIC TRANSFECTION; K-562 CELL LINE; MALE; METABOLISM; RANDOMIZATION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; INDOLES; K562 CELLS; MALE; MICE; MICE, NUDE; MOLECULAR CHAPERONES; PACLITAXEL; PROTEIN INHIBITORS OF ACTIVATED STAT; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING 3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; THIOCARBAMATES; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84925642316     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3443     Document Type: Article

References (55)

1. Wang X, Crowe PJ, Goldstein D and Yang JL. STAT3 inhibition, a novel approach to enhancing targeted therapy in human cancers (Review). Int J Oncol. 2012.
2. Bharti AC, Donato N and Aggarwal BB. Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells. J Immunol. 2003; 171: 3863-3871.
3. Aggarwal BB, Sethi G, Ahn KS, Sandur SK, Pandey MK, Kunnumakkara AB, Sung B and Ichikawa H. Targeting signal-transducer-and-activator-of-transcription-3 for prevention and therapy of cancer: modern target but ancient solution. Ann N Y Acad Sci. 2006; 1091: 151-169.
4. Aggarwal BB, Kunnumakkara AB, Harikumar KB, Gupta SR, Tharakan ST, Koca C, Dey S and Sung B. Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann N Y Acad Sci. 2009; 1171: 59-76.
5. McCann GA, Naidu S, Rath KS, Bid HK, Tierney BJ, Suarez A, Varadharaj S, Zhang J, Hideg K, Houghton P, Kuppusamy P, Cohn DE and Selvendiran K. Targeting constitutively-activated STAT3 in hypoxic ovarian cancer, using a novel STAT3 inhibitor. Oncoscience. 2014; 1: 216-228.
6. Zimmer S, Kahl P, Buhl TM, Steiner S, Wardelmann E, Merkelbach-Bruse S, Buettner R and Heukamp LC. Epidermal growth factor receptor mutations in non-small cell lung cancer influence downstream Akt, MAPK and Stat3 signaling. J Cancer Res Clin Oncol. 2009; 135: 723-730.
7. Looyenga BD, Hutchings D, Cherni I, Kingsley C, Weiss GJ and Mackeigan JP. STAT3 is activated by JAK2 independent of key oncogenic driver mutations in non-small cell lung carcinoma. PLoS One. 2012; 7: e30820.
8. Jiang R, Jin Z, Liu Z, Sun L, Wang L and Li K. Correlation of activated STAT3 expression with clinicopathologic features in lung adenocarcinoma and squamous cell carcinoma. Mol Diagn Ther. 2011; 15: 347-352.
9. Xu YH and Lu S. A meta-analysis of STAT3 and phospho-STAT3 expression and survival of patients with non-small-cell lung cancer. Eur J Surg Oncol. 2014; 40: 311-317.
10. Chung CD, Liao J, Liu B, Rao X, Jay P, Berta P and Shuai K. Specific inhibition of Stat3 signal transduction by PIAS3. Science. 1997; 278: 1803-1805.
11. Endo TA, Masuhara M, Yokouchi M, Suzuki R, Sakamoto H, Mitsui K, Matsumoto A, Tanimura S, Ohtsubo M, Misawa H, Miyazaki T, Leonor N, Taniguchi T, Fujita T, Kanakura Y, Komiya S, et al. A new protein containing an SH2 domain that inhibits JAK kinases. Nature. 1997; 387: 921-924.
12. Naka T, Narazaki M, Hirata M, Matsumoto T, Minamoto S, Aono A, Nishimoto N, Kajita T, Taga T, Yoshizaki K, Akira S and Kishimoto T. Structure and function of a new STAT-induced STAT inhibitor. Nature. 1997; 387: 924-929.
13. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ, Gonda TJ, Alexander WS, Metcalf D, Nicola NA and Hilton DJ. A family of cytokine-inducible inhibitors of signalling. Nature. 1997; 387: 917-921.
14. Rakesh K and Agrawal DK. Controlling cytokine signaling by constitutive inhibitors. Biochem Pharmacol. 2005; 70: 649-657.
15. Wang L and Banerjee S. Differential PIAS3 expression in human malignancy. Oncol Rep. 2004; 11: 1319-1324.
16. Ogata Y, Osaki T, Naka T, Iwahori K, Furukawa M, Nagatomo I, Kijima T, Kumagai T, Yoshida M, Tachibana I and Kawase I. Overexpression of PIAS3 suppresses cell growth and restores the drug sensitivity of human lung cancer cells in association with PI3-K/Akt inactivation. Neoplasia. 2006; 8: 817-825.
17. Wible BA, Wang L, Kuryshev YA, Basu A, Haldar S and Brown AM. Increased K+ efflux and apoptosis induced by the potassium channel modulatory protein KChAP/PIAS3beta in prostate cancer cells. J Biol Chem. 2002; 277: 17852-17862.
18. Krebs DL and Hilton DJ. SOCS proteins: negative regulators of cytokine signaling. Stem Cells. 2001; 19: 378-387.
19. Brender C, Nielsen M, Kaltoft K, Mikkelsen G, Zhang Q, Wasik M, Billestrup N and Odum N. STAT3-mediated constitutive expression of SOCS-3 in cutaneous T-cell lymphoma. Blood. 2001; 97: 1056-1062.
20. Mehta RG, Liu J, Constantinou A, Thomas CF, Hawthorne M, You M, Gerhuser C, Pezzuto JM, Moon RC and Moriarty RM. Cancer chemopreventive activity of brassinin, a phytoalexin from cabbage. Carcinogenesis. 1995; 16: 399-404.
21. Mezencev R, Mojzis J, Pilatova M and Kutschy P. Antiproliferative and cancer chemopreventive activity of phytoalexins: focus on indole phytoalexins from crucifers. Neoplasma. 2003; 50: 239-245.
22. Pilatova M, Sarissky M, Kutschy P, Mirossay A, Mezencev R, Curillova Z, Suchy M, Monde K, Mirossay L and Mojzis J. Cruciferous phytoalexins: antiproliferative effects in T-Jurkat leukemic cells. Leuk Res. 2005; 29: 415-421.
23. Pedras MS, Montaut S and Suchy M. Phytoalexins from the crucifer rutabaga: structures, syntheses, biosyntheses, and antifungal activity. J Org Chem. 2004; 69: 4471-4476.
24. Banerjee T, Duhadaway JB, Gaspari P, Sutanto-Ward E, Munn DH, Mellor AL, Malachowski WP, Prendergast GC and Muller AJ. A key in vivo antitumor mechanism of action of natural product-based brassinins is inhibition of indoleamine 2, 3-dioxygenase. Oncogene. 2008; 27: 2851-2857.
25. Izutani Y, Yogosawa S, Sowa Y and Sakai T. Brassinin induces G1 phase arrest through increase of p21 and p27 by inhibition of the phosphatidylinositol 3-kinase signaling pathway in human colon cancer cells. Int J Oncol. 2012; 40: 816-824.
26. Mehta RG, Liu J, Constantinou A, Hawthorne M, Pezzuto JM, Moon RC and Moriarty RM. Structure-activity relationships of brassinin in preventing the development of carcinogen-induced mammary lesions in organ culture. Anticancer Res. 1994; 14: 1209-1213.
27. Csomos P, Zupko I, Rethy B, Fodor L, Falkay G and Bernath G. Isobrassinin and its analogues: novel types of antiproliferative agents. Bioorg Med Chem Lett. 2006; 16: 6273-6276.
28. Gerhauser C, You M, Liu J, Moriarty RM, Hawthorne M, Mehta RG, Moon RC and Pezzuto JM. Cancer chemopreventive potential of sulforamate, a novel analogue of sulforaphane that induces phase 2 drug-metabolizing enzymes. Cancer Res. 1997; 57: 272-278.
29. Kim SM, Park JH, Kim KD, Nam D, Shim BS, Kim SH, Ahn KS, Choi SH and Ahn KS. Brassinin induces apoptosis in PC-3 human prostate cancer cells through the suppression of PI3K/Akt/mTOR/S6K1 signaling cascades. Phytother Res. 2014; 28: 423-431.
30. Yu H and Jove R. The STATs of cancer-new molecular targets come of age. Nat Rev Cancer. 2004; 4: 97-105.
31. Brierley MM and Fish EN. Stats: multifaceted regulators of transcription. J Interferon Cytokine Res. 2005; 25: 733-744.
32. Bowman T, Garcia R, Turkson J and Jove R. STATs in oncogenesis. Oncogene. 2000; 19: 2474-2488.
33. Gao SP, Mark KG, Leslie K, Pao W, Motoi N, Gerald WL, Travis WD, Bornmann W, Veach D, Clarkson B and Bromberg JF. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest. 2007; 117: 3846-3856.
34. Cortas T, Eisenberg R, Fu P, Kern J, Patrick L and Dowlati A. Activation state EGFR and STAT-3 as prognostic markers in resected non-small cell lung cancer. Lung Cancer. 2007; 55: 349-355.
35. Haura EB, Zheng Z, Song L, Cantor A and Bepler G. Activated epidermal growth factor receptor-Stat-3 signaling promotes tumor survival in vivo in non-small cell lung cancer. Clin Cancer Res. 2005; 11: 8288-8294.
36. Song L, Turkson J, Karras JG, Jove R and Haura EB. Activation of Stat3 by receptor tyrosine kinases and cytokines regulates survival in human non-small cell carcinoma cells. Oncogene. 2003; 22: 4150-4165.
37. Dabir S, Kluge A and Dowlati A. The association and nuclear translocation of the PIAS3-STAT3 complex is ligand and time dependent. Mol Cancer Res. 2009; 7: 1854-1860.
38. Kluge A, Dabir S, Kern J, Nethery D, Halmos B, Ma P and Dowlati A. Cooperative interaction between protein inhibitor of activated signal transducer and activator of transcription-3 with epidermal growth factor receptor blockade in lung cancer. Int J Cancer. 2009; 125: 1728-1734.
39. Brantley EC, Nabors LB, Gillespie GY, Choi YH, Palmer CA, Harrison K, Roarty K and Benveniste EN. Loss of protein inhibitors of activated STAT-3 expression in glioblastoma multiforme tumors: implications for STAT-3 activation and gene expression. Clin Cancer Res. 2008; 14: 4694-4704.
40. Evans MK, Yu CR, Lohani A, Mahdi RM, Liu X, Trzeciak AR and Egwuagu CE. Expression of SOCS1 and SOCS3 genes is differentially regulated in breast cancer cells in response to proinflammatory cytokine and growth factor signals. Oncogene. 2007; 26: 1941-1948.
41. Fojtova M, Boudny V, Kovarik A, Lauerova L, Adamkova L, Souckova K, Jarkovsky J and Kovarik J. Development of IFN-gamma resistance is associated with attenuation of SOCS genes induction and constitutive expression of SOCS 3 in melanoma cells. Br J Cancer. 2007; 97: 231-237.
42. Takeuchi K, Sakai I, Narumi H, Yasukawa M, Kojima K, Minamoto Y, Fujisaki T, Tanimoto K, Hara M, Numata A, Gondo H, Takahashi M, Fujii N, Masuda K and Fujita S. Expression of SOCS3 mRNA in bone marrow cells from CML patients associated with cytogenetic response to IFN-alpha. Leuk Res. 2005; 29: 173-178.
43. Yokogami K, Wakisaka S, Avruch J and Reeves SA. Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR. Curr Biol. 2000; 10: 47-50.
44. Shao H, Cheng HY, Cook RG and Tweardy DJ. Identification and characterization of signal transducer and activator of transcription 3 recruitment sites within the epidermal growth factor receptor. Cancer Res. 2003; 63: 3923-3930.
45. Tsang DK and Crowe DL. The mitogen activated protein kinase pathway is required for proliferation but not invasion of human squamous cell carcinoma lines. Int J Oncol. 1999; 15: 519-523.
46. Snaddon J, Parkinson EK, Craft JA, Bartholomew C and Fulton R. Detection of functional PTEN lipid phosphatase protein and enzyme activity in squamous cell carcinomas of the head and neck, despite loss of heterozygosity at this locus. Br J Cancer. 2001; 84: 1630-1634.
47. Gough DJ, Koetz L and Levy DE. The MEK-ERK pathway is necessary for serine phosphorylation of mitochondrial STAT3 and Ras-mediated transformation. PLoS One. 2013; 8: e83395.
48. Catlett-Falcone R, Landowski TH, Oshiro MM, Turkson J, Levitzki A, Savino R, Ciliberto G, Moscinski L, Fernandez-Luna JL, Nunez G, Dalton WS and Jove R. Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells. Immunity. 1999; 10: 105-115.
49. Nielsen M, Kaestel CG, Eriksen KW, Woetmann A, Stokkedal T, Kaltoft K, Geisler C, Ropke C and Odum N. Inhibition of constitutively activated Stat3 correlates with altered Bcl-2/Bax expression and induction of apoptosis in mycosis fungoides tumor cells. Leukemia. 1999; 13: 735-738.
50. Park D, Magis AT, Li R, Owonikoko TK, Sica GL, Sun SY, Ramalingam SS, Khuri FR, Curran WJ and Deng X. Novel small-molecule inhibitors of Bcl-XL to treat lung cancer. Cancer Res. 2013; 73: 5485-5496.
51. Leech SH, Olie RA, Gautschi O, Simoes-Wust AP, Tschopp S, Haner R, Hall J, Stahel RA and Zangemeister-Wittke U. Induction of apoptosis in lung-cancer cells following bcl-xL anti-sense treatment. Int J Cancer. 2000; 86: 570-576.
52. Vaishampayan U, Parchment RE, Jasti BR and Hussain M. Taxanes: an overview of the pharmacokinetics and pharmacodynamics. Urology. 1999; 54: 22-29.
53. Ramalingam S and Belani CP. Paclitaxel for non-small cell lung cancer. Expert Opin Pharmacother. 2004; 5: 1771-1780.
54. Kim SM, Lee JH, Sethi G, Kim C, Baek SH, Nam D, Chung WS, Kim SH, Shim BS and Ahn KS. Bergamottin, a natural furanocoumarin obtained from grapefruit juice induces chemosensitization and apoptosis through the inhibition of STAT3 signaling pathway in tumor cells. Cancer Lett. 2014; 354: 153-163.
55. Manu KA, Shanmugam MK, Li F, Chen L, Siveen KS, Ahn KS, Kumar AP and Sethi G. Simvastatin sensitizes human gastric cancer xenograft in nude mice to capecitabine by suppressing nuclear factor-kappa B-regulated gene products. J Mol Med (Berl). 2014; 92: 267-276.