Galiellalactone induces cell cycle arrest and apoptosis through the ATM/ATR pathway in prostate cancer cells

Oncotarget

Volumn 7, Issue 4, 2016, Pages 4490-4506

  García, Víctor ^a   Lara Chica, Maribel ^a   Cantarero, Irene ^a   Sterner, Olov ^b   Calzado, Marco A ^a   Muñoz, Eduardo ^a  

^a HOSPITAL UNIVERSITARIO REINA SOFÍA   (Spain)

^b LUND UNIVERSITY   (Sweden)

Author keywords

ATM ATR; Cancer; Cell cycle; CHK1; Galiellalactone

Indexed keywords

7 HYDROXYSTAUROSPORINE; ACETYLCYSTEINE; AMBROXOL; ANTINEOPLASTIC AGENT; ATM PROTEIN; ATR PROTEIN; CAFFEINE; CASPASE; CHECKPOINT KINASE 1; EPIGALLOCATECHIN GALLATE; GALIELLALACTONE; HISTONE H2AX; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE C; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ATM PROTEIN, HUMAN; ATR PROTEIN, HUMAN; LACTONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL MIGRATION; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DU145 CELL LINE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROTUBULE; MOUSE; NONHUMAN; PROSTATE CANCER; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; CELL CYCLE CHECKPOINT; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHOSPHORYLATION; PROSTATIC NEOPLASMS; TUMOR CELL CULTURE; WOUND HEALING;

ANIMALS; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; BLOTTING, WESTERN; CELL CYCLE CHECKPOINTS; CELL MOVEMENT; CELL PROLIFERATION; COMET ASSAY; DNA DAMAGE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOENZYME TECHNIQUES; LACTONES; MALE; MICE; MICE, NUDE; PHOSPHORYLATION; PROSTATIC NEOPLASMS; TUMOR CELLS, CULTURED; WOUND HEALING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84957946417     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6606     Document Type: Article

References (55)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA: a cancer journal for clinicians. 2015; 65:87-108.
2. Feldman BJ, Feldman D. The development of androgenindependent prostate cancer. Nature reviews Cancer. 2001; 1:34-45.
3. Pienta KJ, Bradley D. Mechanisms underlying the development of androgen-independent prostate cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2006; 12:1665-1671.
4. Katzenwadel A, Wolf P. Androgen deprivation of prostate cancer: Leading to a therapeutic dead end. Cancer letters. 2015.
5. Karantanos T, Corn PG, Thompson TC. Prostate cancer progression after androgen deprivation therapy: mechanisms of castrate resistance and novel therapeutic approaches. Oncogene. 2013; 32:5501-5511.
6. Barton BE, Karras JG, Murphy TF, Barton A, Huang HF. Signal transducer and activator of transcription 3 (STAT3) activation in prostate cancer: Direct STAT3 inhibition induces apoptosis in prostate cancer lines. Molecular cancer therapeutics. 2004; 3:11-20.
7. Chung SS, Giehl N, Wu Y, Vadgama JV. STAT3 activation in HER2-overexpressing breast cancer promotes epithelial-mesenchymal transition and cancer stem cell traits. International journal of oncology. 2014; 44:403-411.
8. Harada D, Takigawa N, Kiura K. The Role of STAT3 in Non-Small Cell Lung Cancer. Cancers. 2014; 6:708-722.
9. Corvinus FM, Orth C, Moriggl R, Tsareva SA, Wagner S, Pfitzner EB, Baus D, Kaufmann R, Huber LA, Zatloukal K, Beug H, Ohlschlager P, Schutz A, et al. Persistent STAT3 activation in colon cancer is associated with enhanced cell proliferation and tumor growth. Neoplasia. 2005; 7:545-555.
10. Siveen KS, Sikka S, Surana R, Dai X, Zhang J, Kumar AP, Tan BK, Sethi G, Bishayee A. Targeting the STAT3 signaling pathway in cancer: role of synthetic and natural inhibitors. Biochimica et biophysica acta. 2014; 1845:136-154.
11. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nature reviews Cancer. 2004; 4:253-265.
12. Verma NK, Dourlat J, Davies AM, Long A, Liu WQ, Garbay C, Kelleher D, Volkov Y. STAT3-stathmin interactions control microtubule dynamics in migrating T-cells. The Journal of biological chemistry. 2009; 284:12349-12362.
13. Ng DC, Lin BH, Lim CP, Huang G, Zhang T, Poli V, Cao X. Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin. The Journal of cell biology. 2006; 172:245-257.
14. Silver DL, Naora H, Liu J, Cheng W, Montell DJ. Activated signal transducer and activator of transcription (STAT) 3: localization in focal adhesions and function in ovarian cancer cell motility. Cancer research. 2004; 64:3550-3558.
15. Sano S, Itami S, Takeda K, Tarutani M, Yamaguchi Y, Miura H, Yoshikawa K, Akira S, Takeda J. Keratinocytespecific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. The EMBO journal. 1999; 18:4657-4668.
16. Wake MS, Watson CJ. STAT3 the oncogene-still eluding therapy? The FEBS journal. 2015; 282:2600-2611.
17. Johansson M, Sterner O. Synthesis of (-)-galiellalactone. The Journal of antibiotics. 2002; 55:663-665.
18. Weidler M, Rether J, Anke T, Erkel G. Inhibition of interleukin-6 signaling by galiellalactone. FEBS letters. 2000; 484:1-6.
19. Don-Doncow N, Escobar Z, Johansson M, Kjellstrom S, Garcia V, Munoz E, Sterner O, Bjartell A, Hellsten R. Galiellalactone is a direct inhibitor of the transcription factor STAT3 in prostate cancer cells. The Journal of biological chemistry. 2014; 289:15969-15978.
20. Hellsten R, Johansson M, Dahlman A, Dizeyi N, Sterner O, Bjartell A. Galiellalactone is a novel therapeutic candidate against hormone-refractory prostate cancer expressing activated Stat3. The Prostate. 2008; 68:269-280.
21. Hellsten R, Johansson M, Dahlman A, Sterner O, Bjartell A. Galiellalactone inhibits stem cell-like ALDH-positive prostate cancer cells. PloS one. 2011; 6:e22118.
22. Canesin G, Evans-Axelsson S, Hellsten R, Sterner O, Krzyzanowska A, Andersson T, Bjartell A. The STAT3 Inhibitor Galiellalactone Effectively Reduces Tumor Growth and Metastatic Spread in an Orthotopic Xenograft Mouse Model of Prostate Cancer. European urology. 2015.
23. Rudolph K, Serwe A, Erkel G. Inhibition of TGF-beta signaling by the fungal lactones (S)-curvularin, dehydrocurvularin, oxacyclododecindione and galiellalactone. Cytokine. 2013; 61:285-296.
24. Perez M, Soler-Torronteras R, Collado JA, Limones CG, Hellsten R, Johansson M, Sterner O, Bjartell A, Calzado MA, Munoz E. The fungal metabolite galiellalactone interferes with the nuclear import of NF-kappaB and inhibits HIV-1 replication. Chemicobiological interactions. 2014; 214:69-76.
25. Hausding M, Tepe M, Ubel C, Lehr HA, Rohrig B, Hohn Y, Pautz A, Eigenbrod T, Anke T, Kleinert H, Erkel G, Finotto S. Induction of tolerogenic lung CD4+ T cells by local treatment with a pSTAT-3 and pSTAT-5 inhibitor ameliorated experimental allergic asthma. International immunology. 2011; 23:1-15.
26. Bollmann F, Jackel S, Schmidtke L, Schrick K, Reinhardt C, Jurk K, Wu Z, Xia N, Li H, Erkel G, Walter U, Kleinert H, Pautz A. Anti-Inflammatory and Anti-Thrombotic Effects of the Fungal Metabolite Galiellalactone in Apolipoprotein E-Deficient Mice. PloS one. 2015; 10:e0130401.
27. Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nature reviews Cancer. 2009; 9:153-166.
28. Vermeulen K, Van Bockstaele DR, Berneman ZN. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell proliferation. 2003; 36:131-149.
29. Karanika S, Karantanos T, Li L, Corn PG, Thompson TC. DNA damage response and prostate cancer: defects, regulation and therapeutic implications. Oncogene. 2015; 34:2815-2822.
30. Smith J, Tho LM, Xu N, Gillespie DA. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Advances in cancer research. 2010; 108:73-112.
31. Wang H, Zhang X, Teng L, Legerski RJ. DNA damage checkpoint recovery and cancer development. Experimental cell research. 2015; 334:350-358.
32. Pabla N, Huang S, Mi QS, Daniel R, Dong Z. ATR-Chk2 signaling in p53 activation and DNA damage response during cisplatin-induced apoptosis. The Journal of biological chemistry. 2008; 283:6572-6583.
33. Tanaka T, Halicka HD, Traganos F, Seiter K, Darzynkiewicz Z. Induction of ATM activation, histone H2AX phosphorylation and apoptosis by etoposide: relation to cell cycle phase. Cell cycle. 2007; 6:371-376.
34. Kurz EU, Douglas P, Lees-Miller SP. Doxorubicin activates ATM-dependent phosphorylation of multiple downstream targets in part through the generation of reactive oxygen species. The Journal of biological chemistry. 2004; 279:53272-53281.
35. Xian M, Ito K, Nakazato T, Shimizu T, Chen CK, Yamato K, Murakami A, Ohigashi H, Ikeda Y, Kizaki M. Zerumbone, a bioactive sesquiterpene, induces G2/M cell cycle arrest and apoptosis in leukemia cells via a Fas-and mitochondria-mediated pathway. Cancer science. 2007; 98:118-126.
36. Wang Y, Liu Q, Liu Z, Li B, Sun Z, Zhou H, Zhang X, Gong Y, Shao C. Berberine, a genotoxic alkaloid, induces ATM-Chk1 mediated G2 arrest in prostate cancer cells. Mutation research. 2012; 734:20-29.
37. Arunkumar A, Vijayababu MR, Srinivasan N, Aruldhas MM, Arunakaran J. Garlic compound, diallyl disulfide induces cell cycle arrest in prostate cancer cell line PC-3. Molecular and cellular biochemistry. 2006; 288:107-113.
38. Grivennikov SI, Karin M. Dangerous liaisons: STAT3 and NF-kappaB collaboration and crosstalk in cancer. Cytokine & growth factor reviews. 2010; 21:11-19.
39. Naugler WE, Karin M. NF-kappaB and cancer-identifying targets and mechanisms. Current opinion in genetics & development. 2008; 18:19-26.
40. Habraken Y, Piette J. NF-kappaB activation by double-strand breaks. Biochemical pharmacology. 2006; 72:1132-1141.
41. Koganti S, Hui-Yuen J, McAllister S, Gardner B, Grasser F, Palendira U, Tangye SG, Freeman AF, Bhaduri-McIntosh S. STAT3 interrupts ATR-Chk1 signaling to allow oncovirus-mediated cell proliferation. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111:4946-4951.
42. Barry SP, Townsend PA, Knight RA, Scarabelli TM, Latchman DS, Stephanou A. STAT3 modulates the DNA damage response pathway. International journal of experimental pathology. 2010; 91:506-514.
43. Janssens S, Tschopp J. Signals from within: the DNAdamage-induced NF-kappaB response. Cell death and differentiation. 2006; 13:773-784.
44. Volcic M, Karl S, Baumann B, Salles D, Daniel P, Fulda S, Wiesmuller L. NF-kappaB regulates DNA double-strand break repair in conjunction with BRCA1-CtIP complexes. Nucleic acids research. 2012; 40:181-195.
45. Nehme A, Varadarajan P, Sellakumar G, Gerhold M, Niedner H, Zhang Q, Lin X, Christen RD. Modulation of docetaxel-induced apoptosis and cell cycle arrest by alltrans retinoic acid in prostate cancer cells. British journal of cancer. 2001; 84:1571-1576.
46. Ramaswamy B, Puhalla S. Docetaxel: a tubulin-stabilizing agent approved for the management of several solid tumors. Drugs of today. 2006; 42:265-279.
47. Heng YW, Koh CG. Actin cytoskeleton dynamics and the cell division cycle. The international journal of biochemistry & cell biology. 2010; 42:1622-1633.
48. Poruchynsky MS, Komlodi-Pasztor E, Trostel S, Wilkerson J, Regairaz M, Pommier Y, Zhang X, Kumar Maity T, Robey R, Burotto M, Sackett D, Guha U, Fojo AT. Microtubule-targeting agents augment the toxicity of DNA-damaging agents by disrupting intracellular trafficking of DNA repair proteins. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112:1571-1576.
49. Cliby WA, Lewis KA, Lilly KK, Kaufmann SH. S phase and G2 arrests induced by topoisomerase I poisons are dependent on ATR kinase function. The Journal of biological chemistry. 2002; 277:1599-1606.
50. Zuco V, Benedetti V, Zunino F. ATM-and ATR-mediated response to DNA damage induced by a novel camptothecin, ST1968. Cancer letters. 2010; 292:186-196.
51. Ravery V, Fizazi K, Oudard S, Drouet L, Eymard JC, Culine S, Gravis G, Hennequin C, Zerbib M. The use of estramustine phosphate in the modern management of advanced prostate cancer. BJU international. 2011; 108:1782-1786.
52. Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT. ATM activation by oxidative stress. Science. 2010; 330:517-521.
53. Zafarullah M, Li WQ, Sylvester J, Ahmad M. Molecular mechanisms of N-acetylcysteine actions. Cellular and molecular life sciences: CMLS. 2003; 60:6-20.
54. Sun SY. N-acetylcysteine, reactive oxygen species and beyond. Cancer biology & therapy. 2010; 9:109-110.
55. Johansson M, Sterner O. Synthesis of (+)-galiellalactone. Absolute configuration of galiellalactone. Organic letters. 2001; 3:2843-2845.