Zoledronic acid reverses the epithelial-mesenchymal transition and inhibits self-renewal of breast cancer cells through inactivation of NF-κB

Molecular Cancer Therapeutics

Volumn 12, Issue 7, 2013, Pages 1356-1366

  Schech, Amanda J ^a   Kazi, Armina A ^a,b   Gilani, Rabia A ^a   Brodie, Angela H ^a,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b LOYOLA UNIVERSITY MARYLAND   (United States)

^c UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; UVOMORULIN; ZOLEDRONIC ACID;

ARTICLE; CANCER CELL; CELL ADHESION; CELL CONTACT; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL RENEWAL; CELL STRUCTURE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG EFFECT; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TRIPLE NEGATIVE BREAST CANCER; UPREGULATION;

EID: 84880073201     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-12-0304     Document Type: Article

References (38)

1. Gnant M, Mlineritsch B, Schippinger W, Luschin-Ebengreuth G, Postlberger S, Menzel C, et al. Endocrine therapy plus zoledronic acid in premenopausal breast cancer. N Engl J Med 2009;360:679-91.
2. Eidtmann H, de Boer R, Bundred N, Llombart-Cussac A, Davidson N, Neven P, et al. Efficacy of zoledronic acid in postmenopausal women with early breast cancer receiving adjuvant letrozole: 36-month results of the ZO-FAST study. Ann Oncol 2010;21:2188-94.
3. Gnant M, Mlineritsch B, Stoeger H, Luschin-Ebengreuth G, Heck D, Menzel C, et al. Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 62-month follow-up from the ABCSG-12 randomised trial. Lancet Oncol 2011;12:631-41.
4. Coleman RE, Marshall H, Cameron D, Dodwell D, Burkinshaw R, Keane M, et al. Breast-cancer adjuvant therapy with zoledronic acid. N Engl J Med 2011;365:1396-405.
5. Fromigue O, Lagneaux L, Body JJ. Bisphosphonates induce breast cancer cell death in vitro. J Bone Miner Res 2000;15:2211-21.
6. Senaratne SG, Pirianov G, Mansi JL, Arnett TR, Colston KW. Bisphosphonates induce apoptosis in human breast cancer cell lines. Br J Cancer 2000;82:1459-68. (Pubitemid 30175914)
7. Jagdev SP, Coleman RE, Shipman CM, Rostami-H A, Croucher PI. The bisphosphonate, zoledronic acid, induces apoptosis of breast cancer cells: evidence for synergy with paclitaxel. Br J Cancer 2001;84:1126-34. (Pubitemid 32448513)
8. Senaratne SG, Mansi JL, Colston KW. The bisphosphonate zoledronic acid impairs ras membrane [correction of impairs membrane] localisation and induces cytochrome c release in breast cancer cells. Br J Cancer 2002;86:1479-86. (Pubitemid 34548073)
9. Verdijk R, Franke HR, Wolbers F, Vermes I. Differential effects of bisphosphonates on breast cancer cell lines. Cancer Lett 2007;246:308-12. (Pubitemid 44959401)
10. Almubarak H, Jones A, Chaisuparat R, Zhang M, Meiller TF, Scheper MA. Zoledronic acid directly suppresses cell proliferation and induces apoptosis in highly tumorigenic prostate and breast cancers. J Carcinog 2011;10:2.
11. Boissier S, Ferreras M, Peyruchaud O, Magnetto S, Ebetino FH, Colombel M, et al. Bisphosphonates inhibit breast and prostate carcinoma cell invasion, an early event in the formation of bone metastases. Cancer Res 2000;60:2949-54. (Pubitemid 30395820)
12. Denoyelle C, Hong L, Vannier JP, Soria J, Soria C.New insights into the actions of bisphosphonate zoledronic acid in breast cancer cells by dual RhoA-dependent and -independent effects. Br J Cancer 2003;88:1631-40. (Pubitemid 36713793)
13. Guarino M, Rubino B, Ballabio G. The role of epithelial-mesenchymal transition in cancer pathology. Pathology 2007;39:305-18. (Pubitemid 46897605)
14. Kalluri R, Weinberg RA. The basics of epithelial-mesenchymal transition. J Clin Invest 2009;119:1420-8.
15. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000;2:84-9.
16. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000;2:76-83.
17. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004;117:927-39. (Pubitemid 38798858)
18. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15. (Pubitemid 351636299)
19. Schech AJ, Nemieboka BE, Brodie AH. Zoledronic acid inhibits aromatase activity and phosphorylation: potential mechanism for additive zoledronic acid and letrozole drug interaction. J Steroid Biochem Mol Biol 2012;132:195-202.
20. Jiao W, Miyazaki K, Kitajima Y. Inverse correlation between E-cadherin and snail expression in hepatocellular carcinoma cell lines in vitro and in vivo. Br J Cancer 2002;86:98-101. (Pubitemid 34146348)
21. Sitarz R, Leguit RJ, de Leng WW, Morsink FH, Polkowski WP, Maciejewski R, et al. Cyclooxygenase-2 mediated regulation of E-cadherin occurs in conventional but not early-onset gastric cancer cell lines. Cell Oncol 2009;31:475-85.
22. Lee UJ, Choung SR, Prakash KV, Lee EJ, Lee MY, Kim YJ, et al. Dual knockdown of p65 and p50 subunits of NF-kappaB by siRNA inhibits the induction of inflammatory cytokines and significantly enhance apoptosis in human primary synoviocytes treated with tumor necrosis factor-alpha. Mol Biol Rep 2008;35:291-8.
23. Synthesis-gene.com [Homepage on the internet]. Shanghai: Shine-Gene Molecular Biotech Inc. [cited 2011 Jun 12]. Available from: http://www. synthesisgene.com/tools/Housekeeping-Gene-Primers.pdf.
24. YangMH, Hsu DS, Wang HW, Wang HJ, Lan HY, Yang WH, et al. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition. Nat Cell Biol 2010;12:982-92.
25. Pham CG, Bubici C, Zazzeroni F, Knabb JR, Papa S, Kuntzen C, et al. Upregulation of twist-1 by NF-kappaB blocks cytotoxicity induced by chemotherapeutic drugs. Mol Cell Biol 2007;27:3920-35. (Pubitemid 47010991)
26. Li CW, Xia W, Huo L, Lim SO, Wu Y, Hsu JL, et al.Epithelial-mesenchymal transition induced by TNF-alpha requires NF-kappaB-mediated transcriptional upregulation of Twist1. Cancer Res 2012;72:1290-300.
27. Teronen O, Heikkila P, Konttinen YT, Laitinen M, Salo T, Hanemaaijer R, et al. MMP inhibition and downregulation by bisphosphonates. Ann N Y Acad Sci 1999;878:453-65. (Pubitemid 29353588)
28. Montague R, Hart CA, George NJ, Ramani VA, Brown MD, Clarke NW. Differential inhibition of invasion and proliferation by bisphosphonates: anti-metastatic potential of zoledronic acid in prostate cancer. Eur Urol 2004;46:389-401.
29. Bezzi M, Hasmim M, Bieler G, Dormond O, Ruegg C. Zoledronate sensitizes endothelial cells to tumor necrosis factor-induced programmed cell death: evidence for the suppression of sustained activation of focal adhesion kinase and protein kinase B/Akt. J Biol Chem 2003;278:43603-14. (Pubitemid 37345986)
30. Bellahcene A, Chaplet M, Bonjean K, Castronovo V. Zoledronate inhibits alphavbeta3 and alphavbeta5 integrin cell surface expression in endothelial cells. Endothelium 2007;14:123-30. (Pubitemid 47386391)
31. Romani AA, Desenzani S, Morganti MM, La Monica S, Borghetti AF, Soliani P. Zoledronic acid determines S-phase arrest but fails to induce apoptosis in cholangiocarcinoma cells. Biochem Pharmacol 2009;78:133-41.
32. Okamoto S, Kawamura K, Li Q, Yamanaka M, Yang S, Fukamachi T, et al. Zoledronic acid produces antitumor effects on mesothelioma through apoptosis and S-phase arrest in p53-independent and ras prenylation-independent manners. J Thorac Oncol 2012;7:873-82.
33. Li XY, Lin YC, Huang WL, Lin W, Wang HB, Lin WZ, et al. Zoledronic acid inhibits human nasopharyngeal carcinoma cell proliferation by activating mitochondrial apoptotic pathway. Med Oncol 2012;29:3374-80.
34. Lee MV, Fong EM, Singer FR, Guenette RS. Bisphosphonate treatment inhibits the growth of prostate cancer cells. Cancer Res 2001;61:2602-8. (Pubitemid 32685845)
35. Tenta R, Pitulis N, Tiblalexi D, Consoulas C, Katopodis H, Konstantinidou E, et al. Mechanisms of the action of zoledronic acid on human MG-63 osteosarcoma cells. Horm Metab Res 2008;40:737-45. (Pubitemid 352772688)
36. Di Salvatore M, Orlandi A, Bagala C, Quirino M, Cassano A, Astone A, et al. Anti-tumour and anti-angiogenetic effects of zoledronic acid on human non-small-cell lung cancer cell line. Cell Prolif 2011;44:139-46.
37. Inoue R, Matsuki NA, Jing G, Kanematsu T, Abe K, Hirata M. The inhibitory effect of alendronate, a nitrogen-containing bisphosphonate on the PI3K-akt-NFkappaB pathway in osteosarcoma cells. Br J Pharmacol 2005;146:633-41. (Pubitemid 41573614)
38. Sasaki CY, Barberi TJ, Ghosh P, Longo DL. Phosphorylation of RelA/ p65 on serine 536 defines an I{kappa}B{alpha}-independent NF-{kappa} B pathway. J Biol Chem 2005;280:34538-47. (Pubitemid 41504584)