Cancer Letters
Volume 294, Issue 2 , Pages 245-253 , 28 August 2010

A combination of a DNA-chimera siRNA against PLK-1 and zoledronic acid suppresses the growth of malignant mesothelioma cells in vitro

  • Eri Kawata

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • Division of Internal Medicine, Kyoto Second Red Cross Hospital, 355 Kamannza Marutamachi, Kamigyo-ku, Kyoto 602-8026, Japan
    • These authors contribute equal to this work.
    • ,
  • Eishi Ashihara

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 75 751 3630; fax: +81 75 751 4283.
    • These authors contribute equal to this work.
    • ,
  • Yoko Nakagawa

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Takahiro Kiuchi

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Mai Ogura

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Hisayuku Yao

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Kazuki Sakai

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Ruriko Tanaka

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Rina Nagao

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Asumi Yokota

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Miki Takeuchi

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Shinya Kimura

      Affiliations

    • Division of Hematology, Respiratory Medicine, and Oncology, Department of Internal Medicine, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga 849-8501, Japan
    • ,
  • Hideyo Hirai

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan
    • ,
  • Taira Maekawa

      Affiliations

    • Department of Transfusion Medicine & Cell Therapy, Kyoto University Hospital, 54 Kawahara-cho Shogoin, Sakyo-ku, Kyoto 606-8507, Japan

Received 24 November 2009 ,Revised 6 February 2010 ,Accepted 10 February 2010.

References 

  1. Robinson BW, Lake RA. Advances in malignant mesothelioma. New Engl. J. Med. 2005;353:1591–1603
  2. Halstead JC, Lim E, Venkateswaran RM, Charman SC, Goddard M, Ritchie AJ. Improved survival with VATS pleurectomy–decortication in advanced malignant mesothelioma. Eur. J. Surg. Oncol. 2005;31:314–320
  3. Waller DA. Malignant mesothelioma – British surgical strategies. Lung Cancer. 2004;45(Suppl 1):S81–S84
  4. Carteni G, Manegold C, Garcia GM, Siena S, Zielinski CC, Amadori D, et al. Malignant peritoneal mesothelioma – results from the international expanded access program using pemetrexed alone or in combination with a platinum agent. Lung Cancer. 2009;64:211–218
  5. Taylor P, Castagneto B, Dark G, Marangolo M, Scagliotti GV, van Klaveren RJ, et al. Single-agent pemetrexed for chemonaive and pretreated patients with malignant pleural mesothelioma: results of an international expanded access program. J. Thorac. Oncol. 2008;3:764–771
  6. Baas P, Ardizzoni A, Grossi F, Nackaerts K, Numico G, Van Marck E, et al. The activity of raltitrexed (Tomudex) in malignant pleural mesothelioma: an EORTC phase II study (08992). Eur. J. Cancer. 2003;39:353–357
  7. van Meerbeeck JP, Gaafar R, Manegold C, Van Klaveren RJ, Van Marck EA, Vincent M, et al. Randomized phase III study of cisplatin with or without raltitrexed in patients with malignant pleural mesothelioma: an intergroup study of the European Organisation for Research and Treatment of Cancer Lung Cancer Group and the National Cancer Institute of Canada. J. Clin. Oncol. 2005;23:6881–6889
  8. Lee CW, Murray N, Anderson H, Rao SC, Bishop W. Outcomes with first-line platinum-based combination chemotherapy for malignant pleural mesothelioma: a review of practice in British Columbia. Lung Cancer. 2009;64:308–313
  9. Aelony Y. Raltitrexed and pemetrexed studies in mesothelioma have not shown improved quality of life nor prolonged survival compared with effective pleurodesis with thoracoscopic talc poudrage. J. Clin. Oncol. 2006;24:4667;(author reply 4667–4668)
  10. Bumcrot D, Manoharan M, Koteliansky V, Sah DW. RNAi therapeutics: a potential new class of pharmaceutical drugs. Nat. Chem. Biol. 2006;2:711–719
  11. E. Ashihara, E. Kawata, T. Maekawa, Future prospect of RNA interference for cancer therapies, Curr. Drug Targets. in press.
  12. Boutla A, Delidakis C, Livadaras I, Tsagris M, Tabler M. Short 5′-phosphorylated double-stranded RNAs induce RNA interference in Drosophila. Curr. Biol. 2001;11:1776–1780
  13. Ui-Tei K, Naito Y, Zenno S, Nishi K, Yamato K, Takahashi F, et al. Functional dissection of siRNA sequence by systematic DNA substitution: modified siRNA with a DNA seed arm is a powerful tool for mammalian gene silencing with significantly reduced off-target effect. Nucleic Acids Res. 2008;36:2136–2151
  14. Elbashir SM, Martinez J, Patkaniowska A, Lendeckel W, Tuschl T. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. Embo. J. 2001;20:6877–6888
  15. Barr FA, Sillje HH, Nigg EA. Polo-like kinases and the orchestration of cell division. Nat. Rev. Mol. Cell Biol. 2004;5:429–440
  16. van de Weerdt BC, Medema RH. Polo-like kinases: a team in control of the division. Cell Cycle. 2006;5:853–864
  17. Strebhardt K, Ullrich A. Targeting polo-like kinase 1 for cancer therapy. Nat. Rev. Cancer. 2006;6:321–330
  18. Takai N, Hamanaka R, Yoshimatsu J, Miyakawa I. Polo-like kinases (Plks) and cancer. Oncogene. 2005;24:287–291
  19. Nogawa M, Yuasa T, Kimura S, Tanaka M, Kuroda J, Sato K, et al. Intravesical administration of small interfering RNA targeting PLK-1 successfully prevents the growth of bladder cancer. J. Clin. Invest. 2005;115:978–985
  20. Kawata E, Ashihara E, Kimura S, Takenaka K, Sato K, Tanaka R, et al. Administration of PLK-1 small interfering RNA with atelocollagen prevents the growth of liver metastases of lung cancer. Mol. Cancer Ther. 2008;7:2904–2912
  21. Schoffski P. Polo-like kinase (PLK) inhibitors in preclinical and early clinical development in oncology. Oncologist. 2009;14:559–570
  22. Mross K, Frost A, Steinbild S, Hedbom S, Rentschler J, Kaiser R, et al. Phase I dose escalation and pharmacokinetic study of BI 2536, a novel polo-like kinase 1 inhibitor, in patients with advanced solid tumors. J. Clin. Oncol. 2008;26:5511–5517
  23. Spankuch-Schmitt B, Bereiter-Hahn J, Kaufmann M, Strebhardt K. Effect of RNA silencing of polo-like kinase-1 (PLK1) on apoptosis and spindle formation in human cancer cells. J. Natl. Cancer Inst. 2002;94:1863–1877
  24. Yuasa T, Kimura S, Ashihara E, Habuchi T, Maekawa T. Zoledronic acid – a multiplicity of anti-cancer action. Curr. Med. Chem. 2007;14:2126–2135
  25. Green JR. Bisphosphonates: preclinical review. Oncologist. 2004;9(Suppl 4):3–13
  26. Kuroda J, Kimura S, Segawa H, Kobayashi Y, Yoshikawa T, Urasaki Y, et al. The third-generation bisphosphonate zoledronate synergistically augments the anti-Ph+ leukemia activity of imatinib mesylate. Blood. 2003;102:2229–2235
  27. Matsumoto S, Kimura S, Segawa H, Kuroda J, Yuasa T, Sato K, et al. Efficacy of the third-generation bisphosphonate, zoledronic acid alone and combined with anti-cancer agents against small cell lung cancer cell lines. Lung Cancer. 2005;47:31–39
  28. Yuasa T, Nogawa M, Kimura S, Yokota A, Sato K, Segawa H, et al. A third-generation bisphosphonate, minodronic acid (YM529), augments the interferon alpha/beta-mediated inhibition of renal cell cancer cell growth both in vitro and in vivo. Clin. Cancer Res. 2005;11:853–859
  29. Horie N, Murata H, Nishigaki Y, Matsui T, Segawa H, Nogawa M, et al. The third-generation bisphosphonates inhibit proliferation of murine osteosarcoma cells with induction of apoptosis. Cancer Lett. 2006;238:111–118
  30. Sato K, Yuasa T, Nogawa M, Kimura S, Segawa H, Yokota A, et al. A third-generation bisphosphonate, minodronic acid (YM529), successfully prevented the growth of bladder cancer in vitro and in vivo. Brit. J. Cancer. 2006;95:1354–1361
  31. Chou TC. Drug combination studies and their synergy quantification using the Chou–Talalay method. Cancer Res. 2010;70:440–446
  32. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev. 2006;58:621–681
  33. Kimura S, Kuroda J, Segawa H, Sato K, Nogawa M, Yuasa T, et al. Antiproliferative efficacy of the third-generation bisphosphonate, zoledronic acid, combined with other anticancer drugs in leukemic cell lines. Int. J. Hematol. 2004;79:37–43
  34. Temmink OH, Hoebe EK, van der Born K, Ackland SP, Fukushima M, Peters GJ. Mechanism of trifluorothymidine potentiation of oxaliplatin-induced cytotoxicity to colorectal cancer cells. Brit. J. Cancer. 2007;96:231–240
  35. Keshelava N, Davicioni E, Wan Z, Ji L, Sposto R, Triche TJ, et al. Histone deacetylase 1 gene expression and sensitization of multidrug-resistant neuroblastoma cell lines to cytotoxic agents by depsipeptide. J. Natl. Cancer Inst. 2007;99:1107–1119
  36. Sei S, Mussio JK, Yang QE, Nagashima K, Parchment RE, Coffey MC, et al. Synergistic antitumor activity of oncolytic reovirus and chemotherapeutic agents in non-small cell lung cancer cells. Mol. Cancer. 2009;8:47
  37. Reszka AA, Halasy-Nagy J, Rodan GA. Nitrogen-bisphosphonates block retinoblastoma phosphorylation and cell growth by inhibiting the cholesterol biosynthetic pathway in a keratinocyte model for esophageal irritation. Mol. Pharmacol. 2001;59:193–202
  38. Dai BN, Yang Y, Chau Z, Jhanwar-Uniyal M. Polo-like kinase 1 regulates RhoA during cytokinesis exit in human cells. Cell Proliferat. 2007;40:550–557
  39. Burkard ME, Randall CL, Larochelle S, Zhang C, Shokat KM, Fisher RP, et al. Chemical genetics reveals the requirement for polo-like kinase 1 activity in positioning RhoA and triggering cytokinesis in human cells. Proc. Natl. Acad. Sci. USA. 2007;104:4383–4388
  40. Zelphati O, Szoka FC. Mechanism of oligonucleotide release from cationic liposomes. Proc. Natl. Acad. Sci. USA. 1996;93:11493–11498
  41. Choung S, Kim YJ, Kim S, Park HO, Choi YC. Chemical modification of siRNAs to improve serum stability without loss of efficacy. Biochem. Biophys. Res. Commun. 2006;342:919–927
  42. Behlke MA. Chemical modification of siRNAs for in vivo use. Oligonucleotides. 2008;18:305–319
  43. Chia WJ, Tang BL. Emerging roles for Rab family GTPases in human cancer. Biochim. Biophys. Acta. 2009;1795:110–116
  44. Hattori M, Minato N. Rap1 GTPase: functions, regulation, and malignancy. J. Biochem. 2003;134:479–484
  45. Fehrenbacher N, Bar-Sagi D, Philips M. Ras/MAPK signaling from endomembranes. Mol. Oncol. 2009;3:297–307
  46. Koto K, Horie N, Kimura S, Murata H, Sakabe T, Matsui T, et al. Clinically relevant dose of zoledronic acid inhibits spontaneous lung metastasis in a murine osteosarcoma model. Cancer Lett. 2009;274:271–278
  47. Yano S, Zhang H, Hanibuchi M, Miki T, Goto H, Uehara H, et al. Combined therapy with a new bisphosphonate, minodronate (YM529), and chemotherapy for multiple organ metastases of small cell lung cancer cells in severe combined immunodeficient mice. Clin. Cancer Res. 2003;9:5380–5385
  48. Hiraga T, Williams PJ, Ueda A, Tamura D, Yoneda T. Zoledronic acid inhibits visceral metastases in the 4T1/luc mouse breast cancer model. Clin. Cancer Res. 2004;10:4559–4567
  49. Merrell MA, Wakchoure S, Ilvesaro JM, Zinn K, Gehrs B, Lehenkari PP, et al. Differential effects of Ca(2+) on bisphosphonate-induced growth inhibition in breast cancer and mesothelioma cells. Eur. J. Pharmacol. 2007;559:21–31
  50. Wakchoure S, Merrell MA, Aldrich W, Millender-Swain T, Harris KW, Triozzi P, et al. Bisphosphonates inhibit the growth of mesothelioma cells in vitro and in vivo. Clin. Cancer Res. 2006;12:2862–2868
  51. Raizon A, Schwartz A, Hix W, Rockoff SD. Calcification as a sign of sarcomatous degeneration of malignant pleural mesotheliomas: a new CT finding. J. Comput. Assist. Tomogr. 1996;20:42–44
  52. Liu F, Misra P, Lunsford EP, Vannah JT, Liu Y, Lenkinski RE, et al. A dose- and time-controllable syngeneic animal model of breast cancer microcalcification. Breast Cancer Res. Treat. 2009;
  53. Barr FA, Gruneberg U. Cytokinesis: placing and making the final cut. Cell. 2007;131:847–860
  54. Yoshida S, Bartolini S, Pellman D. Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev. 2009;23:810–823

PII: S0304-3835(10)00096-0

doi: 10.1016/j.canlet.2010.02.008

Cancer Letters
Volume 294, Issue 2 , Pages 245-253 , 28 August 2010

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