Zoledronic acid potentiates mTOR inhibition and abolishes the resistance of osteosarcoma cells to RAD001 (everolimus): Pivotal role of the prenylation process

Cancer Research

Volumn 70, Issue 24, 2010, Pages 10329-10339

  Moriceau, Gatien ^a   Ory, Benjamin ^a,b   Mitrofan, Laura ^c   Riganti, Chiara ^d   Blanchard, Frédéric ^a   Brion, Régis ^a   Charrier, Céline ^a   Battaglia, Séverine ^a   Pilet, Paul ^e   Denis, Marc G ^f   Shultz, Leonard D ^g   Mönkkönen, Jukka ^c   Rédini, Françoise ^a   Heymann, Dominique ^a  

^a UNIVERSITÉ DE NANTES   (France)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

^d UNIVERSITY OF TURIN   (Italy)

^e Universite de Nantes   (France)

^f INSERM   (France)

^g JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EVEROLIMUS; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAS PROTEIN; ZOLEDRONIC ACID;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE METASTASIS; CANCER CELL CULTURE; CANCER RESISTANCE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHEMOSENSITIVITY; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG POTENTIATION; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROTEIN PRENYLATION; SIGNAL TRANSDUCTION;

EID: 78650330534     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-0578     Document Type: Article

References (44)

1. Rosen GMM , Huvos AG, Gutierrez M, Marcove RC. Chemotherapy, en bloc resection, and prosthetic bone replacement in the treatment of osteogenic sarcoma. Cancer 1976;37:1-11.
2. Provisor AJ, Ettinger LJ, Nachman JB, et al. Treatment of nonmetastatic osteosarcoma of the extremity with preoperative and postoperative chemotherapy: a report from the Children's Cancer Group. J Clin Oncol 1997;15:76-84.
3. Kruh GD. Introduction to resistance to anticancer agents. Oncogene 2003;22:7262-4.
4. Liu WM. Enhancing the cytotoxic activity of novel targeted therapies - is there a role for a combinatorial approach? Curr Clin Pharmacol 2008;3:108-17.
5. Gibbs JB, Oliff A. The potential of farnesyltransferase inhibitors as cancer chemotherapeutics. Annu Rev Pharmacol Toxicol 1997;37:143-66.
6. Coxon FP, Helfrich MH, Van't Hof R, et al. Protein geranylgeranylation is required for osteoclast formation, function, and survival: inhibition by bisphosphonates and GGTI-298. J Bone Miner Res 2000;15:1467-76.
7. Heymann D, Ory B, Gouin F, Green JR, Redini F. Bisphosphonates: new therapeutic agents for the treatment of bone tumors. Trends Mol Med 2004;10:337-43.
8. Mackie PS, Fisher JL, Zhou H, Choong PF. Bisphosphonates regulate cell growth and gene expression in the UMR 106-01 clonal rat osteosarcoma cell line. Br J Cancer 2001,84:951-9.
9. Terpos E, Sezer O, Croucher PI, et al. The use of bisphosphonates in multiple myeloma: recommendations of an expert panel on behalf of the European Myeloma Network. Ann Oncol 2009;20:1303-17.
10. Ory B, Blanchard F, Battaglia S, Gouin F, Redini F, Heymann D. Zoledronic acid activates the DNA S-phase checkpoint and induces osteosarcoma cell death characterized by apoptosis-inducing factor and endonuclease-G translocation independently of p53 and retinoblastoma status. Mol Pharmacol 2007;71:333-43.
11. Ottewell PD, Monkkonen H, Jones M, Lefley DV, Coleman RE, Holen I. Antitumor effects of doxorubicin followed by zoledronic acid in a mouse model of breast cancer. J Natl Cancer Inst 2008;100:1167-78.
12. Heymann D, Ory B, Blanchard F, Heymann MF, Coipeau P, Charrier C, et al. Enhanced tumor regression and tissue repair when zoledronic acid is combined with ifosfamide in rat osteosarcoma. Bone 2005;37:74-86.
13. Ory B, Moriceau G, Redini F, Heymann D. mTOR inhibitors (rapamycin and its derivatives) and nitrogen containing bisphosphonates: bifunctional compounds for the treatment of bone tumours. Curr Med Chem 2007;14:1381-7.
14. Vezina C, Kudelski A, Sehgal SN. Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J Antibiot (Tokyo) 1975;28:721-6.
15. Foster DA, Toschi A. Targeting mTOR with rapamycin: one dose does not fit all. Cell Cycle 2009;8:1026-9.
16. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell 2006;124;471-84.
17. Reiling JH, Sabatini DM. Stress and mTORture signaling. Oncogene 2006,25;6373-83.
18. Petiot A, Pattingre S, Arico S, Meley D, Codogno P. Diversity of signaling controls of macroautophagy in mammalian cells. Cell Struct Funct 2002;27:431-41.
19. Mamane Y, Petroulakis E, LeBacquer O, Sonenberg N. mTOR, translation initiation, and cancer. Oncogene 2006;25:6416-22.
20. MacKenzie AR, von Mehren M. Mechanisms of mammalian target of rapamycin inhibition in sarcoma: present and future. Expert Rev Anticancer Ther 2007;7:1145-54.
21. Khariwala SS, Kjaergaard J, Lorenz R, Van Lente F, Shu S, Strome M. Everolimus (RAD) inhibits in vivo growth of murine squamous cell carcinoma (SCC VII). Laryngoscope 2006;116:814-20.
22. Wan X, Mendoza A, Khanna C, Helman LJ. Rapamycin inhibits ezrin-mediated metastatic behavior in a murine model of osteosarcoma. Cancer Res 2005,65:2406-11.
23. Cutler C, Antin JH. Mammalian target of rapamycin inhibition as therapy for hematologic malignancies. Cancer 2004;101:1478.
24. Kauffman HM, Cherikh WS, Cheng Y, Hanto DW, Kahan BD. Maintenance immunosuppression with target-of-rapamycin inhibitors is associated with a reduced incidence of de novo malignancies. Transplantation 2005;80:883-9.
25. Reddy GK, Mughal TI, Rini BI. Current data with mammalian target of rapamycin inhibitors in advanced-stage renal cell carcinoma. Clin Genitourin Cancer 2006;5:110-3.
26. Haritunians T, Mori A, O'Kelly J, Luong QT, Giles FJ, Koeffler HP. Antiproliferative activity of RAD001 (everolimus) as a single agent and combined with other agents in mantle cell lymphoma. Leukemia 2007;21:333-9.
27. Hougthon PJ, Morton CL, Kolb EA, Gorlick R, Lock R, Carol H, et al. Initial testing (stage 1) of the mTOR inhibitor rapamycin by the pediatric preclinical testing program. Pediatr Blood Cancer 2008:50:799-805. (Pubitemid 351354788)
28. Zhou Q, Deng Z, Zhu Y, Long H, Zhang S, Zhao J. mTOR/p70S6K signal transduction pathway contributes to osteosarcoma progression and patient's prognosis. Med Oncol 2010;27:1239-45.
29. Chawla SP, Tolcher AW, Staddon AP, Schuetze S, D'Amato GZ, Blay JY, et al. Survival results with AP23573, a novel mTOR inhibitor, in patients with advanced soft tissue or bone sarcomas: update of phase II trial. ASCO Annual Meeting Proceedings. J Clin Oncol 2007;25(18S):10076.
30. Jiang BH, Liu LZ. Role of mTOR in anticancer drug resistance: perspectives for improved drug treatment. Drug Resist Updat 2008;11:63-76.
31. Klein B, Pals S, Masse R, et al. Studies of bone and soft-tissue tumours induced in rats with radioactive cerium chloride. Int J Cancer 1977;20:112-9.
32. Kamijo A, Koshino T, Uesugi M, Nitto H, Saito T. Inhibition of lung metastasis of osteosarcoma cell line POS-1 transplanted into mice by thigh ligation. Cancer Lett 2002;188:213-9.
33. Joliat MJ, Umeda S, Lyons BL, Lynes MA, Shultz LD. Establishment and characterization of a new osteogenic cell line (MOS-J) from a spontaneous C57BL/6J mouse osteosarcoma. In Vivo 2002;16:223-8.
34. Laezza C, Fiorentino L, Pisanti S, Gazzerro P, Caraglia M, Portella G, et al. Lovastatin induces apoptosis of k-ras-transformed thyroid cells via inhibition of ras farnesylation and by modulating redox state. J Mol Med 2008;86:341-51.
35. Lamoreux F, Richard P, Wittrant Y, Battaglia S, Pilet P, Trichet V, et al. Therapeutic Relevance of Osteoprotegerin Gene Therapy in Osteosarcoma: Blockade of the Vicious Cycle between Tumor Cell Proliferation and Bone Resorption. Cancer Res 2007;67:7308-18.
36. Bjornsti MA, Houghton PJ. The TOR pathway: a target for cancer therapy. Nat Rev Cancer 2004;4:335-48.
37. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 2002;16:472-87.
38. Hara K, Yonezawa K, Weng QP, Kozlowski MT, Belham C, Avruch J. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J Biol Chem 1998;273:14484-94.
39. Sanchez-Fructuoso AI. Everolimus: an update on the mechanism of action, pharmacokinetics and recent clinical trials. Expert Opin Drug Metab Toxicol 2008;4:807-19.
40. O'Reilly KE, Rojo F, She QB, et al. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 2006;66:1500-8.
41. Kim SH, Zukowski K, Novak RF. Rapamycin effects on mTOR signaling in benign, premalignant and malignant human breast epithelial cells. Anticancer Res 2009;29:1143-50.
42. Kiel C, Filchtinski D, Spoermer M, Schreiber G, Kalbitzer HR, Hermann C. Improved binding raf to Ras.GDP is correlated with biological activity. J Biol Chem 2009;284:319893-902.
43. Konstantinopoulos PA, Karamouzis MV, Papavassiliou AG. Post-translational modifications and regulation of the RAS superfamily of GTPases as anticancer targets. Nat Rev Drug Discov 2007;6:541-55.
44. Wittrant Y, Theoleyre S, Chipoy C, et al. RANKL/RANK/OPG: new therapeutic targets in bone tumours and associated osteolysis. Biochim Biophys Acta 2004;1704:49-57.