Insulin-like growth factor-I receptor signaling pathway induces resistance to the apoptotic activities of SCH66336 (Lonafarnib) through Akt/mammalian target of rapamycin-mediated increases in survivin expression

Clinical Cancer Research

Volumn 14, Issue 5, 2008, Pages 1581-1589

  Seung, Hyun Oh ^a   Jin, Quanri ^a   Kim, Edward S ^a   Khuri, Fadlo R ^b   Lee, Ho Young ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; ADENOVIRUS VECTOR; LONAFARNIB; MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; OSI 868; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN TYROSINE KINASE INHIBITOR; SOMATOMEDIN C RECEPTOR; SURVIVIN; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; GENE ACTIVATION; GENE EXPRESSION; GENE OVEREXPRESSION; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SQUAMOUS CELL CARCINOMA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CARCINOMA, SQUAMOUS CELL; CELL CYCLE; DRUG RESISTANCE, NEOPLASM; HEAD AND NECK NEOPLASMS; HUMANS; LUNG NEOPLASMS; MICROTUBULE-ASSOCIATED PROTEINS; NEOPLASM PROTEINS; PHOSPHORYLATION; PIPERIDINES; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; RECEPTOR, IGF TYPE 1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 40949145602     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-07-0952     Document Type: Article

References (56)

1. Parkin DM, Pisani P, Ferlay J. Estimates of the worldwide incidence of 25 major cancers in 1990. Int J Cancer 1999;80:827-41.
2. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-30.
3. Martinez JC, Otley CC, Okuno SH, Foote RL, Kasperbauer JL. Chemotherapy in the management of advanced cutaneous squamous cell carcinoma in organ transplant recipients: theoretical and practical considerations. Dermatol Surg 2004;30:679-86.
4. Browman GP, Hodson DI, Mackenzie RJ, Bestic N, Zuraw L. Choosing a concomitant chemotherapy and radiotherapy regimen for squamous cell head and neck cancer: a systematic review of the published literature with subgroup analysis. Head Neck 2001;23:579-89.
5. Katz ME, McCormick F. Signal transduction from multiple Ras effectors. Curr Opin Genet Dev 1997;7:75-9.
6. Mendelsohn J. The epidermal growth factor receptor as a target for cancer therapy. Endocr Relat Cancer 2001;8:3-9.
7. Rodriguez-Viciana P, Warne PH, Dhand R, et al. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature 1994;370:527-32.
8. Massarelli E, Liu DD, Lee JJ, et al. Akt activation correlates with adverse outcome in tongue cancer. Cancer 2005;104:2430-6.
9. Campbell PM, Der CJ. Oncogenic Ras and its role in tumor cell invasion and metastasis. Semin Cancer Biol 2004;14:105-14.
10. Crul M, de Klerk GJ, Beijnen JH, Schellens JH. Ras biochemistry and farnesyl transferase inhibitors: a literature survey. Anticancer Drugs 2001;12:163-84.
11. O'Regan RM, Khuri FR. Farnesyl transferase inhibitors: the next targeted therapies for breast cancer? Endocr Relat Cancer 2004;11:191-205.
12. Oh SH, Kim WY, Kim JH, et al. Identification of insulin-like growth factor binding protein-3 as a farnesyl transferase inhibitor SCH66336-induced negative regulator of angiogenesis in head and neck squamous cell carcinoma. Clin Cancer Res 2006;12:653-61.
13. Han JY, Oh SH, Morgillo F, et al. Hypoxia-inducible factor 1α and antiangiogenic activity of farnesyltransferase inhibitor SCH66336 in human aerodigestive tract cancer. J Natl Cancer Inst 2005;97:1272-86.
14. Basso AD, Mirza A, Liu G, Long BJ, Bishop WR, Kirschmeier P. The farnesyl transferase inhibitor (FTI) SCH66336 (lonafarnib) inhibits Rheb farnesylation and mTOR signaling. Role in FTI enhancement of taxane and tamoxifen anti-tumor activity. J Biol Chem 2005;280:31101-8.
15. Ashar HR, James L, Gray K, et al. The farnesyl transferase inhibitor SCH 66336 induces a G(2)→M or G(1) pause in sensitive human tumor cell lines. Exp Cell Res 2001;262:17-27.
16. Nagasu T, Yoshimatsu K, Rowell C, Lewis MD, Garcia AM. Inhibition of human tumor xenograft growth by treatment with the farnesyl transferase inhibitor B956. Cancer Res 1995;55:5310-4.
17. Lantry LE, Zhang Z, Yao R, et al. Effect of farnesyltransferase inhibitor FTI-276 on established lung adenomas from A/J mice induced by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone. Carcinogenesis 2000;21:113-6.
18. Adjei AA, Erlichman C, Davis JN, et al. A phase I trial of the farnesyl transferase inhibitor SCH66336: evidence for biological and clinical activity. Cancer Res 2000;60:1871-7.
19. Eskens FA, Awada A, Cutler DL, et al. Phase I and pharmacokinetic study of the oral farnesyl transferase inhibitor SCH 66336 given twice daily to patients with advanced solid tumors. J Clin Oncol 2001;19:1167-75.
20. Chun KH, Lee HY, Hassan K, Khuri F, Hong WK, Lotan R. Implication of protein kinase B/Akt and Bcl-2/Bcl-XL suppression by the farnesyl transferase inhibitor SCH66336 in apoptosis induction in squamous carcinoma cells. Cancer Res 2003;63:4796-800.
21. Blumenschein G, Ludwig C, Thomas G. A randomized phase III trial comparing lonafarnib/carboplatin/paclitaxel versus carboplatin/paclitaxel (CP) in chemotherapy-naive patients with advanced or metastatic non-small cell lung cancer (NSCLC) [abstract O-082]. In: Proceedings from the 11th World Conference on Lung Cancer, Barcelona, Spain, 2005.
22. Sharma S, Kemeny N, Kelsen DP, et al. A phase II trial of farnesyl protein transferase inhibitor SCH 66336, given by twice-daily oral administration, in patients with metastatic colorectal cancer refractory to 5-fluorouracil and irinotecan. Ann Oncol 2002;13:1067-71.
23. Borthakur G, Kantarjian H, Daley G, et al. Pilot study of lonafarnib, a farnesyl transferase inhibitor, in patients with chronic myeloid leukemia in the chronic or accelerated phase that is resistant or refractory to imatinib therapy. Cancer 2006;106:346-52.
24. Krause CJ, Carey TE, Ott RW, Hurbis C, McClatchey KD, Regezi JA. Human squamous cell carcinoma. Establishment and characterization of new permanent cell lines. Arch Otolaryngol 1981;107:703-10.
25. Carney DN, Gazdar AF, Bepler G, et al. Establishment and identification of small cell lung cancer cell lines having classic and variant features. Cancer Res 1985;45:2913-23.
26. Mesri M, Wall NR, Li J, Kim RW, Altieri DC. Cancer gene therapy using a survivin mutant adenovirus. J Clin Invest 2001;108:981-90.
27. Alley MC, Scudiero DA, Monks A, et al. Feasibility of drug screening with panels of human tumor cell lines using a microculture tetrazolium assay. Cancer Res 1988;48:589-601.
28. Liu M, Bryant MS, Chen J, et al. Antitumor activity of SCH 66336, an orally bioavailable tricyclic inhibitor of farnesyl protein transferase, in human tumor xenograft models and wap-ras transgenic mice. Cancer Res 1998;58:4947-56.
29. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer 2003;3:46-54.
30. Mitsiades CS, Mitsiades N, Poulaki V, et al. Activation of NF-κB and upregulation of intracellular antiapoptotic proteins via the IGF-1/Akt signaling in human multiple myeloma cells: therapeutic implications. Oncogene 2002;21:5673-83.
31. Peng X-H, Karna P, Cao Z, Jiang B-H, Zhou M, Yang L. Cross-talk between epidermal growth factor receptor and hypoxia-inducible factor-1α signal pathways increases resistance to apoptosis by up-regulating survivin gene expression. J Biol Chem 2006;281:25903-14.
32. Mirza A, McGuirk M, Hockenberry TN, et al. Human survivin is negatively regulated by wild-type p53 and participates in p53-dependent apoptotic pathway. Oncogene 2002;21:2613-22.
33. Takada Y, Khuri FR, Aggarwal BB. Protein farnesyltransferase inhibitor (SCH 66336) abolishes NF-κB activation induced by various carcinogens and inflammatory stimuli leading to suppression of NF-κB-regulated gene expression and up-regulation of apoptosis. J Biol Chem 2004;279:26287-99.
34. Chakravarti A, Loeffler JS, Dyson NJ. Insulin-like growth factor receptor I mediates resistance to antiepidermal growth factor receptor therapy in primary human glioblastoma cells through continued activation of phosphoinositide 3-kinase signaling. Cancer Res 2002;62:200-7.
35. Lu Y, Zi X, Zhao Y, Mascarenhas D, Pollak M. Insulin-like growth factor-I receptor signaling and resistance to trastuzumab (Herceptin). J Natl Cancer Inst 2001;93:1852-7.
36. Lee CT, Park KH, Adachi Y, et al. Recombinant adenoviruses expressing dominant negative insulin-like growth factor-I receptor demonstrate antitumor effects on lung cancer. Cancer Gene Ther 2003;10:57-63.
37. Vaira V, Lee CW, Goel HL, Bosari S, Languino LR, Altieri DC. Regulation of survivin expression by IGF-1/mTOR signaling. Oncogene 2007;26:2678-84.
38. Jiang K, Coppola D, Crespo NC, et al. The phosphoinositide 3-OH kinase/AKT2 pathway as a critical target for farnesyltransferase inhibitor-induced apoptosis. Mol Cell Biol 2000;20:139-48.
39. Grabowski P, Kuhnel T, Muhr-Wilkenshoff F, et al. Prognostic value of nuclear survivin expression in oesophageal squamous cell carcinoma. Br J Cancer 2003;88:115-9.
40. Miller M, Smith D, Windsor A, Kessling A. Survivin gene expression and prognosis in recurrent colorectal cancer. Gut 2001;48:137-8.
41. Monzo M, Rosell R, Felip E, et al. A novel anti-apoptosis gene: re-expression of survivin messenger RNA as a prognosis marker in non-small-cell lung cancers. J Clin Oncol 1999;17:2100-4.
42. Kennedy SM, O'Driscoll L, Purcell R, et al. Prognostic importance of survivin in breast cancer. Br J Cancer 2003;88:1077-83.
43. Blanc-Brude OP, Mesri M, Wall NR, Plescia J, Dohi T, Altieri DC. Therapeutic targeting of the survivin pathway in cancer: initiation of mitochondrial apoptosis and suppression of tumor-associated angiogenesis. Clin Cancer Res 2003;9:2683-92.
44. Morgillo F, Kim WY, Kim ES, Ciardiello F, Hong WK, Lee HY. Implication of the insulin-like growth factor-IR pathway in the resistance of non-small cell lung cancer cells to treatment with gefitinib. Clin Cancer Res 2007;13:2795-803.
45. Morgillo F, Woo JK, Kim ES, Hong WK, Lee HY. Heterodimerization of insulin-like growth factor receptor/epidermal growth factor receptor and induction of survivin expression counteract the antitumor action of erlotinib. Cancer Res 2006;66:10100-11.
46. Jin Q, Menter DG, Mao L, Hong WK, Lee H-Y. Survivin expression in normal human bronchial epithelial cells: an early and critical step in tumorigenesis induced by tobacco exposure. Carcinogenesis 2007. In press.
47. Pratt MA, Niu MY, Renart LI. Regulation of survivin by retinoic acid and its role in paclitaxel-mediated cytotoxicity in MCF-7 breast cancer cells. Apoptosis 2006;11:589-605.
48. Lu B, Mu Y, Cao C, et al. Survivin as a therapeutic target for radiation sensitization in lung cancer. Cancer Res 2004;64:2840-5.
49. Ikezoe T, Nishioka C, Bandobashi K, et al. Longitudinal inhibition of PI3K/Akt/mTOR signaling by LY294002 and rapamycin induces growth arrest of adult T-cell leukemia cells. Leuk Res 2007;31:673-82.
50. 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.
51. Sarbassov DD, Ali SM, Sengupta S, et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 2006;22:159-68.
52. Glass TL, Liu TJ, Yung WK. Inhibition of cell growth in human glioblastoma cell lines by farnesyltransferase inhibitor SCH66336. Neuro-oncol 2000;2:151-8.
53. Brassard DL, English JM, Malkowski M, Kirschmeier P, Nagabhushan TL, Bishop WR. Inhibitors of farnesyl protein transferase and MEK1,2 induce apoptosis in fibroblasts transformed with farnesylated but not geranylgeranylated H-Ras. Exp Cell Res 2002;273:138-46.
54. Janmaat ML, Rodriguez JA, Gallegos-Ruiz M, Kruyt FA, Giaccone G. Enhanced cytotoxicity induced by gefitinib and specific inhibitors of the Ras or phosphatidyl inositol-3 kinase pathways in non-small cell lung cancer cells. Int J Cancer 2006;118:209-14.
55. Lee HY, Chun KH, Liu B, et al. Insulin-like growth factor binding protein-3 inhibits the growth of non-small cell lung cancer. Cancer Res 2002;62:3530-7.
56. Sun SY, Liu X, Zou W, Yue P, Marcus AI, Khuri FR. The farnesyltransferase inhibitor lonafarnib induces CCAAT/enhancer-binding protein homologous protein-dependent expression of death receptor 5, leading to induction of apoptosis in human cancer cells. J Biol Chem 2007;282:18800-9.