Effects of insulin-like growth factor binding protein-3 and farnesyltransferase inhibitor SCH66336 on Akt expression and apoptosis in non-small-cell lung cancer cells

Journal of the National Cancer Institute

Volumn 96, Issue 20, 2004, Pages 1536-1548

  Lee, Ho Young ^a   Moon, Hojin ^b   Chun, Kyung Hee ^a   Chang, Yoon Soo ^a   Hassan, Khaled ^a   Ji, Lin ^a   Lotan, Reuben ^a   Khuri, Fadlo R ^c   Hong, Waun Ki ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ADENOVIRUS VECTOR; DIMETHYL SULFOXIDE; LONAFARNIB; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN FARNESYLTRANSFERASE INHIBITOR; PROTEIN KINASE B; RAS PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; AKT1 PROTEIN, HUMAN; ANTINEOPLASTIC AGENT; ENZYME INHIBITOR; FARNESYL TRANS TRANSFERASE; MAP2K1 PROTEIN, HUMAN; MAP2K1 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; ONCOPROTEIN; PIPERIDINE DERIVATIVE; PROTEIN SERINE THREONINE KINASE; PYRIDINE DERIVATIVE; TRANSACTIVATOR PROTEIN; TRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; FEMALE; FLOW CYTOMETRY; IC 50; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VOLUME; TUMOR XENOGRAFT; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ADENOVIRUS; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENE VECTOR; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG TUMOR; METABOLISM; NUDE MOUSE; ONCOGENE RAS; SERODIAGNOSIS; XENOGRAFT;

ADENOVIRIDAE; ALKYL AND ARYL TRANSFERASES; ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; DRUG SYNERGISM; ENZYME INHIBITORS; FARNESYLTRANSTRANSFERASE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE PRODUCTS, TAT; GENES, RAS; GENETIC VECTORS; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; LUNG NEOPLASMS; MAP KINASE KINASE 1; MICE; MICE, NUDE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PIPERIDINES; PRECIPITIN TESTS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; RAS PROTEINS; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 6944229580     PISSN: 00278874     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnci/djh286     Document Type: Article

References (56)

1. Gibbs JB. Anticancer drug targets: growth factors and growth factor signaling. J Clin Invest 2000;105:9-13.
2. Brodt P, Samani A, Navab R. Inhibition of the type-I insulin-like growth factor receptor expression and signaling: novel strategies for antimetastatic therapy. Biochem Pharmacol 2000;60:1101-7.
3. Zhang D, Brodt P. Type 1 insulin-like growth factor regulates MT1-MMP synthesis and tumor invasion via PI 3-kinase/Akt signaling. Oncogene 2003;22:974-82.
4. Mauro L, Salerno M, Morelli C, Boterberg T, Bracke ME, Surmacz E. Role of the IGF-I receptor in the regulation of cell-cell adhesion: implications in cancer development and progression. J Cell Physiol 2003;194:108-16.
5. Macaulay VM, Salisbury AJ, Bohula EA, Playford MP, Smorodinsky NI, Shiloh Y. Downregulation of the type 1 insulin-like growth factor in mouse melanoma cells is associated with enhanced radiosensitivity and impaired activation of Atm kinase. Oncogene 2001;20:4029-40.
6. Benini S, Manara MC, Baldini N, Cerisano V, Serra M, Mercuri M, et al. Inhibition of insulin-like growth factor I receptor increases the antitumor activity of doxorubicin and vincristine against Ewing's sarcoma cells. Clin Cancer Res 2001;7:1790-97.
7. Quinn KA, Treston AM, Unsworth EJ, Miller MJ, Vos M, Grimley C, et al. Insulin-like growth factor expression in human cancer cell lines. J Biol Chem 1996;271:11477-83.
8. Shigematsu K, Kataoka Y, Kamito T, Karihara M, Niwa M, Tsuchiyama H. Partial characterization of insulin-like growth factor-1 in primary human lung cancers using immunohistochemical and receptor autoradiographic techniques. Cancer Res 1990;50:2481-90.
9. Lee HY, Chun KH, Liu B, Wiehle SA, Cristiano RJ, Hong WK, et al. Insulin-like growth factor binding protein-3 inhibits the growth of non-small cell lung cancer. Cancer Res 2002;62:3530-7.
10. Chang YS, Wang L, Liu D, Mao L, Khuri FR, Hong WK, et al. Methylation of IGFBP-3 promoter and prognosis of patients with stage I non-small cell lung cancer. Clin Cancer Res 2002;8:3669-75.
11. Chang YS, Gong K, Sun S, Liu D, El-Naggar A, Khuri FR, et al. Clinical significance of IGFBP-3 expression in stage I non-small cell lung cancer. Clin Cancer Res 2002;8:3796-802.
12. Yu H, Spitz MR, Mistry J, Gu J, Hong WK, Wu X. Plasma levels of insulin-like growth factor-I and lung cancer risk: a case-control analysis. J Natl Cancer Inst 1999;91:151-6.
13. London SJ, Yuan JM, Travlos GS, Gao YT, Wilson RE, Ross RK, et al. Insulin-like growth factor I, IGF-binding protein 3, and lung cancer risk in a prospective study of men in China. J Natl Cancer Inst 2002;94:749-54.
14. Rajah R, Valentinis B, Cohen P. Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-β1 on programmed cell death through a p53- and IGF-independent mechanism. J Biol Chem 1997;272:12181-8.
15. Leal SM, Liu Q, Huang SS, Huang JS. The type V transforming growth factor β receptor is the putative insulin-like growth factor binding protein 3 receptor. J Biol Chem 1997;272:20572-6.
16. Qingnan Y, Banerjee K, Paterson, J, Alami N, Shiry L, Leyland-Jones B. Insulin-like growth factor binding protein-3: single-agent and synergistic effects with chemotherapeutic drugs on solid tumor models [abstract 1437]. American Association for Cancer Research, 2003 Jul 11-14.
17. Martin JL, Baxter RC. Oncogenic ras causes resistance to the growth inhibitor insulin-like growth factor binding protein-3 (IGFBP-3) in breast cancer cells. J Biol Chem 1999;274:16407-11.
18. Polosa R, Prosperini G, Leir SH, Holgate ST, Lackie PM, Davies DE. Expression of c-erbB receptors and ligands in human bronchial mucosa. Am J Respir Cell Mol Biol 1999;20:914-23.
19. Mills NE, Fishman CL, Rom WN, Dubin N, Jacobson DR. Increased prevalence of K-ras oncogene mutations in lung adenocarcinoma. Cancer Res 1995;55:1444-7.
20. Rusch V, Baserga R, Cordon-Cardo C, Orazem J, Zaman M, Hoda S, et al. Differential expression of the epidermal growth factor receptor and its ligands in primary non-small cell lung cancers and adjacent benign lung. Cancer Res 1993;53:2379- 85.
21. Kurie JM, Shin HL Lee JS, Morice RC, Ro JY, Lippman SM, et al. Increased epidermal growth factor receptor expression in metaplastic bronchial epithelium. Clin Cancer Res 1996;2:1787-93.
22. Sugio, K, Kishimoto Y, Virmani AK, Hung JY, Gazdar AF. K-ras mutations are a relatively late event in the pathogenesis of lung carcinomas. Cancer Res 1994;54:5811-5.
23. Soria JM, Lee HY, Lee JI, Wang L, Issa JP, Kemp BL, et al. Lack of PTEN expression in NSCLC is related to promoter methylation. Clin Cancer Res 2002;8:1178-94.
24. Massion PP, Kuo WL, Stokoe D, Olshen AB, Treseler PA, Chin K, et al. Genomic copy number analysis of non-small cell lung cancer using array comparative genomic hybridization: implications of the phosphatidylinositol 3-kinase pathway. Cancer Res 2002;62:3636-40.
25. Njoroge FG, Vibulbhan B, Pinto P, Bishop WR, Brayant MS, Nomeir AA, et al. Potent, selective, and orally bioavailable tricyclic pyridyl acetamide N-oxide inhibitors of farnesyl protein transferase with enhanced in vivo antitumor activity. J Med Chem 1998;41:1561-7.
26. Liu M, Bryant MS, Chen J, Lee S, Yaremko B, Lipari P, 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.
27. Nielsen LL, Shi B, Hajian G, Yaremko B, Lipari P, Ferrari E, et al. Combination therapy with the farnesyl protein transferase inhibitor SCH66336 and SCH58500 (p53 adenovirus) in preclinical cancer models. Cancer Res 1999;59:5896-901.
28. Adjei AA, Davis JN, Bruzek LM, Erlichman C, Kaufmann SH. Synergy of the protein farnesyltransferase inhibitor SCH66336 and cisplatin in human cancer cell lines. Clin Cancer Res 2001;7:1438-45.
29. Shi B, Yaremko B, Hajian G, Terracina G, Bishop WR, Liu M, et al. The farnesyl protein transferase inhibitor SCH66336 synergizes with taxanes in vitro and enhances their antitumor activity in vivo. Cancer Chemother Pharmacol 2000;46:387-93.
30. Bueno OF, De Windt LJ, Tymitz KM, Witt SA, Kimball TR, Klevitsky R, et al. The MEK1-ERK1/2 signaling pathway promotes compensated cardiac hypertrophy in transgenic mice. EMBO J 2000;19:6341-50.
31. Chun KH, Kosmeder JW, Sun S, Pezzuto JM, Lotan R, Hong WK, et al. Chemopreventive effects of deguelin, a naturally occurring PI3K/Akt inhibitor, during the malignant transformation of human bronchial epithelial cells. J Natl Cancer Inst 2003;95:291-302.
32. Gibbs JB, Graham SL, Hartman GD, Koblan KS, Kohl NE, Omer CA, et al. Farnesyltransferase inhibitors versus Ras inhibitors. Curr Opin Chem Biol 1997;1:197-203.
33. Nagahara H, Vocero-Akbani AM, Snyder EL, Ho A, Latham DG, Lissy NA, et al. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 1998;4:1449-52.
34. Chang YS, Wang L, Mao L, Karpen SJ, Hong WK, Lee HY. Mechanisms underlying lack of insulin like-growth factor binding protein-3 expression in NSCLC cells. Oncogene 2004;23:6569-80.
35. Bowman AW, Azzalini A. Applied smoothing techniques for data analysis: the kernel approach with S-plus Illustrations. Oxford (U.K.): Oxford University Press; 1997.
36. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regal 1984;22:27-55.
37. Lee HY, Sueoka N, Hong WK, Mangelsdorf DJ, Claret FX, and Kurie JM. All-trans-retinoic acid inhibits Jun N-terminal kinase by increasing dual-specificity phosphatase activity. Mol Cell Biol 1999;19:1973-80.
38. Lesur O, Brisebois M, Thibodeau A, Chagnon F, Lane D, Fullop T. Role of IFN-gamma and IL-2 in rat lung epithelial cell migration and apoptosis after oxidant injury. Am J Physiol Lung Cell Mol Physiol 2004;286:L4-14.
39. Butler AA, Blakesley VA, Poulaki V, Tsokos M, Wood TL, Le Roith D, et al. Stimulation of tumor growth by recombinant human insulin-like growth factor-I (IGF-I) is dependent on the dose and the level of IGF-I receptor expression. Cancer Res 1998;58:3021-7.
40. Greco WR, Bravo G, Parsons JC. The search for synergy: a critical review from a response surface perspective. Pharmacol Rev 1995;47:331-85.
41. Mitsudomi T, Steinberg SM, Nau MM, Carbone D, D'Amico D, Bodner S, et al. p53 gene mutations in non-small cell lung cancer cell lines and their correlation with the presence of ras mutations and clinical features. Oncogene 1992;7:171-80.
42. Mitsudomi T, Viallet J, Mulshine L, Linnoila RI, Minna JD, Gazdar AF. Mutations of ras genes distinguish a subset of non-small cell lung cancer cell lines from small-cell lung cancer cell lines. Oncogene 1991;6:1353-62.
43. Leverrier Y, Thomas J, Mathieu A, Low W, Blanquier B, Marvel J. Role of PI3-kinase in Bcl-X induction and apoptosis inhibition mediated by IL-3 or IGF-1 in Baf-3 cells. Cell Death Differ 1999;6:290-6.
44. Nagahara H, Vocero-Akbani AM, Snyder EC, Ho A, Latham DG, Lissy NA, et al. Transduction of full-length TAT fusion proteins into mammalian cells: TAT-p27Kip1 induces cell migration. Nat Med 1998;4:1449-52.
45. Baxter RC. Signaling pathways involved in antiproliferative effects of IGFBP-3: a review. Mol Pathol 2001;54:145-8.
46. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993;74:609-19.
47. Coll ML, Rosen K, Ladeda V, Filmus J. Increased Bcl-xL expression mediates v-Src-induced resistance to anoikis in intestinal epithelial cells. Oncogene 2002;21:2908-13.
48. Conover CA. Regulation and physiological role of insulin-like growth factor binding proteins. Endocr J 1996;43(Suppl)S43-8.
49. Miyamoto S, Yano K, Sugimoto S, Ishii G, Hasebe T, Endoh Y, et al. Matrix metalloproteinase-7 facilitates insulin-like growth factor bioavailability through its proteinase activity on insulin-like growth factor binding protein 3. Cancer Res 2004;64:665-71.
50. Loechel F, Fox JW, Murphy G, Albrechtsen R, Wewer UM. ADAM 12-S cleaves IGFBP-3 and IGFBP-5 and is inhibited by TIMP-3. Biochem Biophys Res Commun 2000;278:511-5.
51. Kleiner DE, Stetler-Stevenson WG. Matrix metalloproteinases and metastasis. Cancer Chemother Pharmacol 1999;43(Suppl):S42-51.
52. Coverley JA, Baxter RC. Phosphorylation of insulin-like growth factor binding proteins. Mol Cell Endocrinol 1997;128:1-5.
53. Schedlich LJ, Nilsen T, John AP, Jans DA, Baxter RC. Phosphorylation of insulin-like growth factor binding protein-3 by deoxyribonucleic acid-dependent protein kinase reduces ligand binding and enhances nuclear accumulation. Endocrinology 2003;144:1984-93.
54. Jiang K, Coppola D, Crespo NC, Nicosia SV, Hamilton AD, Sebti SM, 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.
55. Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994;269:5241-8.
56. Brognard J, Clark AS, Ni Y, Dennis PA. Akt/protein kinase B is constitutively active in non-small cell lung cancer cells and promotes cellular survival and resistance to chemotherapy and radiation. Cancer Res 2001;61:3986-97.