The farnesyltransferase inhibitor R115777 (ZARNESTRA®) enhances the pro-apoptotic activity of interferon-α through the inhibition of multiple survival pathways

International Journal of Cancer

Volumn 121, Issue 10, 2007, Pages 2317-2330

  Caraglia, Michele ^a   Marra, Monica ^a   Viscomi, Caterina ^b,c   D'Alessandro, Anna Maria ^d   Budillon, Alfredo ^a   Meo, Giuseppina ^a   Arra, Claudio ^a   Barbieri, Antonio ^a   Rapp, Ulf R ^e   Baldi, Alfonso ^d   Tassone, Pierfrancesco ^b,c   Venuta, Salvatore ^b,c   Abbruzzese, Alberto ^d   Tagliaferri, Pierosandro ^b,c  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^c Oncology Center Germaneto   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Apoptosis; Epidermoid cancer; Farnesyl transferase inhibitor; Interferon ; Ras

Indexed keywords

ALPHA2B INTERFERON; CYTOKINE; EPIDERMAL GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BAD; PROTEIN BCL 2; PROTEIN FARNESYLTRANSFERASE INHIBITOR; RAF PROTEIN; RAS PROTEIN; SERINE; TIPIFARNIB;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CELL SURVIVAL; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; ISOPRENYLATION; MONOTHERAPY; MOUSE; MOUSE STRAIN; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL SURVIVAL; FARNESYLTRANSTRANSFERASE; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INTERFERON-ALPHA; MICE; MICE, INBRED BALB C; MICE, NUDE; MITOCHONDRIA; NEOPLASMS; PHOSPHOSERINE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-RAF; QUINOLONES; RAS PROTEINS; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 35348852712     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22964     Document Type: Article

References (40)

1. End DW, Smets G, Todd AV, Applegate TL, Fuery CJ, Angibaud P, Venet M, Sanz G, Poignet H, Skrzat S, Devine A, Wouters W, et al. Characterization of the antitumour effects of the selective farnesyl protein transferase inhibitor R115777 in vivo and in vitro. Clin Cancer Res 2001;7:3544-50.
2. End DW. Farnesyl protein transferase inhibitors and other therapies targeting the Ras signal transduction pathway. Invest New Drugs 1999;17:241-58.
3. Mesa RA. Tipifarnib: farnesyl transferase inhibition at a crossroads. Expert Rev Anticancer Ther 2006;10:313-19.
4. Kelland LR, Smith V, Valenti M, Patterson L, Clarke PA, Detre S, End D, Howes AJ, Dowsett M, Workman P, Johnston SR. Preclinical antitumour activity and pharmacodynamic studies with the farnesyl protein transferase inhibitor R115777 in human breast cancer. Clin Cancer Res 2001;7:3544-50.
5. Budillon A, Tagliaferri P, Caraglia M, Torrisi MR, Normanno N, Iacobelli S, Palmieri G, Stoppelli MP, Frati L, Bianco AR. Upregulation of epidermal growth factor receptor induced by α-interferon in human epidermoid cancer cells. Cancer Res 1991;51:1294-9.
6. Selleri C, Maciejewski JP, Montuori N, Ricci P, Visconte V, Serio B, Luciano L, Rotoli B. Involvement of nitric oxide in farnesyltransferase inhibitor-mediated apoptosis in chronic myeloid leukemia cells. Blood 2003;102:1490-1498.
7. Clark-Lewis I, Sanghera JS, Pelech SL. Definition of a consensus sequence for peptide substrate recognition by p44mpk: the meiosis-activated myelin basic protein kinase. J Biol Chem 1991;266:15180-4.
8. Shields JM, Pruitt K, Mc Fall A, Shaub A, Der CJ. Understanding Ras: 'it ain't over 'til it's over'. Trends Cell Biol 2000;10:147-54.
9. Gullick WJ, Marsden JJ, Whittle N. Expression of epidermal growth factor receptors on human cervical ovarian and vulval carcinomas. Cancer Res 1986;46:285-92.
10. Foncea R, Galvez A, Perez V, Morales MP, Calixto A, Melendez J, Gonzalez-Jara F, Diaz-Araya G, Sapag-Hagar M, Sugden PH, LeRoith D, Lavandero S. Extracellular regulated kinase, but not protein kinase C, is an antiapoptotic signal of insulin-like growth factor-1 on cultured cardiac myocytes. Biochem Biophys Res Commun 2000;273:736-44.
11. Kang C, Yoo S, Hwang B, Kim KW, Kim DW, Kim CM, Kim SH, Chung BS. The inhibition of ERK/MAPK not the activation of JNK/SAPK is primarily required to induce apoptosis in chronic myelogenous leukemic K562 cells. Leuk Res 2000;24:527-34.
12. Jan MS, Liu HS, Lin YS. Bad overexpression sensitizes NIH/3T3 cells to undergo apoptosis which involves caspase activation and ERK inactivation. Biochem Biophys Res Commun 1999;264: 724-9.
13. Nunez G, Benedict MA, Hu Y, Inohara N. Caspases: the proteases of the apoptotic pathway. Oncogene 1998;17:3237-45.
14. Thyrell L, Erickson S, Zhivotovsky B, Pokrovskaja K, Sangfelt O, Castro J, Einhorn S, Grander D. Mechanisms of Interferon-α induced apoptosis in malignant cells. Oncogene 2002;21:1251-62.
15. Caraglia M, Pinto A, Correale P, Zagonel V, Genua G, Leardi A, Pepe S, Bianco AR, Tagliaferri P. 5-Aza-2′-deoxycytidine induces growth inhibition and upregulation of epidermal growth factor receptor on human epithelial cancer cells. Ann Oncol 1994;5:269-76.
16. Budillon A, Di Gennaro E, Caraglia M, Barbarulo D, Abbruzzese A Tagliaferri P. 8-Cl-cAMP antagonizes mitogen-activated protein kinase activation and cell growth stimulation induced by epidermal growth factor. Br J Cancer 1999;81:1134-41.
17. Caraglia M, Tagliaferri P, Marra M, Giuberti G, Budillon A, Gennaro ED, Pepe S, Vitale G, Improta S, Tassone P, Venuta S, Bianco AR, et al. EGF activates an inducible survival response via the RAS → Erk-1/2 pathway to counteract interferon-α-mediated apoptosis in epidermoid cancer cells. Cell Death Differ 2003;10:218-29.
18. Tagliaferri P, Caraglia M, Muraro R, Budillon A, Pinto A, Bianco AR. Pharmacological modulation of peptide growth factor receptor expression on tumour cells as a basis for cancer therapy. Anticancer Drugs 1994;5:379-93.
19. Caraglia M, Abbruzzese A, Leardi A, Pepe S, Budillon A, Baldassare G, Selleri C, Lorenzo SD, Fabbrocini A, Giuberti G, Vitale G, Lupoli G, et al. Interferon-α induces apoptosis in human KB cells through a stress-dependent mitogen activated protein kinase pathway that is antagonized by epidermal growth factor. Cell Death Differ 1999;6:773-80.
20. Widmann C, Gibson S, Jarpe MB, Johnson GL. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 1999;79:143-80.
21. Garrington TP, Johnson GL. Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr Opin Cell Biol 1999;11:211-18.
22. Yan CYI, Greene LA. Prevention of PC12 cell death by N-acetyl- cysteine requires activation of the Ras pathway. J Neurosi 1998;18:4042-9.
23. Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Tanaka M, Shiojima I, Hiroi Y, Yazaki Y. Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest 1997;100:1813-21.
24. von Gise A, Lorenz P, Wellbrock C, Hemmings B, Berberich-Siebelt F, Rapp UR, Troppmair J. Apoptosis suppression by Raf-1 and MEK1 requires MEK- and phosphatidylinositol 3-kinase-dependent signals. J Mol Cell Biol 2001;21:2324-36.
25. Zhou H, Li XM, Meinkoth J, Pittman RN. Akt regulates cell survival and apoptosis at a postmitochondrial level. J Cell Biol 2000;151:483-94.
26. Bruder JT, Heidecker G, Rapp UR. Serum-, TPA-, and. Ras-induced expression from. Ap-1/Ets-driven promoters requires. Raf-1 kinase. Genes Dev 1992;6:545-56.
27. Chou TC, Motzer RJ, Tong Y, Bosl GJ. Computerized quantitation of synergism and antagonism of taxol, topotecan, and cisplatin against human teratocarcinoma cell growth: a rational approach to clinical protocol design. J Natl Cancer Inst 1994;86:1517-24.
28. Magne N, Fischel JL, Dubreuil A, Formento P, Marcie S, Lagrange JL, Milano G. Sequence-dependent effects of ZD1839 ('Iressa') in combination with cytotoxic treatment in human head and neck cancer. Br J Cancer 2002;86:819-27.
29. Solorzano CC, Hwang R, Baker CH, Bucana CD, Pisters PW, Evans DB, Killion JJ, Fidler IJ. Administration of optimal biological dose and schedule of interferon α combined with gemcitabine induces apoptosis in tumor-associated endothelial cells and reduces growth of human pancreatic carcinoma implanted orthotopically in nude mice. Clin Cancer Res 2003;9:1858-67.
30. Sommer K, Peters SO, Robins IH, Raap M, Wiedemann GJ, Remmert S, Sieg P, Bittner C, Feyerabend T. A preclinical model for experimental chemotherapy of human head and neck cancer. Int J Oncology 2001;18:1145-9.
31. Teicher BA. In vivo tumour response end points. In: Teicher BA, ed. Tumour models in cancer research. Totowa, NJ: Humana Press, 2002. 593-616.
32. Zhang B, Prendergast GC, Fenton RG. Farnesyltransferase inhibitors reverse Ras-mediated inhibition of Fas gene expression. Cancer Res 2002;62:450-8.
33. Caraglia M, Budillon A, Tagliaferri P, Marra M, Abbruzzese A, Caponigro F. Isoprenylation of intracellular proteins as a new target for the therapy of human neoplasms: preclinical and clinical implications. Curr Drug Targets 2005;6:301-23.
34. Jin S, Zhuo Y, Guo W, Field J. p21-activated Kinase 1 (Pak1)-dependent phosphorylation of Raf-1 regulates its mitochondrial localization, phosphorylation of BAD, and Bcl-2 association. J Biol Chem 2005;280:24698-705.
35. Darnell JE, Jr, Kerr IM, Stark GR. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 1994;264:1415-21.
36. Wang H, Rapp U, Reed JC. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 1996;87:629-38.
37. Baccarini M. An old kinase on a new path. Raf and apoptosis. Cell Death Differ 2002;9:783-5.
38. Hindley A, Kolch W. Extracellular signal regulated kinase (ERK)/mitogen activated protein kinase (MAPK)-independent functions of Raf kinases. J Cell Sci 2002;115:1575-81.
39. Kerkhoff E, Rapp UR. Cell cycle targets of Ras/Raf signalling. Oncogene 1998;17:457-62.
40. Boccellino M, Giuberti G, Quagliuolo L, Marra M, D'Alessandro AM, Fujita H, Giovane A, Abbruzzese A, Caraglia M. Apoptosis induced by interferon-α and antagonized by EGF is regulated by caspase-3-mediated cleavage of gelsolin in human epidermoid cancer cells. J Cell Physiol 2004;201:71-83.