A cytotoxic ribonuclease reduces the expression level of P-glycoprotein in multidrug-resistant cell lines

Investigational New Drugs

Volumn 30, Issue 3, 2012, Pages 880-888

  Castro, Jessica ^a   Ribó, Marc ^a   Puig, Teresa ^a   Colomer, Ramon ^b   Vilanova, Maria ^a   Benito, Antoni ^a  

^a UNIVERSITY OF GIRONA   (Spain)

^b MD ANDERSON CANCER CENTER   (Spain)

Author keywords

Human pancreatic ribonuclease; Multiple drug resistance; Onconase; P glycoprotein

Indexed keywords

CYTOTOXIC AGENT; DOXORUBICIN; ENZYME VARIANT; FUMITREMORGIN C; GLUTATHIONE TRANSFERASE; GLYCOPROTEIN P; NUCLEAR RNA; PANCREATIC RIBONUCLEASE; PE5; RANPIRNASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VERLUKAST;

ARTICLE; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; DRUG EFFECT; DRUG POTENTIATION; DRUG PROTEIN BINDING; DRUG SENSITIVITY; FEMALE; FLOW CYTOMETRY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IC 50; IN VITRO STUDY; LUNG CANCER; MULTIDRUG RESISTANCE; ONCOGENE NEU; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RNA CLEAVAGE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; HUMANS; P-GLYCOPROTEIN; RIBONUCLEASES;

EID: 84864364340     PISSN: 01676997     EISSN: 15730646     Source Type: Journal    
DOI: 10.1007/s10637-011-9636-2     Document Type: Article

References (42)

1. Ozben T (2006) Mechanisms and strategies to overcome multiple drug resistance in cancer. FEBS Lett 580:2903-2909 (Pubitemid 43729172)
2. Scotto KW, Johnson RA (2001) Transcription of the multidrug resistancegeneMDR1: atherapeutictarget. MolInterv 1:117-125
3. Costanzi J, Sidransky D, Navon A, Goldsweig H (2005) Ribonucleases as a novel pro-apoptotic anticancer strategy: review of the preclinical and clinical data for ranpirnase. Cancer Investig 23:643-650 (Pubitemid 43286666)
4. Vasandani VM, Burris JA, Sung C (1999) Reversible nephrotox-icity of onconase and effect of lysine pH on renal onconase uptake. Cancer Chemother Pharmacol 44:164-169 (Pubitemid 29297064)
5. Bosch M, Benito A, Ribo M, Puig T, Beaumelle B, Vilanova M (2004) A nuclear localization sequence endows human pancreatic ribonuclease with cytotoxic activity. Biochemistry 43:2167-2177 (Pubitemid 38279962)
6. Rodriguez M, Benito A, Tubert P, Castro J, Ribo M, Beaumelle B, Vilanova M (2006) A cytotoxic ribonuclease variant with a discontinuous nuclear localization signal constituted by basic residues scattered over three areas of the molecule. J Mol Biol 360:548-557 (Pubitemid 43975119)
7. Tubert P, Rodriguez M, Ribo M, Benito A, Vilanova M (2010) The nuclear transport capacity of a human-pancreatic ribonuclease variant is critical for its cytotoxicity. Invest New Drugs. doi: 10.1007/s10637-010-9426-2
8. Castro J, Ribo M, Navarro S, Nogues MV, Vilanova M, Benito A (2011) A human ribonuclease induces apoptosis associated with p21WAF1/CIP1 induction and JNK inactivation. BMC Cancer 11:9
9. LelandPA, Schultz LW, KimBM, Raines RT (1998) Ribonuclease A variants with potent cytotoxic activity. Proc Natl Acad Sci USA 95:10407-10412 (Pubitemid 28413080)
10. Canals A, Ribo M, Benito A, Bosch M, Mombelli E, Vilanova M (1999) Production ofengineered human pancreatic ribonucleases, solving expression and purification problems, and enhancing thermostability Protein Expr Purif 17:169-181 (Pubitemid 29504392)
11. Ribo M, Bosch M, Torrent G, Benito A, Beaumelle B, Vilanova M (2004) Quantitative analysis, using MALDI-TOF mass spec-trometry, of the N-terminal hydrolysis and cyclization reactions of the activation process ofonconase. Eur J Biochem 271:1163-1171 (Pubitemid 38373049)
12. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T (1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4:2411-2423
13. Menendez JA, Vazquez-Martin A, Colomer R, Brunet J, Carrasco-Pancorbo A, Garcia-Villalba R, Fernandez-Gutierrez A, Segura-Carretero A (2007) Olive oil's bitter principle reverses acquired autoresistance to trastuzumab (Herceptin) in HER2-overexpressing breast cancer cells. BMC Cancer 7:80
14. Pesic M, Markovic JZ, Jankovic D, Kanazir S, Markovic ID, Rakic L, Ruzdijic S (2006) Induced resistance in the human non small cell lung carcinoma (NCI-H460) cell line in vitro by anticancer drugs. J Chemother 18:66-73
15. Berenbaum MC (1989) What is synergy? Pharmacol Rev41:93-141 (Pubitemid 20019599)
16. Gehrmann ML, Fenselau C, Hathout Y (2004) Highly altered protein expression profile in the adriamycin resistant MCF-7 cell line. J Proteome Res 3:403-409 (Pubitemid 39207343)
17. Li J, Xu LZ, He KL, Guo WJ, Zheng YH, Xia P, Chen Y (2001) Reversal effects of nomegestrol acetate on multidrug resistance in adriamycin-resistant MCF7 breast cancer cell line. Breast Cancer Res 3:253-263 (Pubitemid 32633348)
18. Azzariti A, Colabufo NA, Berardi F, Porcelli L, Niso M, Simone GM, Perrone R, Paradiso A (2006) Cyclohexylpiperazine derivative PB28, a sigma2 agonist and sigma1 antagonistreceptor, inhibits cell growth, modulates P-glycoprotein, and synergizes with anthracy-clines in breast cancer. Mol Cancer Ther 5:1807-1816 (Pubitemid 44323249)
19. Stavrovskaya AA, Stromskaya TP (2008) Transport proteins of the ABC family and multidrug resistance of tumor cells. Biochem (Mosc) 73:592-604 (Pubitemid 351775081)
20. Lacroix M, Leclercq G (2004) Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Res Treat 83:249-289 (Pubitemid 38264873)
21. Ogretmen B, Safa AR (1997) Expression of the mutated p53 tumor suppressor protein and its molecular and biochemical characterization in multidrug resistant MCF-7/Adr human breast cancer cells. Oncogene 14:499-506 (Pubitemid 27087113)
22. Pesic M, Podolski A, Rakic L, Ruzdijic S (2009) Purine analogs sensitize the multidrug resistant cell line (NCI-H460/R) to doxorubicin and stimulate the cell growth inhibitory effect of verapamil. Invest New Drugs. doi:10.1007/s10637-009-9277-x
23. Gottesman MM, Fojo T, Bates SE (2002) Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2: 48-58 (Pubitemid 37328807)
24. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL (1987) Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235:177-182 (Pubitemid 17231334)
25. Menendez JA, Lupu R, Colomer R (2004) Inhibition of tumor-associated fatty acid synthase hyperactivity induces synergistic chemosensitization of HER -2/neu -overexpressing human breast cancer cells to docetaxel (taxotere). Breast Cancer Res Treat 84:183-195 (Pubitemid 38393368)
26. Paik S et al (1998) erbB-2 and response to doxorubicin in patients with axillary lymph node-positive, hormone receptor-negative breast cancer. J Natl Cancer Inst 90:1361-1370 (Pubitemid 28439960)
27. Rybak SM et al (1996) Enhancement ofvincristine cytotoxicity in drug-resistant cells by simultaneous treatment with onconase, an antitumor ribonuclease. J Natl Cancer Inst 88:747-753 (Pubitemid 26195922)
28. Osborn MT, Chambers TC (1996) Role of the stress-activated/c-Jun NH2-terminal protein kinase pathway in the cellular response to adriamycin and other chemotherapeutic drugs. J Biol Chem 271:30950-30955
29. Ledoux S, Yang R, Friedlander G, Laouari D (2003) Glucose depletion enhances P-glycoprotein expression in hepatoma cells: role of endoplasmic reticulum stress response. Cancer Res 63:7284-7290 (Pubitemid 37413469)
30. Comerford KM, Cummins EP, Taylor CT (2004) c-Jun NH2-terminal kinase activation contributes to hypoxia-inducible factor 1alpha-dependent P-glycoprotein expression in hypoxia. Cancer Res 64:9057-9061 (Pubitemid 39665517)
31. Zhou J, Liu M, Aneja R, Chandra R, Lage H, Joshi HC (2006) Reversal of P-glycoprotein-mediated multidrug resistance in cancer cells by the c-Jun NH2-terminal kinase. Cancer Res 66:445-452 (Pubitemid 43166053)
32. Ikeguchi M, Teeter LD, Eckersberg T, Ganapathi R, Kuo MT (1991) Structural and functional analyses of the promoter of the murine multidrug resistance gene mdr3/mdr1a reveal a negative element containing the AP-1 binding site. DNA Cell Biol 10: 639-649
33. Volm M (1993) P-glycoprotein associated expression ofc-fos and c-jun products in human lung carcinomas. Anticancer Res 13:375-378 (Pubitemid 23196773)
34. Smolewski P et al (2008) Ex vivo cytotoxic activity of endoribonucleases, onconase (ranpirnase) and R-amphinase, against acute myeloblastic leukemia cells. ASH Annual Meeting Abstracts 112:4010
35. Smolewski P, Linke-Szewczyk A, Cebula B, Shogen K, Ardelt W, Darzynkiewicz Z, Robak T (2008) Activity of anti-tumor endoribonucleases, onconase (ranpirnase) and R-amphinase in chronic lymphocytic leukemia. ASH Annual Meeting Abstracts 112:4205
36. Ardelt W, Shogen K, Darzynkiewicz Z (2008) Onconase and amphinase, the antitumor ribonucleases from Rana pipiens oocytes. Curr Pharm Biotechnol 9:215-225 (Pubitemid 352024698)
37. Robinson LJ, Roberts WK, Ling TT, Lamming D, Sternberg SS, Roepe PD (1997) Human MDR 1 protein overexpression delays the apoptotic cascade in Chinese hamster ovary fibroblasts. Biochemistry 36:11169-11178 (Pubitemid 27398436)
38. Ruth AC, Roninson IB (2000) Effects of the multidrug transporter P-glycoprotein on cellular responses to ionizing radiation. Cancer Res 60:2576-2578 (Pubitemid 30318226)
39. Lehne G, Rugstad HE (1998) Cytotoxic effect of the cyclosporin PSC 833 in multidrug-resistant leukaemia cells with increased expression of P-glycoprotein. Br J Cancer 78:593-600 (Pubitemid 28375590)
40. Lehne G, Sorensen DR, Tjonnfjord GE, Beiske C, Hagve TA, Rugstad HE, Clausen OP (2002) The cyclosporin PSC 833 increases survival and delays engraftment of human multidrug-resistant leukemia cells in xenotransplanted NOD-SCID mice. Leukemia 16:2388-2394 (Pubitemid 36054372)
41. Smyth MJ, Krasovskis E, Sutton VR, Johnstone RW (1998) The drug efflux protein, P-glycoprotein, additionally protects drug-resistant tumor cells from multiple forms of caspase-dependent apoptosis. Proc Natl Acad Sci USA 95:7024-7029
42. Katoh SY, Ueno M, Takakura N (2008) Involvement of MDR1 function in proliferation oftumour cells. J Biochem 143:517-524 (Pubitemid 351451765)