Chemotherapeutic sensitization of leptomycin B resistant lung cancer cells by pretreatment with doxorubicin

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Lu, Chuanwen ^a   Shao, Changxia ^a   Cobos, Everardo ^b   Singh, Kamaleshwar P ^a   Gao, Weimin ^a,b  

^a TEXAS TECH UNIVERSITY   (United States)

^b TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; LEPTOMYCIN B; PROTEIN P21; PROTEIN P53; PROTEIN P62; PROTEOME; SERINE; SURVIVIN; THREONINE; ANTINEOPLASTIC AGENT; BIRC5 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; INHIBITOR OF APOPTOSIS PROTEIN; NUCLEAR PROTEIN; UNSATURATED FATTY ACID;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE PHASE; CONTROLLED STUDY; DRUG RESISTANCE; DRUG SENSITIZATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IC 50; LUNG CANCER; MASS SPECTROMETRY; MOLECULAR MECHANICS; SIGNAL TRANSDUCTION; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; WESTERN BLOTTING; WILD TYPE; AMINO ACID SEQUENCE; CELL CYCLE; DRUG EFFECT; LUNG TUMOR; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; PROTEOMICS; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FATTY ACIDS, UNSATURATED; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; LUNG NEOPLASMS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEOMICS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84857811505     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032895     Document Type: Article

References (64)

1. AmericanCancerSociety (2011) Cancer Facts & Figures 2011.
2. Cetin K, Ettinger DS, Hei YJ, O'Malley CD, (2011) Survival by histologic subtype in stage IV nonsmall cell lung cancer based on data from the Surveillance, Epidemiology and End Results Program. Clin Epidemiol 3: 139-148.
3. Carbone DP, Felip E, (2011) Adjuvant therapy in non-small cell lung cancer: future treatment prospects and paradigms. Clin Lung Cancer 12: 261-271.
4. Coory M, Gkolia P, Yang IA, Bowman RV, Fong KM, (2008) Systematic review of multidisciplinary teams in the management of lung cancer. Lung Cancer 60: 14-21.
5. Mercadante S, Vitrano V, (2010) Pain in patients with lung cancer: pathophysiology and treatment. Lung Cancer 68: 10-15.
6. Provencio M, Sanchez A, Gasent J, Gomez P, Rosell R, (2009) Cancer treatments: can we find treasures at the bottom of the sea? Clin Lung Cancer 10: 295-300.
7. Dempke WC, Suto T, Reck M, (2010) Targeted therapies for non-small cell lung cancer. Lung Cancer 67: 257-274.
8. Adachi Y, Yanagida M, (1989) Higher order chromosome structure is affected by cold-sensitive mutations in a Schizosaccharomyces pombe gene crm1+ which encodes a 115-kD protein preferentially localized in the nucleus and its periphery. J Cell Biol 108: 1195-1207.
9. Kudo N, Wolff B, Sekimoto T, Schreiner EP, Yoneda Y, et al. (1998) Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1. Exp Cell Res 242: 540-547.
10. Mutka SC, Yang WQ, Dong SD, Ward SL, Craig DA, et al. (2009) Identification of nuclear export inhibitors with potent anticancer activity in vivo. Cancer research 69: 510.
11. Nishi K, Yoshida M, Fujiwara D, Nishikawa M, Horinouchi S, et al. (1994) Leptomycin B targets a regulatory cascade of crm1, a fission yeast nuclear protein, involved in control of higher order chromosome structure and gene expression. J Biol Chem 269: 6320-6324.
12. Shao C, Lu C, Chen L, Koty PP, Cobos E, et al. (2011) p53-Dependent anticancer effects of leptomycin B on lung adenocarcinoma. Cancer Chemother Pharmacol 67: 1369-1380.
13. Wang W, Budhu A, Forgues M, Wang XW, (2005) Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication. Nat Cell Biol 7: 823-830.
14. van der Watt PJ, Maske CP, Hendricks DT, Parker MI, Denny L, et al. (2008) The Karyopherin proteins, Crm1 and Karyopherin beta1, are overexpressed in cervical cancer and are critical for cancer cell survival and proliferation. Int J Cancer 124: 1829-1840.
15. Noske A, Weichert W, Niesporek S, Roske A, Buckendahl AC, et al. (2008) Expression of the nuclear export protein chromosomal region maintenance/exportin 1/Xpo1 is a prognostic factor in human ovarian cancer. Cancer 112: 1733-1743.
16. Yao Y, Dong Y, Lin F, Zhao H, Shen Z, et al. (2009) The expression of CRM1 is associated with prognosis in human osteosarcoma. Oncol Rep 21: 229-235.
17. Chen L, Shao C, Cobos E, Wang JS, Gao W, (2010) 4-(Methylnitro-Samino)-1-(3-Pyridyl)-1-Butanone Induces Crm1-Dependent P53 Nuclear Accumulation In Human Bronchial Epithelial Cells. Toxicol Sci 116: 206-215.
18. Chen L, Moore JE, Samathanam C, Shao C, Cobos E, et al. (2011) CRM1-dependent p53 nuclear accumulation in lung lesions of a bitransgenic mouse lung tumor model. Oncol Rep 26: 223-228.
19. Cook A, Bono F, Jinek M, Conti E, (2007) Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 76: 647-671.
20. Ossareh-Nazari B, Bachelerie F, Dargemont C, (1997) Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278: 141-144.
21. Clarke AR, Purdie CA, Harrison DJ, Morris RG, Bird CC, et al. (1993) Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362: 849-852.
22. Kuerbitz SJ, Plunkett BS, Walsh WV, Kastan MB, (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Natl Acad Sci U S A 89: 7491-7495.
23. Lowe SW, Ruley HE, Jacks T, Housman DE, (1993) p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell 74: 957-967.
24. Aas T, Børresen AL, Geisler S, Smith-Sørensen B, Johnsen H, et al. (1996) Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nature Medicine 2: 811-814.
25. Kojima K, Konopleva M, Samudio IJ, Shikami M, Cabreira-Hansen M, et al. (2005) MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy. Blood 106: 3150.
26. Wang S, Konorev EA, Kotamraju S, Joseph J, Kalivendi S, et al. (2004) Doxorubicin induces apoptosis in normal and tumor cells via distinctly different mechanisms. intermediacy of H(2)O(2)- and p53-dependent pathways. J Biol Chem 279: 25535-25543.
27. Riganti C, Miraglia E, Viarisio D, Costamagna C, Pescarmona G, et al. (2005) Nitric oxide reverts the resistance to doxorubicin in human colon cancer cells by inhibiting the drug efflux. Cancer Res 65: 516-525.
28. Sung JM, Cho HJ, Yi H, Lee CH, Kim HS, et al. (2008) Characterization of a stem cell population in lung cancer A549 cells. Biochem Biophys Res Commun 371: 163-167.
29. Mi J, Zhang X, Rabbani ZN, Liu Y, Reddy SK, et al. (2008) RNA aptamer-targeted inhibition of NF-kappa B suppresses non-small cell lung cancer resistance to doxorubicin. Mol Ther 16: 66-73.
30. Outomuro D, Grana DR, Azzato F, Milei J, (2007) Adriamycin-induced myocardial toxicity: new solutions for an old problem? Int J Cardiol 117: 6-15.
31. Lee TK, Lau TC, Ng IO, (2002) Doxorubicin-induced apoptosis and chemosensitivity in hepatoma cell lines. Cancer Chemother Pharmacol 49: 78-86.
32. Song X, Liu X, Chi W, Liu Y, Wei L, et al. (2006) Hypoxia-induced resistance to cisplatin and doxorubicin in non-small cell lung cancer is inhibited by silencing of HIF-1alpha gene. Cancer Chemother Pharmacol 58: 776-784.
33. Swift LP, Rephaeli A, Nudelman A, Phillips DR, Cutts SM, (2006) Doxorubicin-DNA adducts induce a non-topoisomerase II-mediated form of cell death. Cancer Res 66: 4863-4871.
34. Lu J, Suzuki T, Satoh M, Chen S, Tomonaga T, et al. (2008) Involvement of aldolase A in X-ray resistance of human HeLa and UV(r)-1 cells. Biochem Biophys Res Commun 369: 948-952.
35. Shao C, Chen L, Lu C, Shen CL, Gao W, (2011) A gel-based proteomic analysis of the effects of green tea polyphenols on ovariectomized rats. Nutrition 27: 681-686.
36. You J, Hu FQ, Du YZ, Yuan H, (2008) Improved cytotoxicity of doxorubicin by enhancing its nuclear delivery mediated via nanosized micelles. Nanotechnology 19: 255103.
37. Blagosklonny MV, (2002) Sequential activation and inactivation of G2 checkpoints for selective killing of p53-deficient cells by microtubule-active drugs. Oncogene 21: 6249-6254.
38. Yoshida M, Nishikawa M, Nishi K, Abe K, Horinouchi S, et al. (1990) Effects of leptomycin B on the cell cycle of fibroblasts and fission yeast cells. Exp Cell Res 187: 150-156.
39. Ogura M, (2001) [Adriamycin (doxorubicin)]. Gan To Kagaku Ryoho 28: 1331-1338.
40. Meek DW, (1998) Multisite phosphorylation and the integration of stress signals at p53. Cell Signal 10: 159-166.
41. Abraham RT, (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 15: 2177-2196.
42. Zhu J, Zhou W, Jiang J, Chen X, (1998) Identification of a novel p53 functional domain that is necessary for mediating apoptosis. J Biol Chem 273: 13030-13036.
43. Walker KK, Levine AJ, (1996) Identification of a novel p53 functional domain that is necessary for efficient growth suppression. Proc Natl Acad Sci U S A 93: 15335-15340.
44. Cai X, Liu X, (2008) Inhibition of Thr-55 phosphorylation restores p53 nuclear localization and sensitizes cancer cells to DNA damage. Proc Natl Acad Sci U S A 105: 16958-16963.
45. McVean M, Xiao H, Isobe K, Pelling JC, (2000) Increase in wild-type p53 stability and transactivational activity by the chemopreventive agent apigenin in keratinocytes. Carcinogenesis 21: 633-639.
46. Freedman DA, Levine AJ, (1998) Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol 18: 7288-7293.
47. Lain S, Midgley C, Sparks A, Lane EB, Lane DP, (1999) An inhibitor of nuclear export activates the p53 response and induces the localization of HDM2 and p53 to U1A-positive nuclear bodies associated with the PODs. Exp Cell Res 248: 457-472.
48. Lain S, Xirodimas D, Lane DP, (1999) Accumulating active p53 in the nucleus by inhibition of nuclear export: a novel strategy to promote the p53 tumor suppressor function. Exp Cell Res 253: 315-324.
49. Lecane PS, Kiviharju TM, Sellers RG, Peehl DM, (2003) Leptomycin B stabilizes and activates p53 in primary prostatic epithelial cells and induces apoptosis in the LNCaP cell line. Prostate 54: 258-267.
50. Smart P, Lane EB, Lane DP, Midgley C, Vojtesek B, et al. (1999) Effects on normal fibroblasts and neuroblastoma cells of the activation of the p53 response by the nuclear export inhibitor leptomycin B. Oncogene 18: 7378-7386.
51. Zhang Y, Xiong Y, (2001) A p53 amino-terminal nuclear export signal inhibited by DNA damage-induced phosphorylation. Science 292: 1910-1915.
52. Esrig D, Elmajian D, Groshen S, Freeman JA, Stein JP, et al. (1994) Accumulation of nuclear p53 and tumor progression in bladder cancer. N Engl J Med 331: 1259-1264.
53. Sardao VA, Oliveira PJ, Holy J, Oliveira CR, Wallace KB, (2009) Doxorubicin-induced mitochondrial dysfunction is secondary to nuclear p53 activation in H9c2 cardiomyoblasts. Cancer Chemother Pharmacol 64: 811-827.
54. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825.
55. Lohr K, Moritz C, Contente A, Dobbelstein M, (2003) p21/CDKN1A mediates negative regulation of transcription by p53. J Biol Chem 278: 32507-32516.
56. Li F, Altieri DC, (1999) Transcriptional analysis of human survivin gene expression. Biochem J 344 Pt 2: 305-311.
57. Ikeda M, Okamoto I, Tamura K, Satoh T, Yonesaka K, et al. (2007) Down-regulation of survivin by ultraviolet C radiation is dependent on p53 and results in G(2)-M arrest in A549 cells. Cancer Lett 248: 292-298.
58. Knauer SK, Kramer OH, Knosel T, Engels K, Rodel F, et al. (2007) Nuclear export is essential for the tumor-promoting activity of survivin. FASEB J 21: 207-216.
59. Turner JG, Sullivan DM, (2008) CRM1-mediated nuclear export of proteins and drug resistance in cancer. Curr Med Chem 15: 2648-2655.
60. Park I, Chung J, Walsh CT, Yun Y, Strominger JL, et al. (1995) Phosphotyrosine-independent binding of a 62-kDa protein to the src homology 2 (SH2) domain of p56lck and its regulation by phosphorylation of Ser-59 in the lck unique N-terminal region. Proc Natl Acad Sci U S A 92: 12338-12342.
61. Pankiv S, Lamark T, Bruun JA, Øvervatn A, Bjørkøy G, et al. (2010) Nucleocytoplasmic shuttling of p62/SQSTM1 and its role in recruitment of nuclear polyubiquitinated proteins to promyelocytic leukemia bodies. Journal of Biological Chemistry 285: 5941.
62. Geetha T, Wooten MW, (2002) Structure and functional properties of the ubiquitin binding protein p62. FEBS Lett 512: 19-24.
63. Rachubinski RA, Marcus SL, Capone JP, (1999) The p56(lck)-interacting protein p62 stimulates transcription via the SV40 enhancer. J Biol Chem 274: 18278-18284.
64. Tasdemir E, Chiara Maiuri M, Morselli E, Criollo A, D'Amelio M, et al. (2008) A dual role of p53 in the control of autophagy. Autophagy 4: 810-814.