XPO1/CRM1 inhibition causes antitumor effects by mitochondrial accumulation of eIF5A

Clinical Cancer Research

Volumn 21, Issue 14, 2015, Pages 3286-3297

  Miyake, Takahito ^a   Pradeep, Sunila ^a   Wu, Sherry Y ^a   Rupaimoole, Rajesha ^a   Zand, Behrouz ^a   Wen, Yunfei ^a   Gharpure, Kshipra M ^a   Nagaraja, Archana S ^a   Hu, Wei ^a   Cho, Min Soon ^a   Dalton, Heather J ^a   Previs, Rebecca A ^a   Taylor, Morgan L ^a   Hisamatsu, Takeshi ^a   Kang, Yu ^a   Liu, Tao ^a   Shacham, Sharon ^b   McCauley, Dilara ^b   Hawke, David H ^a   Wiktorowicz, John E ^c   Coleman, Robert L ^a   Sood, Anil K ^a   more..

^a UNIVERSITY OF TEXAS   (United States)

^b Karyopharm Therapeutics   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; CASPASE 9; ENZYME INHIBITOR; EXPORTIN 1; GROWTH FACTOR; INITIATION FACTOR 5A; INSULIN LIKE GROWTH FACTOR 2 MRNA BINDING PROTEIN; KPT 185; PACLITAXEL; PROTEIN P53; RETINOBLASTOMA PROTEIN; SELECTIVE INHIBITOR OF NUCLEAR EXPORT; SELINEXOR; SMALL INTERFERING RNA; TOPOTECAN; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG; CELL RECEPTOR; EXPORTIN 1 PROTEIN; INITIATION FACTOR; KARYOPHERIN; RNA BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BIOACCUMULATION; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; EMBRYO; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INCUBATION TIME; MITOCHONDRIAL ACCUMULATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR DYNAMICS; MONOTHERAPY; MOUSE; NONHUMAN; OVARIAN CANCER CELL LINE; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; SURVIVAL RATE; SURVIVAL TIME; TUMOR VOLUME; ACTIVE TRANSPORT; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; DRUG SCREENING; EXPERIMENTAL MAMMARY NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; MITOCHONDRION; NUDE MOUSE; OVARY TUMOR; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TUMOR CELL LINE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENZYME INHIBITORS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOHISTOCHEMISTRY; KARYOPHERINS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, NUDE; MITOCHONDRIA; OVARIAN NEOPLASMS; PEPTIDE INITIATION FACTORS; PROTEOMICS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TANDEM MASS SPECTROMETRY; TRANSFECTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84942912732     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-1953     Document Type: Article

References (50)

1. Freedman DA, Levine AJ. Nuclear export is required for degradation of endogenous p53 by MDM2 and human papillomavirus E6. Mol Cell Biol 1998;18:7288-93.
2. Xu D, Grishin NV, Chook YM. NESdb: a database of NES-containing CRM1 cargoes. Mol Biol Cell 2012;23:3673-6.
3. Yao Y, Dong Y, Lin F, Zhao H, Shen Z, Chen P, et al. The expression of CRM1 is associated with prognosis in human osteosarcoma. Oncol Rep 2009;21:229-35.
4. Huang WY, Yue L, Qiu WS, Wang LW, Zhou XH, Sun YJ. Prognostic value of CRM1 in pancreas cancer. Clin Invest Med 2009;32:E315.
5. Akagi I, Okayama H, Schetter AJ, Robles AI, Kohno T, Bowman ED, et al. Combination of protein coding and non-coding gene expression as a robust prognostic classifier in stage I lung adenocarcinoma. Cancer Res 2013;73:3821-32.
6. Noske A, Weichert W, Niesporek S, Roske A, Buckendahl AC, Koch I, et al. Expression of the nuclear export protein chromosomal region maintenance/exportin 1/Xpo1 is a prognostic factor in human ovarian cancer. Cancer 2008;112:1733-43.
7. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, et al. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci U S A 1999;96:9112-7.
8. Newlands ES, Rustin GJ, Brampton MH. Phase I trial of elactocin. Br J Cancer 1996;74:648-9.
9. Mutka SC, Yang WQ, Dong SD, Ward SL, Craig DA, Timmermans PB, et al. Identification of nuclear export inhibitors with potent anticancer activity in vivo. Cancer Res 2009;69:510-7.
10. Etchin J, Sanda T, Mansour MR, Kentsis A, Montero J, Le BT, et al. KPT-330 inhibitor of CRM1 (XPO1)-mediated nuclear export has selective anti-leukaemic activity in preclinical models of T-cell acute lymphoblastic leukaemia and acute myeloid leukaemia. Br J Haematol 2013;161:117-27.
11. Razak ARA, Soerensen MM, Mahipal A, Shacham S, Yau CYF, Lassen UN, et al. First-in-class, first-in-human phase I trial of KPT-330, a selective inhibitor of nuclear export (SINE) in patients (pts) with advanced solid tumors. ASCO Meeting Abstracts 2013;31:2505.
12. Facchiano AM, Stiuso P, Chiusano ML, Caraglia M, Giuberti G, Marra M, et al. Homology modelling of the human eukaryotic initiation factor 5A (eIF-5A). Protein Eng 2001;14:881-90.
13. Sun Z, Cheng Z, Taylor CA, McConkey BJ, Thompson JE. Apoptosis induction by eIF5A1 involves activation of the intrinsic mitochondrial pathway. J Cell Physiol 2010;223:798-809.
14. Sood AK, Seftor EA, Fletcher MS, Gardner LM, Heidger PM, Buller RE, et al. Molecular determinants of ovarian cancer plasticity. Am J Pathol 2001;158:1279-88.
15. Yoneda J, Kuniyasu H, Crispens MA, Price JE, Bucana CD, Fidler IJ. Expression of angiogenesis-related genes and progression of human ovarian carcinomas in nude mice. J Natl Cancer Inst 1998;90:447-54.
16. Lin DL, Chang C. p53 is a mediator for radiation-repressed human TR2 orphan receptor expression in MCF-7 cells, a new pathway from tumor suppressor to member of the steroid receptor superfamily. J Biol Chem 1996;271:14649-52.
17. Katayose D, Gudas J, Nguyen H, Srivastava S, Cowan KH, Seth P. Cytotoxic effects of adenovirus-mediatedwild-type p53 protein expression in normal and tumor mammary epithelial cells. Clin Cancer Res 1995;1:889-97.
18. Kamat AA, Kim TJ, Landen CN Jr, Lu C, Han LY, Lin YG, et al. Metronomic chemotherapy enhances the efficacy of antivascular therapy in ovarian cancer. Cancer Res 2007;67:281-8.
19. Zhao L, Wientjes MG, Au JL. Evaluation of combination chemotherapy: integration of nonlinear regression, curve shift, isobologram, and combination index analyses. Clin Cancer Res 2004;10:7994-8004.
20. Lu C, Kamat AA, Lin YG, Merritt WM, Landen CN, Kim TJ, et al. Dual targeting of endothelial cells and pericytes in antivascular therapy for ovarian carcinoma. Clin Cancer Res 2007;13:4209-17.
21. Lee JW, Han HD, Shahzad MM, Kim SW, Mangala LS, Nick AM, etal. EphA2 immunoconjugate as molecularly targeted chemotherapy for ovarian carcinoma. J Natl Cancer Inst 2009;101:1193-205.
22. Hu X, Rea HC, Wiktorowicz JE, Perez-Polo JR. Proteomic analysis of hypoxia/ischemia-induced alteration of cortical development and dopamine neurotransmission in neonatal rat. J Proteom Res 2006;5:2396-404.
23. Straub C, Pazdrak K, Young TW, Stafford SJ, Wu Z, Wiktorowicz JE, et al. Toward the Proteome of the human peripheral blood eosinophil. Proteomics Clin Appl 2009;3:1151-73.
24. Guptarak J, Wiktorowicz JE, Sadygov RG, Zivadinovic D, Paulucci-Holthauzen A, Vergara L, et al. The cancer drug tamoxifen - a potential therapeutic treatment for spinal cord injury. J Neurotrauma 2014;31:268-83.
25. Lopez MF, Berggren K, Chernokalskaya E, Lazarev A, Robinson M, Patton WF. A comparison of silver stain and SYPRO Ruby protein gel stain with respect to protein detection in two dimensional gels and identification by peptide mass profiling. Electrophoresis 2000;21:3673-83.
26. Azmi AS, Aboukameel A, Bao B, Sarkar FH, Philip PA, Kauffman M, et al. Selective inhibitors of nuclear export block pancreatic cancer cell proliferation and reduce tumor growth in mice. Gastroenterology 2013;144:447-56.
27. Turner JG, Dawson J, Sullivan DM. Nuclear export of proteins and drug resistance in cancer. Biochem Pharmacol 2012;83:1021-32.
28. Bernardini MQ, Baba T, Lee PS, Barnett JC, Sfakianos GP, Secord AA, et al. Expression signatures of TP53 mutations in serous ovarian cancers. BMC Cancer 2010;10:237.
29. Cancer Genome Atlas Research N. Integrated genomic analyses of ovarian carcinoma. Nature 2011;474:609-15.
30. Croce AC, Bottiroli G, Supino R, Favini E, Zuco V, Zunino F. Subcellular localization of the camptothecin analogues, topotecan and gimatecan. Biochem Pharmacol 2004;67:1035-45.
31. Ishfaq M, Maeta K, Maeda S, Natsume T, Ito A, Yoshida M. Acetylation regulates subcellular localization of eukaryotic translation initiation factor 5A (eIF5A). FEBS Lett 2012;586:3236-41.
32. Nielsen J, Adolph SK, Rajpert-De Meyts E, Lykke-Andersen J, Koch G, Christiansen J, et al. Nuclear transit of human zipcode-binding protein IMP1. Biochem J 2003;376:383-91.
33. Garzon R, Brown PdN, Yee K, Lancet JE, Gutierrez M, Gabrail N, etal. Phase I trial of selinexor (KPT-330), a first-in-class oral selective inhibitor of nuclear export (SINE) in patients (pts) with advanced acute myelogenous leukemia (AML). Blood 2013;122:1440.
34. Gutierrez M, de Nully Brown P, Gabrail N, Baz R, Reece DE, Savona M, etal. Anti tumor activity of selinexor (KPT-330), a first-in-class oral selective inhibitor of nuclear export (SINE) XPO1/CRM1 antagonist in patients (pts) with relapsed/refractory multiple myeloma (MM) or waldenstrom's macroglobulinemia (WM). Blood 2013;122:1942.
35. Walker CJ, Oaks JJ, Santhanam R, Neviani P, Harb JG, Ferenchak G, et al. Preclinical and clinical efficacy of XPO1/CRM1 inhibition by the karyopherin inhibitor KPT-330 in Ph+ leukemias. Blood 2013;122:3034-44.
36. Lu X, Errington J, Curtin NJ, Lunec J, Newell DR. The impact of p53 status on cellular sensitivity to antifolate drugs. Clin Cancer Res 2001;7:2114-23.
37. Forbes S, Clements J, Dawson E, Bamford S, Webb T, Dogan A, et al. Cosmic 2005. Br J Cancer 2006;94:318-22.
38. O'Connor PM, Jackman J, Bae I, Myers TG, Fan S, Mutoh M, et al. Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res 1997;57:4285-300.
39. Finn RS, Dering J, Ginther C, Wilson CA, Glaspy P, Tchekmedyian N, et al. Dasatinib, an orally active small molecule inhibitor of both the src and abl kinases, selectively inhibits growth of basal-type/"triple-negative" breast cancer cell lines growing in vitro. Breast Cancer Res Treat 2007;105:319-26.
40. Cooper HL, Park MH, Folk JE, Safer B, Braverman R. Identification of the hypusine-containing protein hy+ as translation initiation factor eIF-4D. Proc Natl Acad Sci U S A 1983;80:1854-7.
41. Jao DL, Chen KY. Tandem affinity purification revealed the hypusinedependent binding of eukaryotic initiation factor 5A to the translating 80S ribosomal complex. J Cell Biochem 2006;97:583-98.
42. Li CH, Ohn T, Ivanov P, Tisdale S, Anderson P. eIF5A promotes translation elongation, polysome disassembly and stress granule assembly. PLoS One 2010;5:e9942.
43. Wolff EC, Kang KR, Kim YS, Park MH. Posttranslational synthesis of hypusine: evolutionary progression and specificity of the hypusine modification. Amino Acids 2007;33:341-50.
44. Zanelli CF, Maragno AL, Gregio AP, Komili S, Pandolfi JR, Mestriner CA, et al. eIF5A binds to translational machinery components and affects translation in yeast. Biochem Biophys Res Commun 2006;348:1358-66.
45. Yisraeli JK. VICKZ proteins: a multi-talented family of regulatory RNA-binding proteins. Biol Cell 2005;97:87-96.
46. Kobel M, Weidensdorfer D, Reinke C, Lederer M, Schmitt WD, Zeng K, et al. Expression of the RNA-binding protein IMP1 correlates with poor prognosis in ovarian carcinoma. Oncogene 2007;26:7584-9.
47. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, Meng X, et al. Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1. Nature 2005;438:512-5.
48. Stohr N, Kohn M, Lederer M, Glass M, Reinke C, Singer RH, et al. IGF2BP1 promotes cell migrationbyregulating MK5 and PTEN signaling. Genes Dev 2012;26:176-89.
49. Stohr N, Huttelmaier S. IGF2BP1: a post-transcriptional "driver" of tumor cell migration. Cell Adh Migr 2012;6:312-8.
50. Vainer G, Vainer-Mosse E, Pikarsky A, Shenoy SM, Oberman F, Yeffet A, et al. A role for VICKZ proteins in the progression of colorectal carcinomas: regulating lamellipodia formation. J Pathol 2008;215:445-56.