Expression, function, and targeting of the nuclear exporter chromosome region maintenance 1 (CRM1) protein

Pharmacology and Therapeutics

Volumn 153, Issue , 2015, Pages 25-35

  Ishizawa, Jo ^a   Kojima, Kensuke ^a,b   Hail, Numsen ^a   Tabe, Yoko ^c   Andreeff, Michael ^a  

^a UNIVERSITY OF TEXAS   (United States)

^b SAGA UNIVERSITY   (Japan)

^c JUNTENDO UNIVERSITY   (Japan)

Author keywords

CRM1; Hematological malignancies; KPT 330; Nuclear export; Ribosomal biogenesis; SINE

Indexed keywords

ACRYLIC ACID DERIVATIVE; ANGUINOMYCIN; CBS 9106; EXPORTIN 1; GONIOTHALAMIN; KOS 2464; LEPTOMYCIN B; PROTEIN INHIBITOR; RATJADONE ANALOG; RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CELL RECEPTOR; EXPORTIN 1 PROTEIN; KARYOPHERIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ARTICLE; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL TRIAL (TOPIC); CYTOLOGY; GLIOMA; HUMAN; KIDNEY CARCINOMA; LEUKEMIA; MALIGNANT NEOPLASTIC DISEASE; MANTLE CELL LYMPHOMA; MULTIPLE MYELOMA; NONHUMAN; NUCLEAR EXPORT SIGNAL; OSTEOSARCOMA; OVARY CANCER; PANCREAS CANCER; PHILADELPHIA CHROMOSOME POSITIVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; T CELL ACUTE LYMPHOBLASTIC LEUKEMIA; UTERINE CERVIX CANCER; ACTIVE TRANSPORT; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; BIOSYNTHESIS; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PATHOLOGY; PHYSIOLOGY; PROCEDURES;

ACTIVE TRANSPORT, CELL NUCLEUS; ANTINEOPLASTIC AGENTS; HUMANS; KARYOPHERINS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; NEOPLASMS; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84938421995     PISSN: 01637258     EISSN: 1879016X     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2015.06.001     Document Type: Review

References (87)

1. Y. Adachi, and M. Yanagida 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 4 1989 1195 1207
2. A. Aloisi, S. Di Gregorio, F. Stagno, P. Guglielmo, F. Mannino, M.P. Sormani, and et al. BCR-ABL nuclear entrapment kills human CML cells: ex vivo study on 35 patients with the combination of imatinib mesylate and leptomycin B Blood 107 4 2006 1591 1598
3. B. Bai, H.M. Moore, and M. Laiho CRM1 and its ribosome export adaptor NMD3 localize to the nucleolus and affect rRNA synthesis Nucleus 4 4 2013 315 325
4. S. Bonazzi, S. Guttinger, I. Zemp, U. Kutay, and K. Gademann Total synthesis, configuration, and biological evaluation of anguinomycin C Angew Chem Int Ed Engl 46 45 2007 8707 8710
5. J.M. Brown, and G. Wilson Apoptosis genes and resistance to cancer therapy: what does the experimental and clinical data tell us? Cancer Biol Ther 2 5 2003 477 490
6. A. Burzlaff, M. Kalesse, C. Kasper, and T. Scheper Multi parameter in vitro testing of ratjadone using flow cytometry Appl Microbiol Biotechnol 62 2-3 2003 174 179
7. E. Craig, Z.K. Zhang, K.P. Davies, and G.V. Kalpana A masked NES in INI1/hSNF5 mediates hCRM1-dependent nuclear export: implications for tumorigenesis EMBO J 21 1-2 2002 31 42
8. B. Culjkovic, I. Topisirovic, L. Skrabanek, M. Ruiz-Gutierrez, and K.L. Borden eIF4E is a central node of an RNA regulon that governs cellular proliferation J Cell Biol 175 3 2006 415 426
9. D. Daelemans, E. Afonina, J. Nilsson, G. Werner, J. Kjems, E. De Clercq, and et al. A synthetic HIV-1 Rev inhibitor interfering with the CRM1-mediated nuclear export Proc Natl Acad Sci U S A 99 22 2002 14440 14445
10. X. Dong, A. Biswas, and Y.M. Chook Structural basis for assembly and disassembly of the CRM1 nuclear export complex Nat Struct Mol Biol 16 5 2009 558 560
11. X. Dong, A. Biswas, K.E. Suel, L.K. Jackson, R. Martinez, H. Gu, and et al. Structural basis for leucine-rich nuclear export signal recognition by CRM1 Nature 458 7242 2009 1136 1141
12. A.M. Eiring, P. Neviani, R. Santhanam, J.J. Oaks, J.S. Chang, M. Notari, and et al. Identification of novel posttranscriptional targets of the BCR/ABL oncoprotein by ribonomics: requirement of E2F3 for BCR/ABL leukemogenesis Blood 111 2 2008 816 828
13. J. Etchin, T. Sanda, M.R. Mansour, A. Kentsis, J. Montero, B.T. Le, and 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 161 1 2013 117 127
14. J. Etchin, Q. Sun, A. Kentsis, A. Farmer, Z.C. Zhang, T. Sanda, and et al. Antileukemic activity of nuclear export inhibitors that spare normal hematopoietic cells Leukemia 27 1 2013 66 74
15. B. Falini, N. Bolli, J. Shan, M.P. Martelli, A. Liso, A. Pucciarini, and et al. Both carboxy-terminus NES motif and mutated tryptophan(s) are crucial for aberrant nuclear export of nucleophosmin leukemic mutants in NPMc + AML Blood 107 11 2006 4514 4523
16. B. Falini, C. Mecucci, E. Tiacci, M. Alcalay, R. Rosati, L. Pasqualucci, and et al. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype N Engl J Med 352 3 2005 254 266
17. A. Fatica, and D. Tollervey Making ribosomes Curr Opin Cell Biol 14 3 2002 313 318
18. M. Fornerod, M. Ohno, M. Yoshida, and I.W. Mattaj CRM1 is an export receptor for leucine-rich nuclear export signals Cell 90 6 1997 1051 1060
19. M. Fukuda, S. Asano, T. Nakamura, M. Adachi, M. Yoshida, M. Yanagida, and et al. CRM1 is responsible for intracellular transport mediated by the nuclear export signal Nature 390 6657 1997 308 311
20. K. Gademann Controlling protein transport by small molecules Curr Drug Targets 12 11 2011 1574 1580
21. I.E. Gallouzi, C.M. Brennan, and J.A. Steitz Protein ligands mediate the CRM1-dependent export of HuR in response to heat shock RNA 7 9 2001 1348 1361
22. L. Golomb, D.R. Bublik, S. Wilder, R. Nevo, V. Kiss, K. Grabusic, and et al. Importin 7 and exportin 1 link c-Myc and p53 to regulation of ribosomal biogenesis Mol Cell 45 2 2012 222 232
23. S. Granneman, and S.J. Baserga Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing Curr Opin Cell Biol 17 3 2005 281 286
24. T. Hamamoto, T. Uozumi, and T. Beppu Leptomycins A and B, new antifungal antibiotics. III. Mode of action of leptomycin B on Schizosaccharomyces pombe J Antibiot (Tokyo) 38 11 1985 1573 1580
25. V. Havelange, P. Ranganathan, S. Geyer, D. Nicolet, X. Huang, X. Yu, and et al. Implications of the miR-10 family in chemotherapy response of NPM1-mutated AML. [Research Support, N I H, Extramural Research Support, Non-U S Gov't] Blood 123 15 2014 2412 2415
26. Y. Hayakawa, K.Y. Sohda, K. Shin-Ya, T. Hidaka, and H. Seto Anguinomycins C and D, new antitumor antibiotics with selective cytotoxicity against transformed cells J Antibiot (Tokyo) 48 9 1995 954 961
27. T. Hideshima, C. Mitsiades, G. Tonon, P.G. Richardson, and K.C. Anderson Understanding multiple myeloma pathogenesis in the bone marrow to identify new therapeutic targets Nat Rev Cancer 7 8 2007 585 598
28. W.Y. Huang, L. Yue, W.S. Qiu, L.W. Wang, X.H. Zhou, and Y.J. Sun Prognostic value of CRM1 in pancreas cancer Clin Invest Med 32 6 2009 E315
29. H. Inoue, M. Kauffman, S. Shacham, Y. Landesman, J. Yang, C.P. Evans, and et al. CRM1 blockade by selective inhibitors of nuclear export attenuates kidney cancer growth J Urol 189 6 2013 2317 2326
30. K. Jewers, M.B. Burbage, G. Blunden, and W.J. Griffin Brisbagenin and brisbenone, two new spirostanes from Cordyline species Steroids 24 2 1974 203 208
31. L. Jin, Y. Tabe, K. Kojima, Y. Zhou, S. Pittaluga, M. Konopleva, and et al. MDM2 antagonist Nutlin-3 enhances bortezomib-mediated mitochondrial apoptosis in TP53-mutated mantle cell lymphoma Cancer Lett 299 2 2010 161 170
32. T.R. Kau, J.C. Way, and P.A. Silver Nuclear transport and cancer: from mechanism to intervention Nat Rev Cancer 4 2 2004 106 117
33. A.A. Khutornenko, V.V. Roudko, B.V. Chernyak, A.B. Vartapetian, P.M. Chumakov, and A.G. Evstafieva Pyrimidine biosynthesis links mitochondrial respiration to the p53 pathway Proc Natl Acad Sci U S A 107 29 2010 12828 12833
34. A. Kohler, and E. Hurt Exporting RNA from the nucleus to the cytoplasm Nat Rev Mol Cell Biol 8 10 2007 761 773
35. K. Kojima, S.M. Kornblau, V. Ruvolo, A. Dilip, S. Duvvuri, R.E. Davis, and et al. Prognostic impact and targeting of CRM1 in acute myeloid leukemia Blood 121 20 2013 4166 4174
36. K. Komiyama, K. Okada, S. Tomisaka, I. Umezawa, T. Hamamoto, and T. Beppu Antitumor activity of leptomycin B J Antibiot (Tokyo) 38 3 1985 427 429
37. N. Kudo, N. Matsumori, H. Taoka, D. Fujiwara, E.P. Schreiner, B. Wolff, and 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 96 16 1999 9112 9117
38. N. Kudo, B. Wolff, T. Sekimoto, E.P. Schreiner, Y. Yoneda, M. Yanagida, and et al. Leptomycin B inhibition of signal-mediated nuclear export by direct binding to CRM1 Exp Cell Res 242 2 1998 540 547
39. J. Kuruvilla, M. Gutierrez, B.D. Shah, N.Y. Gabrail, P. de Nully Brown, R.M., and et al. Preliminary evidence of anti tumor activity of selinexor (KPT-330) in a phase I trial Ofa first-in-class oral selective inhibitor of nuclear export (SINE) in patients (pts) with relapsed/refractory non Hodgkin's lymphoma (NHL) and chronic lymphocytic leukemia (CLL) Blood 122 21 2013 (Abstract 90)
40. U. Kutay, and S. Guttinger Leucine-rich nuclear-export signals: born to be weak Trends Cell Biol 15 3 2005 121 124
41. R. Lapalombella, Q. Sun, K. Williams, L. Tangeman, S. Jha, Y. Zhong, and et al. Selective inhibitors of nuclear export show that CRM1/XPO1 is a target in chronic lymphocytic leukemia Blood 120 23 2012 4621 4634
42. Z. Li, and S.R. Hann The Myc-nucleophosmin-ARF network: a complex web unveiled Cell Cycle 8 17 2009 2703 2707
43. S.P. Linke, K.C. Clarkin, A. Di Leonardo, A. Tsou, and G.M. Wahl A reversible, p53-dependent G0/G1 cell cycle arrest induced by ribonucleotide depletion in the absence of detectable DNA damage Genes Dev 10 8 1996 934 947
44. C.A. London, L.F. Bernabe, S. Barnard, W.C. Kisseberth, A. Borgatti, M. Henson, and et al. Preclinical evaluation of the novel, orally bioavailable Selective Inhibitor of Nuclear Export (SINE) KPT-335 in spontaneous canine cancer: results of a phase I study PLoS ONE 9 2 2014 e87585
45. J. Long, B. Parkin, P. Ouillette, D. Bixby, K. Shedden, H. Erba, and et al. Multiple distinct molecular mechanisms influence sensitivity and resistance to MDM2 inhibitors in adult acute myelogenous leukemia Blood 116 1 2010 71 80
46. C.M. Lucas, R.J. Harris, A. Giannoudis, M. Copland, J.R. Slupsky, and R.E. Clark Cancerous inhibitor of PP2A (CIP2A) at diagnosis of chronic myeloid leukemia is a critical determinant of disease progression Blood 117 24 2011 6660 6668
47. L.B. Maggi Jr., M. Kuchenruether, D.Y. Dadey, R.M. Schwope, S. Grisendi, R.R. Townsend, and et al. Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome Mol Cell Biol 28 23 2008 7050 7065
48. N. Meani, and M. Alcalay Role of nucleophosmin in acute myeloid leukemia Expert Rev Anticancer Ther 9 9 2009 1283 1294
49. T. Meissner, E. Krause, and U. Vinkemeier Ratjadone and leptomycin B block CRM1-dependent nuclear export by identical mechanisms FEBS Lett 576 1-2 2004 27 30
50. T. Monecke, T. Guttler, P. Neumann, A. Dickmanns, D. Gorlich, and R. Ficner Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP Science 324 5930 2009 1087 1091
51. S.C. Mutka, W.Q. Yang, S.D. Dong, S.L. Ward, D.A. Craig, P.B. Timmermans, and et al. Identification of nuclear export inhibitors with potent anticancer activity in vivo Cancer Res 69 2 2009 510 517
52. P. Neviani, R. Santhanam, R. Trotta, M. Notari, B.W. Blaser, S. Liu, and et al. The tumor suppressor PP2A is functionally inactivated in blast crisis CML through the inhibitory activity of the BCR/ABL-regulated SET protein Cancer Cell 8 5 2005 355 368
53. E.S. Newlands, G.J. Rustin, and M.H. Brampton Phase I trial of elactocin Br J Cancer 74 4 1996 648 649
54. A. Noske, W. Weichert, S. Niesporek, A. Roske, A.C. Buckendahl, I. Koch, and et al. Expression of the nuclear export protein chromosomal region maintenance/exportin 1/Xpo1 is a prognostic factor in human ovarian cancer Cancer 112 8 2008 1733 1743
55. B. Ossareh-Nazari, F. Bachelerie, and C. Dargemont Evidence for a role of CRM1 in signal-mediated nuclear protein export Science 278 5335 1997 141 144
56. X.S. Puente, M. Pinyol, V. Quesada, L. Conde, G.R. Ordonez, N. Villamor, and et al. Whole-genome sequencing identifies recurrent mutations in chronic lymphocytic leukaemia Nature 475 7354 2011 101 105
57. P. Ranganathan, X. Yu, C. Na, R. Santhanam, S. Shacham, M. Kauffman, and et al. Preclinical activity of a novel CRM1 inhibitor in acute myeloid leukemia Blood 120 9 2012 1765 1773
58. I. Raska, K. Koberna, J. Malinsky, H. Fidlerova, and M. Masata The nucleolus and transcription of ribosomal genes Biol Cell 96 8 2004 579 594
59. K. Sakakibara, N. Saito, T. Sato, A. Suzuki, Y. Hasegawa, J.M. Friedman, and et al. CBS9106 is a novel reversible oral CRM1 inhibitor with CRM1 degrading activity Blood 118 14 2011 3922 3931
60. S. Santagata, M.L. Mendillo, Y.C. Tang, A. Subramanian, C.C. Perley, S.P. Roche, and et al. Tight coordination of protein translation and HSF1 activation supports the anabolic malignant state Science 341 6143 2013 1238303
61. M. Savona, R. Garzon, P. de Nully Brown, K. Yee, J.E. Lancet, and M. Gutierrez 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 122 21 2013 (Abstract 1440)
62. J. Schmidt, E. Braggio, K.M. Kortuem, J.B. Egan, Y.X. Zhu, C.S. Xin, and et al. Genome-wide studies in multiple myeloma identify XPO1/CRM1 as a critical target validated using the selective nuclear export inhibitor KPT-276 Leukemia 27 12 2013 2357 2365
63. C. Shao, C. Lu, L. Chen, P.P. Koty, E. Cobos, and W. Gao p53-Dependent anticancer effects of leptomycin B on lung adenocarcinoma Cancer Chemother Pharmacol 67 6 2011 1369 1380
64. A. Shen, Y. Wang, Y. Zhao, L. Zou, L. Sun, and C. Cheng Expression of CRM1 in human gliomas and its significance in p27 expression and clinical prognosis Neurosurgery 65 1 2009 153 159 (discussion 159-160)
65. Y. Tabe, K. Kojima, L. Jin, H. Iwanami, H. Matsushita, S. Kazuno, and et al. Molecular mechanisms of inhibition of ribosomal biogenesis and translational flux by the Selective Inhibitor of Nuclear Export (SINE) XPO1/CRM1 antagonist KPT-185 in mantle cell lymphoma Blood 122 2013 (Abstract 820)
66. Y.T. Tai, Y. Landesman, C. Acharya, Y. Calle, M.Y. Zhong, M. Cea, and et al. CRM1 inhibition induces tumor cell cytotoxicity and impairs osteoclastogenesis in multiple myeloma: molecular mechanisms and therapeutic implications Leukemia 28 1 2014 155 165
67. Y. Takenaka, T. Fukumori, T. Yoshii, N. Oka, H. Inohara, H.R. Kim, and et al. Nuclear export of phosphorylated galectin-3 regulates its antiapoptotic activity in response to chemotherapeutic drugs Mol Cell Biol 24 10 2004 4395 4406
68. F. Thomas, and U. Kutay Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway J Cell Sci 116 Pt 12 2003 2409 2419
69. R.E. Tiedemann, Y.X. Zhu, J. Schmidt, C.X. Shi, C. Sereduk, H. Yin, and et al. Identification of molecular vulnerabilities in human multiple myeloma cells by RNA interference lethality screening of the druggable genome Cancer Res 72 3 2012 757 768
70. J.G. Turner, J. Dawson, and D.M. Sullivan Nuclear export of proteins and drug resistance in cancer Biochem Pharmacol 83 8 2012 1021 1032
71. J.G. Turner, R. Engel, J.A. Derderian, R. Jove, and D.M. Sullivan Human topoisomerase IIalpha nuclear export is mediated by two CRM-1-dependent nuclear export signals J Cell Sci 117 Pt 14 2004 3061 3071
72. J.G. Turner, D.C. Marchion, J.L. Dawson, M.F. Emmons, L.A. Hazlehurst, P. Washausen, and et al. Human multiple myeloma cells are sensitized to topoisomerase II inhibitors by CRM1 inhibition Cancer Res 69 17 2009 6899 6905
73. P.J. van der Watt, C.P. Maske, D.T. Hendricks, M.I. Parker, L. Denny, D. Govender, and et al. 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 8 2009 1829 1840
74. T. Van Neck, C. Pannecouque, E. Vanstreels, M. Stevens, W. Dehaen, and D. Daelemans Inhibition of the CRM1-mediated nucleocytoplasmic transport by N-azolylacrylates: structure-activity relationship and mechanism of action Bioorg Med Chem 16 21 2008 9487 9497
75. J. van Riggelen, A. Yetil, and D.W. Felsher MYC as a regulator of ribosome biogenesis and protein synthesis Nat Rev Cancer 10 4 2010 301 309
76. P. Vigneri, and J.Y. Wang Induction of apoptosis in chronic myelogenous leukemia cells through nuclear entrapment of BCR-ABL tyrosine kinase Nat Med 7 2 2001 228 234
77. P.K. Vogt, H. Jiang, and M. Aoki Triple layer control: phosphorylation, acetylation and ubiquitination of FOXO proteins Cell Cycle 4 7 2005 908 913
78. J.Y. Wach, S. Guttinger, U. Kutay, and K. Gademann The cytotoxic styryl lactone goniothalamin is an inhibitor of nucleocytoplasmic transport Bioorg Med Chem Lett 20 9 2010 2843 2846
79. C.J. Walker, J.J. Oaks, R. Santhanam, P. Neviani, J.G. Harb, G. Ferenchak, and et al. Preclinical and clinical efficacy of XPO1/CRM1 inhibition by the karyopherin inhibitor KPT-330 in Ph + leukemias Blood 122 17 2013 3034 3044
80. W. Wen, J.L. Meinkoth, R.Y. Tsien, and S.S. Taylor Identification of a signal for rapid export of proteins from the nucleus Cell 82 3 1995 463 473
81. S.P. Whitman, A.S. Ruppert, M.D. Radmacher, K. Mrozek, P. Paschka, C. Langer, and et al. FLT3 D835/I836 mutations are associated with poor disease-free survival and a distinct gene-expression signature among younger adults with de novo cytogenetically normal acute myeloid leukemia lacking FLT3 internal tandem duplications Blood 111 3 2008 1552 1559
82. C.H. Wu, D. Sahoo, C. Arvanitis, N. Bradon, D.L. Dill, and D.W. Felsher Combined analysis of murine and human microarrays and ChIP analysis reveals genes associated with the ability of MYC to maintain tumorigenesis PLoS Genet 4 6 2008 e1000090
83. D. Xu, N.V. Grishin, and Y.M. Chook NESdb: a database of NES-containing CRM1 cargoes Mol Biol Cell 23 18 2012 3673 3676
84. M. Yanada, K. Matsuo, T. Suzuki, H. Kiyoi, and T. Naoe Prognostic significance of FLT3 internal tandem duplication and tyrosine kinase domain mutations for acute myeloid leukemia: a meta-analysis Leukemia 19 8 2005 1345 1349
85. Y. Yao, Y. Dong, F. Lin, H. Zhao, Z. Shen, P. Chen, and et al. The expression of CRM1 is associated with prognosis in human osteosarcoma Oncol Rep 21 1 2009 229 235
86. M. Yoshimura, J. Ishizawa, V. Ruvolo, A. Dilip, A. Quintas-Cardama, T.J. McDonnell, and et al. Induction of p53-mediated transcription and apoptosis by Exportin-1 (XPO1) inhibition in mantle cell lymphoma Cancer Sci 105 7 2014 795 801
87. K. Zhang, M. Wang, A.T. Tamayo, S. Shacham, M. Kauffman, J. Lee, and et al. Novel selective inhibitors of nuclear export CRM1 antagonists for therapy in mantle cell lymphoma Exp Hematol 41 1 2013 67 78 (e64)