Induction of p53-mediated transcription and apoptosis by exportin-1 (XPO1) inhibition in mantle cell lymphoma

Cancer Science

Volumn 105, Issue 7, 2014, Pages 795-801

  Yoshimura, Mariko ^a   Ishizawa, Jo ^b   Ruvolo, Vivian ^b   Dilip, Archana ^b   Quintás Cardama, Alfonso ^b   Mcdonnell, Timothy J ^b   Neelapu, Sattva S ^b   Kwak, Larry W ^b   Shacham, Sharon ^c   Kauffman, Michael ^c   Tabe, Yoko ^d   Yokoo, Masako ^a   Kimura, Shinya ^a   Andreeff, Michael ^b   Kojima, Kensuke ^a,b  

^a SAGA UNIVERSITY   (Japan)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c Karyopharm Therapeutics   (United States)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; KPT SINE; Mantle cell lymphoma; P53; XPO1

Indexed keywords

EXPORTIN 1; PROTEIN P53;

APOPTOSIS; ARTICLE; CANCER PROGNOSIS; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MANTLE CELL LYMPHOMA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; WESTERN BLOTTING;

APOPTOSIS; KPT-SINE; MANTLE CELL LYMPHOMA; P53; XPO1;

ACRYLATES; ANIMALS; APOPTOSIS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, P53; HUMANS; KARYOPHERINS; LYMPHOMA, MANTLE-CELL; MICE; MICE, TRANSGENIC; MUTATION; PROGNOSIS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTION, GENETIC; TRIAZOLES; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84904305023     PISSN: 13479032     EISSN: 13497006     Source Type: Journal    
DOI: 10.1111/cas.12430     Document Type: Article

References (40)

1. Xu D, Grishin NV, Chook YM. NESdb: a database of NES-containing CRM1 cargoes. Mol Biol Cell 2012; 23: 3673-6.
2. Kau TR, Way JC, Silver PA. Nuclear transport and cancer: from mechanism to intervention. Nat Rev Cancer 2004; 4: 106-17.
3. Turner JG, Dawson J, Sullivan DM. Nuclear export of proteins and drug resistance in cancer. Biochem Pharmacol 2012; 83: 1021-32.
4. Yao Y, Dong Y, Lin F et al. The expression of CRM1 is associated with prognosis in human osteosarcoma. Oncol Rep 2009; 21(1): 229-35.
5. Shen A, Wang Y, Zhao Y, Zou L, Sun L, Cheng C. Expression of CRM1 in human gliomas and its significance in p27 expression and clinical prognosis. Neurosurgery 2009; 65(1): 153-9.
6. Noske A, Weichert W, Niesporek S 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. van der Watt PJ, Maske CP, Hendricks DT 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 2009; 124: 1829-40.
8. Zhang K, Wang M, Tamayo AT et al. Novel selective inhibitors of nuclear export CRM1 antagonists for therapy in mantle cell lymphoma. Exp Hematol 2013; 41(1): 67-78.
9. Lapalombella R, Sun Q, Williams K et al. Selective inhibitors of nuclear export show that CRM1/XPO1 is a target in chronic lymphocytic leukemia. Blood 2012; 120: 4621-34.
10. Tai YT, Landesman Y, Acharya C et al. CRM1 inhibition induces tumor cell cytotoxicity and impairs osteoclastogenesis in multiple myeloma: molecular mechanisms and therapeutic implications. Leukemia 2014; 28: 155-65.
11. Kojima K, Kornblau SM, Ruvolo V et al. Prognostic impact and targeting of CRM1 in acute myeloid leukemia. Blood 2013; 121: 4166-74.
12. Jares P, Campo E. Advances in the understanding of mantle cell lymphoma. Br J Haematol 2008; 142: 149-65.
13. Greiner TC, Dasgupta C, Ho VV et al. Mutation and genomic deletion status of ataxia telangiectasia mutated (ATM) and p53 confer specific gene expression profiles in mantle cell lymphoma. Proc Natl Acad Sci U S A 2006; 103: 2352-7.
14. Rubio-Moscardo F, Climent J, Siebert R et al. Mantle-cell lymphoma genotypes identified with CGH to BAC microarrays define a leukemic subgroup of disease and predict patient outcome. Blood 2005; 105: 4445-54.
15. Halldórsdóttir AM, Lundin A, Murray F et al. Impact of TP53 mutation and 17p deletion in mantle cell lymphoma. Leukemia 2011; 25: 1904-8.
16. Hernández L, Beà S, Pinyol M et al. CDK4 and MDM2 gene alterations mainly occur in highly proliferative and aggressive mantle cell lymphomas with wild-type INK4a/ARF locus. Cancer Res 2005; 65: 2199-206.
17. Boyd MT, Vlatkovic N, Rubbi CP. The nucleolus directly regulates p53 export and degradation. J Cell Biol 2011; 194: 689-703.
18. Beckerman R, Prives C. Transcriptional regulation by p53. Cold Spring Harb Perspect Biol 2010; 2: a000935.
19. O'Brate A, Giannakakou P. The importance of p53 location: nuclear or cytoplasmic zip code? Drug Resist Updat 2003; 6: 313-22.
20. Moll UM, LaQuaglia M, Bénard J, Riou G. Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors. Proc Natl Acad Sci U S A 1995; 92: 4407-11.
21. Etchin J, Sun Q, Kentsis A, Farmer A, Zhang ZC, Sanda T, et al. Antileukemic activity of nuclear export inhibitors that spare normal hematopoietic cells. Leukemia 2013; 27(1): 66-74.
22. Petitjean A, Mathe E, Kato S et al. Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Hum Mutat 2007; 28: 622-9.
23. Verhaegen M, Bauer JA, Martín de la Vega C et al. A novel BH3 mimetic reveals a mitogen-activated protein kinase-dependent mechanism of melanoma cell death controlled by p53 and reactive oxygen species. Cancer Res 2006; 66: 11348-59.
24. Bichi R, Shinton SA, Martin ES et al. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proc Natl Acad Sci U S A 2002; 99: 6955-60.
25. Kojima K, Duvvuri S, Ruvolo V, Samaniego F, Younes A, Andreeff M. Decreased sensitivity of 17p-deleted chronic lymphocytic leukemia cells to a small molecule BCL-2 antagonist ABT-737. Cancer 2012; 118: 1023-31.
26. Vassilev LT, Vu BT, Graves B et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2004; 303: 844-8.
27. Garnett MJ, Edelman EJ, Heidorn SJ et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012; 483: 570-5.
28. Azmi AS, Aboukameel A, Bao B et al. Selective inhibitors of nuclear export block pancreatic cancer cell proliferation and reduce tumor growth in mice. Gastroenterology 2013; 144: 447-56.
29. Green DR, Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 2009; 458: 1127-30.
30. Azmi AS, Al-Katib A, Aboukameel A et al. Selective inhibitors of nuclear export for the treatment of non-Hodgkin's lymphomas. Haematologica 2013; 98: 1098-106.
31. Elison JR, Cobrinik D, Claros N, Abramson DH, Lee TC. Small molecule inhibition of HDM2 leads to p53-mediated cell death in retinoblastoma cells. Arch Ophthalmol 2006; 124: 1269-75.
32. Kojima K, Konopleva M, Samudio IJ et al. MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy. Blood 2005; 106: 3150-9.
33. Vaseva AV, Marchenko ND, Moll UM. The transcription-independent mitochondrial p53 program is a major contributor to nutlin-induced apoptosis in tumor cells. Cell Cycle 2009; 8: 1711-9.
34. Kojima K, Konopleva M, McQueen T, O'Brien S, Plunkett W, Andreeff M. Mdm2 inhibitor Nutlin-3a induces p53-mediated apoptosis by transcription-dependent and transcription-independent mechanisms and may overcome Atm-mediated resistance to fludarabine in chronic lymphocytic leukemia. Blood 2006; 108: 993-1000.
35. Kuruvilla J, Gutierrez M, Shah BD 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) [abstract]. Blood 2013; 122 Abstract 90.
36. Razak ARA, Soerensen MM, Mahipal A 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 [abstract]. J Clin Oncol 2013; 31: Abstract 2505.
37. Aziz MH, Shen H, Maki CG. Acquisition of p53 mutations in response to the non-genotoxic p53 activator Nutlin-3. Oncogene 2011; 30: 4678-86.
38. Michaelis M, Rothweiler F, Barth S et al. Adaptation of cancer cells from different entities to the MDM2 inhibitor nutlin-3 results in the emergence of p53-mutated multi-drug-resistant cancer cells. Cell Death Dis 2011; 2: e243.
39. Chaturvedi NK, Rajule RN, Shukla A et al. Novel treatment for mantle cell lymphoma including therapy-resistant tumor by NF-κB and mTOR dual-targeting approach. Mol Cancer Ther 2013; 12: 2006-17.
40. Oberley MJ, Rajguru SA, Zhang C et al. Immunohistochemical evaluation of MYC expression in mantle cell lymphoma. Histopathology 2013; 63: 499-508.