Selective inhibitors of nuclear export (SINE)-A novel class of anti-cancer agents

Journal of Hematology and Oncology

Volumn 7, Issue 1, 2014, Pages

  Parikh, Kaushal ^a   Cang, Shundong ^b   Sekhri, Arunabh ^a   Liu, Delong ^c  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b HENAN PROVINCIAL PEOPLE'S HOSPITAL   (China)

^c ZHENGZHOU UNIVERSITY   (China)

Author keywords

KPT 330; Nuclear export; Selinexor; Sine

Indexed keywords

ANTINEOPLASTIC AGENT; EXPORTIN 1; KPT 127; KPT 185; KPT 205; KPT 227; KPT 251; NEW DRUG; SELECTIVE INHIBITORS OF NUCLEAR EXPORT; SELINEXOR; UNCLASSIFIED DRUG; KARYOPHERIN;

ACUTE LEUKEMIA; ARTICLE; CARCINOGENESIS; CELL NUCLEUS; CHRONIC LEUKEMIA; CYTOPLASM; DRUG MECHANISM; DRUG SYNTHESIS; HEMATOLOGIC MALIGNANCY; HUMAN; INTRACELLULAR TRANSPORT; KIDNEY CARCINOMA; LYMPHOMA; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MULTIPLE MYELOMA; NON SMALL CELL LUNG CANCER; NONHUMAN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN TRANSPORT; SOLID TUMOR; TREATMENT RESPONSE; TRIPLE NEGATIVE BREAST CANCER; ACTIVE TRANSPORT; ANIMAL; DRUG EFFECTS; METABOLISM; NEOPLASMS;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTINEOPLASTIC AGENTS; HUMANS; KARYOPHERINS; NEOPLASMS;

EID: 84924149342     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-014-0078-0     Document Type: Article

References (115)

1. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, Yanagida M, Nishida E: CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 1997, 390:308-311.
2. Xu D, Grishin NV, Chook YM: NESdb: A database of NES-containing CRM1 cargoes. Mol Biol Cell 2012, 23:3673-3676.
3. Nguyen KT, Holloway MP, Altura RA: The CRM1 nuclear export protein in normal development and disease. Int J Biochem Mol Biol 2012, 3:137-151.
4. Cheng Y, Holloway MP, Nguyen K, McCauley D, Landesman Y, Kauffman MG, Shacham S, Altura RA: XPO1 (CRM1) inhibition represses STAT3 activation to drive a survivin-dependent oncogenic switch in triple-negative breast cancer. Mol Cancer Ther 2014, 13:675-686.
5. Kutay U, Hetzer MW: Reorganization of the nuclear envelope during open mitosis. Curr Opin Cell Biol 2008, 20:669-677.
6. Turner JG, Sullivan DM: CRM1-mediated nuclear export of proteins and drug resistance in cancer. Curr Med Chem 2008, 15:2648-2655.
7. Turner JG, Dawson J, Sullivan DM: Nuclear export of proteins and drug resistance in cancer. Biochem Pharmacol 2012, 83:1021-1032.
8. Noske A, Weichert W, Niesporek S, Röske A, Buckendahl AC, Koch I, Sehouli J, Dietel M, Denkert C: Expression of the nuclear export protein chromosomal region maintenance/exportin 1/Xpo1 is a prognostic factor in human ovarian cancer. Cancer 2008, 112:1733-1743.
9. 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, 65:153-159. discussion 159-160.
10. Yao Y, Dong Y, Lin F, Zhao H, Shen Z, Chen P, Sun YJ, Tang LN, Zheng SE: The expression of CRM1 is associated with prognosis in human osteosarcoma. Oncol Rep 2009, 21:229-235.
11. 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.
12. Tai YT, Landesman Y, Acharya C, Calle Y, Zhong MY, Cea M, Tannenbaum D, Cagnetta A, Reagan M, Munshi AA, Senapedis W, Saint-Martin JR, Kashyap T, Shacham S, Kauffman M, Gu Y, Wu L, Ghobrial I, Zhan F, Kung AL, Schey SA, Richardson P, Munshi NC, Anderson KC: CRM1 inhibition induces tumor cell cytotoxicity and impairs osteoclastogenesis in multiple myeloma: molecular mechanisms and therapeutic implications. Leukemia 2014, 28:155-165.
13. Güttler T, Görlich D: Ran-dependent nuclear export mediators: A structural perspective. EMBO J 2011, 30:3457-3474.
14. Monecke T, Güttler T, Neumann P, Dickmanns A, Görlich D, Ficner R: Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP. Science 2009, 324:1087-1091.
15. Fung HY, Chook YM: Atomic basis of CRM1-cargo recognition, release and inhibition. Semin Cancer Biol 2014, http://dx.doi.org/10.1016/j.semcancer.2014.03.002.
16. Mutka SC, Yang WQ, Dong SD, Ward SL, Craig DA, Timmermans PB, Murli S: Identification of nuclear export inhibitors with potent anticancer activity in vivo. Cancer Res 2009, 69:510-517.
17. Sakakibara K, Saito N, Sato T, Suzuki A, Hasegawa Y, Friedman JM, Kufe DW, Vonhoff DD, Iwami T, Kawabe T: CBS9106 is a novel reversible oral CRM1 inhibitor with CRM1 degrading activity. Blood 2011, 118:3922-3931.
18. Kudo N, Matsumori N, Taoka H, Fujiwara D, Schreiner EP, Wolff B, Yoshida M, Horinouchi S: 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, 96:9112-9117.
19. Bonazzi S, Eidam O, Güttinger S, Wach JY, Zemp I, Kutay U, Gademann K: Anguinomycins and derivatives: Total syntheses, modeling, and biological evaluation of the inhibition of nucleocytoplasmic transport. J Am Chem Soc 2010, 132:1432-1442.
20. Daelemans D, Afonina E, Nilsson J, Werner G, Kjems J, De Clercq E, Pavlakis GN, Vandamme AM: A synthetic HIV-1 Rev inhibitor interfering with the CRM1- mediated nuclear export. Proc Natl Acad Sci U S A 2002, 99:14440-14445.
21. Meissner T, Krause E, Vinkemeier U: Ratjadone and leptomycin B block CRM1-dependent nuclear export by identical mechanisms. FEBS Lett 2004, 576:27-30.
22. Newlands ES, Rustin GJ, Brampton MH: Phase I trial of elactocin. Br J Cancer 1996, 74:648-649.
23. Etchin J, Sun Q, Kentsis A, Farmer A, Zhang ZC, Sanda T, Mansour MR, Barcelo C, McCauley D, Kauffman M, Shacham S, Christie AL, Kung AL, Rodig SJ, Chook YM, Look AT: Antileukemic activity of nuclear export inhibitors that spare normal hematopoietic cells. Leukemia 2013, 27:66-74.
24. Lapalombella R, Sun Q, Williams K, Tangeman L, Jha S, Zhong Y, Goettl V, Mahoney E, Berglund C, Gupta S, Farmer A, Mani R, Johnson AJ, Lucas D, Mo X, Daelemans D, Sandanayaka V, Shechter S, McCauley D, Shacham S, Kauffman M, Chook YM, Byrd JC: Selective inhibitors of nuclear export show that CRM1/XPO1 is a target in chronic lymphocytic leukemia. Blood 2012, 120:4621-4634.
25. Ranganathan P, Yu X, Na C, Santhanam R, Shacham S, Kauffman M, Walker A, Klisovic R, Blum W, Caligiuri M, Croce CM, Marcucci G, Garzon R: Preclinical activity of a novel CRM1 inhibitor in acute myeloid leukemia. Blood 2012, 120:1765-1773.
26. Azmi AS, Aboukameel A, Bao B, Sarkar FH, Philip PA, Kauffman M, Shacham S, Mohammad RM: Selective inhibitors of nuclear export block pancreatic cancer cell proliferation and reduce tumor growth in mice. Gastroenterology 2013, 144:447-456.
27. Sells SF, Han SS, Muthukkumar S, Maddiwar N, Johnstone R, Boghaert E, Gillis D, Liu G, Nair P, Monnig S, Collini P, Mattson MP, Sukhatme VP, Zimmer SG, Wood DP, McRoberts JW, Shi Y, Rangnekar VM: Expression and function of the leucine zipper protein Par-4 in apoptosis. Mol Cell Biol 1997, 17:3823-3832.
28. Ahmed MM, Sheldon D, Fruitwala MA, Venkatasubbarao K, Lee EY, Gupta S, Wood C, Mohiuddin M, Strodel WE: Downregulation of PAR-4, a pro-Apoptotic gene, in pancreatic tumors harboring K-ras mutation. Int J Cancer 2008, 122:63-70.
29. Tanaka K, Iwamoto S, Gon G, Nohara T, Iwamoto M, Tanigawa N: Expression of survivin and its relationship to loss of apoptosis in breast carcinomas. Clin Cancer Res 2000, 6:127-134.
30. Dohi T, Okada K, Xia F, Wilford CE, Samuel T, Welsh K, Marusawa H, Zou H, Armstrong R, Matsuzawa S, Zou H, Armstrong R, Matsuzawa S, Salvesen GS, Reed JC, Altieri DC: An IAP-IAP complex inhibits apoptosis. J Biol Chem 2004, 279:34087-34090.
31. Furqan M, Mukhi N, Lee B, Liu D: Dysregulation of JAK-STAT pathway in hematological malignancies and JAK inhibitors for clinical application. Biomarker Res 2013, 1:5.
32. Bromberg J, Darnell JE: The role of STATs in transcriptional control and their impact on cellular function. Oncogene 2000, 19:2468-2473.
33. Rodríguez JA, Span SW, Ferreira CG, Kruyt FA, Giaccone G: CRM1-mediated nuclear export determines the cytoplasmic localization of the antiapoptotic protein Survivin. Exp Cell Res 2002, 275:44-53.
34. Stauber RH, Rabenhorst U, Rekik A, Engels K, Bier C, Knauer SK: Nucleocytoplasmic shuttling and the biological activity of mouse survivin are regulated by an active nuclear export signal. Traffic 2006, 7:1461-1472.
35. Mau-Soerensen M, Razak ARA, Shields AF, Gabrail NY, Gerecitano JF, Shacham S, Lassen UN, Rashal T, Cooksey J, Landesman Y, Pond G, Oza AM, Kauffman M, Siu LL, Bedard PL, Mahaseth H, Mirza MR, Mahipal A: A first-in-class, first-in-human phase I trial of KPT-330 (selinexor), a selective inhibitor of nuclear export (SINE) in patients (pts) with advanced solid tumors. ASCO Meeting Abstracts 2014, 32:2537.
36. Xu C, Zhou Q, Wu Y-l: Can EGFR-TKIs be used in first line treatment for advanced non-small cell lung cancer based on selection according to clinical factors? - A literature-based meta-Analysis. J Hematol Oncol 2012, 5:62.
37. Niu F-Y, Wu Y-L: Novel agents and strategies for overcoming EGFR TKIs resistance. Exp Hematol Oncol 2014, 3:2.
38. Sharma SV, Bell DW, Settleman J, Haber DA: Epidermal growth factor receptor mutations in lung cancer. Nat Rev Cancer 2007, 7:169-181.
39. Stewart DJ: Tumor and host factors that may limit efficacy of chemotherapy in non-small cell and small cell lung cancer. Crit Rev Oncol Hematol 2010, 75:173-234.
40. Stommel JM, Marchenko ND, Jimenez GS, Moll UM, Hope TJ, Wahl GM: A leucine-rich nuclear export signal in the p53 tetramerization domain: Regulation of subcellular localization and p53 activity by NES masking. EMBO J 1999, 18:1660-1672.
41. Sun H, Hattori N, Chien W, Sun Q, Sudo M, GL EL, Ding L, Lim SL, Shacham S, Kauffman M, Nakamaki T, Koeffler HP: KPT-330 has antitumour activity against non-small cell lung cancer. Br J Cancer 2014, 111:281-291.
42. Moll UM, Slade N: p63 and p73: Roles in development and tumor formation. Mol Cancer Res 2004, 2:371-386.
43. Wang S, Han X, Wang J, Yao J, Shi Y: Antitumor effects of a novel chromosome region maintenance 1 (CRM1) inhibitor on non-small cell lung cancer cells in vitro and in mouse tumor xenografts. Plos One 2014, 9:e89848.
44. Belldegrun AS, Klatte T, Shuch B, LaRochelle JC, Miller DC, Said JW, Riggs SB, Zomorodian N, Kabbinavar FF, Dekernion JB, Pantuck AJ: Cancer-specific survival outcomes among patients treated during the cytokine era of kidney cancer (1989-2005): A benchmark for emerging targeted cancer therapies. Cancer 2008, 113:2457-2463.
45. Inoue H, Kauffman M, Shacham S, Landesman Y, Yang J, Evans CP, Weiss RH: CRM1 blockade by selective inhibitors of nuclear export attenuates kidney cancer growth. J Urol 2013, 189:2317-2326.
46. Inoue H, Hwang SH, Wecksler AT, Hammock BD, Weiss RH: Sorafenib attenuates p21 in kidney cancer cells and augments cell death in combination with DNA-damaging chemotherapy. Cancer Biol Ther 2011, 12:827-836.
47. Jerant AF, Johnson JT, Sheridan CD, Caffrey TJ: Early detection and treatment of skin cancer. Am Fam Physician 2000, 62:357-368. 375-356, 381-352.
48. Atefi M, von Euw E, Attar N, Ng C, Chu C, Guo D, Nazarian R, Chmielowski B, Glaspy JA, Comin-Anduix B, Mischel PS, Lo RS, Ribas A: Reversing melanoma cross-resistance to BRAF and MEK inhibitors by co-Targeting the AKT/mTOR pathway. Plos One 2011, 6:e28973.
49. Baldus SE, Schaefer KL, Engers R, Hartleb D, Stoecklein NH, Gabbert HE: Prevalence and heterogeneity of KRAS, BRAF, and PIK3CA mutations in primary colorectal adenocarcinomas and their corresponding metastases. Clin Cancer Res 2010, 16:790-799.
50. Dalle S, Poulalhon N, Thomas L: Vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011, 365:1448-1449. author reply 1450.
51. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, et al: Mutations of the BRAF gene in human cancer. Nature 2002, 417:949-954.
52. Lee B, Mukhi N, Liu D: Current management and novel agents for malignant melanoma. J Hematol Oncol 2012, 5:3.
53. Akinleye A, Furqan M, Mukhi N, Ravella P, Liu D: MEK and the inhibitors: from bench to bedside. J Hematol Oncol 2013, 6:27.
54. Huang T, Karsy M, Zhuge J, Zhong M, Liu D: B-Raf and the inhibitors: from bench to bedside. J Hematol Oncol 2013, 6:30.
55. Ascierto PA, Schadendorf D, Berking C, Agarwala SS, van Herpen CM, Queirolo P, Blank CU, Hauschild A, Beck JT, St-Pierre A, Niazi F, Wandel S, Peters M, Zubel A, Dummer R: MEK162 for patients with advanced melanoma harbouring NRAS or Val600 BRAF mutations: A nonrandomised, open-label phase 2 study. Lancet Oncol 2013, 14:249-256.
56. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, O'Day SJ, Sosman JA, Kirkwood JM, Eggermont AM, Dreno B, Nolop K, Li J, Nelson B, Hou J, Lee RJ, Flaherty KT, McArthur GA, Group B-S: Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011, 364:2507-2516.
57. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, Milhem M, Demidov LV, Hassel JC, Rutkowski P, Mohr P, Dummer R, Trefzer U, Larkin JM, Utikal J, Dreno B, Nyakas M, Middleton MR, Becker JC, Casey M, Sherman LJ, Wu FS, Ouellet D, Martin AM, Patel K, Schadendorf D, Group MS: Improved survival with MEK inhibition in BRAF-mutated melanoma. N Engl J Med 2012, 367:107-114.
58. Ho AL, Grewal RK, Leboeuf R, Sherman EJ, Pfister DG, Deandreis D, Pentlow KS, Zanzonico PB, Haque S, Gavane S, Ghossein RA, Ricarte-Filho JC, Dominguez JM, Shen R, Tuttle RM, Larson SM, Fagin JA: Selumetinib-enhanced radioiodine uptake in advanced thyroid cancer. N Engl J Med 2013, 368:623-632.
59. Janne PA, Shaw AT, Pereira JR, Jeannin G, Vansteenkiste J, Barrios C, Franke FA, Grinsted L, Zazulina V, Smith P, Crino L: Selumetinib plus docetaxel for KRAS-mutant advanced non-small-cell lung cancer: A randomised, multicentre, placebo-controlled, phase 2 study. Lancet Oncol 2013, 14:38-47.
60. Marks JL, Gong Y, Chitale D, Golas B, McLellan MD, Kasai Y, Ding L, Mardis ER, Wilson RK, Solit D, Levine R, Michel K, Thomas RK, Rusch VW, Ladanyi M, Pao W: Novel MEK1 mutation identified by mutational analysis of epidermal growth factor receptor signaling pathway genes in lung adenocarcinoma. Cancer Res 2008, 68:5524-5528.
61. Pathria G, Wagner C, Wagner SN: Inhibition of CRM1-mediated nucleocytoplasmic transport: Triggering human melanoma cell apoptosis by perturbing multiple cellular pathways. J Invest Dermatol 2012, 132:2780-2790.
62. Salas Fragomeni RA, Chung HW, Landesman Y, Senapedis W, Saint-Martin JR, Tsao H, Flaherty KT, Shacham S, Kauffman M, Cusack JC: CRM1 and BRAF inhibition synergize and induce tumor regression in BRAF-mutant melanoma. Mol Cancer Ther 2013, 12:1171-1179.
63. Cagnol S, Chambard JC: ERK and cell death: mechanisms of ERK-induced cell death-Apoptosis, autophagy and senescence. FEBS J 2010, 277:2-21.
64. Mirmohammadsadegh A, Mota R, Gustrau A, Hassan M, Nambiar S, Marini A, Bojar H, Tannapfel A, Hengge UR: ERK1/2 is highly phosphorylated in melanoma metastases and protects melanoma cells from cisplatinmediated apoptosis. J Invest Dermatol 2007, 127:2207-2215.
65. Kojima K, Kornblau SM, Ruvolo V, Dilip A, Duvvuri S, Davis RE, Zhang M, Wang Z, Coombes KR, Zhang N, Qiu YH, Burks JK, Kantarjian H, Shacham S, Kauffman M, Andreeff M: Prognostic impact and targeting of CRM1 in acute myeloid leukemia. Blood 2013, 121:4166-4174.
66. Saha M, Qiu L, Chang H: Targeting p53 by small molecules in hematological malignancies. J Hematol Oncol 2013, 6:23.
67. Pawar R, Singh Bali OP, Malhotra BK, Lamba G: Recent advances and novel agents for FLT3 mutated AML. Stem Cell Invest 2014, 1:7.
68. Cheng K, Sportoletti P, Ito K, Clohessy JG, Teruya-Feldstein J, Kutok JL, Pandolfi PP: The cytoplasmic NPM mutant induces myeloproliferation in a transgenic mouse model. Blood 2010, 115:3341-3345.
69. Yoon K, Smart RC: C/EBPalpha is a DNA damage-inducible p53-regulated mediator of the G1 checkpoint in keratinocytes. Mol Cell Biol 2004, 24:10650-10660.
70. Keeshan K, Santilli G, Corradini F, Perrotti D, Calabretta B: Transcription activation function of C/EBPalpha is required for induction of granulocytic differentiation. Blood 2003, 102:1267-1275.
71. Tenen DG, Hromas R, Licht JD, Zhang DE: Transcription factors, normal myeloid development, and leukemia. Blood 1997, 90:489-519.
72. Mrózek K, Marcucci G, Paschka P, Whitman SP, Bloomfield CD: Clinical relevance of mutations and gene-expression changes in adult acute myeloid leukemia with normal cytogenetics: Are we ready for a prognostically prioritized molecular classification? Blood 2007, 109:431-448.
73. Ikeda H, Kanakura Y, Tamaki T, Kuriu A, Kitayama H, Ishikawa J, Kanayama Y, Yonezawa T, Tarui S, Griffin JD: Expression and functional role of the protooncogene c-kit in acute myeloblastic leukemia cells. Blood 1991, 78:2962-2968.
74. Paschka P, Marcucci G, Ruppert AS, Mrózek K, Chen H, Kittles RA, Vukosavljevic T, Perrotti D, Vardiman JW, Carroll AJ, Kolitz JE, Larson RA, Bloomfield CD, CaLG B: Adverse prognostic significance of KIT mutations in adult acute myeloid leukemia with inv (16) and t (8;21): A Cancer and Leukemia Group B Study. J Clin Oncol 2006, 24:3904-3911.
75. 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.
76. Etchin J, Sanda T, Mansour MR, Kentsis A, Montero J, Le BT, Christie AL, McCauley D, Rodig SJ, Kauffman M, Shacham S, Stone R, Letai A, Kung AL, Thomas Look A: 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, 161:117-127.
77. Pui CH, Evans WE: Treatment of acute lymphoblastic leukemia. N Engl J Med 2006, 354:166-178.
78. Pui CH, Robison LL, Look AT: Acute lymphoblastic leukaemia. Lancet 2008, 371:1030-1043.
79. Zhao Y, Huang H, Wei G: Novel agents and biomarkers for acute lymphoid leukemia. J Hematol Oncol 2013, 6:40.
80. Farnsworth P, Ward D, Reddy V: Persistent complete molecular remission after nilotinib and graft-versus-leukemia effect in an acute lymphoblastic leukemia patient with cytogenetic relapse after allogeneic stem cell transplantation. Exp Hematol Oncol 2012, 1:29.
81. Nagafuji K, Miyamoto T, Eto T, Kamimura T, Taniguchi S, Okamura T, Ohtsuka E, Yoshida T, Higuchi M, Yoshimoto G, Fujisaki T, Abe Y, Takamatsu Y, Yokota S, Akashi K, Harada M: Monitoring of minimal residual disease (MRD) is useful to predict prognosis of adult patients with Ph-negative ALL: Results of a prospective study (ALL MRD2002 Study). J Hematol Oncol 2013, 6:14.
82. Walker CJ, Oaks JJ, Santhanam R, Neviani P, Harb JG, Ferenchak G, Ellis JJ, Landesman Y, Eisfeld AK, Gabrail NY, Smith CL, Caligiuri MA, Hokland P, Roy DC, Reid A, Milojkovic D, Goldman JM, Apperley J, Garzon R, Marcucci G, Shacham S, Kauffman MG, Perrotti D: Preclinical and clinical efficacy of XPO1/CRM1 inhibition by the karyopherin inhibitor KPT-330 in Ph + leukemias. Blood 2013, 122:3034-3044.
83. Yee KWL, Savona M, Sorensen M, Brown P, Blum WG, DeAngelo DJ, Gutierrez M, Garzon R, Schuh AC, Gabrail NY, Wadleigh M, Lancet JE, Shah BD, Berdeja JG, Wagner-Johnston ND, Flinn I, Rashal T, Kauffman M, Shacham S, Stone RM: A phase 1 dose-escalation study of the oral selective inhibitor of nuclear export (SINE) KPT-330 (selinexor) in patients (pts) with relapsed/refractory acute myeloid leukemia (AML). ASCO Meeting Abstracts 2014, 32:7032.
84. Akinleye A, Avvaru P, Furqan M, Song Y, Liu D: Phosphatidylinositol 3-kinase (PI3K) inhibitors as cancer therapeutics. J Hematol Oncol 2013, 6:88.
85. Akinleye A, Chen Y, Mukhi N, Song Y, Liu D: Ibrutinib and novel BTK inhibitors in clinical development. J Hematol Oncol 2013, 6:59.
86. Lu K, Wang X: Therapeutic advancement of chronic lymphocytic leukemia. J Hematol Oncol 2012, 5:55.
87. Wu M, Akinleye A, Zhu X: Novel agents for chronic lymphocytic leukemia. J Hematol Oncol 2013, 6:36.
88. Cang S, Mukhi N, Wang K, Liu D: Novel CD20 monoclonal antibodies for lymphoma therapy. J Hematol Oncol 2012, 5:64.
89. Wang K, Wei G, Liu D: CD19: A biomarker for B cell development, lymphoma diagnosis and therapy. Exp Hematol Oncol 2012, 1:36.
90. Han E, Li X-L, Wang C-R, Li T-F, Han S-Y: Chimeric antigen receptorengineered T cells for cancer immunotherapy: progress and challenges. J Hematol Oncol 2013, 6:47.
91. Chen Y, Liu D: Chimeric antigen receptor (CAR)-directed adoptive immunotherapy: A new era in targeted cancer therapy. Stem Cell Invest 2014, 1:2.
92. Furman RR, Asgary Z, Mascarenhas JO, Liou HC, Schattner EJ: Modulation of NF-kappa B activity and apoptosis in chronic lymphocytic leukemia B cells. J Immunol 2000, 164:2200-2206.
93. Reed JC, Pellecchia M: Apoptosis-based therapies for hematologic malignancies. Blood 2005, 106:408-418.
94. Schmidt J, Braggio E, Kortuem KM, Egan JB, Zhu YX, Xin CS, Tiedemann RE, Palmer SE, Garbitt VM, McCauley D, Kauffman M, Shacham S, Chesi M, Bergsagel PL, Stewart AK: Genome-wide studies in multiple myeloma identify XPO1/CRM1 as a critical target validated using the selective nuclear export inhibitor KPT-276. Leukemia 2013, 27:2357-2365.
95. Grinberg AV, Hu CD, Kerppola TK: Visualization of Myc/Max/Mad family dimers and the competition for dimerization in living cells. Mol Cell Biol 2004, 24:4294-4308.
96. Chng WJ, Huang GF, Chung TH, Ng SB, Gonzalez-Paz N, Troska-Price T, Mulligan G, Chesi M, Bergsagel PL, Fonseca R: Clinical and biological implications of MYC activation: A common difference between MGUS and newly diagnosed multiple myeloma. Leukemia 2011, 25:1026-1035.
97. Golomb L, Bublik DR, Wilder S, Nevo R, Kiss V, Grabusic K, Volarevic S, Oren M: Importin 7 and exportin 1 link c-Myc and p53 to regulation of ribosomal biogenesis. Mol Cell 2012, 45:222-232.
98. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J, Jacobs HM, Kastritis E, Gilpatrick T, Paranal RM, Qi J, Hesi M, Schinzel AC, McKeown MR, Heffernan TP, Vakoc CR, Bergsagel PL, Ghobrial IM, Richardson PG, Young RA, Hahn WC, Anderson KC, Kung AL, Bradner JE, Mitsiades CS: BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011, 146:904-917.
99. Mochizuki K, Nishiyama A, Jang MK, Dey A, Ghosh A, Tamura T, Natsume H, Yao H, Ozato K: The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase. J Biol Chem 2008, 283:9040-9048.
100. Fang X, Zhou X, Wang X: Clinical development of phosphatidylinositol 3-kinase inhibitors for non-Hodgkin lymphoma. Biomarker Res 2013, 1:30.
101. Novero A, Ravella P, Chen Y, Dous G, Liu D: Ibrutinib for B cell malignancies. Exp Hematol Oncol 2014, 3:4.
102. Zhao X, Zhang W, Wang L, Zhao W-L: Genetic methylation and lymphoid malignancies: Biomarkers of tumor progression and targeted therapy. Biomarker Res 2013, 1:24.
103. Fischer K, Cramer P, Busch R, Stilgenbauer S, Bahlo J, Schweighofer CD, Bottcher S, Staib P, Kiehl M, Eckart MJ, Kranz G, Goede V, Elter T, Buhler A, Winkler D, Kneba M, Dohner H, Eichhorst BF, Hallek M, Wendtner CM: Bendamustine combined with rituximab in patients with relapsed and/or refractory chronic lymphocytic leukemia: A multicenter phase II trial of the German Chronic Lymphocytic Leukemia Study Group. J Clin Oncol 2011, 29:3559-3566.
104. Wierda WG, Padmanabhan S, Chan GW, Gupta IV, Lisby S, Osterborg A: Ofatumumab is active in patients with fludarabine-refractory CLL irrespective of prior rituximab: Results from the phase 2 international study. Blood 2011, 118:5126-5129.
105. Yoshimura M, Ishizawa J, Ruvolo V, Dilip A, Quintás-Cardama A, McDonnell TJ, Neelapu SS, Kwak LW, Shacham S, Kauffman M, Tabe Y, Yokoo M, Kimura S, Andreeff M, Kojima K: Induction of p53-mediated transcription and apoptosis by exportin-1 (XPO1) inhibition in mantle cell lymphoma. Cancer Sci 2014, 105(7):795-801.
106. Zhang K, Wang M, Tamayo AT, Shacham S, Kauffman M, Lee J, Zhang L, Ou Z, Li C, Sun L, Ford RJ, Pham LV: Novel selective inhibitors of nuclear export CRM1 antagonists for therapy in mantle cell lymphoma. Exp Hematol 2013, 41:67-78. e64.
107. London CA, Bernabe LF, Barnard S, Kisseberth WC, Borgatti A, Henson M, Wilson H, Jensen K, Ito D, Modiano JF, Bear MD, Pennell ML, Saint-Martin JR, McCauley D, Kauffman M, Shacham S: 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 2014, 9:e87585.
108. Gutierrez M, Goy A, Byrd JC, Flynn JM, Sorensen M, Brown P, Gabrail NY, Savona M, Flinn I, Baz RC, Shah BD, Stone RM, Jacobsen E, Kukreti V, Tiedemann RE, Rashal T, Mirza MR, Shacham S, Kauffman M, Kuruvilla J: A phase 1 dose-escalation study of the oral selective inhibitor of nuclear export (SINE) KPT-330 (selinexor) in patients (pts) with heavily pretreated non-Hodgkin lymphoma (NHL). ASCO Meeting Abstracts 2014, 32:8518.
109. Wei SZL, Efferth T: Polo-like kinase 1 as target for cancer therapy. Exp Hematol Oncol 2012, 1:38.
110. Wang ML, Rule S, Martin P, Goy A, Auer R, Kahl BS, Jurczak W, Advani RH, Romaguera JE, Williams ME, Barrientos JC, Chmielowska E, Radford J, Stilgenbauer S, Dreyling M, Jedrzejczak WW, Johnson P, Spurgeon SE, Li L, Zhang L, Newberry K, Ou Z, Cheng N, Fang B, McGreivy J, Clow F, Buggy JJ, Chang BY, Beaupre DM, Kunkel LA, et al: Targeting BTK with ibrutinib in relapsed or refractory mantle-cell lymphoma. N Engl J Med 2013, 369:507-516.
111. Wiestner A: Targeting B-Cell receptor signaling for anticancer therapy: The Bruton's tyrosine kinase inhibitor ibrutinib induces impressive responses in B-cell malignancies. J Clin Oncol 2013, 31:128-130.
112. Woyach JA, Johnson AJ, Byrd JC: The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood 2012, 120:1175-1184.
113. Zucca E, Bertoni F: Toward new treatments for mantle-cell lymphoma? N Engl J Med 2013, 369:571-572.
114. Gerecitano J: SINE (selective inhibitor of nuclear export) -Translational science in a new class of anti-cancer agents. J Hematol Oncol 2014, 7:67.
115. Gravina G, Tortoreto M, Mancini A, Addis A, Di Cesare E, Lenzi A, Landesman Y, McCauley D, Kauffman M, Shacham S, Zaffaroni N, Festuccia C: XPO1/CRM1- Selective Inhibitors of Nuclear Export (SINE) reduce tumor spreading and improve overall survival in preclinical models of prostate cancer (PCa). J Hematol Oncol 2014, 7:46.