Silvestrol exhibits significant in vivo and in vitro antileukemic activities and inhibits FLT3 and miR-155 expressions in acute myeloid leukemia

Journal of Hematology and Oncology

Volumn 6, Issue 1, 2013, Pages

  Alachkar, Houda ^a,c   Santhanam, Ramasamy ^a,c   Harb, Jason G ^b,c   Lucas, David M ^a,c   Oaks, Joshua J ^b,c   Hickey, Christopher J ^a,c   Pan, Li ^b   Kinghorn, A Douglas ^b   Caligiuri, Michael A ^a,c   Perrotti, Danilo ^b,c   Byrd, John C ^a,c   Garzon, Ramiro ^a,c   Grever, Michael R ^a,c,d   Marcucci, Guido ^a,c  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d North Doan Office Tower   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CD135 ANTIGEN; MESSENGER RNA; MICRORNA 155; NATURAL PRODUCT; SILVESTROL; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER SURVIVAL; CELL VIABILITY; COLONY FORMATION; COLORIMETRY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; IC 50; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS;

EID: 84874930771     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/1756-8722-6-21     Document Type: Article

References (45)

1. Acute myeloid leukaemia. Estey E, Dohner H, Lancet 2006 368 9550 1894 1907 10.1016/S0140-6736(06)69780-8 17126723
2. Downstream molecular pathways of FLT3 in the pathogenesis of acute myeloid leukemia: biology and therapeutic implications. Takahashi S, J Hematol Oncol 2011 4 13 10.1186/1756-8722-4-13 21453545
3. Structural and functional alterations of FLT3 in acute myeloid leukemia. Meshinchi S, Appelbaum FR, Clin Cancer Res 2009 15 13 4263 4269 10.1158/1078-0432.CCR-08-1123 19549778
4. FLT3 internal tandem duplication associates with adverse outcome and gene- and microRNA-expression signatures in patients 60 years of age or older with primary cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. Whitman SP, Maharry K, Radmacher MD, Becker H, Mrozek K, Margeson D, Holland KB, Wu YZ, Schwind S, Metzeler KH, Wen J, Baer MR, Powell BL, Carter TH, Kolitz JE, Wetzler M, Moore JO, Stone RM, Carroll AJ, Larson RA, Caligiuri MA, Marcucci G, Bloomfield CD, Blood 2010 116 18 3622 3626 10.1182/blood-2010-05-283648 20656931
5. FLT3 mutation and response to intensive chemotherapy in young adult and elderly patients with normal karyotype. Beran M, Luthra R, Kantarjian H, Estey E, Leuk Res 2004 28 6 547 550 10.1016/j.leukres.2003.09.016 15120929
6. Tyrosine kinases as targets for cancer therapy. Krause DS, Van Etten RA, N Engl J Med 2005 353 2 172 187 10.1056/NEJMra044389 16014887
7. Drug resistance in mutant FLT3-positive AML. Weisberg E, Sattler M, Ray A, Griffin JD, Oncogene 2010 29 37 5120 5134 10.1038/onc.2010.273 20622902
8. Low frequency and variability of FLT3 mutations in Korean patients with acute myeloid leukemia. Bang SM, Ahn JY, Park J, Park SH, Park J, Cho EK, Shin DB, Lee JH, Yoo SJ, Jeon IS, Kim YK, Kim HJ, Kim HN, Lee IK, Kang HJ, Shin HY, Ahn HS, J Korean Med Sci 2008 23 5 833 837 10.3346/jkms.2008.23.5.833 18955790
9. Biologic and clinical significance of the FLT3 transcript level in acute myeloid leukemia. Ozeki K, Kiyoi H, Hirose Y, Iwai M, Ninomiya M, Kodera Y, Miyawaki S, Kuriyama K, Shimazaki C, Akiyama H, Nishimura M, Motoji T, Shinagawa K, Takeshita A, Ueda R, Ohno R, Emi N, Naoe T, Blood 2004 103 5 1901 1908 10.1182/blood-2003-06-1845 14604973
10. FLT3 ligand causes autocrine signaling in acute myeloid leukemia cells. Zheng R, Levis M, Piloto O, Brown P, Baldwin BR, Gorin NC, Beran M, Zhu Z, Ludwig D, Hicklin D, Witte L, Li Y, Small D, Blood 2004 103 1 267 274 10.1182/blood-2003-06-1969 12969963
11. Validation of ITD mutations in FLT3 as a therapeutic target in human acute myeloid leukaemia. Smith CC, Wang Q, Chin CS, Salerno S, Damon LE, Levis MJ, Perl AE, Travers KJ, Wang S, Hunt JP, Zarrinkar PP, Schadt EE, Kasarskis A, Kuriyan J, Shah NP, Nature 2012 485 7397 260 263 10.1038/nature11016 22504184
12. SU11652 Inhibits tyrosine kinase activity of FLT3 and growth of MV-4-11 cells. Guo Y, Chen Y, Xu X, Fu X, Zhao ZJ, J Hematol Oncol 2012 5 72 10.1186/1756-8722-5-72 23216927
13. FLT3 as a therapeutic target in AML: still challenging after all these years. Kindler T, Lipka DB, Fischer T, Blood 2010 116 24 5089 5102 10.1182/blood-2010-04-261867 20705759
14. FLT3-mutant allelic burden and clinical status are predictive of response to FLT3 inhibitors in AML. Pratz KW, Sato T, Murphy KM, Stine A, Rajkhowa T, Levis M, Blood 2010 115 7 1425 1432 10.1182/blood-2009-09-242859 20007803
15. A pharmacodynamic study of the FLT3 inhibitor KW-2449 yields insight into the basis for clinical response. Pratz KW, Cortes J, Roboz GJ, Rao N, Arowojolu O, Stine A, Shiotsu Y, Shudo A, Akinaga S, Small D, Karp JE, Levis M, Blood 2009 113 17 3938 3946 10.1182/blood-2008-09-177030 19029442
16. Silvestrol and episilvestrol, potential anticancer rocaglate derivatives from Aglaia silvestris. Hwang BY, Su BN, Chai H, Mi Q, Kardono LB, Afriastini JJ, Riswan S, Santarsiero BD, Mesecar AD, Wild R, Fairchild CR, Vite GD, Rose WC, Farnsworth NR, Cordell GA, Pezzuto JM, Swanson SM, Kinghorn AD, J Org Chem 2004 69 10 3350 3358 10.1021/jo040120f 15132542
17. The relevance of higher plants in lead compound discovery programs. Kinghorn AD, Pan L, Fletcher JN, Chai H, J Nat Prod 2011 74 6 1539 1555 10.1021/np200391c 21650152
18. Silvestrol, a potential anticancer rocaglate derivative from Aglaia foveolata, induces apoptosis in LNCaP cells through the mitochondrial/apoptosome pathway without activation of executioner caspase-3 or -7. Kim S, Hwang BY, Su BN, Chai H, Mi Q, Kinghorn AD, Wild R, Swanson SM, Anticancer Res 2007 27 4B 2175 2183 17695501
19. Silvestrol regulates G2/M checkpoint genes independent of p53 activity. Mi Q, Kim S, Hwang BY, Su BN, Chai H, Arbieva ZH, Kinghorn AD, Swanson SM, Anticancer Res 2006 26 5A 3349 3356 17094452
20. Enantioselective synthesis of the complex rocaglate (-)-silvestrol. Gerard B, Cencic R, Pelletier J, Porco JA Jr, Angew Chem Int Ed Engl 2007 46 41 7831 7834 10.1002/anie.200702707 17806093
21. Therapeutic suppression of translation initiation modulates chemosensitivity in a mouse lymphoma model. Bordeleau ME, Robert F, Gerard B, Lindqvist L, Chen SM, Wendel HG, Brem B, Greger H, Lowe SW, Porco JA Jr, Pelletier J, J Clin Invest 2008 118 7 2651 2660 18551192
22. The novel plant-derived agent silvestrol has B-cell selective activity in chronic lymphocytic leukemia and acute lymphoblastic leukemia in vitro and in vivo. Lucas DM, Edwards RB, Lozanski G, West DA, Shin JD, Vargo MA, Davis ME, Rozewski DM, Johnson AJ, Su BN, Goettl VM, Heerema NA, Lin TS, Lehman A, Zhang X, Jarjoura D, Newman DJ, Byrd JC, Kinghorn AD, Grever MR, Blood 2009 113 19 4656 4666 10.1182/blood-2008-09-175430 19190247
23. Synergistic effect of inhibiting translation initiation in combination with cytotoxic agents in acute myelogenous leukemia cells. Cencic R, Carrier M, Trnkus A, Porco JA Jr, Minden M, Pelletier J, Leuk Res 2010 34 4 535 541 10.1016/j.leukres.2009.07.043 19726085
24. Antitumor activity and mechanism of action of the cyclopenta[b] benzofuran, silvestrol. Cencic R, Carrier M, Galicia-Vázquez G, Bordeleau ME, Sukarieh R, Bourdeau A, Brem B, Teodoro JG, Greger H, Tremblay ML, Porco JA Jr, Pelletier J, PLoS One 2009 4 4 5223 10.1371/journal.pone.0005223 19401772
25. Preclinical activity of a novel CRM1 inhibitor in acute myeloid leukemia. 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, Blood 2012 120 9 1765 1773 10.1182/blood-2012-04-423160 22677130
26. Characterization of silvestrol pharmacokinetics in mice using liquid chromatography-tandem mass spectrometry. Saradhi UV, Gupta SV, Chiu M, Wang J, Ling Y, Liu Z, Newman DJ, Covey JM, Kinghorn AD, Marcucci G, Lucas DM, Grever MR, Phelps MA, Chan KK, AAPS J 2011 13 3 347 356 10.1208/s12248-011-9273-x 21499689
27. MicroRNAs in normal and malignant hematopoiesis. Garzon R, Croce CM, Curr Opin Hematol 2008 15 4 352 358 10.1097/MOH.0b013e328303e15d 18536574
28. Loss of SHIP-1 protein expression in high-risk myelodysplastic syndromes is associated with miR-210 and miR-155. Lee DW, Futami M, Carroll M, Feng Y, Wang Z, Fernandez M, Whichard Z, Chen Y, Kornblau S, Shpall EJ, Bueso-Ramos CE, Corey SJ, Oncogene 2012 31 37 4085 4094 10.1038/onc.2011.579 22249254
29. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. O'Connell RM, Rao DS, Chaudhuri AA, Boldin MP, Taganov KD, Nicoll J, Paquette RL, Baltimore D, J Exp Med 2008 205 3 585 594 10.1084/jem.20072108 18299402
30. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Garzon R, Volinia S, Liu CG, Fernandez-Cymering C, Palumbo T, Pichiorri F, Fabbri M, Coombes K, Alder H, Nakamura T, Flomenberg N, Marcucci G, Calin GA, Kornblau SM, Kantarjian H, Bloomfield CD, Andreeff M, Croce CM, Blood 2008 111 6 3183 3189 10.1182/blood-2007-07-098749 18187662
31. MiR-424 and miR-155 deregulated expression in cytogenetically normal acute myeloid leukaemia: correlation with NPM1 and FLT3 mutation status. Faraoni I, Laterza S, Ardiri D, Ciardi C, Fazi F, Lo-Coco F, J Hematol Oncol 2012 5 26 10.1186/1756-8722-5-26 22681934
32. microRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Vigorito E, Perks KL, Abreu-Goodger C, Bunting S, Xiang Z, Kohlhaas S, Das PP, Miska EA, Rodriguez A, Bradley A, Smith KG, Rada C, Enright AJ, Toellner KM, Maclennan IC, Turner M, Immunity 2007 27 6 847 859 10.1016/j.immuni.2007.10.009 18055230
33. Flt3 receptor inhibition reduces constitutive NFkappaB activation in high-risk myelodysplastic syndrome and acute myeloid leukemia. Grosjean-Raillard J, Ades L, Boehrer S, Tailler M, Fabre C, Braun T, De Botton S, Israel A, Fenaux P, Kroemer G, Apoptosis 2008 13 9 1148 1161 10.1007/s10495-008-0243-4 18670883
34. Over-expression of Flt3 induces NF-kappaB pathway and increases the expression of IL-6. Takahashi S, Harigae H, Ishii KK, Inomata M, Fujiwara T, Yokoyama H, Ishizawa K, Kameoka J, Licht JD, Sasaki T, Kaku M, Leuk Res 2005 29 8 893 899 10.1016/j.leukres.2005.01.008 15978940
35. FLT3-ITD Signaling Induces Oncogenic Mir-155 by NF-κB and STAT5 Pathways In Acute Myeloid Leukemia Thereby Targeting Transcription Factor PU.1. Dennis Gerloff DB-H, Katzerke C, Hartmann J-U, Mueller-Tidow C, Tenen DG, Niederwieser D, Behre G, 53rd ASH Annual Meeting and Exposition San Diego, California 2011
36. Rocaglamide derivatives are potent inhibitors of NF-kappa B activation in T-cells. Baumann B, Bohnenstengel F, Siegmund D, Wajant H, Weber C, Herr I, Debatin KM, Proksch P, Wirth T, J Biol Chem 2002 277 47 44791 44800 10.1074/jbc.M208003200 12237314
37. Dual Targeting of the Cyclin/Rb/E2F and Mitochondrial Pathways in Mantle Cell Lymphoma with the Translation Inhibitor Silvestrol. Alinari L, Prince CJ, Edwards RB, Towns WH, Mani R, Lehman A, Zhang X, Jarjoura D, Pan L, Kinghorn AD, Grever MR, Baiocchi RA, Lucas DM, Clin Cancer Res 2012 18 17 4600 4611 10.1158/1078-0432.CCR-12-0839 22791882
38. The presence of a FLT3 internal tandem duplication in patients with acute myeloid leukemia (AML) adds important prognostic information to cytogenetic risk group and response to the first cycle of chemotherapy: analysis of 854 patients from the United Kingdom Medical Research Council AML 10 and 12 trials. Kottaridis PD, Gale RE, Frew ME, Harrison G, Langabeer SE, Belton AA, Walker H, Wheatley K, Bowen DT, Burnett AK, Goldstone AH, Linch DC, Blood 2001 98 6 1752 1759 10.1182/blood.V98.6.1752 11535508
39. Bench to bedside targeting of FLT3 in acute leukemia. Pratz KW, Levis MJ, Curr Drug Targets 2010 11 7 781 789 10.2174/138945010791320782 20370649
40. FLT3 inhibition and mechanisms of drug resistance in mutant FLT3-positive AML. Weisberg E, Barrett R, Liu Q, Stone R, Gray N, Griffin JD, Drug Resist Updat 2009 12 3 81 89 10.1016/j.drup.2009.04.001 19467916
41. RNAi-induced down-regulation of FLT3 expression in AML cell lines increases sensitivity to MLN518. Walters DK, Stoffregen EP, Heinrich MC, Deininger MW, Druker BJ, Blood 2005 105 7 2952 2954 10.1182/blood-2004-07-2758 15585651
42. NF-kappaB down-regulates expression of the B-lymphoma marker CD10 through a miR-155/PU.1 pathway. Thompson RC, Herscovitch M, Zhao I, Ford TJ, Gilmore TD, J Biol Chem 2011 286 3 1675 1682 10.1074/jbc.M110.177063 20947507
43. Nuclear factor-kappaB is constitutively activated in primitive human acute myelogenous leukemia cells. Guzman ML, Neering SJ, Upchurch D, Grimes B, Howard DS, Rizzieri DA, Luger SM, Jordan CT, Blood 2001 98 8 2301 2307 10.1182/blood.V98.8.2301 11588023
44. Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Garzon R, Garofalo M, Martelli MP, Briesewitz R, Wang L, Fernandez-Cymering C, Volinia S, Liu CG, Schnittger S, Haferlach T, Liso A, Diverio D, Mancini M, Meloni G, Foa R, Martelli MF, Mecucci C, Croce CM, Falini B, Proc Natl Acad Sci U S A 2008 105 10 3945 3950 10.1073/pnas. 0800135105 18308931
45. Inverse correlation between Flt3 and PU.1 expression in acute myeloblastic leukemias. Inomata M, Takahashi S, Harigae H, Kameoka J, Kaku M, Sasaki T, Leuk Res 2006 30 6 659 664 10.1016/j.leukres.2005.07.015 16271760