Antitumor activity of a small-molecule inhibitor of the histone kinase Haspin

Oncogene

Volumn 31, Issue 11, 2012, Pages 1408-1418

  Huertas, D ^a   Soler, M ^a   Moreto, J ^a   Villanueva, A ^a   Martinez, A ^b   Vidal, A ^c   Charlton, M ^d   Moffat, D ^d   Patel, S ^d   McDermott, J ^d   Owen, J ^d   Brotherton, D ^d   Krige, D ^d   Cuthill, S ^d   Esteller, M ^a,e,f  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b CENTER FOR BIOMEDICAL RESEARCH OF LA RIOJA CIBIR   (Spain)

^c HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^d Chroma Therapeutics   (United Kingdom)

^e UNIVERSITY OF BARCELONA   (Spain)

^f INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

epigenetics; histone; inhibitor

Indexed keywords

ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; AURORA KINASE INHIBITOR; CHR 6494; HISTONE H3; PROTEIN HASPIN; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; THREONINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL EXPANSION; CELL STRAIN 3T3; CENTROSOME; CONTROLLED STUDY; DOSE RESPONSE; EX VIVO STUDY; HIGH THROUGHPUT SCREENING; HIGH THROUGHPUT SEQUENCING; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IC 50; IN VIVO STUDY; MALE; METAPHASE; METAPHASE CHROMOSOME; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPINDLE CELL; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; HISTONES; HUMANS; INDAZOLES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, NUDE; MITOSIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PYRIDAZINES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS MUSCULUS;

EID: 84858333989     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.335     Document Type: Article

References (48)

1. Berdasco M, Esteller M. (2010). Aberrant epigenetic landscape in cancer: How cellular identity goes awry. Dev Cell 19: 698-711.
2. Bryan J, Jabbour E, Prescott H, Garcia-Manero G, Issa JP, Kantarjian H. (2010). Current and future management options for myelodysplastic syndromes. Drugs 70: 1381-1394.
3. Carpinelli P, Moll J. (2008). Aurora kinases and their inhibitors: More than one target and one drug. Adv Exp Med Biol 610: 54-73.
4. Cheng A, Balczon R, Zuo Z, Koons JS, Walsh AH, Honkanen RE. (1998). Fostriecin-mediated G2-M-phase growth arrest correlates with abnormal centrosome replication, the formation of aberrant mitotic spindles, and the inhibition of serine/threonine protein phosphatase activity. Cancer Res 58: 3611-3619.
5. Chopra P, Sethi G, Dastidar SG, Ray A. (2010). Polo-like kinase inhibitors: An emerging opportunity for cancer therapeutics. Expert Opin Investig Drugs 19: 27-43.
6. Cuny GD, Robin M, Ulyanova NP, Patnaik D, Pique V, Casano G et al. (2010). Structure-Activity relationship study of acridine analogs as haspin and DYRK2 kinase inhibitors. Bioorg Med Chem Lett 20: 3491-3494.
7. Dai J, Sultan S, Taylor SS, Higgins JM. (2005). The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev 19: 472-488.
8. Dai J, Kateneva AV, Higgins JM. (2009). Studies of haspin-depleted cells reveal that spindle-pole integrity in mitosis requires chromosome cohesion. J Cell Sci 122: 4168-4176.
9. Dai J, Sullivan BA, Higgins JM. (2006). Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev Cell 11: 741-750.
10. Dar AA, Goff LW, Majid S, Berlin J, El-Rifai W. (2010). Aurora kinase inhibitors-rising stars in cancer therapeutics? Mol Cancer Ther 9: 268-278.
11. Dave SS, Fu K, Wright GW, Lam LT, Kluin P, Boerma EJ et al. (2006). Lymphoma/leukemia molecular profiling project. Molecular diagnosis of Burkitt0s lymphoma. N Engl J Med 354: 2431-2442.
12. D'Alise AM, Amabile G, Iovino M, Di Giorgio FP, Bartiromo M, Sessa F et al. (2008). Reversine, a novel Aurora kinases inhibitor, inhibits colony formation of human acute myeloid leukemia cells. Mol Cancer Ther 7: 1140-1149.
13. Eswaran J, Patnaik D, Filippakopoulos P, Wang F, Stein RL, Murray JW et al. (2009). Structure and functional characterization of the atypical human kinase haspin. Proc Natl Acad Sci USA 106: 20198-20203.
14. Folkman J. (2007). Angiogenesis: An organizing principle for drug discovery? Nat Rev Drug Discov 6: 273-286.
15. Girdler F, Gascoigne KE, Eyers PA, Hartmuth S, Crafter C, Foote KM et al. (2006). Validating Aurora B as an anti-cancer drug target. J Cell Sci 119: 3664-3675.
16. Gleixner KV, Ferenc V, Peter B, Gruze A, Meyer RA, Hadzijusufovic E et al. (2010). Polo-like kinase 1 (Plk1) as a novel drug target in chronic myeloid leukemia: Overriding imatinib resistance with the Plk1 inhibitor BI 2536. Cancer Res 70: 1513-1523.
17. Götze K, Platzbecker U, Giagounidis A, Haase D, Lübbert M, Aul C et al. (2010). Azacitidine for treatment of patients with myelodysplastic syndromes (MDS): Practical recommendations of the German MDS Study Group. Ann Hematol, 89: 841-850.
18. Graham JS, Kaye SB, Brown R. (2009). The promises and pitfalls of epigenetic therapies in solid tumours. Eur J Cancer 45: 1129-1136.
19. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose- Adeogun AO, Nakayama T et al. (2004). VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 10: 262-267.
20. Higgins JM. (2001). Haspin-like proteins: A new family of evolutionarily conserved putative eukaryotic protein kinases. Protein Sci 10: 1677-1684.
21. Johnson EF, Stewart KD, Woods KW, Giranda VL, Luo Y. (2007). Pharmacological and functional comparison of the polo-like kinase family: Insight into inhibitor and substrate specificity. Biochemistry 46: 9551-9563.
22. Jones PA, Baylin SB. (2007). The epigenomics of cancer. Cell 128: 683-692.
23. Kelly AE, Ghenoiu C, Xue JZ, Zierhut C, Kimura H, Funabiki H. (2010). Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330: 235-239.
24. Kim MS, Kwon HJ, Lee YM, Baek JH, Jang JE, Lee SW et al. (2001). Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 7: 437-443.
25. Kouzarides T. (2007). Chromatin modifications and their function. Cell 128: 693-705.
26. Lane AA, Chabner BA. (2009). Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 27: 5459-5468.
27. Malumbres M, Pevarello P, Barbacid M, Bischoff JR. (2008). CDK inhibitors in cancer therapy: What is next? Trends Pharmacol Sci 29: 16-21.
28. Macurek L, Lindqvist A, Medema RH. (2009). Aurora-A and hBora join the game of Polo. Cancer Res 69: 4555-4558.
29. Marks PA. (2010). Histone deacetylase inhibitors: A chemical genetics approach to understanding cellular functions. Biochim Biophys Acta 1799: 717-725.
30. Martínez A, Zudaire E, Portal-Núñez S, Guédez L, Libutti SK, Stetler- Stevenson WG et al. (2004)Proadrenomedullin N-terminal 20 peptide is a potent angiogenic factor and its inhibition results in reduction of tumor growth. Cancer Res 64: 6489-6494.
31. Ma X, Ezzeldin HH, Diasio RB. (2009). Histone deacetylase inhibitors: Current status and overview of recent clinical trials. Drugs 69: 1911-1934.
32. Musacchio A, Salmon ED. (2007). The spindle-Assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8: 379-393.
33. Nakai R, Lida S, Takahashi T, Tsujita T, Okamoto S, Takada C et al. (2009). K858, a novel inhibitor of mitotic kinesin Eg5 and antitumor agent, induces cell death in cancer cells. Cancer Res 69: 3901-3909.
34. Nilsson J, Yekezare M, Minshull J, Pines J. (2008). The APC/C maintains the spindle assembly checkpoint by targeting Cdc20 for destruction. Nat Cell Biol 10: 1411-1420.
35. Oke A, Pearce D, Wilkinson RW, Crafter C, Odedra R, Cavenagh J et al. (2009). AZD1152 rapidly and negatively affects the growth and survival of human acute myeloid leukemia cells in vitro and in vivo. Cancer Res 69: 4150-4158.
36. Patnaik D, Jun Xian, Glicksman MA, Cuny GD, Stein RL, Higgins JM. (2008). Identification of small molecule inhibitors of the mitotic kinase haspin by high-throughput screening using a homogeneous time-resolved fluorescence resonance energy transfer assay. J Biomol Screen 13: 1025-1034.
37. Rebacz B, Larsen TO, Clausen MH, Rnnest MH, Löffler H, Ho AD et al. (2007). Identification of griseofulvin as an inhibitor of centrosomal clustering in a phenotype-based screen. Cancer Res 67: 6342-6350.
38. Rosasco-Nitcher SE, LanW, Khorasanizadeh S, Stukenberg PT. (2008). Centromeric Aurora-B activation requires TD-60, microtubules, and substrate priming phosphorylation. Science 319: 469-472.
39. Rosenwald A, Alizadeh AA, Widhopf G, Simon R, Davis RE, Yu X et al. (2001). Relation of gene expression phenotype to immunoglobulin mutation genotype in B cell chronic lymphocytic leukemia. J Exp Med 194: 1639-1647.
40. Stemmann O, Gorr IH, Boos D. (2006). Anaphase topsy-turvy: Cdk1 a securin, separase a CKI. Cell Cycle 5: 11-13.
41. Takeuchi T, Takahashi N, Ishi K, Kusayanagi T, Kuramochi K, Sugawara F. (2009). Antitumor antibiotic fostriecin covalently binds to cysteine-269 residue of protein phosphatase 2A catalytic subunit in mammalian cells. Bioorg Med Chem 17: 8113-8122.
42. Tao Y, Leteur C, Calderaro J, Girdler F, Zhang P, Frascogna V et al. (2009). The aurora B kinase inhibitor AZD1152 sensitizes cancer cells to fractionated irradiation and induces mitotic catastrophe. Cell Cycle 8: 3172-3181.
43. Thompson SL, Bakhoum SF, Compton DA. (2010). Mechanisms of chromosomal instability. Curr Biol 20: R285-R295.
44. Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H et al. (2006). Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci USA 103: 10660-10665.
45. Villa F, Capasso P, Tortorici M, Forneris F, de Marco A, Mattevi A et al. (2009). Crystal structure of the catalytic domain of Haspin, an atypical kinase implicated in chromatin organization. Proc Natl Acad Sci USA 106: 20204-20209.
46. Wang F, Dai J, Daum JR, Niedzialkowska E, Banerjee B, Stukenberg PT et al. (2010). Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330: 231-235.
47. Yamagishi Y, Honda T, Tanno Y, Watanabe Y. (2010). Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330: 239-243.
48. Zubia A, Ropero S, Otaegui D, Ballestar E, Fraga MF, Boix-Chornet M et al. (2009). Identification of (1H)-pyrroles as histone deacetylase inhibitors with antitumoral activity. Oncogene 28: 1477-1484.