Aurora A and B kinases as targets for cancer: Will they be selective for tumors?

Expert Review of Anticancer Therapy

Volumn 6, Issue 1, 2006, Pages 109-120

  Matthews, Nick ^a   Visintin, Cristina ^b   Hartzoulakis, Basil ^c   Jarvis, Ashley ^c   Selwood, David L ^b  

^a Inploid Ltd   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c NCE Discovery Ltd   (United Kingdom)

Author keywords

Aurora A kinase; Aurora B kinase; Clinical status; Inhibitors; Mutations; Resistance

Indexed keywords

2,4 DIMETHYL 5 (2 OXO 1H INDOL 3 YLMETHYLENE) 3 PYRROLEPROPIONIC ACID; ANTINEOPLASTIC AGENT; AT 9283; AURORA A KINASE; AURORA B KINASE; AURORA C KINASE; AURORA KINASE INHIBITOR; AZD 1152; BIBI 1489; HESPERADIN; IMATINIB; LY 2181308; MLN 8054; MP 235; MP 529; N [4 [6 METHOXY 7 (3 MORPHOLINOPROPOXY) 4 QUINAZOLINYLAMINO]PHENYL]BENZAMIDE; PACLITAXEL; PHA 680632; PHA 739 358; PHA 739358; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; R 763; SNS 314; UNCLASSIFIED DRUG; VX 680; AURORA KINASE; ENZYME INHIBITOR; LIGAND;

ANTINEOPLASTIC ACTIVITY; BONE MARROW SUPPRESSION; BONE MARROW TOXICITY; CANCER INHIBITION; CANCER RESISTANCE; CENTROSOME; CHRONIC MYELOID LEUKEMIA; CLINICAL TRIAL; CYTOKINESIS; DRUG BIOAVAILABILITY; DRUG CYTOTOXICITY; DRUG PROTEIN BINDING; DRUG SCREENING; DRUG SELECTIVITY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; ENZYME STRUCTURE; GENE EXPRESSION; HUMAN; LIGAND BINDING; MITOSIS; NONHUMAN; ONCOGENE; PHYSICAL CHEMISTRY; REVIEW; SEQUENCE ALIGNMENT; STRUCTURE ACTIVITY RELATION; TUMOR XENOGRAFT; CELL CYCLE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; DRUG RESISTANCE; ENZYMOLOGY; METABOLISM; NEOPLASM; PHYSIOLOGY;

ANTINEOPLASTIC AGENTS; CELL CYCLE; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; HUMANS; LIGANDS; MOLECULAR STRUCTURE; NEOPLASMS; PROTEIN-SERINE-THREONINE KINASES;

EID: 85047694628     PISSN: 14737140     EISSN: 17448328     Source Type: Journal    
DOI: 10.1586/14737140.6.1.109     Document Type: Review

References (72)

1. Brown JR, Koretke KK, Birkeland ML et al. Evolutionary relationships of Aurora kinases: implications for model organism studies and the development of anticancer drugs. BMC Evol. Biol. 4(1), 39 (2004).
2. Giet R, Prigent C. Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases. J. Cell Sci. 112(Pt.21), 3591-3601 (1999).
3. Hu HM, Chuang CK, Lee MJ et al. Genomic organization, expression, and chromosome localization of a third Aurora-related kinase gene, Aiel. DNA Cell Biol. 19(11), 679-688 (2000).
4. Manning G, Whyte DB, Martinez R et al. The protein kinase complement of the human genome. Science 298(5600), 1912-1934 (2002).
5. Vankayalapati H, Bearss DJ, Saldanha JW et al. Targeting Aurora 2 kinase in oncogenesis: a structural bioinformatics approach to target validation and rational drug design. Mol. Cancer Ther. 2(3), 283-294 (2003).
6. Cheetham GM, Knegtel RM, Coll JT et al. Crystal structure of Aurora-2, an oncogenic serine/threonine kinase. J. Biol. Chem. 277(45), 42419-42422 (2002).
7. Carmena M, Earnshaw WC. The cellular geography of Aurora kinases. Nature Rev. Mol. Cell Biol. 4(11), 842-854 (2003).
8. Kufer TA, Nigg EA, Sillje HH. Regulation of Aurora-A kinase on the mitotic spindle. Chromosoma 112(4), 159-163 (2003).
9. Terada Y, Uetake Y, Kuriyama R. Interaction of Aurora-A and centrosomin at the microtubule-nucleating site in Drosophila and mammalian cells. J. Cell Biol. 162(5), 757-763 (2003).
10. Hirota T, Kunitoku N, Sasayama T et al. Aurora-A and an interacting activator, the LIM protein Ajuba, are required for mitotic commitment in human cells. Cell 114(5), 585-598 (2003).
11. Katayama H, Zhou H, Li Q et al. Interaction and feedback regulation between STK15/BTAK/Aurora-A kinase and protein phosphatase 1 through mitotic cell division cycle. J. Biol. Chem. 276(49), 46219-46224 (2001).
12. Liu Q, Kaneko S, Yang L et al. Aurora-A abrogation of p53 DNA binding and transactivation activity by phosphorylation of serine 215. J. Biol. Chem. 279(50), 52175-52182 (2004).
13. Sakai H, Urano T, Ookata K et al. MBD3 and HDAC1, two components of the NURD complex, are localized at Aurora-A-positive centrosomes in M phase. J. Biol. Chem. 277(50), 48714-48723 (2002).
14. Ouchi M, Fujiuchi N, Sasai K et al. BRCA1 phosphorylation by Aurora-A in the regulation of G2 to M transition. J. Biol. Chem. 279(19), 19643-19648 (2004).
15. Marumoto T, Honda S, Hara T et al. Aurora-A kinase maintains the fidelity of early and late mitotic events in HeLa cells. J. Biol. Chem. 278(51), 51786-51795 (2003).
16. Honda R, Korner R, Nigg EA. Exploring the functional interactions between Aurora B, INCENP, and survivin in mitosis. Mol. Biol. Cell 14(8), 3325-3341 (2003).
17. Walter AO, Seghezzi W, Korver W et al. The mitotic serine/threonine kinase Aurora2/AIK is regulated by phosphorylation and degradation. Oncogene 19(42), 4906-4916 (2000).
18. Adams RR, Carmena M, Earnshaw WC. Chromosomal passengers and the (Aurora) ABCs of mitosis. Trends Cell Biol. 11(2), 49-54 (2001).
19. Bolton MA, Lan W, Powers SE et al. Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol. Biol. Cell 13(9), 3064-3077 (2002).
20. Chen J, Jin S, Tahir SK et al. Survivin enhances Aurora-B kinase activity and localizes Aurora-B in human cells. J. Biol. Chem. 278(1), 486-490 (2003).
21. Gassmann R, Carvalho A, Henzing AJ et al. Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle. J. Cell Biol. 166(2), 179-191 (2004).
22. Morrison C, Henzing AJ, Jensen ON et al. Proteomic analysis of human metaphase chromosomes reveals topoisomerase II alpha as an Aurora B substrate. Nucleic Acids Res. 30(23), 5318-5327 (2002).
23. Goto H, Yasui Y, Kawajiri A et al. Aurora-B regulates the cleavage furrow-specific vimentin phosphorylation in the cytokinetic process. J. Biol. Chem. 278(10), 8526-8530 (2003).
24. Shu F, Guo S, Dang Y et al. Human aurora-B binds to a proteasome α-subunit HC8 and undergoes degradation in a proteasome-dependent manner. Mol. Cell Biochem. 254(1-2), 157-162 (2003).
25. Ditchfield C, Johnson VL, Tighe A et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 161(2), 267-280 (2003).
26. Hauf S, Cole RW, LaTerra S et al. The small molecule Hesperadin reveals a role for Aurora B in correcting kinetochore-microtubule attachment and in maintaining the spindle assembly checkpoint. J. Cell Biol. 161(2), 281-294 (2003).
27. Bernard M, Sanseau P, Henry C et al. Cloning of STK13, a third human protein kinase related to Drosophila Aurora and budding yeast Ipl1 that maps on chromosome 19q13.3-ter. Genomics 53(3), 406-409 (1998).
28. Tseng TC, Chen SH, Hsu YP et al. Protein kinase profile of sperm and eggs: cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol. 17(10), 823-833 (1998).
29. Kimura M, Matsuda Y, Yoshioka T et al. Cell cycle-dependent expression and centrosome localization of a third human aurora/Ipl1-related protein kinase, AIK3. J. Biol. Chem. 274(11), 7334-7340 (1999).
30. Sasai K, Katayama H, Stenoien DL et al. Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil. Cytoskeleton 59(4), 249-263 (2004).
31. Sen S, Zhou H, White RA. A putative serine/threonine kinase encoding gene BTAK on chromosome 20q13 is amplified and overexpressed in human breast cancer cell lines. Oncogene 14(18), 2195-2200 (1997).
32. Bischoff JR, Anderson L, Zhu Y et al. A homologue of Drosophila Aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17(11), 3052-3065 (1998).
33. Rojanala S, Han H, Munoz RM et al. The mitotic serine threonine kinase, Aurora-2, is a potential target for drug development in human pancreatic cancer. Mol. Cancer Ther. 3(4), 451-457 (2004).
34. Li D, Zhu J, Firozi PF et al. Overexpression of oncogenic STK15/BTAK/Aurora A kinase in human pancreatic cancer. Clin. Cancer Res. 9(3), 991-997 (2003).
35. Jeng YM, Peng SY, Lin CY et al. Overexpression and amplification of Aurora-A in hepatocellular carcinoma. Clin. Cancer Res. 10(6), 2065-2071 (2004).
36. Hoque A, Carter J, Yia W et al. Loss of Aurora A/STK15/BTAK overexpression correlates with transition of in situ to invasive ductal carcinoma of the breast. Cancer Epidemiol. Biomarkers Prev. 12(12), 1518-1522 (2003).
37. Moreno-Bueno G, Sanchez-Estevez C, Cassia R et al. Differential gene expression profile in endometrioid and nonendometrioid endometrial carcinoma: STK15 is frequently overexpressed and amplified in nonendometrioid carcinomas. Cancer Res. 63(18), 5697-5702 (2003).
38. Gritsko TM, Coppola D, Paciga JE et al. Activation and overexpression of centrosome kinase BTAK/Aurora-A in human ovarian cancer. Clin. Cancer Res. 9(4), 1420-1426 (2003).
39. Reichardt W, Jung V, Brunner C et al. The putative serine/threonine kinase gene STK15 on chromosome 20q13.2 is amplified in human gliomas. Oncol. Rep. 10(5), 1275-1279 (2003).
40. Hamada M, Yakushijin Y, Ohtsuka M et al. Aurora2/BTAK/STK15 is involved in cell cycle checkpoint and cell survival of aggressive non-Hodgkin's lymphoma. Br. J. Haematol. 121(3), 439-447 (2003).
41. Littlepage LE, Wu H, Andresson T et al. Identification of phosphorylated residues that affect the activity of the mitotic kinase Aurora-A. Proc. Natl Acad. Sci. USA 99(24), 15440-15445 (2002).
42. Anand S, Penrhyn-Lowe S, Venkitaraman AR. AURORA-A amplification overrides the mitotic spindle assembly checkpoint, inducing resistance to Taxol. Cancer Cell 3(1), 51-62 (2003).
43. Adams RR, Eckley DM, Vagnarelli P et al. Human INCENP colocalizes with the Aurora-B/AIRK2 kinase on chromosomes and is overexpressed in tumor cells. Chromosoma 110(2), 65-74 (2001).
44. Ota T, Suto S, Katayama H et al. Increased mitotic phosphorylation of histone H3 attributable to AIM-1/Aurora-B overexpression contributes to chromosome number instability. Cancer Res. 62(18), 5168-5177 (2002).
45. Araki K, Nozaki K, Ueba T et al. High expression of Aurora-B/Aurora and Ipl1-like midbody-associated protein (AIM-1) in astrocytomas. J. Neurooncol. 67(1-2), 53-(A (2004).
46. Sorrentino R, Libertini S, Pallante PL et al. Aurora B overexpression associates with the thyroid carcinoma undifferentiated phenotype and is required for thyroid carcinoma cell proliferation. J. Clin. Endocrinol. Metab. 90(2), 928-935 (2005).
47. Chieffi P, Troncone G, Caleo A et al. Aurora B expression in normal testis and seminomas. J. Endocrinol. 181(2), 263-270 (2004).
48. Katayama H, Ota T, Jisaki F et al. Mitotic kinase expression and colorectal cancer progression. J. Natl Cancer Inst. 91(13), 1160-1162 (1999).
49. Altieri DC. Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 22(53), 8581-8589 (2003).
50. Takahashi T, Futamura M, Yoshimi N et al. Centrosomal kinases, HsAIRK1 and HsAIRK3, are overexpressed in primary colorectal cancers. Jpn. J. Cancer Res. 91(10), 1007-1014 (2000).
51. Mahadevan D, Bearss DJ, Vankayalapati H. Structure-based design of novel anticancer agents targeting Aurora kinases. Curr. Med. Chem. Anti-Canc. Agents 3(1), 25-34 (2003).
52. Mortlock AA, Keen NJ, Jung FH et al. Progress in the development of selective inhibitors of aurora kinases. Curr. Top. Med. Chem. 5(8), 807-821 (2005).
53. Sessa F, Mapelli M, Ciferri C et al. Mechanism of Aurora B activation by INCENP and inhibition by hesperadin. Mol. Cell 18(3), 379-391 (2005).
54. Wang Z, Canagarajah BJ, Boehm JC et al. Structural basis of inhibitor selectivity in MAPKs. Structure 6(9), 1117-1128 (1998).
55. Blencke S, Zech B, Engkvist O et al. Characterization of a conserved structural determinant controlling protein kinase sensitivity to selective inhibitors. Chem. Biol. 11(5), 691-701 (2004).
56. Knight ZA, Shokat KM. Features of selective kinase inhibitors. Chem. Biol. 12(6), 621-637 (2005).
57. Burgess MR, Skaggs BJ, Shah NP et al. Comparative analysis of two clinically active BCR-ABL kinase inhibitors reveals the role of conformation-specific binding in resistance. Proc. Natl. Acad. Sci. USA 102(9), 3395-3400 (2005).
58. Daub H, Specht K, Ullrich A. Strategies to overcome resistance to targeted protein kinase inhibitors. Nature Rev. Drug Discov. 3(12), 1001-1010 (2004).
59. Keen N, Taylor S. Aurora-kinase inhibitors as anticancer agents. Nature Rev. Cancer 4(12), 927-936 (2004).
60. Margolis RL, Lohez OD, Andreassen PR. G1 tetraploidy checkpoint and the suppression of tumorigenesis. J. Cell Biochem. 88(4), 673-683 (2003).
61. Andreassen PR, Lohez OD, Lacroix FB et al. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol. Biol. Cell 12(5), 1315-1328 (2001).
62. Lohez OD, Reynaud C, Borel F et al. Arrest of mammalian fibroblasts in G1 in response to actin inhibition is dependent on retinoblastoma pocket proteins but not on p53. J. Cell Biol. 161(1), 67-77 (2003).
63. Yang H, Burke T, Dempsey J et al. Mitotic requirement for Aurora A kinase is bypassed in the absence of Aurora B kinase. FEBS Lett. 579(16), 3385-3391 (2005).
64. Hata T, Furukawa T, Sunamura M et al. RNA interference targeting Aurora kinase A suppresses tumor growth and enhances the taxane chemosensitivity in human pancreatic cancer cells. Cancer Res. 65(7), 2899-2905 (2005).
65. Harrington EA, Bebbington D, Moore J et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nature Med. 10(3), 262-267 (2004).
66. Fancelli D, Berta D, Bindi S et al. Potent and selective Aurora inhibitors identified by the expansion of a novel scaffold for protein kinase inhibition. J. Med. Chem. 48(8), 3080-3084 (2005).
67. Lipinski CA, Lombardo F, Dominy BW et al. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46(1-3), 3-26 (2001).
68. Veber DF, Johnson SR, Cheng HY et al. Molecular properties that influence the oral bioavailability of drug candidates. J. Med. Chem. 45 (12), 2615-2623 (2002).
69. Vassilev LT, Vu BT, Graves B et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303(5659), 844-848 (2004).
70. Nowakowski J, Cronin CN, McRee DE et al. Structures of the cancer-related Aurora-A, FAK, and EphA2 protein kinases from nanovolume crystallography. Structure 10(12), 1659-1667 (2002).
71. Bayliss R, Sardon T, Vernos I et al. Structural basis of Aurora-A activation by TPX2 at the mitotic spindle. Mol. Cell 12(4), 851-862 (2003).
72. Wallace AC, Laskowski RA, Thornton JM. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Engl. 8(2), 127-134 (1995).