Tumour selective targeting of cell cycle kinases for cancer treatment

Current Opinion in Pharmacology

Volumn 13, Issue 4, 2013, Pages 529-535

  Aarts, Marieke ^a   Linardopoulos, Spiros ^a   Turner, Nicholas C ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALISERTIB; ANTINEOPLASTIC AGENT; AURORA A KINASE; AURORA A KINASE INHIBITOR; AURORA B KINASE; AURORA C KINASE; BARASERTIB; CYCLIN D1; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 1 INHIBITOR; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR; CYCLIN DEPENDENT KINASE INHIBITOR 2A; PALBOCICLIB; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOTRANSFERASE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN P53; PROTEIN WEE1; THYMIDINE KINASE INHIBITOR; UNCLASSIFIED DRUG; WEE1 INHIBITOR;

ACUTE GRANULOCYTIC LEUKEMIA; ANEUPLOIDY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER COMBINATION CHEMOTHERAPY; CANCER HORMONE THERAPY; CANCER SURVIVAL; CCND1 GENE; CDKN2A GENE; CELL CYCLE CHECKPOINT; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL PROLIFERATION; CHEMOSENSITIVITY; DRUG SYNTHESIS; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SPECIFICITY; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; G2 PHASE CELL CYCLE CHECKPOINT; HUMAN; M PHASE CELL CYCLE CHECKPOINT; MALIGNANT NEOPLASTIC DISEASE; MITOSIS; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; S PHASE CELL CYCLE CHECKPOINT; TUMOR SUPPRESSOR GENE;

EID: 84885958958     PISSN: 14714892     EISSN: 14714973     Source Type: Journal    
DOI: 10.1016/j.coph.2013.03.012     Document Type: Review

References (66)

1. Kastan MB, Bartek J: Cell-cycle checkpoints and cancer. Nature 2004, 432:316-323. (Pubitemid 39551659)
2. Le Tourneau C, Faivre S, Laurence V, Delbaldo C, Vera K, Girre V, Chiao J, Armour S, Frame S, Green SR, Gianella-Borradori A et al.: Phase I evaluation of seliciclib (R-roscovitine), a novel oral cyclin-dependent kinase inhibitor, in patients with advanced malignancies. Eur J Cancer 2010, 46:3243-3250.
3. Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL: Cyclin D as a therapeutic target in cancer. Nat Rev Cancer 2011, 11:558-572.
4. Malumbres M, Barbacid M: Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer 2009, 9:153-166.
5. Fry DW, Harvey PJ, Keller PR, Elliott WL, Meade M, Trachet E, Albassam M, Zheng X, Leopold WR, Pryer NK, Toogood PL: Specific inhibition of cyclin-dependent kinase 4/6 by PD 0332991 and associated antitumor activity in human tumor xenografts. Mol Cancer Ther 2004, 3:1427-1438.
6. Puyol M, Martin A, Dubus P, Mulero F, Pizcueta P, Khan G, Guerra C, Santamaria D, Barbacid M: A synthetic lethal interaction between K-Ras oncogenes and Cdk4 unveils a therapeutic strategy for non-small cell lung carcinoma. Cancer Cell 2010, 18:63-73.
7. Huillard E, Hashizume R, Phillips JJ, Griveau A, Ihrie RA, Aoki Y, Nicolaides T, Perry A, Waldman T, McMahon M, Weiss WA et al.: Cooperative interactions of BRAFV600E kinase and CDKN2A locus deficiency in pediatric malignant astrocytoma as a basis for rational therapy. Proc Natl Acad Sci U S A 2012, 109:8710-8715.
8. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, Speed D, Lynch AG, Samarajiwa S, Yuan Y, Graf S et al.: The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352.
9. Witkiewicz AK, Knudsen KE, Dicker AP, Knudsen ES: The meaning of p16(ink4a) expression in tumors: functional significance, clinical associations and future developments. Cell Cycle 2011, 10:2497-2503.
10. Wiedemeyer WR, Dunn IF, Quayle SN, Zhang J, Chheda MG, Dunn GP, Zhuang L, Rosenbluh J, Chen S, Xiao Y, Shapiro GI et al.: Pattern of retinoblastoma pathway inactivation dictates response to CDK4/6 inhibition in GBM. Proc Natl Acad Sci U S A 2010, 107:11501-11506.
11. Konecny GE, Winterhoff B, Kolarova T, Qi J, Manivong K, Dering J, Yang G, Chalukya M, Wang HJ, Anderson L, Kalli KR et al.: Expression of p16 and retinoblastoma determines response to CDK4/6 inhibition in ovarian cancer. Clin Cancer Res 2011, 17:1591-1602.
12. Malumbres M, Sotillo R, Santamaria D, Galan J, Cerezo A, Ortega S, Dubus P, Barbacid M: Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 2004, 118:493-504. (Pubitemid 39485668)
13. Miller TW, Balko JM, Fox EM, Ghazoui Z, Dunbier A, Anderson H, Dowsett M, Jiang A, Smith RA, Maira SM, Manning HC et al.: ERalpha-dependent E2F transcription can mediate resistance to estrogen deprivation in human breast cancer. Cancer Discov 2011, 1:338-351.
14. Thangavel C, Dean JL, Ertel A, Knudsen KE, Aldaz CM, Witkiewicz AK, Clarke R, Knudsen ES: Therapeutically activating RB: reestablishing cell cycle control in endocrine therapyresistant breast cancer. Endocr Relat Cancer 2011, 18:333-345.
15. Finn RS, Crown JP, Lang I, Boer K, Bondarenko IM, Kulyk SO, Ettl J, Patel R, Pinter T, Schmidt M, Shparyk Y et al.: Results of a randomized phase 2 study of PD 0332991, a cyclin-dependent kinase (CDK) 4/6 inhibitor, in combination with letrozole vs letrozole alone for first-line treatment of ER+/HER2S advanced breast cancer. Cancer Res 2012, 72(24 Suppl):S1-S6.
16. Lindqvist A, Rodriguez-Bravo V, Medema RH: The decision to enter mitosis: feedback and redundancy in the mitotic entry network. J Cell Biol 2009, 185:193-202.
17. Diril MK, Ratnacaram CK, Padmakumar VC, Du T, Wasser M, Coppola V, Tessarollo L, Kaldis P: Cyclin-dependent kinase 1 (Cdk1) is essential for cell division and suppression of DNA re-replication but not for liver regeneration. Proc Natl Acad Sci U S A 2012, 109:3826-3831.
18. Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, Schinzel AC, Sandy P, Meylan E, Scholl C, Frohling S et al.: Systematic RNA interference reveals that oncogenic KRASdriven cancers require TBK1. Nature 2009, 462:108-112.
19. Goga A, Yang D, Tward AD, Morgan DO, Bishop JM: Inhibition of CDK1 as a potential therapy for tumors over-expressing MYC. Nat Med 2007, 13:820-827. (Pubitemid 47038193)
20. Mayes PA, Dolloff NG, Daniel CJ, Liu JJ, Hart LS, Kuribayashi K, Allen JE, Jee DI, Dorsey JF, Liu YY, Dicker DT et al.: Overcoming hypoxia-induced apoptotic resistance through combinatorial inhibition of GSK-3beta and CDK1. Cancer Res 2011, 71:5265-5275.
21. Strebhardt K: Multifaceted polo-like kinases: drug targets and antitargets for cancer therapy. Nat Rev Drug Discov 2010, 9:643-660.
22. van Vugt MA, Yaffe MB: Cell cycle re-entry mechanisms after DNA damage checkpoints: giving it some gas to shut off the breaks! Cell Cycle 2010, 9:2097-2101.
23. Lens SM, Voest EE, Medema RH: Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nat Rev Cancer 2010, 10:825-841.
24. Raab M, Kappel S, Kramer A, Sanhaji M, Matthess Y, Kurunci- Csacsko E, Calzada-Wack J, Rathkolb B, Rozman J, Adler T, Busch DH et al.: Toxicity modelling of Plk1-targeted therapies in genetically engineered mice and cultured primary mammalian cells. Nat Commun 2011, 2.
25. Luo J, Emanuele MJ, Li D, Creighton CJ, Schlabach MR, Westbrook TF, Wong KK, Elledge SJ: A genome-wide RNAi screen identifies multiple synthetic lethal interactions with the Ras oncogene. Cell 2009, 137:835-848.
26. Deeraksa A, Pan J, Sha Y, Liu XD, Eissa NT, Lin SH, Yu-Lee LY: Plk1 is upregulated in androgen-insensitive prostate cancer cells and its inhibition leads to necroptosis. Oncogene 2012 http://dx.doi.org/10.1038/onc.2012.309. [Epub ahead of print].
27. Dasmahapatra G, Patel H, Nguyen T, Attkisson E, Grant S: PLK1 inhibitors synergistically potentiate HDAC inhibitor lethality in imatinib mesylate-sensitive or -resistant BCR/ ABL+ leukemia cells in vitro and in vivo. Clin Cancer Res 2013, 19:404-414.
28. Matulonis UA, Sharma S, Ghamande S, Gordon MS, Del Prete SA, Ray-Coquard I, Kutarska E, Liu H, Fingert H, Zhou X, Danaee H et al.: Phase II study of MLN8237 (alisertib), an investigational Aurora A kinase inhibitor, in patients with platinum-resistant or -refractory epithelial ovarian, fallopian tube, or primary peritoneal carcinoma. Gynecol Oncol 2012, 127:63-69.
29. Olmos D, Barker D, Sharma R, Brunetto AT, Yap TA, Taegtmeyer AB, Barriuso J, Medani H, Degenhardt YY, Allred AJ, Smith DA et al.: Phase I study of GSK461364, a specific and competitive Polo-like kinase 1 inhibitor, in patients with advanced solid malignancies. Clin Cancer Res 2011, 17:3420-3430.
30. Mross K, Frost A, Steinbild S, Hedbom S, Rentschler J, Kaiser R, Rouyrre N, Trommeshauser D, Hoesl CE, Munzert G: Phase I dose escalation and pharmacokinetic study of BI 2536, a novel Polo-like kinase 1 inhibitor, in patients with advanced solid tumors. J Clin Oncol 2008, 26:5511-5517.
31. Jimeno A, Li J, Messersmith WA, Laheru D, Rudek MA, Maniar M, Hidalgo M, Baker SD, Donehower RC: Phase I study of ON 01910.Na, a novel modulator of the Polo-like kinase 1 pathway, in adult patients with solid tumors. J Clin Oncol 2008, 26:5504-5510.
32. Ma CX, Cai S, Li S, Ryan CE, Guo Z, Schaiff WT, Lin L, Hoog J, Goiffon RJ, Prat A, Aft RL et al.: Targeting Chk1 in p53-deficient triple-negative breast cancer is therapeutically beneficial in human-in-mouse tumor models. J Clin Invest 2012, 122:1541-1552.
33. Morgan MA, Parsels LA, Zhao L, Parsels JD, Davis MA, Hassan MC, Arumugarajah S, Hylander-Gans L, Morosini D, Simeone DM, Canman CE et al.: Mechanism of radiosensitization by the Chk1/2 inhibitor AZD7762 involves abrogation of the G2 checkpoint and inhibition of homologous recombinational DNA repair. Cancer Res 2010, 70:4972-4981.
34. Vance S, Liu E, Zhao L, Parsels JD, Parsels LA, Brown JL, Maybaum J, Lawrence TS, Morgan MA: Selective radiosensitization of p53 mutant pancreatic cancer cells by combined inhibition of Chk1 and PARP1. Cell Cycle 2011, 10:4321-4329.
35. Petermann E, Woodcock M, Helleday T: Chk1 promotes replication fork progression by controlling replication initiation. Proc Natl Acad Sci U S A 2010, 107:16090-16095.
36. Kramer A, Mailand N, Lukas C, Syljuasen RG, Wilkinson CJ, Nigg EA, Bartek J, Lukas J: Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 2004, 6:884-891. (Pubitemid 39207253)
37. Zachos G, Black EJ, Walker M, Scott MT, Vagnarelli P, Earnshaw WC, Gillespie DA: Chk1 is required for spindle checkpoint function. Dev Cell 2007, 12:247-260. (Pubitemid 46193970)
38. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C, Orntoft T et al.: DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870. (Pubitemid 40558993)
39. Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, Johansson F, Helleday T, Sehested M, Lukas J, Bartek J: Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 2005, 25:3553-3562. (Pubitemid 40559562)
40. Brooks K, Oakes V, Edwards B, Ranall M, Leo P, Pavey S, Pinder A, Beamish H, Mukhopadhyay P, Lambie D, Gabrielli B: A potent Chk1 inhibitor is selectively cytotoxic in melanomas with high levels of replicative stress. Oncogene 2012.
41. Gilad O, Nabet BY, Ragland RL, Schoppy DW, Smith KD, Durham AC, Brown EJ: Combining ATR suppression with oncogenic Ras synergistically increases genomic instability, causing synthetic lethality or tumorigenesis in a dosagedependent manner. Cancer Res 2010, 70:9693-9702.
42. Murga M, Campaner S, Lopez-Contreras AJ, Toledo LI, Soria R, Montana MF, D'Artista L, Schleker T, Guerra C, Garcia E, Barbacid M et al.: Exploiting oncogene-induced replicative stress for the selective killing of Myc-driven tumors. Nat Struct Mol Biol 2011, 18:1331-1335.
43. Hirai H, Iwasawa Y, Okada M, Arai T, Nishibata T, Kobayashi M, Kimura T, Kaneko N, Ohtani J, Yamanaka K, Itadani H et al.: Smallmolecule inhibition of Wee1 kinase by MK-1775 selectively sensitizes p53-deficient tumor cells to DNA-damaging agents. Mol Cancer Ther 2009, 8:2992-3000.
44. Hirai H, Arai T, Okada M, Nishibata T, Kobayashi M, Sakai N, Imagaki K, Ohtani J, Sakai T, Yoshizumi T, Mizuarai S et al.: MK- 1775, a small molecule Wee1 inhibitor, enhances anti-tumor efficacy of various DNA-damaging agents, including 5- fluorouracil. Cancer Biol Ther 2010, 9:514-522.
45. Dominguez-Kelly R, Martin Y, Koundrioukoff S, Tanenbaum ME, Smits VA, Medema RH, Debatisse M, Freire R: Wee1 controls genomic stability during replication by regulating the Mus81- Eme1 endonuclease. J Cell Biol 2011, 194:567-579.
46. Beck H, Nahse-Kumpf V, Larsen MS, O'Hanlon KA, Patzke S, Holmberg C, Mejlvang J, Groth A, Nielsen O, Syljuasen RG, Sorensen CS: Cyclin-dependent kinase suppression by WEE1 kinase protects the genome through control of replication initiation and nucleotide consumption. Mol Cell Biol 2012, 32:4226-4236.
47. Krajewska M, Heijink AM, Bisselink YJ, Seinstra RI, Sillje HH, de Vries EG, van Vugt MA: Forced activation of Cdk1 via wee1 inhibition impairs homologous recombination. Oncogene 2012 http://dx.doi.org/10.1038/onc.2012.296. [Epub ahead of print].
48. Aarts M, Sharpe R, Garcia-Murillas I, Gevensleben H, Hurd MS, Shumway SD, Toniatti C, Ashworth A, Turner NC: Forced mitotic entry of S-phase cells as a therapeutic strategy induced by inhibition of WEE1. Cancer Discov 2012, 2:524-539.
49. Wilsker D, Petermann E, Helleday T, Bunz F: Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc Natl Acad Sci U S A 2008, 105:20752-20757.
50. Mannefeld M, Klassen E, Gaubatz S: B-MYB is required for recovery from the DNA damage-induced G2 checkpoint in p53 mutant cells. Cancer Res 2009, 69:4073-4080.
51. Mir SE, De Witt Hamer PC, Krawczyk PM, Balaj L, Claes A, Niers JM, Van Tilborg AA, Zwinderman AH, Geerts D, Kaspers GJ, Peter Vandertop W et al.: In silico analysis of kinase expression identifies WEE1 as a gatekeeper against mitotic catastrophe in glioblastoma. Cancer Cell 2010, 18:244-257.
52. Guertin AD, Martin MM, Roberts B, Hurd M, Qu X, Miselis NR, Liu Y, Li J, Feldman I, Benita Y, Bloecher A et al.: Unique functions of CHK1 and WEE1 underlie synergistic anti-tumor activity upon pharmacologic inhibition. Cancer Cell Int 2012, 12:45.
53. Foley EA, Kapoor TM: Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat Rev Mol Cell Biol 2013, 14:25-37.
54. Yang Z, Loncarek J, Khodjakov A, Rieder CL: Extra centrosomes and/or chromosomes prolong mitosis in human cells. Nat Cell Biol 2008, 10:748-751. (Pubitemid 351772940)
55. Abrieu A, Magnaghi-Jaulin L, Kahana JA, Peter M, Castro A, Vigneron S, Lorca T, Cleveland DW, Labbe JC: Mps1 is a kinetochore-associated kinase essential for the vertebrate mitotic checkpoint. Cell 2001, 106:83-93. (Pubitemid 32709960)
56. Daniel J, Coulter J, Woo JH, Wilsbach K, Gabrielson E: High levels of the Mps1 checkpoint protein are protective of aneuploidy in breast cancer cells. Proc Natl Acad Sci U S A 2011, 108:5384-5389.
57. Colombo R, Caldarelli M, Mennecozzi M, Giorgini ML, Sola F, Cappella P, Perrera C, Depaolini SR, Rusconi L, Cucchi U, Avanzi N et al.: Targeting the mitotic checkpoint for cancer therapy with NMS-P715, an inhibitor of MPS1 kinase. Cancer Res 2010, 70:10255-10264.
58. Tardif KD, Rogers A, Cassiano J, Roth BL, Cimbora DM, McKinnon R, Peterson A, Douce TB, Robinson R, Dorweiler I, Davis T et al.: Characterization of the cellular and antitumor effects of MPI-0479605, a small-molecule inhibitor of the mitotic kinase Mps1. Mol Cancer Ther 2011, 10:2267-2275.
59. Shen WH, Balajee AS, Wang J, Wu H, Eng C, Pandolfi PP, Yin Y: Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 2007, 128:157-170. (Pubitemid 46048887)
60. Brough R, Frankum JR, Sims D, Mackay A, Mendes-Pereira AM, Bajrami I, Costa-Cabral S, Rafiq R, Ahmad AS, Cerone MA, Natrajan R et al.: Functional viability profiles of breast cancer. Cancer Discov 2011, 1:260-273.
61. Bonet C, Giuliano S, Ohanna M, Bille K, Allegra M, Lacour JP, Bahadoran P, Rocchi S, Ballotti R, Bertolotto C: Aurora B is regulated by the mitogen-activated protein kinase/ extracellular signal-regulated kinase (MAPK/ERK) signaling pathway and is a valuable potential target in melanoma cells. J Biol Chem 2012, 287:29887-29898.
62. Goto H, Yasui Y, Nigg EA, Inagaki M: Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 2002, 7:11-17. (Pubitemid 34121301)
63. Carpinelli P, Moll J: Aurora kinase inhibitors: identification and preclinical validation of their biomarkers. Expert Opin Ther Targets 2008, 12:69-80. (Pubitemid 351247163)
64. Marxer M, Foucar CE, Man WY, Chen Y, Ma HT, Poon RY: Tetraploidization increases sensitivity to Aurora B kinase inhibition. Cell Cycle 2012, 11:2567-2577.
65. Gully CP, Velazquez-Torres G, Shin JH, Fuentes-Mattei E, Wang E, Carlock C, Chen J, Rothenberg D, Adams HP, Choi HH, Guma S et al.: Aurora B kinase phosphorylates and instigates degradation of p53. Proc Natl Acad Sci U S A 2012, 109:E1513-E1522.
66. Lowenberg B, Muus P, Ossenkoppele G, Rousselot P, Cahn JY, Ifrah N, Martinelli G, Amadori S, Berman E, Sonneveld P, Jongen- Lavrencic M et al.: Phase 1/2 study to assess the safety, efficacy, and pharmacokinetics of barasertib (AZD1152) in patients with advanced acute myeloid leukemia. Blood 2011, 118:6030-6036.